当前期刊: Molecular Ecology Go to current issue    加入关注   
显示样式:        排序: 导出
  • Host and Symbiont Genetic Determinants of Nutritional Phenotype in a Natural Population of the Pea Aphid
    Mol. Ecol. (IF 5.855) Pub Date : 2020-01-16
    Seung Ho Chung; Benjamin J. Parker; Frances Blow; Jennifer A. Brisson; Angela E. Douglas

    A defining feature of the nutritional ecology of plant sap feeding insects is that the dietary deficit of essential amino acids (EAAs) in plant sap is supplemented by EAA‐provisioning microbial symbionts in the insect. Here, we demonstrated substantial variation in the nutritional phenotype of 208 genotypes of the pea aphid Acyrthosiphon pisum collected from natural populations. Specifically, the genotypes varied in performance (larval growth rates) on four test diets lacking EAA arginine, histidine, methionine or aromatic EAAs (phenylalanine and tryptophan), relative to the diet containing all EAAs. These data indicate that EAA supply from the symbiotic bacteria Buchnera can meet total aphid nutritional demand for only a subset of the EAA/aphid genotype combinations. We then correlated SNPs identified in the aphid and Buchnera genomes by reduced genome sequencing against aphid performance for each EAA deletion diet. This yielded significant associations between performance on the histidine‐free diet and Buchnera SNPs, including metabolism genes predicted to influence histidine biosynthesis. Aphid genetic correlates of performance were obtained for all four deletion diets, with associations on the arginine‐free diet and aromatic‐free diets dominated by genes functioning in regulation of metabolic and cellular processes. The specific aphid genes associated with performance on different EAA deletion diets are largely non‐overlapping, indicating some independence in the regulatory circuits determining aphid phenotype for the different EAAs. This study demonstrates how variation in phenotype of associations collected from natural populations can be applied to elucidate the genetic basis of ecologically‐important traits in systems intractable to traditional forward/reverse genetic techniques.

  • Genomic and phenomic analysis of island ant community assembly
    Mol. Ecol. (IF 5.855) Pub Date : 2020-01-14
    Clive T. Darwell; Georg Fischer; Eli M. Sarnat; Nicholas R. Friedman; Cong Liu; Guilherme Baiao; Alexander S. Mikheyev; Evan P. Economo

    Island biodiversity has long fascinated biologists as it typically presents tractable systems for unpicking the eco‐evolutionary processes driving community assembly. In general, two recurring themes are of central theoretical interest. First, immigration, diversification, and extinction typically depend on island geographical properties (e.g., area, isolation, and age). Second, predictable ecological and evolutionary trajectories readily occur after colonization, such as the evolution of adaptive trait syndromes, trends toward specialization, adaptive radiation, and eventual ecological decline. Hypotheses such as the taxon cycle draw on several of these themes to posit particular constraints on colonization and subsequent eco‐evolutionary dynamics. However, it has been challenging to examine these integrated dynamics with traditional methods. Here, we combine phylogenomics, population genomics and phenomics, to unravel community assembly dynamics among Pheidole (Hymenoptera, Formicidae) ants in the isolated Fijian archipelago. We uphold basic island biogeographic predictions that isolated islands accumulate diversity primarily through in situ evolution rather than dispersal, and population genomic support for taxon cycle predictions that endemic species have decreased dispersal ability and demography relative to regionally widespread taxa. However, rather than trending toward island syndromes, ecomorphological diversification in Fiji was intense, filling much of the genus‐level global morphospace. Furthermore, while most endemic species exhibit demographic decline and reduced dispersal, we show that the archipelago is not an evolutionary dead‐end. Rather, several endemic species show signatures of population and range expansion, including a successful colonization to the Cook islands. These results shed light on the processes shaping island biotas and refine our understanding of island biogeographic theory.

  • Beyond the landscape: Resistance modelling infers physical and behavioural gene flow barriers to a mobile carnivore across a metropolitan area
    Mol. Ecol. (IF 5.855) Pub Date : 2020-01-14
    Sophia E. Kimmig; Joscha Beninde; Miriam Brandt; Anna Schleimer; Stephanie Kramer‐Schadt; Heribert Hofer; Konstantin Börner; Christoph Schulze; Ulrich Wittstatt; Mike Heddergott; Tanja Halczok; Christoph Staubach; Alain C. Frantz

    Urbanization affects key aspects of wildlife ecology. Dispersal in urban wildlife species may be impacted by geographical barriers but also by a species’ inherent behavioural variability. There are no functional connectivity analyses using continuous individual‐based sampling across an urban‐rural continuum that would allow a thorough assessment of the relative importance of physical and behavioural dispersal barriers. We used 16 microsatellite loci to genotype 374 red foxes (Vulpes vulpes) from the city of Berlin and surrounding rural regions in Brandenburg in order to study genetic structure and dispersal behaviour of a mobile carnivore across the urban‐rural landscape. We assessed functional connectivity by applying an individual‐based landscape genetic optimization procedure. Three commonly used genetic distance measures yielded different model selection results, with only the results of an eigenvector‐based multivariate analysis reasonably explaining genetic differentiation patterns. Genetic clustering methods and landscape resistance modelling supported the presence of an urban population with reduced dispersal across the city border. Artificial structures (railways, motorways) served as main dispersal corridors within the cityscape, yet urban foxes avoided densely built‐up areas. We show that despite their ubiquitous presence in urban areas, their mobility and behavioural plasticity, foxes were affected in their dispersal by anthropogenic presence. Distinguishing between man‐made structures and sites of human activity, rather than between natural and artificial structures, is thus essential for better understanding urban fox dispersal. This differentiation may also help to understand dispersal of other urban wildlife and to predict how behaviour can shape population genetic structure beyond physical barriers.

  • Resilience in reef‐building corals: The ecological and evolutionary importance of the host response to thermal stress
    Mol. Ecol. (IF 5.855) Pub Date : 2020-01-14
    Crawford Drury

    Coral reefs are under extreme threat due to a number of stressors, but temperature increases due to changing climate are the most severe. Rising ocean temperatures coupled with local extremes lead to extensive bleaching, where the coral‐algal symbiosis breaks down and corals may die, compromising the structure and function of reefs. Although the symbiotic nature of the coral colony has historically been a focus of research on coral resilience, the host itself is a foundational component in the response to thermal stress. Fixed effects in the coral host set trait baselines through evolutionary processes, acting on many loci of small effect to create mosaics of thermal tolerance across latitudes and individual coral reefs. These genomic differences can be strongly heritable, producing wide variation among clones of different genotypes or families of a specific larval cross. Phenotypic plasticity is overlaid on these baselines and a growing body of knowledge demonstrates the potential for acclimatization of reef‐building corals through a variety of mechanisms that promote resilience and stress tolerance. The long‐term persistence of coral reefs will require many of these mechanisms to adjust to warmer temperatures within a generation, bridging the gap to reproductive events that allow recombination of standing diversity and adaptive change. Business‐as‐usual climate scenarios will probably lead to the loss of some coral populations or species in the future, so the interaction between intragenerational effects and evolutionary pressure is critical for the survival of reefs.

  • Sky islands as foci for divergence of fig trees and their pollinators in South‐West China
    Mol. Ecol. (IF 5.855) Pub Date : 2020-01-14
    Jun‐Yin Deng; Rong‐Hua Fu; Stephen G. Compton; Mei Liu; Qin Wang; Chuan Yuan; Lu‐Shui Zhang; Yan Chen

    The dynamics of populations and their divergence over time have shaped current levels of biodiversity and in the case of the ‘sky islands’ of mountainous SW China have resulted in an area of exceptional botanical diversity. Ficus tikoua is a prostrate fig tree sub‐endemic to the area that displays unique intraspecific diversity, producing figs typical of different pollination modes in different parts of its range. By combining climate models, genetic variation in populations of the tree’s obligate fig wasp pollinators and distributions of the different plant phenotypes, we examined how this unusual situation may have developed. We identified three genetically distinct groups of a single Ceratosolen pollinator species that have largely parapatric distributions. The complex topography of the region contributed to genetic divergence among the pollinators by facilitating geographic isolation and providing refugia. Migration along elevations in response to climate oscillations further enhanced genetic differentiation of the three pollinator groups. Their distributions loosely correspond to the distributions of the functionally significant morphological differences in the male figs of their host plants, but postglacial expansion of one group has not been matched by spread of its associated plant phenotype, possibly due to a major river barrier. The results highlight how interplay between the complex topography of the ‘sky‐island’ complex and climate change has shaped intra‐species differentiation and relationship between the plant and its pollinator. Similar processes may explain the exceptional botanical diversity of SW China.

  • To have and not to have sex: when multiple evolutions of conditional use of sex elegantly solve the question in the ant genus Cataglyphis
    Mol. Ecol. (IF 5.855) Pub Date : 2020-01-13
    Doums Claudie; Thibaud Monnin

    Organisms use an amazingly large diversity of mechanisms to pass on their genes to the next generation. Sex is ancestral in eukaryotes, where it remains the most widespread way of reproduction. By combining one's genes with those of a partner, sex entails a dilution of one's genes at each generation. Evolution has been particularly creative in devising mechanisms allowing females to avoid this dilution, from classical parthenogenesis to the elimination of male genes after fertilization (Bell, 1982). Moreover, the term parthenogenesis include various forms. Parthenogenesis can be used for female (thelytoky) or male (arrhenotoky) production and it can be associated with different cytological mechanisms, from strict clonality to meiotic division with the fusion of two of the four products of meiosis to restore diploidy (Suomalainen, Saura, & Lokki, 1987). Understanding the evolution of these diverse reproductive systems remains one of the most exciting and longstanding questions in evolutionary biology. By characterizing the reproductive systems of 11 species from the thermophilic ant genus Cataglyphis, in this issue of Molecular Ecology, Kuhn, Darras, Paknia, & Aron (2020) show the high lability of parthenogenesis, with multiple independent evolution of facultative thelytoky from sexual ancestors. The diversity of life history traits and social characteristics of this genus (e.g. mode of colony foundation, female polyandry) provides a unique and exciting opportunity to investigate the social and environmental factors driving the evolution of reproductive systems in social Hymenoptera.

  • Lineage‐specific adaptation to climate involves flowering time in North American Arabidopsis lyrata
    Mol. Ecol. (IF 5.855) Pub Date : 2020-01-13
    Nora Walden; Kay Lucek; Yvonne Willi

    Adaptation to local climatic conditions is commonly found within species, but whether it involves the same intraspecific genomic variants is unknown. We studied this question in North American Arabidopsis lyrata, whose current distribution is shaped by post‐glacial range expansion from two refugia, resulting in two distinct genetic clusters covering comparable climatic gradients. Using pooled whole‐genome sequence data of 41 outcrossing populations, we identified loci associated with three niche‐determining climatic variables in the two clusters and compared these outliers. Little evidence was found for parallelism in climate adaptation for single nucleotide polymorphisms (SNPs) and for genes with an accumulation of outlier SNPs. Significantly increased selection coefficients supported them as candidates of climate adaptation. However, the fraction of gene ontology (GO) terms shared between clusters was higher compared to outlier SNPs and outlier genes, suggesting that selection acts on similar pathways but not necessarily the same genes. Enriched GO terms involved responses to abiotic and biotic stress, circadian rhythm and development, with flower development and reproduction being among the most frequently detected. In line with GO enrichment, regulators of flowering time were detected as outlier genes. Our results suggest that while adaptation to environmental gradients on the genomic level are lineage‐specific in A. lyrata, similar biological processes seem to be involved. Differential loss of standing genetic variation, probably driven by genetic drift, can in part account for the lack of parallel evolution on the genomic level.

