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  • Linking the fine-scale social environment to mating decisions: a future direction for the study of extra-pair paternity
    Biol. Rev. (IF 11.615) Pub Date : 2018-03-13
    Adriana A. Maldonado-Chaparro, Pierre-Olivier Montiglio, Wolfgang Forstmeier, Bart Kempenaers, Damien R. Farine

    ABSTRACTVariation in extra-pair paternity (EPP) among individuals of the same population could result from stochastic demography or from individual differences in mating strategies. Although the adaptive value of EPP has been widely studied, much less is known about the characteristics of the social environment that drive the observed patterns of EPP. Here, we demonstrate how concepts and well-developed tools for the study of social behaviour (such as social network analysis) can enhance the study of extra-pair mating decisions (focussing in particular on avian mating systems). We present several hypotheses that describe how characteristics of the social environment in which individuals are embedded might influence the levels of EPP in a socially monogamous population. We use a multi-level social approach (Hinde, 1976) to achieve a detailed description of the social structure and social dynamics of individuals in a group. We propose that the pair-bond, the direct (local) social environment and the indirect (extended) social environment, can contribute in different ways to the variation observed in the patterns of EPP, at both the individual and the population level. A strength of this approach is that it integrates into the analysis (indirect) interactions with all potential mates in a population, thus extending the current framework to study extra-pair mating behaviour. We also encourage the application of social network methods such as temporal dynamic analysis to depict temporal changes in the patterns of interactions among individuals in a group, and to study how this affects mating behaviour. We argue that this new framework will contribute to a better understanding of the proximate mechanisms that drive variation in EPP within populations in socially monogamous species, and might ultimately provide insights into the evolution and maintenance of mating systems.

  • Function and underlying mechanisms of seasonal colour moulting in mammals and birds: what keeps them changing in a warming world?
    Biol. Rev. (IF 11.615) Pub Date : 2018-03-05
    Marketa Zimova, Klaus Hackländer, Jeffrey M. Good, José Melo-Ferreira, Paulo Célio Alves, L. Scott Mills

    ABSTRACT Animals that occupy temperate and polar regions have specialized traits that help them survive in harsh, highly seasonal environments. One particularly important adaptation is seasonal coat colour (SCC) moulting. Over 20 species of birds and mammals distributed across the northern hemisphere undergo complete, biannual colour change from brown in the summer to completely white in the winter. But as climate change decreases duration of snow cover, seasonally winter white species (including the snowshoe hare Lepus americanus, Arctic fox Vulpes lagopus and willow ptarmigan Lagopus lagopus) become highly contrasted against dark snowless backgrounds. The negative consequences of camouflage mismatch and adaptive potential is of high interest for conservation. Here we provide the first comprehensive review across birds and mammals of the adaptive value and mechanisms underpinning SCC moulting. We found that across species, the main function of SCC moults is seasonal camouflage against snow, and photoperiod is the main driver of the moult phenology. Next, although many underlying mechanisms remain unclear, mammalian species share similarities in some aspects of hair growth, neuroendocrine control, and the effects of intrinsic and extrinsic factors on moult phenology. The underlying basis of SCC moults in birds is less understood and differs from mammals in several aspects. Lastly, our synthesis suggests that due to limited plasticity in SCC moulting, evolutionary adaptation will be necessary to mediate future camouflage mismatch and a detailed understanding of the SCC moulting will be needed to manage populations effectively under climate change.

  • The changing role of ornamental horticulture in alien plant invasions
    Biol. Rev. (IF 11.615) Pub Date : 2018-03-05
    Mark van Kleunen, Franz Essl, Jan Pergl, Giuseppe Brundu, Marta Carboni, Stefan Dullinger, Regan Early, Pablo González-Moreno, Quentin J. Groom, Philip E. Hulme, Christoph Kueffer, Ingolf Kühn, Cristina Máguas, Noëlie Maurel, Ana Novoa, Madalin Parepa, Petr Pyšek, Hanno Seebens, Rob Tanner, Julia Touza, Laura Verbrugge, Ewald Weber, Wayne Dawson, Holger Kreft, Patrick Weigelt, Marten Winter, Günther Klonner, Matthew V. Talluto, Katharina Dehnen-Schmutz

    ABSTRACT The number of alien plants escaping from cultivation into native ecosystems is increasing steadily. We provide an overview of the historical, contemporary and potential future roles of ornamental horticulture in plant invasions. We show that currently at least 75% and 93% of the global naturalised alien flora is grown in domestic and botanical gardens, respectively. Species grown in gardens also have a larger naturalised range than those that are not. After the Middle Ages, particularly in the 18th and 19th centuries, a global trade network in plants emerged. Since then, cultivated alien species also started to appear in the wild more frequently than non-cultivated aliens globally, particularly during the 19th century. Horticulture still plays a prominent role in current plant introduction, and the monetary value of live-plant imports in different parts of the world is steadily increasing. Historically, botanical gardens – an important component of horticulture – played a major role in displaying, cultivating and distributing new plant discoveries. While the role of botanical gardens in the horticultural supply chain has declined, they are still a significant link, with one-third of institutions involved in retail-plant sales and horticultural research. However, botanical gardens have also become more dependent on commercial nurseries as plant sources, particularly in North America. Plants selected for ornamental purposes are not a random selection of the global flora, and some of the plant characteristics promoted through horticulture, such as fast growth, also promote invasion. Efforts to breed non-invasive plant cultivars are still rare. Socio-economical, technological, and environmental changes will lead to novel patterns of plant introductions and invasion opportunities for the species that are already cultivated. We describe the role that horticulture could play in mediating these changes. We identify current research challenges, and call for more research efforts on the past and current role of horticulture in plant invasions. This is required to develop science-based regulatory frameworks to prevent further plant invasions.

  • Degradation for better survival? Role of ubiquitination in epithelial morphogenesis
    Biol. Rev. (IF 11.615) Pub Date : 2018-03-01
    Xiaoxiang Cheng, Jun Zheng, Gang Li, Verena Göbel, Hongjie Zhang

    ABSTRACT As a prevalent post-translational modification, ubiquitination is essential for many developmental processes. Once covalently attached to the small and conserved polypeptide ubiquitin (Ub), a substrate protein can be directed to perform specific biological functions via its Ub-modified form. Three sequential catalytic reactions contribute to this process, among which E3 ligases serve to identify target substrates and promote the activated Ub to conjugate to substrate proteins. Ubiquitination has great plasticity, with diverse numbers, topologies and modifications of Ub chains conjugated at different substrate residues adding a layer of complexity that facilitates a huge range of cellular functions. Herein, we highlight key advances in the understanding of ubiquitination in epithelial morphogenesis, with an emphasis on the latest insights into its roles in cellular events involved in polarized epithelial tissue, including cell adhesion, asymmetric localization of polarity determinants and cytoskeletal organization. In addition, the physiological roles of ubiquitination are discussed for typical examples of epithelial morphogenesis, such as lung branching, vascular development and synaptic formation and plasticity. Our increased understanding of ubiquitination in epithelial morphogenesis may provide novel insights into the molecular mechanisms underlying epithelial regeneration and maintenance.

  • The stepwise development of the lamprey visual system and its evolutionary implications
    Biol. Rev. (IF 11.615) Pub Date : 2018-02-28
    Daichi G. Suzuki, Sten Grillner

    ABSTRACT Lampreys, which represent the oldest group of living vertebrates (cyclostomes), show unique eye development. The lamprey larva has only eyespot-like immature eyes beneath a non-transparent skin, whereas after metamorphosis, the adult has well-developed image-forming camera eyes. To establish a functional visual system, well-organised visual centres as well as motor components (e.g. trunk muscles for locomotion) and interactions between them are needed. Here we review the available knowledge concerning the structure, function and development of the different parts of the lamprey visual system. The lamprey exhibits stepwise development of the visual system during its life cycle. In prolarvae and early larvae, the ‘primary’ retina does not have horizontal and amacrine cells, but does have photoreceptors, bipolar cells and ganglion cells. At this stage, the optic nerve projects mostly to the pretectum, where the dendrites of neurons in the nucleus of the medial longitudinal fasciculus (nMLF) appear to receive direct visual information and send motor outputs to the neck and trunk muscles. This simple neural circuit may generate negative phototaxis. Through the larval period, the lateral region of the retina grows again to form the ‘secondary’ retina and the topographic retinotectal projection of the optic nerve is formed, and at the same time, the extra-ocular muscles progressively develop. During metamorphosis, horizontal and amacrine cells differentiate for the first time, and the optic tectum expands and becomes laminated. The adult lamprey then has a sophisticated visual system for image-forming and visual decision-making. In the adult lamprey, the thalamic pathway (retina–thalamus–cortex/pallium) also transmits visual stimuli. Because the primary, simple light-detecting circuit in larval lamprey shares functional and developmental similarities with that of protochordates (amphioxus and tunicates), the visual development of the lamprey provides information regarding the evolutionary transition of the vertebrate visual system from the protochordate-type to the vertebrate-type.

  • Colony formation in the cyanobacterium Microcystis
    Biol. Rev. (IF 11.615) Pub Date : 2018-02-22
    Man Xiao, Ming Li, Colin S. Reynolds

    ABSTRACT Morphological evolution from a unicellular to multicellular state provides greater opportunities for organisms to attain larger and more complex living forms. As the most common freshwater cyanobacterial genus, Microcystis is a unicellular microorganism, with high phenotypic plasticity, which forms colonies and blooms in lakes and reservoirs worldwide. We conducted a systematic review of field studies from the 1990s to 2017 where Microcystis was dominant. Microcystis was detected as the dominant genus in waterbodies from temperate to subtropical and tropical zones. Unicellular Microcystis spp. can be induced to form colonies by adjusting biotic and abiotic factors in laboratory. Colony formation by cell division has been induced by zooplankton filtrate, high Pb2+ concentration, the presence of another cyanobacterium (Cylindrospermopsis raciborskii), heterotrophic bacteria, and by low temperature and light intensity. Colony formation by cell adhesion can be induced by zooplankton grazing, high Ca2+ concentration, and microcystins. We hypothesise that single cells of all Microcystis morphospecies initially form colonies with a similar morphology to those found in the early spring. These colonies gradually change their morphology to that of M. ichthyoblabe, M. wesenbergii and M. aeruginosa with changing environmental conditions. Colony formation provides Microcystis with many ecological advantages, including adaption to varying light, sustained growth under poor nutrient supply, protection from chemical stressors and protection from grazing. These benefits represent passive tactics responding to environmental stress. Microcystis colonies form at the cost of decreased specific growth rates compared with a unicellular habit. Large colony size allows Microcystis to attain rapid floating velocities (maximum recorded for a single colony, ∼ 10.08 m h−1) that enable them to develop and maintain a large biomass near the surface of eutrophic lakes, where they may shade and inhibit the growth of less-buoyant species in deeper layers. Over time, accompanying species may fail to maintain viable populations, allowing Microcystis to dominate. Microcystis blooms can be controlled by artificial mixing. Microcystis colonies and non-buoyant phytoplankton will be exposed to identical light conditions if they are evenly distributed over the water column. In that case, green algae and diatoms, which generally have a higher growth rate than Microcystis, will be more successful. Under such mixing conditions, other phytoplankton taxa could recover and the dominance of Microcystis would be reduced. This review advances our understanding of the factors and mechanisms affecting Microcystis colony formation and size in the field and laboratory through synthesis of current knowledge. The main transition pathways of morphological changes in Microcystis provide an example of the phenotypic plasticity of organisms during morphological evolution from a unicellular to multicellular state. We emphasise that the mechanisms and factors influencing competition among various close morphospecies are sometimes paradoxical because these morphospecies are potentially a single species. Further work is required to clarify the colony-forming process in different Microcystis morphospecies and the seasonal variation in this process. This will allow researchers to grow laboratory cultures that more closely reflect field morphologies and to optimise artificial mixing to manage blooms more effectively.

  • Integrins promote axonal regeneration after injury of the nervous system
    Biol. Rev. (IF 11.615) Pub Date : 2018-02-15
    Bart Nieuwenhuis, Barbara Haenzi, Melissa R. Andrews, Joost Verhaagen, James W. Fawcett

    ABSTRACT Integrins are cell surface receptors that form the link between extracellular matrix molecules of the cell environment and internal cell signalling and the cytoskeleton. They are involved in several processes, e.g. adhesion and migration during development and repair. This review focuses on the role of integrins in axonal regeneration. Integrins participate in spontaneous axonal regeneration in the peripheral nervous system through binding to various ligands that either inhibit or enhance their activation and signalling. Integrin biology is more complex in the central nervous system. Integrins receptors are transported into growing axons during development, but selective polarised transport of integrins limits the regenerative response in adult neurons. Manipulation of integrins and related molecules to control their activation state and localisation within axons is a promising route towards stimulating effective regeneration in the central nervous system.

  • Evolution and development of scyphozoan jellyfish
    Biol. Rev. (IF 11.615) Pub Date : 2018-02-14
    Rebecca R. Helm

    ABSTRACT Scyphozoan jellyfish, or scyphomedusae, are conspicuous members of many ocean ecosystems, and have large impacts on human health and industry. Most scyphomedusae are the final stage in a complex life cycle that also includes two intermediate stages: the larval planula and benthic polyp. In species with all three life-cycle stages, the metamorphosis of a polyp into a juvenile scyphomedusa (ephyra) is termed strobilation, and polyps can produce one ephyra (termed monodisc strobilation) or many ephyrae (termed polydisc strobilation). In contrast to species with planula, polyp and medusa stages, a handful of scyphozoan species possess modified life cycles with reduced or absent stages. The evolutionary patterns associated with strobilation and life-cycle type have not been thoroughly investigated, and many studies of ephyra development and strobilation induction are not yet synthesized. Herein, I place the development of scyphomedusae in an evolutionary context. I first review the current evolutionary hypotheses for Scyphozoa. Next, I review what is known about scyphomedusa development across a broad diversity of species, including the first signs of strobilation, the formation of strobila segments, and the morphogenesis of ephyrae. I then review cases where the canonical scyphozoan life cycle has been modified, and take advantage of phylogenetic hypotheses to place these observations in an evolutionary context. I show that the evolution of monodisc strobilation occurred at least twice, and that the loss of intermediate life-cycle stages occurred several times independently; by contrast, the reduction of the medusa stage appears to have occurred within a single clade. I then briefly review the major natural cues of strobilation induction. Finally, I summarize what is currently known about the molecular mechanisms of strobilation induction and ephyra development. I conclude with suggestions for future directions in the field.