  • Evolutionary signal in the gut microbiomes of 74 bird species from Equatorial Guinea
    Mol. Ecol. (IF 5.855) Pub Date : 2020-01-13
    Darien C. Capunitan; Oscar Johnson; Ryan S. Terrill; Sarah M. Hird

    How the microbiome interacts with hosts across evolutionary time is poorly understood. Datasets including many host species are required to conduct comparative analyses. Here, we have analyzed 142 intestinal microbiome samples from 92 birds belonging to 74 species from Equatorial Guinea, using the 16S rRNA gene. Using four definitions for microbial taxonomic units (97%OTU, 99%OTU, 99%OTU with singletons removed, ASV), we conducted alpha and beta diversity analyses. We find that raw abundances and diversity varied between the datasets but relative patterns were largely consistent across datasets. Host taxonomy, diet and locality were significantly associated with microbiomes, at generally similar levels using three distance metrics. Phylogenetic comparative methods assessed the evolutionary relationship between the microbiome as a trait of a host species and the underlying bird phylogeny. Using multiple ways of defining “microbiome traits”, we find that a neutral Brownian motion model does not explain variation in microbiomes. Instead, we find a White Noise model (indicating little phylogenetic signal), is most likely. There was some support for the Ornstein‐Uhlenbeck model (that invokes selection), but the level of support was similar to that of a White Noise simulation, further supporting the White Noise model as the best explanation for the evolution of the microbiome as a trait of avian hosts. Our study demonstrates that both environment and evolution play a role in the gut microbiome and the relationship does not follow a neutral model; these biological results are qualitatively robust to analytical choices.

  • Host dispersal shapes the population structure of a tick‐borne bacterial pathogen
    Mol. Ecol. (IF 5.855) Pub Date : 2020-01-09
    Ana Cláudia Norte; Gabriele Margos; Noémie S. Becker; Jaime Albino Ramos; Maria Sofia Núncio; Volker Fingerle; Pedro Miguel Araújo; Peter Adamík; Haralambos Alivizatos; Emilio Barba; Rafael Barrientos; Laure Cauchard; Tibor Csörgő; Anastasia Diakou; Niels J. Dingemanse; Blandine Doligez; Anna Dubiec; Tapio Eeva; Barbara Flaisz; Tomas Grim; Michaela Hau; Dieter Heylen; Sándor Hornok; Savas Kazantzidis; David Kováts; František Krause; Ivan Literak; Raivo Mänd; Lucia Mentesana; Jennifer Morinay; Marko Mutanen; Júlio Manuel Neto; Markéta Nováková; Juan José Sanz; Luís Pascoal da Silva; Hein Sprong; Ina‐Sabrina Tirri; János Török; Tomi Trilar; Zdeněk Tyller; Marcel E. Visser; Isabel Lopes de Carvalho

    Birds are hosts for several zoonotic pathogens. Because of their high mobility, especially of longdistance migrants, birds can disperse these pathogens, affecting their distribution and phylogeography. We focused on Borrelia burgdorferi sensu lato, which includes the causative agents of Lyme borreliosis, as an example for tick‐borne pathogens, to address the role of birds as propagation hosts of zoonotic agents at a large geographical scale. We collected ticks from passerine birds in 11 European countries. B. burgdorferi s.l. prevalence in Ixodes spp. was 37% and increased with latitude. The fieldfare Turdus pilaris and the blackbird T. merula carried ticks with the highest Borrelia prevalence (92 and 58%, respectively), whereas robin Erithacus rubecula ticks were the least infected (3.8%). Borrelia garinii was the most prevalent genospecies (61%), followed by B. valaisiana (24%), B. afzelii (9%), B. turdi (5%) and B. lusitaniae (0.5%). A novel Borrelia genospecies “Candidatus Borrelia aligera” was also detected. Multilocus sequence typing (MLST) analysis of B. garinii isolates together with the global collection of B. garinii genotypes obtained from the Borrelia MLST public database revealed that: (a) there was little overlap among genotypes from different continents, (b) there was no geographical structuring within Europe, and (c) there was no evident association pattern detectable among B. garinii genotypes from ticks feeding on birds, questing ticks or human isolates. These findings strengthen the hypothesis that the population structure and evolutionary biology of tick‐borne pathogens are shaped by their host associations and the movement patterns of these hosts.

  • Share the wealth: trees with greater ectomycorrhizal species overlap share more carbon
    Mol. Ecol. (IF 5.855) Pub Date : 2020-01-10
    Ido Rog; Nicholas P. Rosenstock; Christian Körner; Tamir Klein

    The mutualistic symbiosis between forest trees and ectomycorrhizal fungi (EMF) is among the most ubiquitous and successful interactions in terrestrial ecosystems. Specific species of EMF are known to colonize specific tree species, benefitting from their carbon source, and in turn, improving their access to soil water and nutrients. EMF also form extensive mycelial networks that can link multiple root‐tips of different trees. Yet the number of tree species connected by such mycelial networks, and the traffic of material across them, are just now under study. Recently we reported substantial belowground carbon transfer between Picea, Pinus, Larix and Fagus trees in a mature forest. Here we analyze the EMF community of these same individual trees and identify the most likely taxa responsible for the observed carbon transfer. Among the nearly 1200 EMF root‐tips examined, 50‐70% belong to operational taxonomic units (OTUs) that were associated with 3 or 4 tree host species, and 90% of all OTUs were associated with at least two tree species. Sporocarp 13C signals indicated that carbon originating from labeled Picea trees was transferred among trees through EMF networks. Interestingly, phylogenetically more closely related tree species exhibited more similar EMF communities and exchanged more carbon. Our results show that belowground carbon transfer is well orchestrated by the evolution of EMFs and tree symbiosis.

  • Biogeography, habitat transitions and hybridization in a radiation of South American silverside fishes revealed by mitochondrial and genomic RAD data
    Mol. Ecol. (IF 5.855) Pub Date : 2020-01-09
    Lily C. Hughes; Yamila P. Cardoso; Julie A. Sommer; Roberto Cifuentes; Mariela Cuello; Gustavo M. Somoza; Mariano González‐Castro; Luiz R. Malabarba; Victor Cussac; Evelyn M. Habit; Ricardo Betancur‐R; Guillermo Ortí

    Rivers and lake systems in the southern cone of South America have been widely influenced by historic glaciations events, carrying important implications on the evolution of aquatic organisms including prompting transitions between marine and freshwater habitats and by triggering hybridization among incipient species via waterway connectivity and stream capture events. Silverside fishes (Odontesthes) in the region comprise a radiation of 19 marine and freshwater species that have been hypothesized on the basis of morphological or mitochondrial DNA data to have either transitioned repeatedly into continental waters from the sea or colonized marine habitats following freshwater diversification. New ddRAD data presented here provide a robust framework to investigate biogeographic history and habitat transitions in Odontesthes. We show that Odontesthes silversides originally diversified in the Pacific but independently colonized the Atlantic three times, producing three independent marine‐to‐freshwater transitions. Our results also indicate recent introgression of marine mitochondrial haplotypes into two freshwater clades, with more recurring instances of hybridization among Atlantic‐ versus. Pacific‐slope species. In Pacific freshwater drainages, hybridization with a marine species appears to be geographically isolated and may be related to glaciation events. Substantial structural differences of estuarine gradients between these two geographic areas may have influenced the frequency, intensity, and evolutionary effects of hybridization events.

  • Assessing changes in genomic divergence following a century of human‐mediated secondary contact among wild and captive‐bred ducks
    Mol. Ecol. (IF 5.855) Pub Date : 2020-01-08
    Philip Lavretsky; Nancy Rotzel McInerney; Jonathon E. Mohl; Joshua I. Brown; Helen F. James; Kevin G. McCracken; Robert C. Fleischer

    Along with manipulating habitat, the direct release of domesticated individuals into the wild is a practice used worldwide to augment wildlife populations. We test between possible outcomes of human‐mediated secondary contact using genomic techniques at both historical and contemporary timescales for two iconic duck species. First, we sequence several thousand ddRAD‐seq loci for contemporary mallards (Anas platyrhynchos) throughout North America and two domestic mallard types (i.e., known game‐farm mallards and feral Khaki Campbell's). We show that North American mallards may well be becoming a hybrid swarm due to interbreeding with domesticated game‐farm mallards released for hunting. Next, to attain a historical perspective, we applied a bait‐capture array targeting thousands of loci in century‐old (1842–1915) and contemporary (2009–2010) mallard and American black duck (Anas rubripes) specimens. We conclude that American black ducks and mallards have always been closely related, with a divergence time of ~600,000 years before present, and likely evolved through prolonged isolation followed by limited bouts of gene flow (i.e., secondary contact). They continue to maintain genetic separation, a finding that overturns decades of prior research and speculation suggesting the genetic extinction of the American black duck due to contemporary interbreeding with mallards. Thus, despite having high rates of hybridization, actual gene flow is limited between mallards and American black ducks. Conversely, our historical and contemporary data confirm that the intensive stocking of game‐farm mallards during the last ~100 years has fundamentally changed the genetic integrity of North America's wild mallard population, especially in the east. It thus becomes of great interest to ask whether the iconic North American mallard is declining in the wild due to introgression of maladaptive traits from domesticated forms. Moreover, we hypothesize that differential gene flow from domestic game‐farm mallards into the wild mallard population may explain the overall temporal increase in differentiation between wild black ducks and mallards, as well as the uncoupling of genetic diversity and effective population size estimates across time in our results. Finally, our findings highlight how genomic methods can recover complex population histories by capturing DNA preserved in traditional museum specimens.

  • Contrasting impacts of a novel specialist vector on multihost viral pathogen epidemiology in wild and managed bees
    Mol. Ecol. (IF 5.855) Pub Date : 2020-01-07
    Robyn Manley; Ben Temperton; Mike Boots; Lena Wilfert

    Typically, pathogens infect multiple host species. Such multihost pathogens can show considerable variation in their degree of infection and transmission specificity, which has important implications for potential disease emergence. Transmission of multihost pathogens can be driven by key host species and changes in such transmission networks can lead to disease emergence. We study two viruses that show contrasting patterns of prevalence and specificity in managed honeybees and wild bumblebees, black queen cell virus (BQCV) and slow bee paralysis virus (SBPV), in the context of the novel transmission route provided by the virus‐vectoring Varroa destructor. Our key result is that viral communities and RNA virus genetic variation are structured by location, not host species or V. destructor presence. Interspecific transmission is pervasive with the same viral variants circulating between pollinator hosts in each location; yet, we found virus‐specific host differences in prevalence and viral load. Importantly, V. destructor presence increases the prevalence in honeybees and, indirectly, in wild bumblebees, but in contrast to its impact on deformed wing virus (DWV), BQCV and SBPV viral loads are not increased by Varroa presence, and do not show genetic evidence of recent emergence. Effective control of Varroa in managed honeybee colonies is necessary to mitigate further disease emergence, and alleviate disease pressure on our vital wild bee populations. More generally, our results highlight the over‐riding importance of geographical location to the epidemiological outcome despite the complexity of multihost‐parasite interactions.