  • Behavioural mating displays depend on mitochondrial function: a potential mechanism for linking behaviour to individual condition
    Biol. Rev. (IF 11.615) Pub Date : 2018-02-13
    Rebecca E. Koch, Geoffrey E. Hill

    ABSTRACT Males of many animal species court females using complex behavioural displays that are challenging to produce, and some of these displays have been shown to be associated with aspects of male quality. However, the mechanisms by which behavioural displays are linked to individual condition remain uncertain. Herein, we illustrate fundamental mechanistic connections between mitochondrial function and neurogenesis, energy production, and a variety of pathways that underlie the ability of an individual to perform complex behaviours. We consider the biomedical evidence for how mitochondrial activity shapes neurogenesis during development and neural function in adulthood, and how both genetics and environmental conditions can cause variation in mitochondrial function in wild animals. An individual's mitochondrial phenotype determines not just metabolism and available energy, but also appears to serve as an important driver of capacity to perform cognitively complex and other challenging display behaviours. We apply this concept to the example of birdsong, a well-studied display behaviour with known links to neural pathways, and we describe how mitochondrial involvement in a variety of important internal processes creates links between display quality and key traits like immunocompetence. By synthesizing the intimate involvement of mitochondria in neural processes with the physiological bases of display behaviour, we aim to provide new mechanistic explanations for information that females may gain by assessing complex male displays.

  • Amyloids of multiple species: are they helpful in survival?
    Biol. Rev. (IF 11.615) Pub Date : 2018-02-13
    Arun Upadhyay, Amit Mishra

    ABSTRACT Amyloids are primarily known for their roles in neurodegenerative disorders, as well as in systemic diseases like diabetes. Evolutionary forces tend to maintain a healthy set of heritable characteristics, while eliminating toxic or unfavourable elements; but amyloids seem to represent an exception to this fundamental concept. In addition to their presence in mammals, amyloids also persist in the proteome of many lower organisms that may be linked with possible roles in survival, which are still unexplored. Herein, we address some unanswered questions regarding amyloids: are these well-structured proteinaceous aggregates a by-product of inefficient folding events, or have they been retained in our protein repertoire for as yet unknown functional roles; and how do protein misfolding and associated disorders originate, despite the presence of protein quality-control systems inside the cells? This review aims to extend our current understanding about the multifaceted useful properties of amyloids and their functional interactions with other molecular pathways in various species; this may provide new insights to identify novel therapeutic strategies for ageing and neurodegenerative diseases.

  • The role of mate-choice copying in speciation and hybridization
    Biol. Rev. (IF 11.615) Pub Date : 2018-02-08
    Susana A. M. Varela, Margarida Matos, Ingo Schlupp

    ABSTRACT Mate-choice copying, a social, non-genetic mechanism of mate choice, occurs when an individual (typically a female) copies the mate choice of other individuals via a process of social learning. Over the past 20 years, mate-choice copying has consistently been shown to affect mate choice in several species, by altering the genetically based expression of mating preferences. This behaviour has been claimed by several authors to have a significant role in evolution. Because it can cause or increase skews in male mating success, it seems to have the potential to induce a rapid change of the directionality and rate of sexual selection, possibly leading to divergent evolution and speciation. Theoretical work has, however, been challenging this view, showing that copying may decelerate sexual selection and that linkage disequilibrium cannot be established between the copied preference and the male trait, because females copy from unrelated individuals in the population, making an invasion of new and potentially fitter male traits difficult. Given this controversy, it is timely to ask about the real impact of mate-choice copying in speciation. We propose that a solution to this impasse may be the existence of some degree of habitat selection, which would create a spatial structure, causing scenarios of micro-allopatry and thus overcoming the problem of the lack of linkage disequilibrium. As far as we are aware, the potential role of mate-choice copying on fostering speciation in micro-allopatry has not been tackled. Also important is that the role of mate-choice copying has generally been discussed as being a barrier to gene flow. However, in our view, mate-choice copying may actually play a key role in facilitating gene flow, thereby fostering hybridization. Yet, the role of mate-choice copying in hybridization has so far been overlooked, although the conditions under which it might occur are more likely, or less restricted, than those favouring speciation. Hence, a conceptual framework is needed to identify the exact mechanisms and the conditions under which speciation or hybridization are expected. Here, we develop such a framework to be used as a roadmap for future research at the intersection of these research areas.

  • Intergenerational effects of nutrition on immunity: a systematic review and meta-analysis
    Biol. Rev. (IF 11.615) Pub Date : 2017-11-27
    Catherine E. Grueber, Lindsey J. Gray, Katrina M. Morris, Stephen J. Simpson, Alistair M. Senior

    ABSTRACT Diet and immunity are both highly complex processes through which organisms interact with their environment and adapt to variable conditions. Parents that are able to transmit information to their offspring about prevailing environmental conditions have a selective advantage by ‘priming’ the physiology of their offspring. We used a meta-analytic approach to test the effect of parental diet on offspring immune responses. Using the geometric framework for nutrition (a method for analysing diet compositions wherein food nutrient components are expressed as axes in a Cartesian coordinate space) to define dietary manipulations in terms of their energy and macronutrient compositions, we compiled the results of 226 experiments from 38 published papers on the intergenerational effects of diet on immunity, across a range of study species and immunological responses. We observed intergenerational impacts of parental nutrition on a number of offspring immunological processes, including expression of pro-inflammatory biomarkers as well as decreases in anti-inflammatory markers in response to certain parental diets. For example, across our data set as a whole (encompassing several types of dietary manipulation), dietary stress in parents was seen to significantly increase pro-inflammatory cytokine levels measured in offspring (overall d = 0.575). All studies included in our analysis were from experiments in which the offspring were raised on a normal or control diet, so our findings suggest that a nutrition-dependent immune state can be inherited, and that this immune state is maintained in the short term, despite offspring returning to an ‘optimal’ diet. We demonstrate how the geometric framework for nutrition can be used to disentangle the role that different forms of dietary manipulation can have on intergenerational immunity. For example, offspring B-cell responses were significantly decreased when parents were raised on a range of different diets. Similarly, our approach allowed us to show that a parental diet elevated in protein (regardless of energy composition and relative to a control diet) can increase expression of inflammatory markers while decreasing B-cell-associated markers. By conducting a systematic review of the literature, we have identified important gaps that impair our understanding of the intergenerational effects of diet, such as a paucity of experimental studies involving increased protein and decreased energy, and a lack of studies directed at the whole-organism consequences of these processes, such as immune resilience to infection. The results of our analyses inform our understanding of the effects of diet on physiological state across diverse biological fields, including biomedical sciences, maintenance of agricultural breed stock and conservation breeding programs, among others.

  • A conceptual framework for understanding the perspectives on the causes of the science–practice gap in ecology and conservation
    Biol. Rev. (IF 11.615) Pub Date : 2017-11-20
    Diana Bertuol-Garcia, Carla Morsello, Charbel N. El-Hani, Renata Pardini

    ABSTRACT Applying scientific knowledge to confront societal challenges is a difficult task, an issue known as the science–practice gap. In Ecology and Conservation, scientific evidence has been seldom used directly to support decision-making, despite calls for an increasing role of ecological science in developing solutions for a sustainable future. To date, multiple causes of the science–practice gap and diverse approaches to link science and practice in Ecology and Conservation have been proposed. To foster a transparent debate and broaden our understanding of the difficulties of using scientific knowledge, we reviewed the perceived causes of the science–practice gap, aiming to: (i) identify the perspectives of ecologists and conservation scientists on this problem, (ii) evaluate the predominance of these perspectives over time and across journals, and (iii) assess them in light of disciplines studying the role of science in decision-making. We based our review on 1563 sentences describing causes of the science–practice gap extracted from 122 articles and on discussions with eight scientists on how to classify these sentences. The resulting process-based framework describes three distinct perspectives on the relevant processes, knowledge and actors in the science–practice interface. The most common perspective assumes only scientific knowledge should support practice, perceiving a one-way knowledge flow from science to practice and recognizing flaws in knowledge generation, communication, and/or use. The second assumes that both scientists and decision-makers should contribute to support practice, perceiving a two-way knowledge flow between science and practice through joint knowledge-production/integration processes, which, for several reasons, are perceived to occur infrequently. The last perspective was very rare, and assumes scientists should put their results into practice, but they rarely do. Some causes (e.g. cultural differences between scientists and decision-makers) are shared with other disciplines, while others seem specific to Ecology and Conservation (e.g. inadequate research scales). All identified causes require one of three general types of solutions, depending on whether the causal factor can (e.g. inadequate research questions) or cannot (e.g. scientific uncertainty) be changed, or if misconceptions (e.g. undervaluing abstract knowledge) should be solved. The unchanged predominance of the one-way perspective over time may be associated with the prestige of evidence-based conservation and suggests that debates in Ecology and Conservation lag behind trends in other disciplines towards bidirectional views ascribing larger roles to decision-makers. In turn, the two-way perspective seems primarily restricted to research traditions historically isolated from mainstream conservation biology. All perspectives represented superficial views of decision-making by not accounting for limits to human rationality, complexity of decision-making contexts, fuzzy science–practice boundaries, ambiguity brought about by science, and different types of knowledge use. However, joint knowledge-production processes from the two-way perspective can potentially allow for democratic decision-making processes, explicit discussions of values and multiple types of science use. To broaden our understanding of the interface and foster productive science–practice linkages, we argue for dialogue among different research traditions within Ecology and Conservation, joint knowledge-production processes between scientists and decision-makers and interdisciplinarity across Ecology, Conservation and Political Science in both research and education.

  • Identification of de novo germline mutations and causal genes for sporadic diseases using trio-based whole-exome/genome sequencing
    Biol. Rev. (IF 11.615) Pub Date : 2017-11-20
    Zi-Bing Jin, Zhongshan Li, Zhenwei Liu, Yi Jiang, Xue-Bi Cai, Jinyu Wu

    ABSTRACT Whole-genome or whole-exome sequencing (WGS/WES) of the affected proband together with normal parents (trio) is commonly adopted to identify de novo germline mutations (DNMs) underlying sporadic cases of various genetic disorders. However, our current knowledge of the occurrence and functional effects of DNMs remains limited and accurately identifying the disease-causing DNM from a group of irrelevant DNMs is complicated. Herein, we provide a general-purpose discussion of important issues related to pathogenic gene identification based on trio-based WGS/WES data. Specifically, the relevance of DNMs to human sporadic diseases, current knowledge of DNM biogenesis mechanisms, and common strategies or software tools used for DNM detection are reviewed, followed by a discussion of pathogenic gene prioritization. In addition, several key factors that may affect DNM identification accuracy and causal gene prioritization are reviewed. Based on recent major advances, this review both sheds light on how trio-based WGS/WES technologies can play a significant role in the identification of DNMs and causal genes for sporadic diseases, and also discusses existing challenges.

  • Reconstructing pectoral appendicular muscle anatomy in fossil fish and tetrapods over the fins-to-limbs transition
    Biol. Rev. (IF 11.615) Pub Date : 2017-11-10
    Julia L. Molnar, Rui Diogo, John R. Hutchinson, Stephanie E. Pierce

    ABSTRACT The question of how tetrapod limbs evolved from fins is one of the great puzzles of evolutionary biology. While palaeontologists, developmental biologists, and geneticists have made great strides in explaining the origin and early evolution of limb skeletal structures, that of the muscles remains largely unknown. The main reason is the lack of consensus about appendicular muscle homology between the closest living relatives of early tetrapods: lobe-finned fish and crown tetrapods. In the light of a recent study of these homologies, we re-examined osteological correlates of muscle attachment in the pectoral girdle, humerus, radius, and ulna of early tetrapods and their close relatives. Twenty-nine extinct and six extant sarcopterygians were included in a meta-analysis using information from the literature and from original specimens, when possible. We analysed these osteological correlates using parsimony-based character optimization in order to reconstruct muscle anatomy in ancestral lobe-finned fish, tetrapodomorph fish, stem tetrapods, and crown tetrapods. Our synthesis revealed that many tetrapod shoulder muscles probably were already present in tetrapodomorph fish, while most of the more-distal appendicular muscles either arose later from largely undifferentiated dorsal and ventral muscle masses or did not leave clear correlates of attachment in these taxa. Based on this review and meta-analysis, we postulate a stepwise sequence of specific appendicular muscle acquisitions, splits, and fusions that led from the ancestral sarcopterygian pectoral fin to the ancestral tetrapod forelimb. This sequence largely agrees with previous hypotheses based on palaeontological and comparative work, but it is much more comprehensive in terms of both muscles and taxa. Combined with existing information about the skeletal system, our new synthesis helps to illuminate the genetic, developmental, morphological, functional, and ecological changes that were key components of the fins-to-limbs transition.

  • Tick attachment cement – reviewing the mysteries of a biological skin plug system
    Biol. Rev. (IF 11.615) Pub Date : 2017-11-08
    Johannes Suppan, Benedikt Engel, Martina Marchetti-Deschmann, Sylvia Nürnberger

    ABSTRACT The majority of ticks in the family Ixodidae secrete a substance anchoring their mouthparts to the host skin. This substance is termed cement. It has adhesive properties and seals the lesion during feeding. The particular chemical composition and the curing process of the cement are unclear. This review summarizes the literature, starting with a historical overview, briefly introducing the different hypotheses on the origin of the adhesive and how the tick salivary glands have been identified as its source. Details on the sequence of cement deposition, the curing process and detachment are provided. Other possible functions of the cement, such as protection from the host immune system and antimicrobial properties, are presented. Histochemical and ultrastructural data of the intracellular granules in the salivary gland cells, as well as the secreted cement, suggest that proteins constitute the main material, with biochemical data revealing glycine to be the dominant amino acid. Applied methods and their restrictions are discussed. Tick cement is compared with adhesives of other animals such as barnacles, mussels and sea urchins. Finally, we address the potential of tick cement for the field of biomaterial research and in particular for medical applications in future.

  • Scaling biodiversity responses to hydrological regimes
    Biol. Rev. (IF 11.615) Pub Date : 2017-11-08
    Robert J. Rolls, Jani Heino, Darren S. Ryder, Bruce C. Chessman, Ivor O. Growns, Ross M. Thompson, Keith B. Gido

    ABSTRACT Of all ecosystems, freshwaters support the most dynamic and highly concentrated biodiversity on Earth. These attributes of freshwater biodiversity along with increasing demand for water mean that these systems serve as significant models to understand drivers of global biodiversity change. Freshwater biodiversity changes are often attributed to hydrological alteration by water-resource development and climate change owing to the role of the hydrological regime of rivers, wetlands and floodplains affecting patterns of biodiversity. However, a major gap remains in conceptualising how the hydrological regime determines patterns in biodiversity's multiple spatial components and facets (taxonomic, functional and phylogenetic). We synthesised primary evidence of freshwater biodiversity responses to natural hydrological regimes to determine how distinct ecohydrological mechanisms affect freshwater biodiversity at local, landscape and regional spatial scales. Hydrological connectivity influences local and landscape biodiversity, yet responses vary depending on spatial scale. Biodiversity at local scales is generally positively associated with increasing connectivity whereas landscape-scale biodiversity is greater with increasing fragmentation among locations. The effects of hydrological disturbance on freshwater biodiversity are variable at separate spatial scales and depend on disturbance frequency and history and organism characteristics. The role of hydrology in determining habitat for freshwater biodiversity also depends on spatial scaling. At local scales, persistence, stability and size of habitat each contribute to patterns of freshwater biodiversity yet the responses are variable across the organism groups that constitute overall freshwater biodiversity. We present a conceptual model to unite the effects of different ecohydrological mechanisms on freshwater biodiversity across spatial scales, and develop four principles for applying a multi-scaled understanding of freshwater biodiversity responses to hydrological regimes. The protection and restoration of freshwater biodiversity is both a fundamental justification and a central goal of environmental water allocation worldwide. Clearer integration of concepts of spatial scaling in the context of understanding impacts of hydrological regimes on biodiversity will increase uptake of evidence into environmental flow implementation, identify suitable biodiversity targets responsive to hydrological change or restoration, and identify and manage risks of environmental flows contributing to biodiversity decline.

  • Towards an eco-phylogenetic framework for infectious disease ecology
    Biol. Rev. (IF 11.615) Pub Date : 2017-11-08
    Nicholas M. Fountain-Jones, William D. Pearse, Luis E. Escobar, Ana Alba-Casals, Scott Carver, T. Jonathan Davies, Simona Kraberger, Monica Papeş, Kurt Vandegrift, Katherine Worsley-Tonks, Meggan E. Craft

    ABSTRACT Identifying patterns and drivers of infectious disease dynamics across multiple scales is a fundamental challenge for modern science. There is growing awareness that it is necessary to incorporate multi-host and/or multi-parasite interactions to understand and predict current and future disease threats better, and new tools are needed to help address this task. Eco-phylogenetics (phylogenetic community ecology) provides one avenue for exploring multi-host multi-parasite systems, yet the incorporation of eco-phylogenetic concepts and methods into studies of host pathogen dynamics has lagged behind. Eco-phylogenetics is a transformative approach that uses evolutionary history to infer present-day dynamics. Here, we present an eco-phylogenetic framework to reveal insights into parasite communities and infectious disease dynamics across spatial and temporal scales. We illustrate how eco-phylogenetic methods can help untangle the mechanisms of host–parasite dynamics from individual (e.g. co-infection) to landscape scales (e.g. parasite/host community structure). An improved ecological understanding of multi-host and multi-pathogen dynamics across scales will increase our ability to predict disease threats.

  • The function and mechanism of vocal accommodation in humans and other primates
    Biol. Rev. (IF 11.615) Pub Date : 2017-11-07
    Hanna Ruch, Yvonne Zürcher, Judith M. Burkart

    ABSTRACT The study of non-human animals, in particular primates, can provide essential insights into language evolution. A critical element of language is vocal production learning, i.e. learning how to produce calls. In contrast to other lineages such as songbirds, vocal production learning of completely new signals is strikingly rare in non-human primates. An increasing body of research, however, suggests that various species of non-human primates engage in vocal accommodation and adjust the structure of their calls in response to environmental noise or conspecific vocalizations. To date it is unclear what role vocal accommodation may have played in language evolution, in particular because it summarizes a variety of heterogeneous phenomena which are potentially achieved by different mechanisms. In contrast to non-human primates, accommodation research in humans has a long tradition in psychology and linguistics. Based on theoretical models from these research traditions, we provide a new framework which allows comparing instances of accommodation across species, and studying them according to their underlying mechanism and ultimate biological function. We found that at the mechanistic level, many cases of accommodation can be explained with an automatic perception–production link, but some instances arguably require higher levels of vocal control. Functionally, both human and non-human primates use social accommodation to signal social closeness or social distance to a partner or social group. Together, this indicates that not only some vocal control, but also the communicative function of vocal accommodation to signal social closeness and distance must have evolved prior to the emergence of language, rather than being the result of it. Vocal accommodation as found in other primates has thus endowed our ancestors with pre-adaptations that may have paved the way for language evolution.

  • Ediacaran developmental biology
    Biol. Rev. (IF 11.615) Pub Date : 2017-11-03
    Frances S. Dunn, Alexander G. Liu, Philip C. J. Donoghue

    ABSTRACT Rocks of the Ediacaran System (635–541 Ma) preserve fossil evidence of some of the earliest complex macroscopic organisms, many of which have been interpreted as animals. However, the unusual morphologies of some of these organisms have made it difficult to resolve their biological relationships to modern metazoan groups. Alternative competing phylogenetic interpretations have been proposed for Ediacaran taxa, including algae, fungi, lichens, rhizoid protists, and even an extinct higher-order group (Vendobionta). If a metazoan affinity can be demonstrated for these organisms, as advocated by many researchers, they could prove informative in debates concerning the evolution of the metazoan body axis, the making and breaking of axial symmetries, and the appearance of a metameric body plan. Attempts to decipher members of the enigmatic Ediacaran macrobiota have largely involved study of morphology: comparative analysis of their developmental phases has received little attention. Here we present what is known of ontogeny across the three iconic Ediacaran taxa Charnia masoni, Dickinsonia costata and Pteridinium simplex, together with new ontogenetic data and insights. We use these data and interpretations to re-evaluate the phylogenetic position of the broader Ediacaran morphogroups to which these taxa are considered to belong (rangeomorphs, dickinsoniomorphs and erniettomorphs). We conclude, based on the available evidence, that the affinities of the rangeomorphs and the dickinsoniomorphs lie within Metazoa.

  • Structure, function, and regulation of mitofusin-2 in health and disease
    Biol. Rev. (IF 11.615) Pub Date : 2017-10-25
    Gursimran Chandhok, Michael Lazarou, Brent Neumann

    ABSTRACT Mitochondria are highly dynamic organelles that constantly migrate, fuse, and divide to regulate their shape, size, number, and bioenergetic function. Mitofusins (Mfn1/2), optic atrophy 1 (OPA1), and dynamin-related protein 1 (Drp1), are key regulators of mitochondrial fusion and fission. Mutations in these molecules are associated with severe neurodegenerative and non-neurological diseases pointing to the importance of functional mitochondrial dynamics in normal cell physiology. In recent years, significant progress has been made in our understanding of mitochondrial dynamics, which has raised interest in defining the physiological roles of key regulators of fusion and fission and led to the identification of additional functions of Mfn2 in mitochondrial metabolism, cell signalling, and apoptosis. In this review, we summarize the current knowledge of the structural and functional properties of Mfn2 as well as its regulation in different tissues, and also discuss the consequences of aberrant Mfn2 expression.

  • Innovation not recovery: dynamic redox promotes metazoan radiations
    Biol. Rev. (IF 11.615) Pub Date : 2017-10-16
    Rachel Wood, Douglas H. Erwin

    ABSTRACT Environmental fluctuations in redox may reinforce rather than hinder evolutionary transitions, such that variability in near-surface oceanic oxygenation can promote morphological evolution and novelty. Modern, low-oxygen regions are heterogeneous and dynamic habitats that support low diversity and are inhabited by opportunistic and non-skeletal metazoans. We note that several major radiation episodes follow protracted or repeating intervals (>1 million years) of persistent and dynamic shallow marine redox (oceanic anoxic events). These are also often associated with short-lived mass-extinction events (<0.5 million years) where skeletal benthic incumbents are removed, and surviving or newly evolved benthos initially inhabit transient oxic habitats. We argue that such intervals create critical opportunities for the generation of evolutionary novelty, followed by innovation and diversification. We develop a general model for redox controls on the distribution and structure of the shallow marine benthos in a dominantly anoxic world, and compile data from the terminal Ediacaran–mid-Cambrian (∼560–509 Ma), late Cambrian–Ordovician (∼500–445 Ma), and Permo-Triassic (∼255–205 Ma) to test these predictions. Assembly of phylogenetic data shows that prolonged and widespread anoxic intervals indeed promoted morphological novelty in soft-bodied benthos, providing the ancestral stock for subsequently skeletonized lineages to appear as innovations once oxic conditions became widespread and stable, in turn promoting major evolutionary diversification. As a result, we propose that so-called ‘recovery’ intervals after mass extinctions might be better considered as ‘innovation’ intervals.

  • Tethyan changes shaped aquatic diversification
    Biol. Rev. (IF 11.615) Pub Date : 2017-10-12
    Zhonge Hou, Shuqiang Li

    ABSTRACT The Tethys Ocean existed between the continents of Gondwana and Laurasia from the Triassic to the Pliocene. Analyses of multiple biogeographic and phylogenetic histories reveal that the subsequent breakup of the Tethys greatly influenced the distributions of many species. The ancestral Tethyan realm broke into five biogeographic provinces, including the present-day East Pacific, West Atlantic, East Atlantic, Mediterranean Sea, and Indo-West Pacific. Palaeogeographic maps illustrate the Mesozoic Atlantic opening, the Cenozoic closure of the Tethys, the Messinian Salinity Crisis, the mid-Miocene closure of the Central American Seaway, and Quaternary geological changes. Further, we consider Cenozoic sea-level changes and the formation of freshwater habitats. These reconstructions allow assessment of patterns of aquatic diversification for marine and freshwater animals, and comparison of vicariance and dispersal processes. Estimated divergence times indicate that fragmentation of the Tethys was responsible for the vicariant speciation of aquatic animals because these dates are consistent with associated tectonic events. The opening of the Atlantic Ocean during the Cretaceous is responsible for the earliest isolation between the West and East Atlantic. The mid-Miocene closure of the Tethys, which blocked global equatorial currents, appears to have isolated the Atlantic/Mediterranean Sea and Indo-West Pacific. Finally, formation of the Isthmus of Panama isolated East Pacific and West Atlantic marine organisms. Dispersals related to the Messinian Salinity Crisis and Quaternary sea-level changes influenced population structuring. Tethyan changes affected marine habitats, created new freshwater habitats, inland caves and ancient lakes along the Alps and Himalayas, and influenced anchialine caves at the edge of the ancient sea. The extensive new habitats provided opportunities for colonisation and rapid diversification. Future work should focus on testing the biological impact of the series of Tethyan changes.

  • How intraspecific variation in seed-dispersing animals matters for plants
    Biol. Rev. (IF 11.615) Pub Date : 2017-10-10
    Rafał Zwolak

    ABSTRACT Seed dispersal by animals is a complex phenomenon, characterized by multiple mechanisms and variable outcomes. Most researchers approach this complexity by analysing context-dependency in seed dispersal and investigating extrinsic factors that might influence interactions between plants and seed dispersers. Intrinsic traits of seed dispersers provide an alternative way of making sense of the enormous variation in seed fates. I review causes of intraspecific variability in frugivorous and granivorous animals, discuss their effects on seed dispersal, and outline likely consequences for plant populations and communities. Sources of individual variation in seed-dispersing animals include sexual dimorphism, changes associated with growth and ageing, individual specialization, and animal personalities. Sexual dimorphism of seed-dispersing animals influences seed fate through diverse mechanisms that range from effects caused by sex-specific differences in body size, to influences of male versus female cognitive functions. These differences affect the type of seed treatment (e.g. dispersal versus predation), the number of dispersed seeds, distance of seed dispersal, and likelihood that seeds are left in favourable sites for seeds or seedlings. The best-documented consequences of individual differences associated with growth and ageing involve quantity of dispersed seeds and the quality of seed treatment in the mouth and gut. Individual specialization on different resources affects the number of dispersed plant species, and therefore the connectivity and architecture of seed-dispersal networks. Animal personalities might play an important role in shaping interactions between plants and dispersers of their seeds, yet their potential in this regard remains overlooked. In general, intraspecific variation in seed-dispersing animals often influences plants through effects of these individual differences on the movement ecology of the dispersers. Two conditions are necessary for individual variation to exert a strong influence on seed dispersal. First, the individual differences in traits should translate into differences in crucial characteristics of seed dispersal. Second, individual variation is more likely to be important when the proportions of particular types of individuals fluctuate strongly in a population or vary across space; when proportions are static, it is less likely that intraspecific differences will be responsible for changes in the dynamics and outcomes of plant–animal interactions. In conclusion, focusing on variation among foraging animals rather than on species averages might bring new, mechanistic insights to the phenomenon of seed dispersal. While this shift in perspective is unlikely to replace the traditional approach (based on the assumption that all important variation occurs among species), it provides a complementary alternative to decipher the enormous variation observed in animal-mediated seed dispersal.