  • Identification of a genetic network for an ecologically relevant behavioural phenotype in Drosophila melanogaster
    Mol. Ecol. (IF 5.855) Pub Date : 2020-01-07
    Wenyu Zhang; Guy Richard Reeves; Diethard Tautz

    Pupation site choice of Drosophila third‐instar larvae is critical for the survival of individuals, as pupae are exposed to various biotic and abiotic dangers while immobilized during the 3–4 days of metamorphosis. This singular behavioural choice is sensitive to both environmental and genetic factors. Here, we developed a high‐throughput phenotyping approach to assay the variation in pupation height in Drosophila melanogaster, while controlling for possibly confounding factors. We find substantial variation of mean pupation height among sampled natural stocks and we show that the Drosophila Genetic Reference Panel (DGRP) reflects this variation. Using the DGRP stocks for genome‐wide association (GWA) mapping, 16 loci involved in determining pupation height could be resolved. The candidate genes in these loci are enriched for high expression in the larval central nervous system. A genetic network could be constructed from the candidate loci, which places scribble (scrib) at the centre, plus other genes known to be involved in nervous system development, such as Epidermal growth factor receptor (Egfr) and p53. Using gene disruption lines, we could functionally validate several of the initially identified loci, as well as additional loci predicted from network analysis. Our study shows that the combination of high‐throughput phenotyping with a genetic analysis of variation captured from the wild can be used to approach the genetic dissection of an environmentally relevant behavioural phenotype.

  • Heritability of inter‐pack aggression in a wild pedigreed population of North American gray wolves
    Mol. Ecol. (IF 5.855) Pub Date : 2020-01-06
    Bridgett M. vonHoldt; Alexandra L. DeCandia; Elizabeth Heppenheimer; Ilana Janowitz‐Koch; Ruoyao Shi; Hua Zhou; Christopher A. German; Kristin E. Brzeski; Kira A. Cassidy; Daniel R. Stahler; Janet S. Sinsheimer

    Aggression is a quantitative trait deeply entwined with individual fitness. Mapping the genomic architecture underlying such traits is complicated by complex inheritance patterns, social structure, pedigree information, and gene pleiotropy. Here, we leveraged the pedigree of a reintroduced population of gray wolves in Yellowstone National Park, Wyoming USA to examine the heritability of and the genetic variation associated with aggression. Since their reintroduction, many ecological and behavioral aspects have been documented, providing unmatched records of aggressive behavior across multiple generations of a wild population of wolves. Using a linear mixed model, a robust genetic relationship matrix, 12,288 SNPs, and 111 wolves, we estimated the SNP‐based heritability of aggression to be 37% and an additional 14% of the phenotypic variation explained by shared environmental exposures. We identified 598 SNP genotypes from 425 gray wolves to resolve a consensus pedigree that was included in a heritability analysis of 141 individuals with SNP genotype, meta‐data, and aggression data. The pedigree‐based heritability estimate for aggression is 14%, and an additional 16% of the phenotypic variation explained by shared environmental exposures. We find strong effects of breeding status and relative pack size on aggression. Through an integrative approach, these results provide a framework for understanding the genetic architecture of a complex trait that influences individual fitness, with linkages to reproduction, in a social carnivore. Along with few other studies, we present here the incredible utility of a pedigreed natural population for dissecting a complex, fitness‐related behavioral trait.

  • Nonspecific expression of fertilization genes in the crown‐of‐thorns Acanthaster cf. solaris: Unexpected evidence of hermaphroditism in a coral reef predator
    Mol. Ecol. (IF 5.855) Pub Date : 2020-01-03
    Vanessa Guerra; Gwilym Haynes; Maria Byrne; Nina Yasuda; Souta Adachi; Masako Nakamura; Shu Nakachi; Michael W. Hart

    The characterization of gene expression in gametes has advanced our understanding of the molecular basis for ecological variation in reproductive success and the evolution of reproductive isolation. These advances are especially significant for ecologically important keystone predators such as the coral‐eating crown‐of‐thorns sea stars (COTS, Acanthaster) which are the most influential predator species in Indo‐Pacific coral reef ecosystems and the focus of intensive management efforts. We used RNA‐seq and transcriptome assemblies to characterize the expression of genes in mature COTS gonads. We described the sequence and domain organization of eight genes with sex‐specific expression and well known functions in fertilization in other echinoderms. We found unexpected expression of genes in one ovary transcriptome that are characteristic of males and sperm, including genes that encode the sperm‐specific guanylate cyclase receptor for an egg pheromone, and the sperm acrosomal protein bindin. In a reassembly of previously published RNA‐seq data from COTS testes, we found a complementary pattern: strong expression of four genes that are otherwise well known to encode egg‐specific fertilization proteins, including the egg receptor for bindin (EBR1) and the acrosome reaction‐inducing substance in the egg coat (ARIS1, ARIS2, ARIS3). We also found histological evidence of both eggs and sperm developing in the same gonad in several COTS individuals from a parallel study. These results suggest the occurrence of hermaphrodites, and the potential for reproductive assurance via self‐fertilization. Our findings have implications for management of COTS populations, especially in consideration of the large size and massive fecundity of these sea stars.

  • The microbiota influences the Drosophila melanogaster life history strategy
    Mol. Ecol. (IF 5.855) Pub Date : 2020-01-03
    Amber W. Walters; Rachel C. Hughes; Tanner B. Call; Carson J. Walker; Hailey Wilcox; Samara C. Petersen; Seth M. Rudman; Peter D. Newell; Angela E. Douglas; Paul S. Schmidt; John M. Chaston

    Organisms are locally adapted when members of a population have a fitness advantage in one location relative to conspecifics in other geographies. For example, across latitudinal gradients, some organisms may trade off between traits that maximize fitness components in one, but not both, of somatic maintenance or reproductive output. Latitudinal gradients in life history strategies are traditionally attributed to environmental selection on an animal's genotype, without any consideration of the possible impact of associated microorganisms (“microbiota”) on life history traits. Here, we show in Drosophila melanogaster, a key model for studying local adaptation and life history strategy, that excluding the microbiota from definitions of local adaptation is a major shortfall. First, we reveal that an isogenic fly line reared with different bacteria varies the investment in early reproduction versus somatic maintenance. Next, we show that in wild fruit flies, the abundance of these same bacteria was correlated with the latitude and life history strategy of the flies, suggesting geographic specificity of the microbiota composition. Variation in microbiota composition of locally adapted D. melanogaster could be attributed to both the wild environment and host genetic selection. Finally, by eliminating or manipulating the microbiota of fly lines collected across a latitudinal gradient, we reveal that host genotype contributes to latitude‐specific life history traits independent of the microbiota and that variation in the microbiota can suppress or reverse the differences between locally adapted fly lines. Together, these findings establish the microbiota composition of a model animal as an essential consideration in local adaptation.

  • Comparative genomics reveals divergent thermal selection in warm‐ and cold‐tolerant marine mussels
    Mol. Ecol. (IF 5.855) Pub Date : 2020-01-03
    Iva Popovic; Cynthia Riginos

    Investigating the history of natural selection among closely related species can elucidate how genomes diverge in response to disparate environmental pressures. Molecular evolutionary approaches can be integrated with knowledge of gene functions to examine how evolutionary divergence may affect ecologically relevant traits such as temperature tolerance and species distribution limits. Here, we integrate transcriptome‐wide analyses of molecular evolution with knowledge from physiological studies to develop hypotheses regarding the functional classes of genes under positive selection in one of the world's most widespread invasive species, the warm‐tolerant marine mussel Mytilus galloprovincialis. Based on existing physiological information, we test the hypothesis that genomic functions previously linked to divergent temperature adaptation at the whole‐organism level show accelerated molecular divergence between warm‐adapted M. galloprovincialis and cold‐adapted congeners. Combined results from codon model tests and analyses of polymorphism and divergence reveal that divergent selection has affected genomic functions previously associated with species‐specific expression responses to heat stress, namely oxidative stress defence and cytoskeletal stabilization. Examining specific loci implicated in thermal tolerance among Mytilus species (based on interspecific biochemical or expression patterns), we find close functional similarities between known thermotolerance candidate genes under positive selection and positively selected loci under predicted genomic functions (those associated with divergent expression responses). Taken together, our findings suggest a contribution of temperature‐dependent selection in the molecular divergence between warm‐ and cold‐adapted Mytilus species that is largely consistent with results from physiological studies. More broadly, this study provides an example of how independent experimental evidence from ecophysiological investigations can inform evolutionary hypotheses about molecular adaptation in closely related nonmodel species.

  • Ear mite infection is associated with altered microbial communities in genetically depauperate Santa Catalina Island foxes (Urocyon littoralis catalinae)
    Mol. Ecol. (IF 5.855) Pub Date : 2020-01-02
    Alexandra L. DeCandia; Lara J. Brenner; Julie L. King; Bridgett M. vonHoldt

    The host‐associated microbiome is increasingly recognized as a critical player in health and immunity. Recent studies have shown that disruption of commensal microbial communities can contribute to disease pathogenesis and severity. Santa Catalina Island foxes (Urocyon littoralis catalinae) present a compelling system in which to examine microbial dynamics in wildlife due to their depauperate genomic structure and extremely high prevalence of ceruminous gland tumors. Although the precise cause is yet unknown, infection with ear mites (Otodectes cynotis) has been linked to chronic inflammation, which is associated with abnormal cell growth and tumor development. Given the paucity of genomic variation in these foxes, other dimensions of molecular diversity, such as commensal microbes, may be critical to host response and disease pathology. We characterized the host‐associated microbiome across six body sites of Santa Catalina Island foxes, and performed differential abundance testing between healthy and mite‐infected ear canals. We found that mite infection was significantly associated with reduced microbial diversity and evenness, with the opportunistic pathogen Staphylococcus pseudintermedius dominating the ear canal community. These results suggest that secondary bacterial infection may contribute to the sustained inflammation associated with tumor development. As the emergence of antibiotic resistant strains remains a concern of the medical, veterinary, and conservation communities, uncovering high relative abundance of S. pseudintermedius provides critical insight into the pathogenesis of this complex system. Through use of culture‐independent sequencing techniques, this study contributes to the broader effort of applying a more inclusive understanding of molecular diversity to questions within wildlife disease ecology.

  • Ancient DNA suggests modern wolves trace their origin to a Late Pleistocene expansion from Beringia
    Mol. Ecol. (IF 5.855) Pub Date : 2020-01-02
    Liisa Loog; Olaf Thalmann; Mikkel‐Holger S. Sinding; Verena J. Schuenemann; Angela Perri; Mietje Germonpré; Herve Bocherens; Kelsey E. Witt; Jose A. Samaniego Castruita; Marcela S. Velasco; Inge K. C. Lundstrøm; Nathan Wales; Gontran Sonet; Laurent Frantz; Hannes Schroeder; Jane Budd; Elodie‐Laure Jimenez; Sergey Fedorov; Boris Gasparyan; Andrew W. Kandel; Martina Lázničková‐Galetová; Hannes Napierala; Hans‐Peter Uerpmann; Pavel A. Nikolskiy; Elena Y. Pavlova; Vladimir V. Pitulko; Karl‐Heinz Herzig; Ripan S. Malhi; Eske Willerslev; Anders J. Hansen; Keith Dobney; M. Thomas P. Gilbert; Johannes Krause; Greger Larson; Anders Eriksson; Andrea Manica

    Grey wolves (Canis lupus) are one of the few large terrestrial carnivores that have maintained a wide geographical distribution across the Northern Hemisphere throughout the Pleistocene and Holocene. Recent genetic studies have suggested that, despite this continuous presence, major demographic changes occurred in wolf populations between the Late Pleistocene and early Holocene, and that extant wolves trace their ancestry to a single Late Pleistocene population. Both the geographical origin of this ancestral population and how it became widespread remain unknown. Here, we used a spatially and temporally explicit modelling framework to analyse a data set of 90 modern and 45 ancient mitochondrial wolf genomes from across the Northern Hemisphere, spanning the last 50,000 years. Our results suggest that contemporary wolf populations trace their ancestry to an expansion from Beringia at the end of the Last Glacial Maximum, and that this process was most likely driven by Late Pleistocene ecological fluctuations that occurred across the Northern Hemisphere. This study provides direct ancient genetic evidence that long‐range migration has played an important role in the population history of a large carnivore, and provides insight into how wolves survived the wave of megafaunal extinctions at the end of the last glaciation. Moreover, because Late Pleistocene grey wolves were the likely source from which all modern dogs trace their origins, the demographic history described in this study has fundamental implications for understanding the geographical origin of the dog.