  • Ecological and evolutionary legacy of megafauna extinctions
    Biol. Rev. (IF 11.615) Pub Date : 2017-10-09
    Mauro Galetti, Marcos Moleón, Pedro Jordano, Mathias M. Pires, Paulo R. Guimarães, Thomas Pape, Elizabeth Nichols, Dennis Hansen, Jens M. Olesen, Michael Munk, Jacqueline S. Mattos, Andreas H. Schweiger, Norman Owen-Smith, Christopher N. Johnson, Robert J. Marquis, Jens-Christian Svenning

    ABSTRACT For hundreds of millions of years, large vertebrates (megafauna) have inhabited most of the ecosystems on our planet. During the late Quaternary, notably during the Late Pleistocene and the early Holocene, Earth experienced a rapid extinction of large, terrestrial vertebrates. While much attention has been paid to understanding the causes of this massive megafauna extinction, less attention has been given to understanding the impacts of loss of megafauna on other organisms with whom they interacted. In this review, we discuss how the loss of megafauna disrupted and reshaped ecological interactions, and explore the ecological consequences of the ongoing decline of large vertebrates. Numerous late Quaternary extinct species of predators, parasites, commensals and mutualistic partners were associated with megafauna and were probably lost due to their strict dependence upon them (co-extinctions). Moreover, many extant species have megafauna-adapted traits that provided evolutionary benefits under past megafauna-rich conditions, but are now of no or limited use (anachronisms). Morphological evolution and behavioural changes allowed some of these species partially to overcome the absence of megafauna. Although the extinction of megafauna led to a number of co-extinction events, several species that likely co-evolved with megafauna established new interactions with humans and their domestic animals. Species that were highly specialized in interactions with megafauna, such as large predators, specialized parasites, and large commensalists (e.g. scavengers, dung beetles), and could not adapt to new hosts or prey were more likely to die out. Partners that were less megafauna dependent persisted because of behavioural plasticity or by shifting their dependency to humans via domestication, facilitation or pathogen spill-over, or through interactions with domestic megafauna. We argue that the ongoing extinction of the extant megafauna in the Anthropocene will catalyse another wave of co-extinctions due to the enormous diversity of key ecological interactions and functional roles provided by the megafauna.

  • Reappraising the early evidence of durophagy and drilling predation in the fossil record: implications for escalation and the Cambrian Explosion
    Biol. Rev. (IF 11.615) Pub Date : 2017-10-02
    Russell D. C. Bicknell, John R. Paterson

    ABSTRACT The Cambrian Explosion is arguably the most extreme example of a biological radiation preserved in the fossil record, and studies of Cambrian Lagerstätten have facilitated the exploration of many facets of this key evolutionary event. As predation was a major ecological driver behind the Explosion – particularly the radiation of biomineralising metazoans – the evidence for shell crushing (durophagy), drilling and puncturing predation in the Cambrian (and possibly the Ediacaran) is considered. Examples of durophagous predation on biomineralised taxa other than trilobites are apparently rare, reflecting predator preference, taphonomic and sampling biases, or simply lack of documentation. The oldest known example of durophagy is shell damage on the problematic taxon Mobergella holsti from the early Cambrian (possibly Terreneuvian) of Sweden. Using functional morphology to identify (or perhaps misidentify) durophagous predators is discussed, with emphasis on the toolkit used by Cambrian arthropods, specifically the radiodontan oral cone and the frontal and gnathobasic appendages of various taxa. Records of drill holes and possible puncture holes in Cambrian shells are mostly on brachiopods, but the lack of prey diversity may represent either a true biological signal or a result of various biases. The oldest drilled Cambrian shells occur in a variety of Terreneuvian-aged taxa, but specimens of the ubiquitous Ediacaran shelly fossil Cloudina also show putative drilling traces. Knowledge on Cambrian shell drillers is sorely lacking and there is little evidence or consensus concerning the taxonomic groups that made the holes, which often leads to the suggestion of an unknown ‘soft bodied driller’. Useful methodologies for deciphering the identities and capabilities of shell drillers are outlined. Evidence for puncture holes in Cambrian shelly taxa is rare. Such holes are more jagged than drill holes and possibly made by a Cambrian ‘puncher’. The Cambrian arthropod Yohoia may have used its frontal appendages in a jack-knifing manner, similar to Recent stomatopod crustaceans, to strike and puncture shells rapidly. Finally, Cambrian durophagous and shell-drilling predation is considered in the context of escalation – an evolutionary process that, amongst other scenarios, involves predators (and other ‘enemies’) as the predominant agents of natural selection. The rapid increase in diversity and abundance of biomineralised shells during the early Cambrian is often attributed to escalation: enemies placed selective pressure on prey, forcing phenotypic responses in prey and, by extension, in predator groups over time. Unfortunately, few case studies illustrate long-term patterns in shelly fossil morphologies that may reflect the influence of predation throughout the Cambrian. More studies on phenotypic change in hard-shelled lineages are needed to convincingly illustrate escalation and the responses of prey during the Cambrian.

  • Biological hierarchies and the nature of extinction
    Biol. Rev. (IF 11.615) Pub Date : 2017-09-24
    Curtis R. Congreve, Amanda R. Falk, James C. Lamsdell

    ABSTRACT Hierarchy theory recognises that ecological and evolutionary units occur in a nested and interconnected hierarchical system, with cascading effects occurring between hierarchical levels. Different biological disciplines have routinely come into conflict over the primacy of different forcing mechanisms behind evolutionary and ecological change. These disconnects arise partly from differences in perspective (with some researchers favouring ecological forcing mechanisms while others favour developmental/historical mechanisms), as well as differences in the temporal framework in which workers operate. In particular, long-term palaeontological data often show that large-scale (macro) patterns of evolution are predominantly dictated by shifts in the abiotic environment, while short-term (micro) modern biological studies stress the importance of biotic interactions. We propose that thinking about ecological and evolutionary interactions in a hierarchical framework is a fruitful way to resolve these conflicts. Hierarchy theory suggests that changes occurring at lower hierarchical levels can have unexpected, complex effects at higher scales due to emergent interactions between simple systems. In this way, patterns occurring on short- and long-term time scales are equally valid, as changes that are driven from lower levels will manifest in different forms at higher levels. We propose that the dual hierarchy framework fits well with our current understanding of evolutionary and ecological theory. Furthermore, we describe how this framework can be used to understand major extinction events better. Multi-generational attritional loss of reproductive fitness (MALF) has recently been proposed as the primary mechanism behind extinction events, whereby extinction is explainable solely through processes that result in extirpation of populations through a shutdown of reproduction. While not necessarily explicit, the push to explain extinction through solely population-level dynamics could be used to suggest that environmentally mediated patterns of extinction or slowed speciation across geological time are largely artefacts of poor preservation or a coarse temporal scale. We demonstrate how MALF fits into a hierarchical framework, showing that MALF can be a primary forcing mechanism at lower scales that still results in differential survivorship patterns at the species and clade level which vary depending upon the initial environmental forcing mechanism. Thus, even if MALF is the primary mechanism of extinction across all mass extinction events, the primary environmental cause of these events will still affect the system and result in differential responses. Therefore, patterns at both temporal scales are relevant.

  • Comparing species interaction networks along environmental gradients
    Biol. Rev. (IF 11.615) Pub Date : 2017-09-22
    Loïc Pellissier, Camille Albouy, Jordi Bascompte, Nina Farwig, Catherine Graham, Michel Loreau, Maria Alejandra Maglianesi, Carlos J. Melián, Camille Pitteloud, Tomas Roslin, Rudolf Rohr, Serguei Saavedra, Wilfried Thuiller, Guy Woodward, Niklaus E. Zimmermann, Dominique Gravel

    ABSTRACT Knowledge of species composition and their interactions, in the form of interaction networks, is required to understand processes shaping their distribution over time and space. As such, comparing ecological networks along environmental gradients represents a promising new research avenue to understand the organization of life. Variation in the position and intensity of links within networks along environmental gradients may be driven by turnover in species composition, by variation in species abundances and by abiotic influences on species interactions. While investigating changes in species composition has a long tradition, so far only a limited number of studies have examined changes in species interactions between networks, often with differing approaches. Here, we review studies investigating variation in network structures along environmental gradients, highlighting how methodological decisions about standardization can influence their conclusions. Due to their complexity, variation among ecological networks is frequently studied using properties that summarize the distribution or topology of interactions such as number of links, connectance, or modularity. These properties can either be compared directly or using a procedure of standardization. While measures of network structure can be directly related to changes along environmental gradients, standardization is frequently used to facilitate interpretation of variation in network properties by controlling for some co-variables, or via null models. Null models allow comparing the deviation of empirical networks from random expectations and are expected to provide a more mechanistic understanding of the factors shaping ecological networks when they are coupled with functional traits. As an illustration, we compare approaches to quantify the role of trait matching in driving the structure of plant–hummingbird mutualistic networks, i.e. a direct comparison, standardized by null models and hypothesis-based metaweb. Overall, our analysis warns against a comparison of studies that rely on distinct forms of standardization, as they are likely to highlight different signals. Fostering a better understanding of the analytical tools available and the signal they detect will help produce deeper insights into how and why ecological networks vary along environmental gradients.

  • ATAD3 proteins: brokers of a mitochondria–endoplasmic reticulum connection in mammalian cells
    Biol. Rev. (IF 11.615) Pub Date : 2017-09-20
    Jacques Baudier

    ABSTRACT In yeast, a sequence of physical and genetic interactions termed the endoplasmic reticulum (ER)–mitochondria organizing network (ERMIONE) controls mitochondria–ER interactions and mitochondrial biogenesis. Several functions that characterize ERMIONE complexes are conserved in mammalian cells, suggesting that a similar tethering complex must exist in metazoans. Recent studies have identified a new family of nuclear-encoded ATPases associated with diverse cellular activities (AAA+-ATPase) mitochondrial membrane proteins specific to multicellular eukaryotes, called the ATPase family AAA domain-containing protein 3 (ATAD3) proteins (ATAD3A and ATAD3B). These proteins are crucial for normal mitochondrial–ER interactions and lie at the heart of processes underlying mitochondrial biogenesis. ATAD3A orthologues have been studied in flies, worms, and mammals, highlighting the widespread importance of this gene during embryonic development and in adulthood. ATAD3A is a downstream effector of target of rapamycin (TOR) signalling in Drosophila and exhibits typical features of proteins from the ERMIONE-like complex in metazoans. In humans, mutations in the ATAD3A gene represent a new link between altered mitochondrial–ER interaction and recognizable neurological syndromes. The primate-specific ATAD3B protein is a biomarker of pluripotent embryonic stem cells. Through negative regulation of ATAD3A function, ATAD3B supports mitochondrial stemness properties.

  • The evolution of gonad expenditure and gonadosomatic index (GSI) in male and female broadcast-spawning invertebrates
    Biol. Rev. (IF 11.615) Pub Date : 2017-09-18
    Geoff A. Parker, Steven A. Ramm, Jussi Lehtonen, Jonathan M. Henshaw

    ABSTRACT Sedentary broadcast-spawning marine invertebrates, which release both eggs and sperm into the water for fertilization, are of special interest for sexual selection studies. They provide unique insight into the early stages of the evolutionary succession leading to the often-intense operation of both pre- and post-mating sexual selection in mobile gonochorists. Since they are sessile or only weakly mobile, adults can interact only to a limited extent with other adults and with their own fertilized offspring. They are consequently subject mainly to selection on gamete production and gamete success, and so high gonad expenditure is expected in both sexes. We review literature on gonadosomatic index (GSI; the proportion of body tissue devoted to gamete production) of gonochoristic broadcast spawners, which we use as a proxy for gonad expenditure. We show that such taxa most often have a high GSI that is approximately equal in both sexes. When GSI is asymmetric, female GSI usually exceeds male GSI, at least in echinoderms (the majority of species recorded). Intriguingly, though, higher male GSI also occurs in some species and appears more common than female-biased GSI in certain orders of gastropod molluscs. Our limited data also suggest that higher male GSI may be the prevalent pattern in sperm casters (where only males release gametes). We explore how selection might have shaped these patterns using game theoretic models for gonad expenditure that consider possible trade-offs with (i) somatic maintenance or (ii) growth, while also considering sperm competition, sperm limitation, and polyspermy. Our models of the trade-off between somatic tissue (which increases survival) and gonad (which increases reproductive success) predict that GSI should be equal for the two sexes when sperm competition is intense, as is probably common in broadcast spawners due to synchronous spawning in aggregations. Higher female GSI occurs under low sperm competition. Sperm limitation appears unlikely to alter these conclusions qualitatively, but can also act as a force to keep male GSI high, and close to that of females. Polyspermy can act to reduce male GSI. Higher male than female GSI is predicted to be less common (as observed in the data), but can occur when ova/ovaries are sufficiently more resource-intensive to produce than sperm/testes, for which some evidence exists. We also show that sex-specific trade-offs between gonads and growth can generate different life-history strategies for males and females, with males beginning reproduction earlier. This could lead to apparently higher male GSI in empirical studies if immature females are included in calculations of mean GSI. The existence of higher male GSI nonetheless remains somewhat problematic and requires further investigation. When sperm limitation is low, we suggest that the natural logarithm of the male/female GSI ratio may be a suitable index for sperm competition level in broadcast spawners, and that this may also be considered as an index for internally fertilizing taxa.

  • New-age ideas about age-old sex: separating meiosis from mating could solve a century-old conundrum
    Biol. Rev. (IF 11.615) Pub Date : 2017-09-14
    Michael Brandeis

    ABSTRACT Ever since Darwin first addressed it, sexual reproduction reigns as the ‘queen’ of evolutionary questions. Multiple theories tried to explain how this apparently costly and cumbersome method has become the universal mode of eukaryote reproduction. Most theories stress the adaptive advantages of sex by generating variation, they fail however to explain the ubiquitous persistence of sexual reproduction also where adaptation is not an issue. I argue that the obstacle for comprehending the role of sex stems from the conceptual entanglement of two distinct processes – gamete production by meiosis and gamete fusion by mating (mixis). Meiosis is an ancient, highly rigid and evolutionary conserved process identical and ubiquitous in all eukaryotes. Mating, by contrast, shows tremendous evolutionary variability even in closely related clades and exhibits wonderful ecological adaptability. To appreciate the respective roles of these two processes, which are normally linked and alternating, we require cases where one takes place without the other. Such cases are rather common. The heteromorphic sex chromosomes Y and W, that do not undergo meiotic recombination are an evolutionary test case for demonstrating the role of meiosis. Substantial recent genomic evidence highlights the accelerated rates of change and attrition these chromosomes undergo in comparison to those of recombining autosomes. I thus propose that the most basic role of meiosis is conserving integrity of the genome. A reciprocal case of meiosis without bi-parental mating, is presented by self-fertilization, which is fairly common in flowering plants, as well as most types of apomixis. I argue that deconstructing sex into these two distinct processes – meiosis and mating – will greatly facilitate their analysis and promote our understanding of sexual reproduction.

  • Causes and consequences of variation in offspring body mass: meta-analyses in birds and mammals
    Biol. Rev. (IF 11.615) Pub Date : 2017-04-09
    Victor Ronget, Jean-Michel Gaillard, Tim Coulson, Michael Garratt, François Gueyffier, Jean-Christophe Lega, Jean-François Lemaître

    ABSTRACT Early survival is highly variable and strongly influences observed population growth rates in most vertebrate populations. One of the major potential drivers of survival variation among juveniles is body mass. Heavy juveniles are better fed and have greater body reserves, and are thus assumed to survive better than light individuals. In spite of this, some studies have failed to detect an influence of body mass on offspring survival, questioning whether offspring body mass does indeed consistently influence juvenile survival, or whether this occurs in particular species/environments. Furthermore, the causes for variation in offspring mass are poorly understood, although maternal mass has often been reported to play a crucial role. To understand why offspring differ in body mass, and how this influences juvenile survival, we performed phylogenetically corrected meta-analyses of both the relationship between offspring body mass and offspring survival in birds and mammals and the relationship between maternal mass and offspring mass in mammals. We found strong support for an overall positive effect of offspring body mass on survival, with a more pronounced influence in mammals than in birds. An increase of one standard deviation of body mass increased the odds of offspring survival by 71% in mammals and by 44% in birds. A cost of being too fat in birds in terms of flight performance might explain why body mass is a less reliable predictor of offspring survival in birds. We then looked for moderators explaining the among-study differences reported in the intensity of this relationship. Surprisingly, sex did not influence the intensity of the offspring mass–survival relationship and phylogeny only accounted for a small proportion of observed variation in the intensity of that relationship. Among the potential factors that might affect the relationship between mass and survival in juveniles, only environmental conditions was influential in mammals. Offspring survival was most strongly influenced by body mass in captive populations and wild populations in the absence of predation. We also found support for the expected positive effect of maternal mass on offspring mass in mammals (rpearson = 0.387). As body mass is a strong predictor of early survival, we expected heavier mothers to allocate more to their offspring, leading them to be heavier and so to have a higher survival. However, none of the potential factors we tested for variation in the maternal mass–offspring mass relationship had a detectable influence. Further studies should focus on linking these two relationships to determine whether a strong effect of offspring size on early survival is associated with a high correlation coefficient between maternal mass and offspring mass.

  • Superorganismality and caste differentiation as points of no return: how the major evolutionary transitions were lost in translation
    Biol. Rev. (IF 11.615) Pub Date : 2017-05-15
    Jacobus J. Boomsma, Richard Gawne

    ABSTRACT More than a century ago, William Morton Wheeler proposed that social insect colonies can be regarded as superorganisms when they have morphologically differentiated reproductive and nursing castes that are analogous to the metazoan germ-line and soma. Following the rise of sociobiology in the 1970s, Wheeler's insights were largely neglected, and we were left with multiple new superorganism concepts that are mutually inconsistent and uninformative on how superorganismality originated. These difficulties can be traced to the broadened sociobiological concept of eusociality, which denies that physical queen–worker caste differentiation is a universal hallmark of superorganismal colonies. Unlike early evolutionary naturalists and geneticists such as Weismann, Huxley, Fisher and Haldane, who set out to explain the acquisition of an unmated worker caste, the goal of sociobiology was to understand the evolution of eusociality, a broad-brush convenience category that covers most forms of cooperative breeding. By lumping a diverse spectrum of social systems into a single category, and drawing attention away from the evolution of distinct quantifiable traits, the sociobiological tradition has impeded straightforward connections between inclusive fitness theory and the major evolutionary transitions paradigm for understanding irreversible shifts to higher organizational complexity. We evaluate the history by which these inconsistencies accumulated, develop a common-cause approach for understanding the origins of all major transitions in eukaryote hierarchical complexity, and use Hamilton's rule to argue that they are directly comparable. We show that only Wheeler's original definition of superorganismality can be unambiguously linked to irreversible evolutionary transitions from context-dependent reproductive altruism to unconditional differentiation of permanently unmated castes in the ants, corbiculate bees, vespine wasps and higher termites. We argue that strictly monogamous parents were a necessary, albeit not sufficient condition for all transitions to superorganismality, analogous to single-zygote bottlenecking being a necessary but not sufficient condition for the convergent origins of complex soma across multicellular eukaryotes. We infer that conflict reduction was not a necessary condition for the origin of any of these major transitions, and conclude that controversies over the status of inclusive fitness theory primarily emanate from the arbitrarily defined sociobiological concepts of superorganismality and eusociality, not from the theory itself.

  • A suite of essential biodiversity variables for detecting critical biodiversity change
    Biol. Rev. (IF 11.615) Pub Date : 2017-04-26
    Dirk S. Schmeller, Lauren V. Weatherdon, Adeline Loyau, Alberte Bondeau, Lluis Brotons, Neil Brummitt, Ilse R. Geijzendorffer, Peter Haase, Mathias Kuemmerlen, Corinne S. Martin, Jean-Baptiste Mihoub, Duccio Rocchini, Hannu Saarenmaa, Stefan Stoll, Eugenie C. Regan

    ABSTRACT Key global indicators of biodiversity decline, such as the IUCN Red List Index and the Living Planet Index, have relatively long assessment intervals. This means they, due to their inherent structure, function as late-warning indicators that are retrospective, rather than prospective. These indicators are unquestionably important in providing information for biodiversity conservation, but the detection of early-warning signs of critical biodiversity change is also needed so that proactive management responses can be enacted promptly where required. Generally, biodiversity conservation has dealt poorly with the scattered distribution of necessary detailed information, and needs to find a solution to assemble, harmonize and standardize the data. The prospect of monitoring essential biodiversity variables (EBVs) has been suggested in response to this challenge. The concept has generated much attention, but the EBVs themselves are still in development due to the complexity of the task, the limited resources available, and a lack of long-term commitment to maintain EBV data sets. As a first step, the scientific community and the policy sphere should agree on a set of priority candidate EBVs to be developed within the coming years to advance both large-scale ecological research as well as global and regional biodiversity conservation. Critical ecological transitions are of high importance from both a scientific as well as from a conservation policy point of view, as they can lead to long-lasting biodiversity change with a high potential for deleterious effects on whole ecosystems and therefore also on human well-being. We evaluated candidate EBVs using six criteria: relevance, sensitivity to change, generalizability, scalability, feasibility, and data availability and provide a literature-based review for eight EBVs with high sensitivity to change. The proposed suite of EBVs comprises abundance, allelic diversity, body mass index, ecosystem heterogeneity, phenology, range dynamics, size at first reproduction, and survival rates. The eight candidate EBVs provide for the early detection of critical and potentially long-lasting biodiversity change and should be operationalized as a priority. Only with such an approach can science predict the future status of global biodiversity with high certainty and set up the appropriate conservation measures early and efficiently. Importantly, the selected EBVs would address a large range of conservation issues and contribute to a total of 15 of the 20 Aichi targets and are, hence, of high biological relevance.

  • Developmental temperatures and phenotypic plasticity in reptiles: a systematic review and meta-analysis
    Biol. Rev. (IF 11.615) Pub Date : 2017-05-02
    Daniel W. A. Noble, Vaughn Stenhouse, Lisa E. Schwanz

    ABSTRACT Early environments can profoundly influence an organism in ways that persist over its life. In reptiles, early thermal environments (nest temperatures) can impact offspring phenotype and survival in important ways, yet we still lack an understanding of whether general trends exist and the magnitude of impact. Understanding these patterns is important in predicting how climate change will affect reptile populations and the role of phenotypic plasticity in buffering populations. We compiled data from 175 reptile studies to examine, and quantify, the effect of incubation temperature on phenotype and survival. Using meta-analytic approaches (standardized mean difference between incubation treatments, Hedges' g), we show that across all trait types examined there is, on average, a moderate to large magnitude of effect of incubation temperatures (absolute effect: |g| = 0.75). Unsurprisingly, this influence was extremely large for incubation duration, as predicted, with warmer temperatures decreasing incubation time overall (g = −8.42). Other trait types, including behaviour, physiology, morphology, performance, and survival experienced reduced, but still mostly moderate to large effects, with particularly strong effects on survival. Moreover, the impact of incubation temperature persisted at least one-year post-hatching, suggesting that these effects have the potential to impact fitness in the long term. The magnitude of effect increased as the change in temperature increased (e.g. 6°C versus 2°C) in almost all cases, and tended to decrease when temperatures of the treatments fluctuated around a mean temperature compared to when they were constant. The effect also depended on the mid-temperature of the comparison, but not in consistent ways, with some traits experiencing the greatest effects at extreme temperatures, while others did not. The highly heterogeneous nature of the effects we observe, along with a large amount of unexplained variability, indicates that the shape of reaction norms between phenotype and temperature, along with ecological and/or experimental factors, are important when considering general patterns. Our analyses provide new insights into the effects of incubation environments on reptile phenotype and survival and allow general, albeit coarse, predictions for taxa experiencing warming nest temperatures under climatic change.

  • Biologically meaningful scents: a framework for understanding predator–prey research across disciplines
    Biol. Rev. (IF 11.615) Pub Date : 2017-04-26
    Michael H. Parsons, Raimund Apfelbach, Peter B. Banks, Elissa Z. Cameron, Chris R. Dickman, Anke S. K. Frank, Menna E. Jones, Ian S. McGregor, Stuart McLean, Dietland Müller-Schwarze, Elisa E. Sparrow, Daniel T. Blumstein

    ABSTRACT Fear of predation is a universal motivator. Because predators hunt using stealth and surprise, there is a widespread ability among prey to assess risk from chemical information – scents – in their environment. Consequently, scents often act as particularly strong modulators of memory and emotions. Recent advances in ecological research and analytical technology are leading to novel ways to use this chemical information to create effective attractants, repellents and anti-anxiolytic compounds for wildlife managers, conservation biologists and health practitioners. However, there is extensive variation in the design, results, and interpretation of studies of olfactory-based risk discrimination. To understand the highly variable literature in this area, we adopt a multi-disciplinary approach and synthesize the latest findings from neurobiology, chemical ecology, and ethology to propose a contemporary framework that accounts for such disparate factors as the time-limited stability of chemicals, highly canalized mechanisms that influence prey responses, and the context within which these scents are detected (e.g. availability of alternative resources, perceived shelter, and ambient physical parameters). This framework helps to account for the wide range of reported responses by prey to predator scents, and explains, paradoxically, how the same individual predator scent can be interpreted as either safe or dangerous to a prey animal depending on how, when and where the cue was deposited. We provide a hypothetical example to illustrate the most common factors that influence how a predator scent (from dingoes, Canis dingo) may both attract and repel the same target organism (kangaroos, Macropus spp.). This framework identifies the catalysts that enable dynamic scents, odours or odorants to be used as attractants as well as deterrents. Because effective scent tools often relate to traumatic memories (fear and/or anxiety) that cause future avoidance, this information may also guide the development of appeasement, enrichment and anti-anxiolytic compounds, and help explain the observed variation in post-traumatic-related behaviours (including post-traumatic stress disorder, PTSD) among diverse terrestrial taxa, including humans.

  • Impacts of taxonomic inertia for the conservation of African ungulate diversity: an overview
    Biol. Rev. (IF 11.615) Pub Date : 2017-04-21
    Spartaco Gippoliti, Fenton P. D. Cotterill, Dietmar Zinner, Colin P. Groves

    ABSTRACT We review the state of African ungulate taxonomy over the last 120 years, with an emphasis on the introduction of the polytypic species concept and the discipline's general neglect since the middle of the 20th century. We single out negative consequences of ‘orthodox’ taxonomy, highlighting numerous cases of neglect of threatened lineages, unsound translocations that led to lineage introgression, and cases of maladaptation to local conditions including parasitic infections. Additionally, several captive breeding programmes have been hampered by chromosome rearrangements caused by involuntary lineage mixing. We advocate that specimen-based taxonomy should regain its keystone role in mammal research and conservation biology, with its scientific values augmented with genomic evidence. While integration with molecular biology, ecology and behaviour is needed for a full understanding of ungulate alpha diversity, we stress that morphological diversity has been neglected despite its tremendous practical importance for some groups of ‘utilizers’ such as trophy hunters, wildlife tourists and conservationists. We conclude that there is no evidence that purported ‘taxonomic inflation’ has adverse effects on ungulate conservation: rather, it is taxonomic inertia that has such adverse effects. We stress that sound science, founded on robust taxonomy, should underpin effective sustainable management (hunting, ranching, captive breeding and reintroduction programmes) of this unique African natural resource.

  • Phylogenetic perspectives on reef fish functional traits
    Biol. Rev. (IF 11.615) Pub Date : 2017-05-02
    Sergio R. Floeter, Mariana G. Bender, Alexandre C. Siqueira, Peter F. Cowman

    ABSTRACT Functional traits have been fundamental to the evolution and diversification of entire fish lineages on coral reefs. Yet their relationship with the processes promoting speciation, extinction and the filtering of local species pools remains unclear. We review the current literature exploring the evolution of diet, body size, water column use and geographic range size in reef-associated fishes. Using published and new data, we mapped functional traits on to published phylogenetic trees to uncover evolutionary patterns that have led to the current functional diversity of fishes on coral reefs. When examining reconstructed patterns for diet and feeding mode, we found examples of independent transitions to planktivory across different reef fish families. Such transitions and associated morphological alterations may represent cases in which ecological opportunity for the exploitation of different resources drives speciation and adaptation. In terms of body size, reconstructions showed that both large and small sizes appear multiple times within clades of mid-sized fishes and that extreme body sizes have arisen mostly in the last 10 million years (Myr). The reconstruction of range size revealed many cases of disparate range sizes among sister species. Such range size disparity highlights potential vicariant processes through isolation in peripheral locations. When accounting for peripheral speciation processes in sister pairs, we found a significant relationship between labrid range size and lineage age. The diversity and evolution of traits within lineages is influenced by trait–environment interactions as well as by species and trait–trait interactions, where the presence of a given trait may trigger the development of related traits or behaviours. Our effort to assess the evolution of functional diversity across reef fish clades adds to the burgeoning research focusing on the evolutionary and ecological roles of functional traits. We argue that the combination of a phylogenetic and a functional approach will improve the understanding of the mechanisms of species assembly in extraordinarily rich coral reef communities.