  • Insects and incest: Sib‐mating tolerance in natural populations of a parasitoid wasp
    Mol. Ecol. (IF 5.855) Pub Date : 2020-01-02
    Marie Collet; Isabelle Amat; Sandrine Sauzet; Alexandra Auguste; Xavier Fauvergue; Laurence Mouton; Emmanuel Desouhant

    Sib‐mating avoidance is a pervasive behaviour that is expected to evolve in species subject to inbreeding depression. Although laboratory studies provide elegant demonstrations, small‐scaled bioassays minimize the costs of mate finding and choice, and thus may produce spurious findings. We therefore combined laboratory experiments with field observations to examine the existence of inbreeding avoidance using the parasitoid wasp Venturia canescens. In the laboratory, our approach consisted of mate‐choice experiments to assess kin discrimination in population cages with competitive interactions. A higher mating probability after sib rejections suggested that females could discriminate their sibs; however, in contrast to previous findings, sib‐mating avoidance was not observed. To compare our laboratory results to field data, we captured 241 individuals from two populations. Females laid eggs in the lab, and 226 daughters were obtained. All individuals were genotyped at 18 microsatellite loci, which allowed inference of the genotype of each female's mate and subsequently the relatedness within each mating pair. We found that the observed rate of sib‐mating did not differ from the probability that sibs encountered one another at random in the field, which is consistent with an absence of sib‐mating avoidance. In addition, we detected a weak but significant male‐biased dispersal, which could reduce encounters between sibs. We also found weak fitness costs associated with sib‐mating. As such, the sex‐biased dispersal that we found is probably sufficient to mitigate these costs. These results imply that kin discrimination has probably evolved for purposes other than mate choice, such as superparasitism avoidance.

  • Speciation history of European (Anguilla anguilla) and American eel (A. rostrata), analysed using genomic data
    Mol. Ecol. (IF 5.855) Pub Date : 2020-01-02
    Natacha Nikolic; Shenglin Liu; Magnus W. Jacobsen; Bjarni Jónsson; Louis Bernatchez; Pierre‐Alexandre Gagnaire; Michael M. Hansen

    Speciation in the ocean could differ from terrestrial environments due to fewer barriers to gene flow. Hence, sympatric speciation might be common, with American and European eel being candidates for exemplifying this. They show disjunct continental distributions on both sides of the Atlantic, but spawn in overlapping regions of the Sargasso Sea from where juveniles are advected to North American, European and North African coasts. Hybridization and introgression are known to occur, with hybrids almost exclusively observed in Iceland. Different speciation scenarios have been suggested, involving either vicariance or sympatric ecological speciation. Using RAD sequencing and whole‐genome sequencing data from parental species and F1 hybrids, we analysed speciation history based on the joint allele frequency spectrum (JAFS) and pairwise sequentially Markovian coalescent (PSMC) plots. JAFS supported a model involving a split without gene flow 150,000–160,000 generations ago, followed by secondary contact 87,000–92,000 generations ago, with 64% of the genome experiencing restricted gene flow. This supports vicariance rather than sympatric speciation, likely associated with Pleistocene glaciation cycles and ocean current changes. Whole‐genome PSMC analysis of F1 hybrids from Iceland suggested divergence 200,000 generations ago and indicated subsequent gene flow rather than strict isolation. Finally, simulations showed that results from both approaches (JAFS and PSMC) were congruent. Hence, there is strong evidence against sympatric speciation in North Atlantic eels. These results reiterate the need for careful consideration of cases of possible sympatric speciation, as even in seemingly barrier‐free oceanic environments palaeoceanographic factors may have promoted vicariance and allopatric speciation.

  • Telomere length is repeatable, shortens with age and reproductive success, and predicts remaining lifespan in a long‐lived seabird
    Mol. Ecol. (IF 5.855) Pub Date : 2020-01-02
    Coraline Bichet; Sandra Bouwhuis; Christina Bauch; Simon Verhulst; Peter H. Becker; Oscar Vedder

    Telomeres are protective caps at the end of chromosomes, and their length is positively correlated with individual health and lifespan across taxa. Longitudinal studies have provided mixed results regarding the within‐individual repeatability of telomere length. While some studies suggest telomere length to be highly dynamic and sensitive to resource‐demanding or stressful conditions, others suggest that between‐individual differences are mostly present from birth and relatively little affected by the later environment. This dichotomy could arise from differences between species, but also from methodological issues. In our study, we used the highly reliable Terminal Restriction Fragment analysis method to measure telomeres over a 10‐year period in adults of a long‐lived seabird, the common tern (Sterna hirundo). Telomeres shortened with age within individuals. The individual repeatability of age‐dependent telomere length was high (>0.53), and independent of the measurement interval (i.e., one vs. six years). A small (R2 = .01), but significant part of the between‐individual variation in telomere length was, however, explained by the number of fledglings produced in the previous year, while reproduction in years prior to the previous year had no effect. We confirmed that age‐dependent telomere length predicted an individual's remaining lifespan. Overall, our study suggests that the majority of between‐individual variation in adult telomere length is consistent across adult life, and that a smaller part of the variation can be explained by dynamic factors, such as reproduction.

  • Temperature‐mediated shifts in salamander transcriptomic responses to the amphibian‐killing fungus
    Mol. Ecol. (IF 5.855) Pub Date : 2020-01-01
    Amy Ellison; Kelly Zamudio; Karen Lips; Carly Muletz‐Wolz

    Life processes of ectothermic vertebrates are intimately linked to the temperature of their environment, influencing their metabolism, reproduction, behaviour and immune responses. In amphibians infected by the generalist chytrid pathogen Batrachochytrium dendrobatidis (Bd), host survival, infection prevalence and infection intensity are often temperature‐ and/or seasonally dependent. However, the transcriptional underpinnings of thermal differences in infection responses remain unknown. Measuring the impact of temperature on host responses to infection is a key component for understanding climatic influences on chytrid disease dynamics. The Bd‐responsive gene pathways in frogs are well documented, but our understanding of salamander immune expression profiles during infection with chytrids remains limited. Here we characterize the transcriptomic responses of Plethodon cinereus using RNA sequencing by comparing skin and splenic gene expression of individuals uninfected, succumbing to Bd infection and naturally cleared of Bd infection at three temperatures. We suggest that amphibian temperature‐dependent susceptibility to Bd is probably driven by shifts in expression of the innate and adaptive immune axes. Our study shows increased expression of transcripts associated with inflammation at lower temperatures and a shift towards increased expression of adaptive immune genes, including MHC (major histocompatibility complex), at higher temperatures. In the face of climate change, and as concerns for the spread of emergent chytrid pathogens increase, our results provide important functional genomic resources to help understand how these pathogenic fungi may continue to affect amphibian communities globally in the future.

  • Transcriptomic signatures of social experience during early development in a highly social cichlid fish
    Mol. Ecol. (IF 5.855) Pub Date : 2019-12-30
    Cecilia Nyman; Francois Olivier Hebert; Mathilde Bessert‐Nettelbeck; Nadia Aubin‐Horth; Barbara Taborsky

    The social environment encountered early during development can temporarily or permanently influence life history decisions and behaviour of individuals and correspondingly shape molecular pathways. In the highly social cichlid fish Neolamprologus pulcher, deprivation of brood care permanently affects social behaviour and alters the expression of stress axis genes in juveniles and adults. It is unclear when gene expression patterns change during early life depending on social experience, and which genes are involved. We compared brain gene expression of N. pulcher at two time points during the social experience phase when juveniles were reared either with or without brood care, and one time point shortly afterwards. We compared (a) whole transcriptomes and (b) expression of 79 genes related to stress regulation, in order to define a neurogenomic state of stress for each fish. At developmental day 75, that is, after the social experience phase, 43 genes were down‐regulated in fish having experienced social deprivation, while two genes involved in learning and memory and in post‐translational modifications of proteins (PTM), respectively, were up‐regulated. Down‐regulated genes were mainly associated with immunity, PTM and brain function. In contrast, during the experience phase no genes were differentially expressed when assessing the whole transcriptome. When focusing on the neurogenomic state associated with the stress response, we found that individuals from the two social treatments differed in how their brain gene expression profiles changed over developmental stages. Our results indicate that the early social environment influences the transcriptional activation in fish brains, both during and after an early social experience, possibly affecting plasticity, immune system function and stress axis regulation.

  • Molecular responses to freshwater limitation in the mangrove tree Avicennia germinans (Acanthaceae)
    Mol. Ecol. (IF 5.855) Pub Date : 2019-12-30
    Mariana Vargas Cruz; Gustavo Maruyama Mori; Dong‐Ha Oh; Maheshi Dassanayake; Maria Imaculada Zucchi; Rafael Silva Oliveira; Anete Pereira de Souza

    Environmental variation along the geographical space can shape populations by natural selection. In the context of global warming and changing precipitation regimes, it is crucial to understand the role of environmental heterogeneity in tropical trees adaptation, given their disproportional contribution to water and carbon biogeochemical cycles. Here, we investigated how heterogeneity in freshwater availability along tropical wetlands has influenced molecular variations of the black mangrove (Avicennia germinans). A total of 57 trees were sampled at seven sites differing markedly in precipitation regime and riverine freshwater inputs. Using 2,297 genome‐wide single nucleotide polymorphic markers, we found signatures of natural selection by the association between variations in allele frequencies and environmental variables, including the precipitation of the warmest quarter and the annual precipitation. Additionally, we found candidate loci for selection based on statistical deviations from neutral expectations of interpopulation differentiation. Most candidate loci within transcribed sequences were functionally associated with central aspects of drought tolerance or plant response to drought. Moreover, our results suggest the occurrence of the rapid evolution of a population, probably in response to sudden and persistent limitations in plant access to soil water, following a road construction in 1974. Observations supporting rapid evolution included the reduction in tree size and changes in allele frequencies and in transcript expression associated with increased drought tolerance through the accumulation of osmoprotectants and antioxidants, biosynthesis of cuticles, protection against protein degradation, stomatal closure, photorespiration and photosynthesis. We describe a major role of spatial heterogeneity in freshwater availability in the specialization of this typically tropical tree.

  • Among‐family variation in survival and gene expression uncovers adaptive genetic variation in a threatened fish
    Mol. Ecol. (IF 5.855) Pub Date : 2019-12-29
    Avril M. Harder; Janna R. Willoughby; William R. Ardren; Mark R. Christie

    Variation in among‐family transcriptional responses to different environmental conditions can help to identify adaptive genetic variation, even prior to a selective event. Coupling differential gene expression with formal survival analyses allows for the disentanglement of treatment effects, required for understanding how individuals plastically respond to environmental stressors, from the adaptive genetic variation responsible for differential survival. We combined these two approaches to investigate responses to an emerging conservation issue, thiamine (vitamin B1) deficiency, in a threatened population of Atlantic salmon (Salmo salar). Thiamine is an essential vitamin that is increasingly limited in many ecosystems. In Lake Champlain, Atlantic salmon cannot acquire thiamine in sufficient quantities to support natural reproduction; fertilized eggs must be reared in hatcheries and treated with supplemental thiamine. We evaluated transcriptional responses (via RNA sequencing) to thiamine treatment across families and found 3,616 genes differentially expressed between control (no supplemental thiamine) and treatment individuals. Fewer genes changed expression equally across families (i.e., additively) than exhibited genotype × environment interactions in response to thiamine. Differentially expressed genes were related to known physiological effects of thiamine deficiency, including oxidative stress, cardiovascular irregularities and neurological abnormalities. We also identified 1,446 putatively adaptive genes that were strongly associated with among‐family survival in the absence of thiamine treatment, many of which related to neurogenesis and visual perception. Our results highlight the utility of coupling RNA sequencing with formal survival analyses to identify candidate genes that underlie the among‐family variation in survival required for an adaptive response to natural selection.