  • The interplay between autophagy and tumorigenesis: exploiting autophagy as a means of anticancer therapy
    Biol. Rev. (IF 11.615) Pub Date : 2017-05-02
    Juan Lorente, Carolina Velandia, Jose A. Leal, Yoelsis Garcia-Mayea, Alex Lyakhovich, Hiroshi Kondoh, Matilde E. LLeonart

    ABSTRACT In wild-type cells, autophagy represents a tumour-suppressor mechanism, and dysfunction of the autophagy machinery increases genomic instability, DNA damage, oxidative stress and stem/progenitor expansion, which are events associated with cancer onset. Autophagy occurs at a basal level in all cells depending on cell type and cellular microenvironment. However, the role of autophagy in cancer is diverse and can promote different outcomes even in a single tumour. For example, in hypoxic tumour regions, autophagy emerges as a protective mechanism and allows cancer cell survival. By contrast, in cancer cells surrounding the tumour mass, the induction of autophagy by radio- or chemotherapy promotes cell death and significantly reduces the tumour mass. Importantly, inhibition of autophagy compromises tumorigenesis by mechanisms that are not entirely understood. The aim of this review is to explain the apparently contradictory role of autophagy as a mechanism that both promotes and inhibits tumorigenesis using different models. The induction/inhibition of autophagy as a mechanism for cancer treatment is also discussed.

  • The long-term persistence of phytoplankton resting stages in aquatic ‘seed banks’
    Biol. Rev. (IF 11.615) Pub Date : 2017-05-05
    Marianne Ellegaard, Sofia Ribeiro

    ABSTRACT In the past decade, research on long-term persistence of phytoplankton resting stages has intensified. Simultaneously, insight into life-cycle variability in the diverse groups of phytoplankton has also increased. Aquatic ‘seed banks’ have tremendous significance and show many interesting parallels to terrestrial seed beds of vascular plants, but are much less studied. It is therefore timely to review the phenomenon of long-term persistence of aquatic resting stages in sediment seed banks. Herein we compare function, morphology and physiology of phytoplankton resting stages to factors central for persistence of terrestrial seeds. We review the types of resting stages found in different groups of phytoplankton and focus on the groups for which long-term (multi-decadal) persistence has been shown: dinoflagellates, diatoms, green algae and cyanobacteria. We discuss the metabolism of long-term dormancy in phytoplankton resting stages and the ecological, evolutionary and management implications of this important trait. Phytoplankton resting stages exhibiting long-term viability are characterized by thick, often multi-layered walls and accumulation vesicles containing starch, lipids or other materials such as pigments, cyanophycin or unidentified granular materials. They are reported to play central roles in evolutionary resilience and survival of catastrophic events. Promising areas for future research include the role of hormones in mediating dormancy, elucidating the mechanisms behind metabolic shut-down and testing bet-hedging hypotheses.

  • Beyond chemoreception: diverse tasks of soluble olfactory proteins in insects
    Biol. Rev. (IF 11.615) Pub Date : 2017-05-07
    Paolo Pelosi, Immacolata Iovinella, Jiao Zhu, Guirong Wang, Francesca R. Dani

    ABSTRACT Odorant-binding proteins (OBPs) and chemosensory proteins (CSPs) are regarded as carriers of pheromones and odorants in insect chemoreception. These proteins are typically located in antennae, mouth organs and other chemosensory structures; however, members of both classes of proteins have been detected recently in other parts of the body and various functions have been proposed. The best studied of these non-sensory tasks is performed in pheromone glands, where OBPs and CSPs solubilise hydrophobic semiochemicals and assist their controlled release into the environment. In some cases the same proteins are expressed in antennae and pheromone glands, thus performing a dual role in receiving and broadcasting the same chemical message. Several reports have described OBPs and CSPs in reproductive organs. Some of these proteins are male specific and are transferred to females during mating. They likely carry semiochemicals with different proposed roles, from inhibiting other males from approaching mated females, to marking fertilized eggs, but further experimental evidence is still needed. Before being discovered in insects, the presence of binding proteins in pheromone glands and reproductive organs was widely reported in mammals, where vertebrate OBPs, structurally different from OBPs of insects and belonging to the lipocalin superfamily, are abundant in rodent urine, pig saliva and vaginal discharge of the hamster, as well as in the seminal fluid of rabbits. In at least four cases CSPs have been reported to promote development and regeneration: in embryo maturation in the honeybee, limb regeneration in the cockroach, ecdysis in larvae of fire ants and in promoting phase shift in locusts. Both OBPs and CSPs are also important in nutrition as solubilisers of lipids and other essential components of the diet. Particularly interesting is the affinity for carotenoids of CSPs abundantly secreted in the proboscis of moths and butterflies and the occurrence of the same (or very similar CSPs) in the eyes of the same insects. A role as a carrier of visual pigments for these proteins in insects parallels that of retinol-binding protein in vertebrates, a lipocalin structurally related to OBPs of vertebrates. Other functions of OBPs and CSPs include anti-inflammatory action in haematophagous insects, resistance to insecticides and eggshell formation. Such multiplicity of roles and the high success of both classes of proteins in being adapted to different situations is likely related to their stable scaffolding determining excellent stability to temperature, proteolysis and denaturing agents. The wide versatility of both OBPs and CSPs in nature has suggested several different uses for these proteins in biotechnological applications, from biosensors for odours to scavengers for pollutants and controlled releasers of chemicals in the environment.

  • Did some red alga-derived plastids evolve via kleptoplastidy? A hypothesis
    Biol. Rev. (IF 11.615) Pub Date : 2017-05-23
    Andrzej Bodył

    ABSTRACT The evolution of plastids has a complex and still unresolved history. These organelles originated from a cyanobacterium via primary endosymbiosis, resulting in three eukaryotic lineages: glaucophytes, red algae, and green plants. The red and green algal plastids then spread via eukaryote–eukaryote endosymbioses, known as secondary and tertiary symbioses, to numerous heterotrophic protist lineages. The number of these horizontal plastid transfers, especially in the case of red alga-derived plastids, remains controversial. Some authors argue that the number of plastid origins should be minimal due to perceived difficulties in the transformation of a eukaryotic algal endosymbiont into a multimembrane plastid, but increasingly the available data contradict this argument. I suggest that obstacles in solving this dilemma result from the acceptance of a single evolutionary scenario for the endosymbiont-to-plastid transformation formulated by Cavalier-Smith & Lee (1985). Herein I discuss data that challenge this evolutionary scenario. Moreover, I propose a new model for the origin of multimembrane plastids belonging to the red lineage and apply it to the dinoflagellate peridinin plastid. The new model has several general and practical implications, such as the requirement for a new definition of cell organelles and in the construction of chimeric organisms.

  • An Amazonian rainforest and its fragments as a laboratory of global change
    Biol. Rev. (IF 11.615) Pub Date : 2017-05-30
    William F. Laurance, José L. C. Camargo, Philip M. Fearnside, Thomas E. Lovejoy, G. Bruce Williamson, Rita C. G. Mesquita, Christoph F. J. Meyer, Paulo E. D. Bobrowiec, Susan G. W. Laurance

    ABSTRACT We synthesize findings from one of the world's largest and longest-running experimental investigations, the Biological Dynamics of Forest Fragments Project (BDFFP). Spanning an area of ∼1000 km2 in central Amazonia, the BDFFP was initially designed to evaluate the effects of fragment area on rainforest biodiversity and ecological processes. However, over its 38-year history to date the project has far transcended its original mission, and now focuses more broadly on landscape dynamics, forest regeneration, regional- and global-change phenomena, and their potential interactions and implications for Amazonian forest conservation. The project has yielded a wealth of insights into the ecological and environmental changes in fragmented forests. For instance, many rainforest species are naturally rare and hence are either missing entirely from many fragments or so sparsely represented as to have little chance of long-term survival. Additionally, edge effects are a prominent driver of fragment dynamics, strongly affecting forest microclimate, tree mortality, carbon storage and a diversity of fauna. Even within our controlled study area, the landscape has been highly dynamic: for example, the matrix of vegetation surrounding fragments has changed markedly over time, succeeding from large cattle pastures or forest clearcuts to secondary regrowth forest. This, in turn, has influenced the dynamics of plant and animal communities and their trajectories of change over time. In general, fauna and flora have responded differently to fragmentation: the most locally extinction-prone animal species are those that have both large area requirements and low tolerance of the modified habitats surrounding fragments, whereas the most vulnerable plants are those that respond poorly to edge effects or chronic forest disturbances, and that rely on vulnerable animals for seed dispersal or pollination. Relative to intact forests, most fragments are hyperdynamic, with unstable or fluctuating populations of species in response to a variety of external vicissitudes. Rare weather events such as droughts, windstorms and floods have had strong impacts on fragments and left lasting legacies of change. Both forest fragments and the intact forests in our study area appear to be influenced by larger-scale environmental drivers operating at regional or global scales. These drivers are apparently increasing forest productivity and have led to concerted, widespread increases in forest dynamics and plant growth, shifts in tree-community composition, and increases in liana (woody vine) abundance. Such large-scale drivers are likely to interact synergistically with habitat fragmentation, exacerbating its effects for some species and ecological phenomena. Hence, the impacts of fragmentation on Amazonian biodiversity and ecosystem processes appear to be a consequence not only of local site features but also of broader changes occurring at landscape, regional and even global scales.

  • The comparative study of empathy: sympathetic concern and empathic perspective-taking in non-human animals
    Biol. Rev. (IF 11.615) Pub Date : 2017-05-25
    Ana Pérez-Manrique, Antoni Gomila

    ABSTRACT While empathy is a century-old psychological concept, its study in non-human animals has become the focus of much recent scientific interest, as it promises to provide the clues to understand the evolutionary origins of our social and moral nature. A review of the comparative study of empathy is thus timely to complement and constrain anthropocentric views, and to integrate current findings. However, this is not an easy task. The study of animal empathy has developed using different paradigms, different concepts of the phenomena involved, and the absence of a systematic program. Herein, we carry out a comprehensive review of the literature on complex forms of empathy in non-human animals: sympathetic concern and empathic perspective-taking. In particular, we focus on consolation and targeted helping, as the best examples of each category. In so doing, we try to shed light on the current debate concerning whether these phenomena are exclusively human traits. First, we try to clarify the terminology and taxonomy of forms of empathy, providing operative criteria for these phenomena that are applicable to both human and non-human animals. Second, we discuss whether the available evidence qualifies such behaviour as empathic. Third, we aim to provide an integrative view of the field, clarifying the challenges and conditions to satisfy. We also hope to highlight the importance of the study of these processes for elucidating the evolutionary history of this capacity across the animal kingdom.

  • Cephalopod embryonic shells as a tool to reconstruct reproductive strategies in extinct taxa
    Biol. Rev. (IF 11.615) Pub Date : 2017-05-30
    Vladimir Laptikhovsky, Svetlana Nikolaeva, Mikhail Rogov

    ABSTRACT An exhaustive study of existing data on the relationship between egg size and maximum size of embryonic shells in 42 species of extant cephalopods demonstrated that these values are approximately equal regardless of taxonomy and shell morphology. Egg size is also approximately equal to mantle length of hatchlings in 45 cephalopod species with rudimentary shells. Paired data on the size of the initial chamber versus embryonic shell in 235 species of Ammonoidea, 46 Bactritida, 13 Nautilida, 22 Orthocerida, 8 Tarphycerida, 4 Oncocerida, 1 Belemnoidea, 4 Sepiida and 1 Spirulida demonstrated that, although there is a positive relationship between these parameters in some taxa, initial chamber size cannot be used to predict egg size in extinct cephalopods; the size of the embryonic shell may be more appropriate for this task. The evolution of reproductive strategies in cephalopods in the geological past was marked by an increasing significance of small-egged taxa, as is also seen in simultaneously evolving fish taxa.

  • Managing consequences of climate-driven species redistribution requires integration of ecology, conservation and social science
    Biol. Rev. (IF 11.615) Pub Date : 2017-06-01
    Timothy C. Bonebrake, Christopher J. Brown, Johann D. Bell, Julia L. Blanchard, Alienor Chauvenet, Curtis Champion, I-Ching Chen, Timothy D. Clark, Robert K. Colwell, Finn Danielsen, Anthony I. Dell, Jennifer M. Donelson, Birgitta Evengård, Simon Ferrier, Stewart Frusher, Raquel A. Garcia, Roger B. Griffis, Alistair J. Hobday, Marta A. Jarzyna, Emma Lee, Jonathan Lenoir, Hlif Linnetved, Victoria Y. Martin, Phillipa C. McCormack, Jan McDonald, Eve McDonald-Madden, Nicola Mitchell, Tero Mustonen, John M. Pandolfi, Nathalie Pettorelli, Hugh Possingham, Peter Pulsifer, Mark Reynolds, Brett R. Scheffers, Cascade J. B. Sorte, Jan M. Strugnell, Mao-Ning Tuanmu, Samantha Twiname, Adriana Vergés, Cecilia Villanueva, Erik Wapstra, Thomas Wernberg, Gretta T. Pecl

    ABSTRACT Climate change is driving a pervasive global redistribution of the planet's species. Species redistribution poses new questions for the study of ecosystems, conservation science and human societies that require a coordinated and integrated approach. Here we review recent progress, key gaps and strategic directions in this nascent research area, emphasising emerging themes in species redistribution biology, the importance of understanding underlying drivers and the need to anticipate novel outcomes of changes in species ranges. We highlight that species redistribution has manifest implications across multiple temporal and spatial scales and from genes to ecosystems. Understanding range shifts from ecological, physiological, genetic and biogeographical perspectives is essential for informing changing paradigms in conservation science and for designing conservation strategies that incorporate changing population connectivity and advance adaptation to climate change. Species redistributions present challenges for human well-being, environmental management and sustainable development. By synthesising recent approaches, theories and tools, our review establishes an interdisciplinary foundation for the development of future research on species redistribution. Specifically, we demonstrate how ecological, conservation and social research on species redistribution can best be achieved by working across disciplinary boundaries to develop and implement solutions to climate change challenges. Future studies should therefore integrate existing and complementary scientific frameworks while incorporating social science and human-centred approaches. Finally, we emphasise that the best science will not be useful unless more scientists engage with managers, policy makers and the public to develop responsible and socially acceptable options for the global challenges arising from species redistributions.

  • Managing biological control services through multi-trophic trait interactions: review and guidelines for implementation at local and landscape scales
    Biol. Rev. (IF 11.615) Pub Date : 2017-06-09
    David J. Perović, Sagrario Gámez-Virués, Douglas A. Landis, Felix Wäckers, Geoff M. Gurr, Stephen D. Wratten, Min-Sheng You, Nicolas Desneux

    ABSTRACT Ecological studies are increasingly moving towards trait-based approaches, as the evidence mounts that functions, as opposed to taxonomy, drive ecosystem service delivery. Among ecosystem services, biological control has been somewhat overlooked in functional ecological studies. This is surprising given that, over recent decades, much of biological control research has been focused on identifying the multiple characteristics (traits) of species that influence trophic interactions. These traits are especially well developed for interactions between arthropods and flowers – important for biological control, as floral resources can provide natural enemies with nutritional supplements, which can dramatically increase biological control efficiency. Traits that underpin the biological control potential of a community and that drive the response of arthropods to environmental filters, from local to landscape-level conditions, are also emerging from recent empirical studies. We present an overview of the traits that have been identified to (i) drive trophic interactions, especially between plants and biological control agents through determining access to floral resources and enhancing longevity and fecundity of natural enemies, (ii) affect the biological control services provided by arthropods, and (iii) limit the response of arthropods to environmental filters, ranging from local management practices to landscape-level simplification. We use this review as a platform to outline opportunities and guidelines for future trait-based studies focused on the enhancement of biological control services.

  • The mechanism of coupling between oxido-reduction and proton translocation in respiratory chain enzymes
    Biol. Rev. (IF 11.615) Pub Date : 2017-06-21
    Sergio Papa, Giuseppe Capitanio, Francesco Papa

    ABSTRACT The respiratory chain of mitochondria and bacteria is made up of a set of membrane-associated enzyme complexes which catalyse sequential, stepwise transfer of reducing equivalents from substrates to oxygen and convert redox energy into a transmembrane protonmotive force (PMF) by proton translocation from a negative (N) to a positive (P) aqueous phase separated by the coupling membrane. There are three basic mechanisms by which a membrane-associated redox enzyme can generate a PMF. These are membrane anisotropic arrangement of the primary redox catalysis with: (i) vectorial electron transfer by redox metal centres from the P to the N side of the membrane; (ii) hydrogen transfer by movement of quinones across the membrane, from a reduction site at the N side to an oxidation site at the P side; (iii) a different type of mechanism based on co-operative allosteric linkage between electron transfer at the metal redox centres and transmembrane electrogenic proton translocation by apoproteins. The results of advanced experimental and theoretical analyses and in particular X-ray crystallography show that these three mechanisms contribute differently to the protonmotive activity of cytochrome c oxidase, ubiquinone-cytochrome c oxidoreductase and NADH-ubiquinone oxidoreductase of the respiratory chain. This review considers the main features, recent experimental advances and still unresolved problems in the molecular/atomic mechanism of coupling between the transfer of reducing equivalents and proton translocation in these three protonmotive redox complexes.

  • Osteoblast migration in vertebrate bone
    Biol. Rev. (IF 11.615) Pub Date : 2017-06-19
    Antonia Thiel, Marie K. Reumann, Adele Boskey, Johannes Wischmann, Rüdiger von Eisenhart-Rothe, Philipp Mayer-Kuckuk

    ABSTRACT Bone formation, for example during bone remodelling or fracture repair, requires mature osteoblasts to deposit bone with remarkable spatial precision. As osteoblast precursors derive either from circulation or resident stem cell pools, they and their progeny are required to migrate within the three-dimensional bone space and to navigate to their destination, i.e. to the site of bone formation. An understanding of this process is emerging based on in vitro and in vivo studies of several vertebrate species. Receptors on the osteoblast surface mediate cell adhesion and polarization, which induces osteoblast migration. Osteoblast migration is then facilitated along gradients of chemoattractants. The latter are secreted or released proteolytically by several cell types interacting with osteoblasts, including osteoclasts and vascular endothelial cells. The positions of these cellular sources of chemoattractants in relation to the position of the osteoblasts provide the migrating osteoblasts with tracks to their destination, and osteoblasts possess the means to follow a track marked by multiple chemoattractant gradients. In addition to chemotactic cues, osteoblasts sense other classes of signals and utilize them as landmarks for navigation. The composition of the osseous surface guides adhesion and hence migration efficiency and can also provide steering through haptotaxis. Further, it is likely that signals received from surface interactions modulate chemotaxis. Besides the nature of the surface, mechanical signals such as fluid flow may also serve as navigation signals for osteoblasts. Alterations in osteoblast migration and navigation might play a role in metabolic bone diseases such as osteoporosis.

  • Pathways governing development of stem cell-derived pancreatic β cells: lessons from embryogenesis
    Biol. Rev. (IF 11.615) Pub Date : 2017-06-22
    Sara Al-Khawaga, Bushra Memon, Alexandra E. Butler, Shahrad Taheri, Abdul B. Abou-Samra, Essam M. Abdelalim

    ABSTRACT The loss of functional β cells leads to development of diabetes. Several studies have shown that β cells are specified through several stages of progenitors during pancreas development, each stage defined by the expression of specific transcription factors (TFs). Understanding signalling pathways that control the differentiation and specification processes during embryogenesis will facilitate efforts to obtain functional β cells in vitro. Our current knowledge of the mechanisms involved in pancreatic β cell development and survival under normal or diabetic conditions has come largely from animal studies. However, there are marked differences in islet structure and physiological properties between humans and animals, and not all phenotypes of human diabetes can be recapitulated in animal models. Therefore, human pluripotent stem cells (hPSCs), including human embryonic stem cells (hESCs) and human induced PSCs (hiPSCs) offer a great opportunity for increasing our understanding of the pathways regulating human pancreatic β-cell development and survival. Furthermore, hPSCs provide a renewable source of functional pancreatic β cells for cell replacement therapy as well as disease modelling. Herein, we discuss the signalling pathways involved in the development of pancreatic β cells during embryogenesis. Additionally, we describe how these pathways are manipulated in vitro to differentiate hPSCs into functional β cells. Finally, we highlight the progress that has been made for the applications of those cells in treating and modelling diabetes.

  • Disruptive physiology: olfaction and the microbiome–gut–brain axis
    Biol. Rev. (IF 11.615) Pub Date : 2017-07-04
    John Bienenstock, Wolfgang A. Kunze, Paul Forsythe

    ABSTRACT This review covers the field of olfaction and chemosensation of odorants and puts this information into the context of interactions between microbes and behaviour; the microbiome–gut–brain axis (MGBA). Recent emphasis has also been placed on the concept of the holobiome which states that no single aspect of an organism should be viewed separately and thus must include examination of their associated microbial populations and their influence. While it is known that the microbiome may be involved in the modulation of animal behaviour, there has been little systematized effort to incorporate into such studies the rapidly developing knowledge of the wide range of olfactory systems. The classical olfactory system is evolutionarily conserved in multiple taxa from insects through to fish, reptiles and mammals, and is represented by the largest gene families in vertebrates. Mice have over 1000 different olfactory receptors and humans about 400. They are distributed throughout the body and are even found in spermatozoa where they function in chemotaxis. Each olfactory receptor has the unique functional capability of high-affinity binding to several different molecular ligands. These and other properties render the cataloguing of odorants (odorome) with specific actions a difficult task. Some ectopic olfactory receptors have been shown to have functional effects in the gut and kidney, highlighting the complexity of the systems engaged by odorants. However, there are, in addition to classical olfactory receptors, at least two other families of receptors involved in olfaction that are also widely found expressed on tissues in many different organs in addition to the nervous system and brain: the trace-amine associated and formyl peptide receptors. Bacteria can make many if not most odorants and are responsible for recognition of species and relative relatedness, as well as predator presence, among many other examples. Activation of different combinations of olfactory receptors by bacterial products such as β-phenylethylamine have been shown even to control expression of emotions such as fear and aggression. The number of examples of bacterial products and volatile odorants influencing brain function and behaviour is expanding rapidly. Since it is recognized that many different bacterial products and metabolites also function as social cues, and may themselves be directly or indirectly causative of behavioural change, it becomes ever more important to include olfaction into studies of the MGBA. Clearly there are broader implications for the involvement of olfaction in this rapidly evolving field. These include improvement in our understanding of the pathways engaged in various behaviours, and the identification of novel approaches and new targets in efforts to modulate behavioural changes.

  • Comparative analyses of basal rate of metabolism in mammals: data selection does matter
    Biol. Rev. (IF 11.615) Pub Date : 2017-07-27
    Michel Genoud, Karin Isler, Robert D. Martin

    ABSTRACT Basal rate of metabolism (BMR) is a physiological parameter that should be measured under strictly defined experimental conditions. In comparative analyses among mammals BMR is widely used as an index of the intensity of the metabolic machinery or as a proxy for energy expenditure. Many databases with BMR values for mammals are available, but the criteria used to select metabolic data as BMR estimates have often varied and the potential effect of this variability has rarely been questioned. We provide a new, expanded BMR database reflecting compliance with standard criteria (resting, postabsorptive state; thermal neutrality; adult, non-reproductive status for females) and examine potential effects of differential selectivity on the results of comparative analyses. The database includes 1739 different entries for 817 species of mammals, compiled from the original sources. It provides information permitting assessment of the validity of each estimate and presents the value closest to a proper BMR for each entry. Using different selection criteria, several alternative data sets were extracted and used in comparative analyses of (i) the scaling of BMR to body mass and (ii) the relationship between brain mass and BMR. It was expected that results would be especially dependent on selection criteria with small sample sizes and with relatively weak relationships. Phylogenetically informed regression (phylogenetic generalized least squares, PGLS) was applied to the alternative data sets for several different clades (Mammalia, Eutheria, Metatheria, or individual orders). For Mammalia, a ‘subsampling procedure’ was also applied, in which random subsamples of different sample sizes were taken from each original data set and successively analysed. In each case, two data sets with identical sample size and species, but comprising BMR data with different degrees of reliability, were compared. Selection criteria had minor effects on scaling equations computed for large clades (Mammalia, Eutheria, Metatheria), although less-reliable estimates of BMR were generally about 12–20% larger than more-reliable ones. Larger effects were found with more-limited clades, such as sciuromorph rodents. For the relationship between BMR and brain mass the results of comparative analyses were found to depend strongly on the data set used, especially with more-limited, order-level clades. In fact, with small sample sizes (e.g. <100) results often appeared erratic. Subsampling revealed that sample size has a non-linear effect on the probability of a zero slope for a given relationship. Depending on the species included, results could differ dramatically, especially with small sample sizes. Overall, our findings indicate a need for due diligence when selecting BMR estimates and caution regarding results (even if seemingly significant) with small sample sizes.

  • Biodiversity as a solution to mitigate climate change impacts on the functioning of forest ecosystems
    Biol. Rev. (IF 11.615) Pub Date : 2017-07-10
    Masumi Hisano, Eric B. Searle, Han Y. H. Chen

    ABSTRACT Forest ecosystems are critical to mitigating greenhouse gas emissions through carbon sequestration. However, climate change has affected forest ecosystem functioning in both negative and positive ways, and has led to shifts in species/functional diversity and losses in plant species diversity which may impair the positive effects of diversity on ecosystem functioning. Biodiversity may mitigate climate change impacts on (I) biodiversity itself, as more-diverse systems could be more resilient to climate change impacts, and (II) ecosystem functioning through the positive relationship between diversity and ecosystem functioning. By surveying the literature, we examined how climate change has affected forest ecosystem functioning and plant diversity. Based on the biodiversity effects on ecosystem functioning (BEF), we specifically address the potential for biodiversity to mitigate climate change impacts on forest ecosystem functioning. For this purpose, we formulate a concept whereby biodiversity may reduce the negative impacts or enhance the positive impacts of climate change on ecosystem functioning. Further BEF studies on climate change in natural forests are encouraged to elucidate how biodiversity might influence ecosystem functioning. This may be achieved through the detailed scrutiny of large spatial/long temporal scale data sets, such as long-term forest inventories. Forest management strategies based on BEF have strong potential for augmenting the effectiveness of the roles of forests in the mitigation of climate change impacts on ecosystem functioning.

  • The concepts of asymmetric and symmetric power can help resolve the puzzle of altruistic and cooperative behaviour
    Biol. Rev. (IF 11.615) Pub Date : 2017-07-11
    Tim Phillips

    ABSTRACT Evolutionary theory predicts competition in nature yet altruistic and cooperative behaviour appears to reduce the ability to compete in order to help others compete better. This evolutionary puzzle is usually explained by kin selection where close relatives perform altruistic and cooperative acts to help each other and by reciprocity theory (i.e. direct, indirect and generalized reciprocity) among non-kin. Here, it is proposed that the concepts of asymmetry and symmetry in power and dominance are critical if we are ever to resolve the puzzle of altruism and cooperation towards non-kin. Asymmetry in power and dominance is likely to emerge under competition in nature as individuals strive to gain greater access to the scarce resources needed to survive and reproduce successfully. Yet asymmetric power presents serious problems for reciprocity theory in that a dominant individual faces a temptation to cheat in interactions with subordinates that is likely to far outweigh any individual selective benefits gained through reciprocal mechanisms. Furthermore, action taken by subordinates to deter non-reciprocation by dominants is likely to prove prohibitively costly to their fitness, making successful enforcement of reciprocal mechanisms unlikely. It is also argued here that many apparently puzzling forms of cooperation observed in nature (e.g. cooperative breeding in which unrelated subordinates help dominants to breed) might be best explained by asymmetry in power and dominance. Once it is recognized that individuals in these cooperative interactions are subject to the constraints and opportunities imposed on them by asymmetric power then they can be seen as pursuing a ‘least bad’ strategy to promote individual fitness – one that is nevertheless consistent with evolutionary theory. The concept of symmetric power also provides important insights. It can inhibit reciprocal mechanisms in the sense that symmetric power makes it easier for a cheat to appropriate common resources while incurring fewer penalties. Nevertheless under certain restrictive conditions, symmetric power is seen as likely to promote direct reciprocity through ‘tit for tat’.