  • Genomic processes underlying rapid adaptation of a natural Chironomus riparius population to unintendedly applied experimental selection pressures
    Mol. Ecol. (IF 5.855) Pub Date : 2019-12-30
    Markus Pfenninger; Quentin Foucault

    Evolve and Resquence (E&R) studies are a useful tool to study genomic processes during rapid adaptation, e.g. in the framework of adaptive responses to global climate change. We applied different thermal regimes to a natural Chironomus riparius (Diptera) population in an E&R framework to infer its evolutionary potential for rapid thermal adaptation. We exposed two replicates to three temperatures each (14°C, 20°C and 26°C) for more than two years, the experiment thus lasting 22, 44 or 65 generations, respectively. The two higher temperatures presented a priori moderate, respectively strong selection pressures.

  • Transitions in paternal social status predict patterns of offspring growth and metabolic transcription
    Mol. Ecol. (IF 5.855) Pub Date : 2019-12-29
    Joseph W. Cauceglia; Adam C. Nelson; Nimrod D. Rubinstein; Shweta Kukreja; Lynsey N. Sasso; John A. Beaufort; Oliver J. Rando; Wayne K. Potts

    One type of parental effect occurs when changes in parental phenotype or environment triggers changes to offspring phenotype. Such nongenetic parental effects can be precisely triggered in response to an environmental cue in time‐locked fashion, or in other cases, persist for multiple generations after the cue has been removed, suggesting multiple timescales of action. For parental effects to serve as reliable signals of current environmental conditions, they should be reversible, such that when cues changes, offspring phenotypes change in accordance. Social hierarchy is a prevalent feature of the environment, and current parental social status could signal the environment in which offspring will be born. Here, we sought to address parental effects of social status and their timescale of action in mice. We show that territorial competition in seminatural environments affects offspring growth. Although dominant males are not heavier than nondominant or control males, they produce faster growing offspring, particularly sons. The timing, effect‐size, and sex‐specificity of this association are modulated by maternal social experience. We show that a change in paternal social status is sufficient to modulate offspring weight: from one breeding cycle to the next, status‐ascending males produce heavier sons than before, and status‐descending males produce lighter sons than before. Current paternal status is also highly predictive of liver transcription in sons, including molecular pathways controlling oxidative phosphorylation and iron metabolism. These results are consistent with a parental effect of social experience, although alternative explanations are considered. In summary, changes in paternal social status are associated with changes in offspring growth and metabolism.

  • Genetic consequences of plant edaphic specialization to solfatara fields: Phylogenetic and population genetic analysis of Carex angustisquama (Cyperaceae)
    Mol. Ecol. (IF 5.855) Pub Date : 2019-12-27
    Koki Nagasawa; Hiroaki Setoguchi; Masayuki Maki; Hayato Goto; Keitaro Fukushima; Yuji Isagi; Yoshihisa Suyama; Ayumi Matsuo; Yoshihiro Tsunamoto; Kazuhiro Sawa; Shota Sakaguchi

    Edaphic specialization is one of the main drivers of plant diversification and has multifaceted effects on population dynamics. Carex angustisquama is a sedge plant growing only on heavily acidified soil in solfatara fields, where only extremophytes can survive. Because of the lack of closely related species in similar habitats and its disjunct distribution, the species offers ideal settings to investigate the effects of adaptation to solfatara fields and of historical biogeography on the genetic consequences of plant edaphic specialization to solfatara fields. Here, genome‐wide single nucleotide polymorphisms were used to reveal the phylogenetic origin of C. angustisquama, and 16 expressed sequence tag–simple sequence repeat markers were employed to infer population demography of C angustisquama. Molecular phylogenetic analysis strongly indicated that C. angustisquama formed a monophyletic clade with Carex doenitzii, a species growing on nonacidified soil in the sympatric subalpine zone. The result of population genetic analysis showed that C. angustisquama has much lower genetic diversity than the sister species, and notably, all 16 loci were completely homozygous in most individuals of C. angustisquama. Approximate Bayesian computation analysis supported the model that assumed hierarchical declines of population size through its evolutionary sequence. We propose that the edaphic specialist in solfatara fields has newly attained the adaptation to solfatara fields in the process of speciation. Furthermore, we found evidence of a drastic reduction in genetic diversity in C. angustisquama, suggesting that the repeated founder effects associated with edaphic specialization and subsequent population demography lead to the loss of genetic diversity of this extremophyte in solfatara fields.

  • Strong divergent selection at multiple loci in two closely related species of ragworts adapted to high and low elevations on Mount Etna
    Mol. Ecol. (IF 5.855) Pub Date : 2019-12-24
    Edgar L. Y. Wong; Bruno Nevado; Owen G. Osborne; Alexander S. T. Papadopulos; Jon R. Bridle; Simon J. Hiscock; Dmitry A. Filatov

    Recently diverged species present particularly informative systems for studying speciation and maintenance of genetic divergence in the face of gene flow. We investigated speciation in two closely related Senecio species, S. aethnensis and S. chrysanthemifolius, which grow at high and low elevations, respectively, on Mount Etna, Sicily and form a hybrid zone at intermediate elevations. We used a newly generated genome‐wide single nucleotide polymorphism (SNP) dataset from 192 individuals collected over 18 localities along an elevational gradient to reconstruct the likely history of speciation, identify highly differentiated SNPs, and estimate the strength of divergent selection. We found that speciation in this system involved heterogeneous and bidirectional gene flow along the genome, and species experienced marked population size changes in the past. Furthermore, we identified highly‐differentiated SNPs between the species, some of which are located in genes potentially involved in ecological differences between species (such as photosynthesis and UV response). We analysed the shape of these SNPs’ allele frequency clines along the elevational gradient. These clines show significantly variable coincidence and concordance, indicative of the presence of multifarious selective forces. Selection against hybrids is estimated to be very strong (0.16–0.78) and one of the highest reported in literature. The combination of strong cumulative selection across the genome and previously identified intrinsic incompatibilities probably work together to maintain the genetic and phenotypic differentiation between these species – pointing to the importance of considering both intrinsic and extrinsic factors when studying divergence and speciation.

  • Marine species formation along the rise of Central America: The anomuran crab Megalobrachium
    Mol. Ecol. (IF 5.855) Pub Date : 2019-12-23
    Alexandra Hiller; Harilaos A. Lessios

    The evolution of marine neotropical shallow water species is expected to have been greatly affected by physical events related to the emergence of the Central American Isthmus. The anomuran crab Megalobrachium, a strictly neotropical porcellanid genus, consists of four species in the West Atlantic (WA) and nine in the East Pacific (EP). Dispersal is limited to a relatively short planktonic phase, which lasts approximately two weeks. We obtained DNA sequences of three mitochondrial and two nuclear genes of all but one species of Megalobrachium to construct a time‐calibrated phylogeny of the genus and its historical phylogeography, based on the reconstruction of ancestral areas. The topology of the phylogenetic trees of Megalobrachium produced by Bayesian Inference (BI) and Maximum Likelihood (ML) were virtually congruent. The genus is monophyletic with respect to other porcellanids. Ancestral area reconstruction indicates that it arose in the eastern Pacific 18 million years ago and diversified into at least 13 species that are currently formally recognized and three additional species indicated by our data. Most morphological variation appears to have followed phylogenetic differentiation, though some cryptic speciation has also occurred. Four geminate clades in this genus implicate the gradual emergence of the Central American Isthmus in this diversification, but events preceding the final separation of the oceans as well as within‐ocean events after the cessation of water connections were also important.

  • Absence of founder effect and evidence for adaptive divergence in a recently introduced insular population of white‐tailed deer (Odocoileus virginianus)
    Mol. Ecol. (IF 5.855) Pub Date : 2019-12-20
    Jérémie Fuller; Anne‐Laure Ferchaud; Martin Laporte; Jérémy Le Luyer; Theodore B. Davis; Steeve D. Côté; Louis Bernatchez

    Islands are generally colonized by few individuals which could lead to a founder effect causing loss of genetic diversity and rapid divergence by strong genetic drift. Insular conditions can also induce new selective pressures on populations. Here, we investigated the extent of genetic differentiation within a white‐tailed deer (Odocoileus virginianus) population introduced on an island and its differentiation with its source mainland population. In response to their novel environmental conditions, introduced deer changed phenotypically from mainland individuals, therefore we investigated the genetic bases of the morphological differentiation. The study was conducted on Anticosti Island (Québec, Canada) where 220 individuals were introduced 120 years ago, resulting in a population size over 160,000 individuals. We used genotyping‐by‐sequencing (GBS) to generate 8,518 filtered high‐quality SNPs and compared patterns of genetic diversity and differentiation between the continental and Anticosti Island populations. Clustering analyses indicated a single panmictic island population and no sign of isolation by distance. Our results revealed a weak, albeit highly significant, genetic differentiation between the Anticosti Island population and its source population (mean FST = 0.005), which allowed a population assignment success of 93%. Also, the high genetic diversity maintained in the introduced population supports the absence of a strong founder effect due to the large number of founders followed by rapid population growth. We further used a polygenic approach to assess the genetic bases of the divergent phenotypical traits between insular and continental populations. We found loci related to muscular function and lipid metabolism, which suggested that these could be involved in local adaptation on Anticosti Island. We discuss these results in a harvest management context.

  • Into the bloom: Molecular response of pelagic tunicates to fluctuating food availability
    Mol. Ecol. (IF 5.855) Pub Date : 2019-12-18
    Paolo Sordino; Salvatore D'Aniello; Eric Pelletier; Patrick Wincker; Valeria Nittoli; Lars Stemmann; Maria Grazia Mazzocchi; Fabien Lombard; Daniele Iudicone; Luigi Caputi

    The planktonic tunicates appendicularians and thaliaceans are highly efficient filter feeders on a wide range of prey size including bacteria and have shorter generation times than any other marine grazers. These traits allow some tunicate species to reach high population densities and ensure their success in a favourable environment. However, there are still few studies focusing on which genes and gene pathways are associated with responses of pelagic tunicates to environmental variability. Herein, we present the effect of food availability increase on tunicate community and gene expression at the Marquesas Islands (South‐East Pacific Ocean). By using data from the Tara Oceans expedition, we show that changes in phytoplankton density and composition trigger the success of a dominant larvacean species (an undescribed appendicularian). Transcriptional signature to the autotroph bloom suggests key functions in specific physiological processes, i.e., energy metabolism, muscle contraction, membrane trafficking, and proteostasis. The relative abundance of reverse transcription‐related Pfams was lower at bloom conditions, suggesting a link with adaptive genetic diversity in tunicates in natural ecosystems. Downstream of the bloom, pelagic tunicates were outcompeted by copepods. Our work represents the first metaomics study of the biological effects of phytoplankton bloom on a key zooplankton taxon.