  • Coupling factors and exosomal packaging microRNAs involved in the regulation of bone remodelling
    Biol. Rev. (IF 11.615) Pub Date : 2017-08-10
    Sipin Zhu, Felix Yao, Heng Qiu, Ge Zhang, Huazi Xu, Jiake Xu

    ABSTRACT Bone remodelling is a continuous process by which bone resorption by osteoclasts is followed by bone formation by osteoblasts to maintain skeletal homeostasis. These two forces must be tightly coordinated not only quantitatively, but also in time and space, and its malfunction leads to diseases such as osteoporosis. Recent research focusing on the cross-talk and coupling mechanisms associated with the sequential recruitment of osteoblasts to areas where osteoclasts have removed bone matrix have identified a number of osteogenic factors produced by the osteoclasts themselves. Osteoclast-derived factors and exosomal-containing microRNA (miRNA) can either enhance or inhibit osteoblast differentiation through paracrine and juxtacrine mechanisms, and therefore may have a central coupling role in bone formation. Entwined with angiocrine factors released by vessel-specific endothelial cells and perivascular cells or pericytes, these factors play a critical role in angiogenesis–osteogenesis coupling essential in bone remodelling.

  • Understanding processes at the origin of species flocks with a focus on the marine Antarctic fauna
    Biol. Rev. (IF 11.615) Pub Date : 2017-08-10
    Anne Chenuil, Thomas Saucède, Lenaïg G. Hemery, Marc Eléaume, Jean-Pierre Féral, Nadia Améziane, Bruno David, Guillaume Lecointre, Charlotte Havermans

    ABSTRACT Species flocks (SFs) fascinate evolutionary biologists who wonder whether such striking diversification can be driven by normal evolutionary processes. Multiple definitions of SFs have hindered the study of their origins. Previous studies identified a monophyletic taxon as a SF if it displays high speciosity in an area in which it is endemic (criterion 1), high ecological diversity among species (criterion 2), and if it dominates the habitat in terms of biomass (criterion 3); we used these criteria in our analyses. Our starting hypothesis is that normal evolutionary processes may provide a sufficient explanation for most SFs. We thus clearly separate each criterion and identify which biological (intrinsic) and environmental (extrinsic) traits are most favourable to their realization. The first part focuses on evolutionary processes. We highlight that some popular putative causes of SFs, such as key innovations or ecological speciation, are neither necessary nor sufficient to fulfill some or all of the three criteria. Initial differentiation mechanisms are diverse and difficult to identify a posteriori because a primary differentiation of one type (genetic, ecological or geographical) often promotes other types of differentiation. Furthermore, the criteria are not independent: positive feedbacks between speciosity and ecological diversity among species are expected whatever the initial cause of differentiation, and ecological diversity should enhance habitat dominance at the clade level. We then identify intrinsic and extrinsic factors that favour each criterion. Low dispersal emerges as a convincing driver of speciosity. Except for a genomic architecture favouring ecological speciation, for which assessment is difficult, high effective population sizes are the single intrinsic factor that directly enhances speciosity, ecological diversity and habitat dominance. No extrinsic factor appeared to enhance all criteria simultaneously but a combination of factors (insularity, fragmentation and environmental stability) may favour the three criteria, although the effect is indirect for habitat dominance. We then apply this analytical framework to Antarctic marine environments by analysing data from 18 speciose clades belonging to echinoderms (five unrelated clades), notothenioid fishes (five clades) and peracarid crustaceans (eight clades). Antarctic shelf environments and history appear favourable to endemicity and speciosity, but not to ecological specialization. Two main patterns are distinguished among taxa. (i) In echinoderms, many brooding, species-rich and endemic clades are reported, but without remarkable ecological diversity or habitat dominance. In these taxa, loss of the larval stage is probably a consequence of past Antarctic environmental factors, and brooding is suggested to be responsible for enhanced allopatric speciation (via dispersal limitation). (ii) In notothenioids and peracarids, many clades fulfill all three SF criteria. This could result from unusual features in fish and crustaceans: chromosome instability and key innovations (antifreeze proteins) in notothenioids, ecological opportunity in peracarids, and a genomic architecture favouring ecological speciation in both groups. Therefore, the data do not support our starting point that normal evolutionary factors or processes drive SFs because in these two groups uncommon intrinsic features or ecological opportunity provide the best explanation. The utility of the three-criterion SF concept is therefore questioned and guidelines are given for future studies.

  • An evolutionary perspective on the systems of adaptive immunity
    Biol. Rev. (IF 11.615) Pub Date : 2017-07-26
    Viktor Müller, Rob J. de Boer, Sebastian Bonhoeffer, Eörs Szathmáry

    ABSTRACT We propose an evolutionary perspective to classify and characterize the diverse systems of adaptive immunity that have been discovered across all major domains of life. We put forward a new function-based classification according to the way information is acquired by the immune systems: Darwinian immunity (currently known from, but not necessarily limited to, vertebrates) relies on the Darwinian process of clonal selection to ‘learn’ by cumulative trial-and-error feedback; Lamarckian immunity uses templated targeting (guided adaptation) to internalize heritable information on potential threats; finally, shotgun immunity operates through somatic mechanisms of variable targeting without feedback. We argue that the origin of Darwinian (but not Lamarckian or shotgun) immunity represents a radical innovation in the evolution of individuality and complexity, and propose to add it to the list of major evolutionary transitions. While transitions to higher-level units entail the suppression of selection at lower levels, Darwinian immunity re-opens cell-level selection within the multicellular organism, under the control of mechanisms that direct, rather than suppress, cell-level evolution for the benefit of the individual. From a conceptual point of view, the origin of Darwinian immunity can be regarded as the most radical transition in the history of life, in which evolution by natural selection has literally re-invented itself. Furthermore, the combination of clonal selection and somatic receptor diversity enabled a transition from limited to practically unlimited capacity to store information about the antigenic environment. The origin of Darwinian immunity therefore comprises both a transition in individuality and the emergence of a new information system – the two hallmarks of major evolutionary transitions. Finally, we present an evolutionary scenario for the origin of Darwinian immunity in vertebrates. We propose a revival of the concept of the ‘Big Bang’ of vertebrate immunity, arguing that its origin involved a ‘difficult’ (i.e. low-probability) evolutionary transition that might have occurred only once, in a common ancestor of all vertebrates. In contrast to the original concept, we argue that the limiting innovation was not the generation of somatic diversity, but the regulatory circuitry needed for the safe operation of amplifiable immune responses with somatically acquired targeting. Regulatory complexity increased abruptly by genomic duplications at the root of the vertebrate lineage, creating a rare opportunity to establish such circuitry. We discuss the selection forces that might have acted at the origin of the transition, and in the subsequent stepwise evolution leading to the modern immune systems of extant vertebrates.

  • Impacts of human-induced environmental change in wetlands on aquatic animals
    Biol. Rev. (IF 11.615) Pub Date : 2017-09-19
    Michael Sievers, Robin Hale, Kirsten M. Parris, Stephen E. Swearer

    ABSTRACT Many wetlands harbour highly diverse biological communities and provide extensive ecosystem services; however, these important ecological features are being altered, degraded and destroyed around the world. Despite a wealth of research on how animals respond to anthropogenic changes to natural wetlands and how they use created wetlands, we lack a broad synthesis of these data. While some altered wetlands may provide vital habitat, others could pose a considerable risk to wildlife. This risk will be heightened if such wetlands are ecological traps – preferred habitats that confer lower fitness than another available habitat. Wetlands functioning as ecological traps could decrease both local and regional population persistence, and ultimately lead to extinctions. Most studies have examined how animals respond to changes in environmental conditions by measuring responses at the community and population levels, but studying ecological traps requires information on fitness and habitat preferences. Our current lack of knowledge of individual-level responses may therefore limit our capacity to manage wetland ecosystems effectively since ecological traps require different management practices to mitigate potential consequences. We conducted a global meta-analysis to characterise how animals respond to four key drivers of wetland alteration: agriculture, mining, restoration and urbanisation. Our overarching goal was to evaluate the ecological impacts of human alterations to wetland ecosystems, as well as identify current knowledge gaps that limit both the current understanding of these responses and effective wetland management. We extracted 1799 taxon-specific response ratios from 271 studies across 29 countries. Community- (e.g. richness) and population-level (e.g. density) measures within altered wetlands were largely comparable to those within reference wetlands. By contrast, individual fitness measures (e.g. survival) were often lower, highlighting the potential limitations of using only community- and population-level measures to assess habitat quality. Only four studies provided habitat-preference data, preventing investigation of the potential for altered wetlands to function as ecological traps. This is concerning because attempts to identify ecological traps may detect previously unidentified conservation risks. Although there was considerable variability amongst taxa, amphibians were typically the most sensitive taxon, and thus, may be a valuable bio-indicator of wetland quality. Despite suffering reduced survival and reproduction, measures such as time to and mass at metamorphosis were similar between altered and reference wetlands, suggesting that quantifying metamorphosis-related measures in isolation may not provide accurate information on habitat quality. Our review provides the most detailed evaluation to date of the ecological impacts of human alterations to wetland ecosystems. We emphasise that the role of wetlands in human-altered ecosystems can be complex, as they may represent important habitat but also pose potential risks to animals. Reduced availability of natural wetlands is increasing the importance of altered wetlands for aquatic animals. Consequently, we need to define what represents habitat quality from the perspective of animals, and gain a greater understanding of the underlying mechanisms of habitat selection and how these factors could be manipulated. Furthermore, strategies to enhance the quality of these wetlands should be implemented to maximise their conservation potential.

  • The arms race between heliconiine butterflies and Passiflora plants – new insights on an ancient subject
    Biol. Rev. (IF 11.615) Pub Date : 2017-09-13
    Érika C. P. de Castro, Mika Zagrobelny, Márcio Z. Cardoso, Søren Bak

    ABSTRACT Heliconiines are called passion vine butterflies because they feed exclusively on Passiflora plants during the larval stage. Many features of Passiflora and heliconiines indicate that they have radiated and speciated in association with each other, and therefore this model system was one of the first examples used to exemplify coevolution theory. Three major adaptations of Passiflora plants supported arguments in favour of their coevolution with heliconiines: unusual variation of leaf shape within the genus; the occurrence of yellow structures mimicking heliconiine eggs; and their extensive diversity of defence compounds called cyanogenic glucosides. However, the protection systems of Passiflora plants go beyond these three features. Trichomes, mimicry of pathogen infection through variegation, and production of extrafloral nectar to attract ants and other predators of their herbivores, are morphological defences reported in this plant genus. Moreover, Passiflora plants are well protected chemically, not only by cyanogenic glucosides, but also by other compounds such as alkaloids, flavonoids, saponins, tannins and phenolics. Heliconiines can synthesize cyanogenic glucosides themselves, and their ability to handle these compounds was probably one of the most crucial adaptations that allowed the ancestor of these butterflies to feed on Passiflora plants. Indeed, it has been shown that Heliconius larvae can sequester cyanogenic glucosides and alkaloids from their host plants and utilize them for their own benefit. Recently, it was discovered that Heliconius adults have highly accurate visual and chemosensory systems, and the expansion of brain structures that can process such information allows them to memorize shapes and display elaborate pre-oviposition behaviour in order to defeat visual barriers evolved by Passiflora species. Even though the heliconiine–Passiflora model system has been intensively studied, the forces driving host-plant preference in these butterflies remain unclear. New studies have shown that host-plant preference seems to be genetically controlled, but in many species there is some plasticity in this choice and preferences can even be induced. Although much knowledge regarding the coevolution of Passiflora plants and heliconiine butterflies has accumulated in recent decades, there remain many exciting unanswered questions concerning this model system.

  • Genetics of dispersal
    Biol. Rev. (IF 11.615) Pub Date : 2017-08-03
    Marjo Saastamoinen, Greta Bocedi, Julien Cote, Delphine Legrand, Frédéric Guillaume, Christopher W. Wheat, Emanuel A. Fronhofer, Cristina Garcia, Roslyn Henry, Arild Husby, Michel Baguette, Dries Bonte, Aurélie Coulon, Hanna Kokko, Erik Matthysen, Kristjan Niitepõld, Etsuko Nonaka, Virginie M. Stevens, Justin M. J. Travis, Kathleen Donohue, James M. Bullock, Maria del Mar Delgado

    ABSTRACT Dispersal is a process of central importance for the ecological and evolutionary dynamics of populations and communities, because of its diverse consequences for gene flow and demography. It is subject to evolutionary change, which begs the question, what is the genetic basis of this potentially complex trait? To address this question, we (i) review the empirical literature on the genetic basis of dispersal, (ii) explore how theoretical investigations of the evolution of dispersal have represented the genetics of dispersal, and (iii) discuss how the genetic basis of dispersal influences theoretical predictions of the evolution of dispersal and potential consequences. Dispersal has a detectable genetic basis in many organisms, from bacteria to plants and animals. Generally, there is evidence for significant genetic variation for dispersal or dispersal-related phenotypes or evidence for the micro-evolution of dispersal in natural populations. Dispersal is typically the outcome of several interacting traits, and this complexity is reflected in its genetic architecture: while some genes of moderate to large effect can influence certain aspects of dispersal, dispersal traits are typically polygenic. Correlations among dispersal traits as well as between dispersal traits and other traits under selection are common, and the genetic basis of dispersal can be highly environment-dependent. By contrast, models have historically considered a highly simplified genetic architecture of dispersal. It is only recently that models have started to consider multiple loci influencing dispersal, as well as non-additive effects such as dominance and epistasis, showing that the genetic basis of dispersal can influence evolutionary rates and outcomes, especially under non-equilibrium conditions. For example, the number of loci controlling dispersal can influence projected rates of dispersal evolution during range shifts and corresponding demographic impacts. Incorporating more realism in the genetic architecture of dispersal is thus necessary to enable models to move beyond the purely theoretical towards making more useful predictions of evolutionary and ecological dynamics under current and future environmental conditions. To inform these advances, empirical studies need to answer outstanding questions concerning whether specific genes underlie dispersal variation, the genetic architecture of context-dependent dispersal phenotypes and behaviours, and correlations among dispersal and other traits.

Some contents have been Reproduced with permission of the American Chemical Society.
Some contents have been Reproduced by permission of The Royal Society of Chemistry.
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