  • Efficient but occasionally imperfect vertical transmission of gut mutualistic protists in a wood‐feeding termite
    Mol. Ecol. (IF 5.855) Pub Date : 2019-12-17
    Caroline Michaud; Vincent Hervé; Simon Dupont; Géraldine Dubreuil; Annie M. Bézier; Joël Meunier; Andreas Brune; Franck Dedeine

    Although mutualistic associations between animals and microbial symbionts are widespread in nature, the mechanisms that have promoted their evolutionary persistence remain poorly understood. A vertical mode of symbiont transmission (from parents to offspring) is thought to ensure partner fidelity and stabilization, although the efficiency of vertical transmission has rarely been investigated, especially in cases where hosts harbour a diverse microbial community. Here we evaluated vertical transmission rates of cellulolytic gut oxymonad and parabasalid protists in the wood‐feeding termite Reticulitermes grassei. We sequenced amplicons of the 18S rRNA gene of protists from 24 colonies of R. grassei collected in two populations. For each colony, the protist community was characterized from the gut of 14 swarming reproductives and from a pool of 10 worker guts. A total of 98 operational taxonomic units belonging to 13 species‐level taxa were found. The vertical transmission rate was estimated for each protist present in a colony based on its frequency among the reproductives. The results revealed that transmission rates were high, with an average of 0.897 (±0.164) per protist species. Overall, the protist community did not differ between reproductive sexes, suggesting that both the queen and the king could contribute to the gut microbiota of the offspring. A positive relationship between the transmission rate of protists and their prevalence within populations was also detected. However, transmission rates alone do not explain the prevalence of protists. In conclusion, these findings reveal key forces behind a conserved, multispecies mutualism, raising further questions on the roles of horizontal transfer and negative selection in shaping symbiont prevalence.

  • Two reproductive traits show contrasting genetic architectures in Plantago lanceolata
    Mol. Ecol. (IF 5.855) Pub Date : 2019-12-17
    Matthew M. Marshall; David L. Remington; Elizabeth P. Lacey

    In many species, temperature‐sensitive phenotypic plasticity (i.e., an individual's phenotypic response to temperature) displays a positive correlation with latitude, a pattern presumed to reflect local adaptation. This geographical pattern raises two general questions: (a) Do a few large‐effect genes contribute to latitudinal variation in a trait? (b) Is the thermal plasticity of different traits regulated pleiotropically? To address the questions, we crossed individuals of Plantago lanceolata derived from northern and southern European populations. Individuals naturally exhibited high and low thermal plasticity in floral reflectance and flowering time. We grew parents and offspring in controlled cool‐ and warm‐temperature environments, mimicking what plants would encounter in nature. We obtained genetic markers via genotype‐by‐sequencing, produced the first recombination map for this ecologically important nonmodel species, and performed quantitative trait locus (QTL) mapping of thermal plasticity and single‐environment values for both traits. We identified a large‐effect QTL that largely explained the reflectance plasticity differences between northern and southern populations. We identified multiple smaller‐effect QTLs affecting aspects of flowering time, one of which affected flowering time plasticity. The results indicate that the genetic architecture of thermal plasticity in flowering is more complex than for reflectance. One flowering time QTL showed strong cytonuclear interactions under cool temperatures. Reflectance and flowering plasticity QTLs did not colocalize, suggesting little pleiotropic genetic control and freedom for independent trait evolution. Such genetic information about the architecture of plasticity is environmentally important because it informs us about the potential for plasticity to offset negative effects of climate change.

  • Spatiotemporal landscape genetics: Investigating ecology and evolution through space and time
    Mol. Ecol. (IF 5.855) Pub Date : 2019-12-17
    Lindsey E. Fenderson; Adrienne I. Kovach; Bastien Llamas

    Genetic time‐series data from historical samples greatly facilitate inference of past population dynamics and species evolution. Yet, although climate and landscape change are often touted as post‐hoc explanations of biological change, our understanding of past climate and landscape change influences on evolutionary processes is severely hindered by the limited application of methods that directly relate environmental change to species dynamics through time. Increased integration of spatiotemporal environmental and genetic data will revolutionize the interpretation of environmental influences on past population processes and the quantification of recent anthropogenic impacts on species, and vastly improve prediction of species responses under future climate change scenarios, yielding widespread revelations across evolutionary biology, landscape ecology and conservation genetics. This review encourages greater use of spatiotemporal landscape genetic analyses that explicitly link landscape, climate and genetic data through time by providing an overview of analytical approaches for integrating historical genetic and environmental data in five key research areas: population genetic structure, demography, phylogeography, metapopulation connectivity and adaptation. We also include a tabular summary of key methodological information, suggest approaches for mitigating the particular difficulties in applying these techniques to ancient DNA and palaeoclimate data, and highlight areas for future methodological development.

  • Molecular and behavioural evidence that interdependent photo ‐ and chemosensory systems regulate larval settlement in a marine sponge
    Mol. Ecol. (IF 5.855) Pub Date : 2019-12-16
    Tahsha E. Say; Sandie M. Degnan

    Marine pelagic larvae use a hierarchy of environmental cues to identify a suitable benthic habitat on which to settle and metamorphose into the adult phase of the life cycle. Most larvae are induced to settle by biochemical cues and many species have long been known to preferentially settle in the dark. Combined, these data suggest that larval responses to light and biochemical cues may be linked, but this has yet to be explored at the molecular level. Here, we track the vertical position of larvae of the sponge Amphimedon queenslandica to show that they descend to the benthos at twilight, by which time they are competent to respond to biochemical cues, consistent with them naturally settling in the dark. We use larval settlement assays under three different light regimes, combined with transcriptomics on individual larvae, to identify candidate molecular pathways underlying larval settlement. We find that larvae do not settle in response to biochemical cues if maintained in constant light. Our transcriptome data suggest that constant light actively represses settlement via the sustained up‐regulation of two putative inactivators of chemotransduction in constant light only. Our data suggest that photo‐ and chemosensory systems interact to regulate larval settlement via nitric oxide and cyclic guanosine monophosphate signalling in this sponge, which belongs to one of the earliest‐branching animal phyla.

  • Decomposing demographic contributions to the effective population size with moose as a case study
    Mol. Ecol. (IF 5.855) Pub Date : 2019-12-13
    Aline Magdalena Lee; Ane Marlene Myhre; Stine Svalheim Markussen; Steinar Engen; Erling Johan Solberg; Hallvard Haanes; Knut Røed; Ivar Herfindal; Morten Heim; Bernt‐Erik Sæther

    Levels of random genetic drift are influenced by demographic factors, such as mating system, sex ratio and age structure. The effective population size (Ne) is a useful measure for quantifying genetic drift. Evaluating relative contributions of different demographic factors to Ne is therefore important to identify what makes a population vulnerable to loss of genetic variation. Until recently, models for estimating Ne have required many simplifying assumptions, making them unsuitable for this task. Here, using data from a small, harvested moose population, we demonstrate the use of a stochastic demographic framework allowing for fluctuations in both population size and age distribution to estimate and decompose the total demographic variance and hence the ratio of effective to total population size (Ne/N) into components originating from sex, age, survival and reproduction. We not only show which components contribute most to Ne/N currently, but also which components have the greatest potential for changing Ne/N. In this relatively long‐lived polygynous system we show that Ne/N is most sensitive to the demographic variance of older males, and that both reproductive autocorrelations (i.e., a tendency for the same individuals to be successful several years in a row) and covariance between survival and reproduction contribute to decreasing Ne/N (increasing genetic drift). These conditions are common in nature and can be caused by common hunting strategies. Thus, the framework presented here has great potential to increase our understanding of the demographic processes that contribute to genetic drift and viability of populations, and to inform management decisions.

  • An explicit test of Pleistocene survival in peripheral versus nunatak refugia in two high mountain plant species
    Mol. Ecol. (IF 5.855) Pub Date : 2019-12-12
    Da Pan; Karl Hülber; Wolfgang Willner; Gerald M. Schneeweiss

    Pleistocene climate fluctuations had profound influence on the biogeographical history of many biota. As large areas in high mountain ranges were covered by glaciers, biota were forced either to peripheral refugia (and possibly beyond to lowland refugia) or to interior refugia (nunataks). However, nunatak survival remains controversial as it relies solely on correlative genetic evidence. Here, we test hypotheses of glacial survival using two high alpine plant species (the insect‐pollinated Pedicularis asplenifolia and wind‐pollinated Carex fuliginosa) in the European Alps. Employing the iDDC (integrative Distributional, Demographic and Coalescent) approach, which couples species distribution modelling, spatial and temporal demographic simulation and Approximate Bayesian Computation, we explicitly test three hypotheses of glacial survival: (a) peripheral survival only, (b) nunatak survival only and (c) peripheral plus nunatak survival. In P. asplenifolia the peripheral plus nunatak survival hypothesis was supported by Bayes factors (BF> 100), whereas in C. fuliginosa the peripheral survival only hypothesis, although best supported, could not be unambiguously distinguished from the peripheral plus nunatak survival hypothesis (BF = 5.58). These results are consistent with current habitat preferences (P. asplenifolia extends to higher elevations) and the potential for genetic swamping (i.e., replacement of local genotypes via hybridization with immigrating genotypes [expected to be higher in the wind‐pollinated C. fuliginosa]). Although the persistence of plants on nunataks during glacial periods has been debated and studied over decades, this is one of the first studies to explicitly test the hypothesis instead of solely using correlative evidence.

  • Genomic footprints of a biological invasion: Introduction from Asia and dispersal in Europe of the topmouth gudgeon (Pseudorasbora parva)
    Mol. Ecol. (IF 5.855) Pub Date : 2019-12-10
    Miguel Baltazar‐Soares, Simon Blanchet, Julien Cote, Ali S. Tarkan, Eva Záhorská, Rodolphe E. Gozlan, Christophe Eizaguirre

    Facilitated by the intensification of global trading, the introduction and dispersal of species to areas in which they are historically non‐native is nowadays common. From an evolutionary standpoint, invasions are paradoxical: not only non‐native environments could be different from native ones for which introduced individuals would be ill‐adapted, but also small founding population size should be associated with reduced adaptive potential. As such, biological invasions are considered valuable real‐time evolutionary experiments. Here, we investigated the population structure and adaptive potential of the highly invasive topmouth gudgeon (Pseudorasbora parva) across Europe and East Asia. We RAD‐sequenced 301 specimens from sixteen populations and three distinct within‐catchment invaded regions as well as two locations in the native range. With 13,785 single nucleotide polymorphisms, we provide conclusive evidence for a genome‐wide signature of two distinct invasion events, in Slovakia and Turkey, each originating from a specific area in the native range. A third invaded area, in France, appears to be the result of dispersal within the invasive range. Few loci showed signs of selection, the vast majority of which being identified in the Slovakian region. Functional annotation suggests that faster early stage development, resistance to pollution and immunocompetence contribute to the invasion success of the local habitats. By showing that populations in the invasive range have different evolutionary histories, our study reinforces the idea that populations, rather than species, are the units to consider in invasion biology.

  • Genotypic variation in Norway spruce correlates to fungal communities in vegetative buds
    Mol. Ecol. (IF 5.855) Pub Date : 2019-12-09
    Malin Elfstrand, Linghua Zhou, John Baison, Åke Olson, Karl Lundén, Bo Karlsson, Harry X. Wu, Jan Stenlid, M. Rosario García‐Gil

    The taxonomically diverse phyllosphere fungi inhabit leaves of plants. Thus, apart from the fungi's dispersal capacities and environmental factors, the assembly of the phyllosphere community associated with a given host plant depends on factors encoded by the host's genome. The host genetic factors and their influence on the assembly of phyllosphere communities under natural conditions are poorly understood, especially in trees. Recent work indicates that Norway spruce (Picea abies) vegetative buds harbour active fungal communities, but these are hitherto largely uncharacterized. This study combines internal transcribed spacer sequencing of the fungal communities associated with dormant vegetative buds with a genome‐wide association study (GWAS) in 478 unrelated Norway spruce trees. The aim was to detect host loci associated with variation in the fungal communities across the population, and to identify loci correlating with the presence of specific, latent, pathogens. The fungal communities were dominated by known Norway spruce phyllosphere endophytes and pathogens. We identified six quantitative trait loci (QTLs) associated with the relative abundance of the dominating taxa (i.e., top 1% most abundant taxa). Three additional QTLs associated with colonization by the spruce needle cast pathogen Lirula macrospora or the cherry spruce rust (Thekopsora areolata) in asymptomatic tissues were detected. The identification of the nine QTLs shows that the genetic variation in Norway spruce influences the fungal community in dormant buds and that mechanisms underlying the assembly of the communities and the colonization of latent pathogens in trees may be uncovered by combining molecular identification of fungi with GWAS.

  • An analysis of mating biases in trees
    Mol. Ecol. (IF 5.855) Pub Date : 2019-12-09
    Sascha A. Ismail, Hanna Kokko

    Assortative mating is a deviation from random mating based on phenotypic similarity. As it is much better studied in animals than in plants, we investigate for trees whether kinship of realized mating pairs deviates from what is expected from the set of potential mates and use this information to infer mating biases that may result from kin recognition and/or assortative mating. Our analysis covers 20 species of trees for which microsatellite data is available for adult populations (potential mates) as well as seed arrays. We test whether mean relatedness of observed mating pairs deviates from null expectations that only take pollen dispersal distances into account (estimated from the same data set). This allows the identification of elevated as well as reduced kinship among realized mating pairs, indicative of positive and negative assortative mating, respectively. The test is also able to distinguish elevated biparental inbreeding that occurs solely as a result of related pairs growing closer to each other from further assortativeness. Assortative mating in trees appears potentially common but not ubiquitous: nine data sets show mating bias with elevated inbreeding, nine do not deviate significantly from the null expectation, and two show mating bias with reduced inbreeding. While our data sets lack direct information on phenology, our investigation of the phenological literature for each species identifies flowering phenology as a potential driver of positive assortative mating (leading to elevated inbreeding) in trees. Since active kin recognition provides an alternative hypothesis for these patterns, we encourage further investigations on the processes and traits that influence mating patterns in trees.

  • Signature of sexual conflict is actually conflict resolved
    Mol. Ecol. (IF 5.855) Pub Date : 2019-12-09
    Judith E. Mank, Jacelyn J. Shu, Alison E. Wright

    There has been substantial interest of late in using population genetic methods to study sexual conflict, where an allele increases the fitness of one sex at some cost to the other (Mank, 2017). Population genomic scans for sexual conflict offer an important advance given the difficulties of identifying antagonistic alleles from more traditional methods, and could greatly increase our understanding of the extent and loci of sexual conflict. This is particularly true for studies in natural populations, for which obtaining accurate fitness measurements for each sex can be challenging. In this issue of Molecular Ecology, Bissegger, Laurentino, Roesti, and Berner (2019) present a cautionary tale about how to interpret these population genomic data.

  • Genome‐wide epigenetic isolation by environment in a widespread Anolis lizard
    Mol. Ecol. (IF 5.855) Pub Date : 2019-12-08
    Guinevere O. U. Wogan, Michael L. Yuan, D. Luke Mahler, Ian J. Wang

    Epigenetic changes can provide a pathway for organisms to respond to local environmental conditions by influencing gene expression. However, we still know little about the spatial distribution of epigenetic variation in natural systems, how it relates to the distribution of genetic variation and the environmental structure of the landscape, and the processes that generate and maintain it. Studies examining spatial patterns of genetic and epigenetic variation can provide valuable insights into how ecological and population processes contribute to epigenetic divergence across heterogeneous landscapes. Here, we perform a comparative analysis of spatial genetic and epigenetic variation based on 8,459 single nucleotide polymorphisms (SNPs) and 8,580 single methylation variants (SMVs) from eight populations of the Puerto Rican crested anole, Anolis cristatellus, an abundant lizard in the adaptive radiations of anoles on the Greater Antilles that occupies a diverse range of habitats. Using generalized dissimilarity modelling and multiple matrix regression, we found that genome‐wide epigenetic differentiation is strongly correlated with environmental divergence, even after controlling for the underlying genetic structure. We also detected significant associations between key environmental variables and 96 SMVs, including 42 located in promoter regions or gene bodies. Our results suggest an environmental basis for population‐level epigenetic differentiation in this system and contribute to better understanding how environmental gradients structure epigenetic variation in nature.

  • Evidence for a role of protein phosphorylation in the maintenance of the cnidarian–algal symbiosis
    Mol. Ecol. (IF 5.855) Pub Date : 2019-12-06
    Fabia Simona, Huoming Zhang, Christian R. Voolstra

    The endosymbiotic relationship between cnidarians and photosynthetic dinoflagellate algae provides the foundation of coral reef ecosystems. This essential interaction is globally threatened by anthropogenic disturbance. As such, it is important to understand the molecular mechanisms underpinning the cnidarian–algal association. Here we investigated phosphorylation‐mediated protein signalling as a mechanism of regulation of the cnidarian–algal interaction, and we report on the generation of the first phosphoproteome for the coral model system Aiptasia. Mass spectrometry‐based phosphoproteomics using data‐independent acquisition allowed consistent quantification of over 3,000 phosphopeptides totalling more than 1,600 phosphoproteins across aposymbiotic (symbiont‐free) and symbiotic anemones. Comparison of the symbiotic states showed distinct phosphoproteomic profiles attributable to the differential phosphorylation of 539 proteins that cover a broad range of functions, from receptors to structural and signal transduction proteins. A subsequent pathway enrichment analysis identified the processes of “protein digestion and absorption,” “carbohydrate metabolism,” and “protein folding, sorting and degradation,” and highlighted differential phosphorylation of the “phospholipase D signalling pathway” and “protein processing in the endoplasmic reticulum.” Targeted phosphorylation of the phospholipase D signalling pathway suggests control of glutamate vesicle trafficking across symbiotic compartments, and phosphorylation of the endoplasmic reticulum machinery suggests recycling of symbiosome‐associated proteins. Our study shows for the first time that changes in the phosphorylation status of proteins between aposymbiotic and symbiotic Aiptasia anemones may play a role in the regulation of the cnidarian–algal symbiosis. This is the first phosphoproteomic study of a cnidarian–algal symbiotic association as well as the first application of quantification by data‐independent acquisition in the coral field.

  • Negative frequency‐dependent selection maintains coexisting genotypes during fluctuating selection
    Mol. Ecol. (IF 5.855) Pub Date : 2019-12-05
    Caroline B. Turner, Sean W. Buskirk, Katrina B. Harris, Vaughn S. Cooper

    Natural environments are rarely static; rather selection can fluctuate on timescales ranging from hours to centuries. However, it is unclear how adaptation to fluctuating environments differs from adaptation to constant environments at the genetic level. For bacteria, one key axis of environmental variation is selection for planktonic or biofilm modes of growth. We conducted an evolution experiment with Burkholderia cenocepacia, comparing the evolutionary dynamics of populations evolving under constant selection for either biofilm formation or planktonic growth with populations in which selection fluctuated between the two environments on a weekly basis. Populations evolved in the fluctuating environment shared many of the same genetic targets of selection as those evolved in constant biofilm selection, but were genetically distinct from the constant planktonic populations. In the fluctuating environment, mutations in the biofilm‐regulating genes wspA and rpfR rose to high frequency in all replicate populations. A mutation in wspA first rose rapidly and nearly fixed during the initial biofilm phase but was subsequently displaced by a collection of rpfR mutants upon the shift to the planktonic phase. The wspA and rpfR genotypes coexisted via negative frequency‐dependent selection around an equilibrium frequency that shifted between the environments. The maintenance of coexisting genotypes in the fluctuating environment was unexpected. Under temporally fluctuating environments, coexistence of two genotypes is only predicted under a narrow range of conditions, but the frequency‐dependent interactions we observed provide a mechanism that can increase the likelihood of coexistence in fluctuating environments.

  • Demographic history has shaped the strongly differentiated corkwing wrasse populations in Northern Europe
    Mol. Ecol. (IF 5.855) Pub Date : 2019-12-04
    Morten Mattingsdal, Per Erik Jorde, Halvor Knutsen, Sissel Jentoft, Nils Christian Stenseth, Marte Sodeland, Joana I. Robalo, Michael M. Hansen, Carl André, Enrique Blanco Gonzalez

    Understanding the biological processes involved in genetic differentiation and divergence between populations within species is a pivotal aim in evolutionary biology. One particular phenomenon that requires clarification is the maintenance of genetic barriers despite the high potential for gene flow in the marine environment. Such patterns have been attributed to limited dispersal or local adaptation, and to a lesser extent to the demographic history of the species. The corkwing wrasse (Symphodus melops) is an example of a marine fish species where regions of particular strong divergence are observed. One such genetic break occurred at a surprisingly small spatial scale (FST ~0.1), over a short coastline (<60 km) in the North Sea‐Skagerrak transition area in southwestern Norway. Here, we investigate the observed divergence and purported reproductive isolation using genome resequencing. Our results suggest that historical events during the post‐glacial recolonization route can explain the present population structure of the corkwing wrasse in the northeast Atlantic. While the divergence across the break is strong, we detected ongoing gene flow between populations over the break suggesting recent contact or negative selection against hybrids. Moreover, we found few outlier loci and no clear genomic regions potentially being under selection. We concluded that neutral processes and random genetic drift e.g., due to founder events during colonization have shaped the population structure in this species in Northern Europe. Our findings underline the need to take into account the demographic process in studies of divergence processes.

  • SNP analyses reveal a diverse pool of potential colonists to earthquake‐uplifted coastlines
    Mol. Ecol. (IF 5.855) Pub Date : 2019-12-04
    Johnette C. Peters, Jonathan M. Waters, Ludovic Dutoit, Ceridwen I. Fraser

    In species that form dense populations, major disturbance events are expected to increase the chance of establishment for immigrant lineages. Real‐time tests of the impact of disturbance on patterns of genetic structure are, however, scarce. Central to testing these concepts is determining the pool of potential immigrants dispersing into a disturbed area. In 2016, a 7.8 magnitude earthquake occurred on the South Island of New Zealand. Affecting approximately 100 km of coastline, this quake caused extensive uplift (several metres high), extirpating many intertidal populations, including keystone intertidal kelp species. Following the uplift, we set out to determine the geographic origins of detached kelp specimens which rafted into the disturbed zone. Specifically, we used genotyping‐by‐sequencing (GBS) approaches to compare beach‐cast southern bull‐kelp (Durvillea antarctica and Durvillea poha) samples to established populations throughout the species' ranges, and thus infer the geographic origins of potential colonists reaching the disturbed coast. Our findings revealed an ongoing supply of diverse lineages dispersing to the newly uplifted coastline, suggesting potential for establishment of “exotic” lineages following disturbance. Furthermore, we found that some drifting individuals of each species came from far‐distant regions, some >1,200 km away. These results show that diverse lineages – in many cases from very distant sources – have potential to compete for new space in the wake of an exceptional disturbance event, illustrating the potential of long‐distance dispersal as a key mechanism for reassembly of coastal ecosystems. Furthermore, our findings demonstrate that high‐resolution genomic baselines can be used to robustly assign the provenance of dispersing individuals.

  • Diving into divergence: Differentiation in swimming performances, physiology and gene expression between locally‐adapted sympatric cichlid fishes
    Mol. Ecol. (IF 5.855) Pub Date : 2019-12-04
    Francesca Raffini, Ralf F. Schneider, Paolo Franchini, Andreas F. Kautt, Axel Meyer

    Sympatric speciation occurs without geographical barriers and is thought to often be driven by ecological specialization of individuals that eventually diverge genetically and phenotypically. Distinct morphologies between sympatric populations occupying different niches have been interpreted as such differentiating adaptive phenotypes, yet differences in performance and thus likely adaptiveness between them were rarely tested. Here, we investigated if divergent body shapes of two sympatric crater lake cichlid species from Nicaragua, one being a shore‐associated (benthic) species while the other prefers the open water zones (limnetic), affect cruising (Ucrit) and sprinting (Usprint) swimming abilities – performances particularly relevant to their respective lifestyles. Furthermore, we investigated species differences in oxygen consumption (MO2) across different swimming speeds and compare gene expression in gills and white muscle at rest and during exercise. We found a superior cruising ability in the limnetic Amphilophus zaliosus compared to the benthic Amphilophus astorquii, while sprinting was not different, suggesting that their distinct morphologies affect swimming performance. Increased cruising swimming ability in A. zaliosus was linked to a higher oxygen demand during activity (but not rest), indicating different metabolic rates during exercise ‐ a hypothesis supported by coinciding gene expression patterns of gill transcriptomes. We identified differentially expressed genes linked to swimming physiology, regulation of swimming behaviour and oxygen intake. A combination of physiological and morphological differences may thus underlie adaptations to these species' distinct niches. This complex ecological specialization probably resulted in morphological and physiological trade‐offs that contributed to the rapid establishment and maintenance of divergence with gene flow.

  • The origins and evolutionary history of feral apples in southern Canada
    Mol. Ecol. (IF 5.855) Pub Date : 2019-12-03
    Dane Cronin, Paul Kron, Brian C. Husband

    Feral populations of domesticated crops can establish through two nonmutually exclusive pathways: hybridization with native relatives and recruitment of and recombination between known cultivars. The extent and relative importance of these pathways is not known, especially for woody fruit crops. Here, we examined the evolutionary origins of feral populations of Malus domestica (domestic apple) in southern Canada using a population genetic analysis. We characterized genotypes of 578 putative feral apple trees and evaluated them in relation to genotypes of 156 commercial cultivars, 28 non‐native, ornamental crabapples and 47 native Malus coronaria trees using 14 microsatellite markers. No feral trees were genetic admixtures between domestic and native Malus; however, a minority of trees were admixed with introduced ornamental Malus. Feral trees and commercial cultivars both occurred in two major genetic groups and seven subgroups distributed throughout all commercial growing regions. A total of 42 cultivars, both heritage and currently grown, occurred in probably parental pairs for feral trees, with nine heritage varieties accounting for 72% of parental assignments. We conclude that feral apples in southern Canada are not products of hybridization with native M. coronaria but we cannot exclude ornamental apple species as contributing to the naturalization process. Nonhybrid feral domestic apples have multiple origins, with a prominent signature of early heritage cultivars. These lineages have spread and coexist throughout Ontario, rather than being derived strictly from local sources.

  • Climatic vulnerabilities and ecological preferences of soil invertebrates across biomes
    Mol. Ecol. (IF 5.855) Pub Date : 2019-12-03
    Felipe Bastida, David J. Eldridge, Sebastián Abades, Fernando D. Alfaro, Antonio Gallardo, Laura García‐Velázquez, Carlos García, Stephen C. Hart, Cecilia A. Pérez, Fernanda Santos, Pankaj Trivedi, Mark A. Williams, Manuel Delgado‐Baquerizo

    Unlike plants and vertebrates, the ecological preferences, and potential vulnerabilities of soil invertebrates to environmental change, remain poorly understood in terrestrial ecosystems globally. We conducted a cross‐biome survey including 83 locations across six continents to advance our understanding of the ecological preferences and vulnerabilities of the diversity of dominant and functionally important soil invertebrate taxa, including nematodes, arachnids and rotifers. The diversity of invertebrates was analyzed through amplicon sequencing. Vegetation and climate drove the diversity and dominant taxa of soil invertebrates. Our results suggest that declines in forest cover and plant diversity, and reductions in plant production associated with increases in aridity, can result in reductions of the diversity of soil invertebrates in a drier and more managed world. We further developed global atlases of the diversity of these important soil invertebrates, which were cross‐validated using an independent database. Our study advances the current knowledge of the ecological preferences and vulnerabilities of the diversity and presence of functionally important soil invertebrates in soils from across the globe. This information is fundamental for improving and prioritizing conservation efforts of soil genetic resources and management policies.

  • Free‐living and symbiotic lifestyles of a thermotolerant coral endosymbiont display profoundly distinct transcriptomes under both stable and heat stress conditions
    Mol. Ecol. (IF 5.855) Pub Date : 2019-12-02
    Anthony J. Bellantuono, Katherine E. Dougan, Camila Granados‐Cifuentes, Mauricio Rodriguez‐Lanetty

    Reef‐building corals depend upon a nutritional endosymbiosis with photosynthetic dinoflagellates of the family Symbiodiniaceae for the majority of their energetic needs. While this mutualistic relationship is impacted by numerous stressors, warming oceans are a predominant threat to coral reefs, placing the future of the world's reefs in peril. Some Symbiodiniaceae species exhibit tolerance to thermal stress, but the in hospite symbiont response to thermal stress is underexplored. To describe the underpinnings of symbiosis and heat stress response, we compared in hospite and free‐living transcriptomes of Durusdinium trenchii, a pan‐tropical heat‐tolerant Symbiodiniaceae species, under stable temperature conditions and acute hyperthermal stress. We discovered that symbiotic state was a larger driver of the transcriptional landscape than heat stress. The majority of differentially expressed transcripts between in hospite and free‐living cells were downregulated, suggesting the in hospite condition is associated with the shutdown of numerous processes uniquely required for a free‐living lifestyle. In the free‐living state, we identified enrichment for numerous cell signalling pathways and other functions related to detecting and responding to a changing environment, as well as transcripts relating to mitosis, meiosis, and motility. In contrast, in hospite cells exhibited enhanced transcriptional activity for photosynthesis and carbohydrate transport as well as chromatin modifications and a disrupted circadian clock. Hyperthermal stress induced drastic alteration of transcriptional activity in hospite, suggesting symbiotic engagement with the host elicited an exacerbated stress response when compared to free‐living D. trenchii. Altogether, the dramatic differences in gene expression between in hospite and free‐living D. trenchii indicate the importance of considering symbiotic state in investigations of symbiosis and hyperthermal stress in Symbiodiniaceae.

  • The fire ant social supergene is characterized by extensive gene and transposable element copy number variation
    Mol. Ecol. (IF 5.855) Pub Date : 2019-11-29
    Silvia Fontana, Ni‐Chen Chang, Tiffany Chang, Chih‐Chi Lee, Viet‐Dai Dang, John Wang

    In the fire ant Solenopsis invicta, a supergene composed of ~600 genes and having two variants, SB and Sb, regulates colony social form. In single queen colonies, all individuals carry only the SB allele, while in multiple queen colonies, some individuals carry the Sb allele. In this study, we characterized genes with copy number variation between SB and Sb‐carrying individuals. We showed extensive acquisition of gene duplicates in the Sb genome, with some likely involved in polygyne‐related phenotypes. We found 260 genes with copy number differences between SB and Sb, of which 239 have greater copy number in Sb. We observed transposable element (TE) accumulation on Sb, likely due to the accumulation of repetitive elements on the nonrecombining chromosome. We found a weak correlation between TE copy number and differential expression, suggesting some TEs may still be proliferating in Sb while many of the duplicated TEs have presumably been silenced. Among the 115 non‐TE genes with higher copy in Sb, enzymes responsible for cuticular hydrocarbon synthesis were highly represented. These include a desaturase and an elongase, both potentially responsible for differential queen odour and likely beneficial for polygyne ants. These genes seem to have translocated into the supergene from other chromosomes and proliferated by multiple duplication events. While the presence of TEs in supergenes is well documented, little is known about duplication of non‐TE genes and their possible adaptive role. Overall, our results suggest that gene duplications may be an important factor leading to monogyne and polygyne ant societies.

  • Unravelling virus community ecology in bats through the integration of metagenomics and community ecology
    Mol. Ecol. (IF 5.855) Pub Date : 2019-11-28
    Michelle Wille

    The spillover of viruses from wildlife into agricultural animals or humans has profound socioeconomic and public health impact. Vampire bats, found throughout South America, feed directly on humans and other animals and are an important reservoir for zoonotic viruses, including rabies virus. This has resulted in considerable effort in understanding both the ecology of bat‐borne viruses and the composition and associated correlates of the structure of entire virus communities in wildlife, particularly in the context of disease control interventions. In a From the Cover article in this issue of Molecular Ecology, Bergner et al. (2019) set out to reveal virus community dynamics in vampire bats by interrogating factors that affect the structure, diversity and richness of these communities. Due to the linkage of metagenomic sequence data with community ecology, this study represents an important advance in the field of virus ecology.

  • Climate‐dependent variation in cold tolerance of weedy rice and rice mediated by OsICE1 promoter methylation
    Mol. Ecol. (IF 5.855) Pub Date : 2019-11-25
    Hongjie Xie, Yihao Han, Xinyue Li, Weimin Dai, Xiaoling Song, Kenneth M. Olsen, Sheng Qiang

    The mechanisms by which weedy rice (Oryza sativa f. spontanea) has adapted to endure low‐temperature stress in northern latitudes remain unresolved. In this study, we assessed cold tolerance of 100 rice varieties and 100 co‐occurring weedy rice populations, which were sampled across a broad range of climates in China. A parallel pattern of latitude‐dependent variation in cold tolerance was detected in cultivated rice and weedy rice. At the molecular level, differential cold tolerance was strongly correlated with relative expression levels of CBF cold response pathway genes and with methylation levels in the promoter region of OsICE1, a regulator of this pathway. Among all methylated cytosine sites of the OsICE1 promoter, levels of CHG and CHH methylation were found to be significantly correlated with cold tolerance among accessions. Furthermore, within many of the collection locales, weedy rice shared identical or near‐identical OsICE1 methylation patterns with co‐occurring cultivated rice. These findings provide new insights on the possible roles that methylation variation in the OsICE1 promoter may play in cold tolerance, and they suggest that weedy rice can rapidly acquire cold tolerance via methylation patterns that are shared with co‐occurring rice cultivars.

  • Duplication and diversification of trehalase confers evolutionary advantages on lepidopteran insects
    Mol. Ecol. (IF 5.855) Pub Date : 2019-11-25
    Yanyan Zhou, Xiaotong Li, Susumu Katsuma, Yusong Xu, Liangen Shi, Toru Shimada, Huabing Wang

    Gene duplication provides a major source of new genes for evolutionary novelty and ecological adaptation. However, the maintenance of duplicated genes and their relevance to adaptive evolution has long been debated. Insect trehalase (Treh) plays key roles in energy metabolism, growth, and stress recovery. Here, we show that the duplication of Treh in Lepidoptera (butterflies and moths) is linked with their adaptation to various environmental stresses. Generally, two Treh genes are present in insects: Treh1 and Treh2. We report three distinct forms of Treh in lepidopteran insects, where Treh1 was duplicated into two gene clusters (Treh1a and Treh1b). These gene clusters differ in gene expression patterns, enzymatic properties, and subcellular localizations, suggesting that the enzymes probably underwent sub‐ and/or neofunctionalization in the lepidopteran insects. Interestingly, selective pressure analysis provided significant evidence of positive selection on duplicate Treh1b gene in lepidopteran insect lineages. Most positively selected sites were located in the alpha‐helical region, and several sites were close to the trehalose binding and catalytic sites. Subcellular adaptation of duplicate Treh1b driven by positive selection appears to have occurred as a result of selected changes in specific sequences, allowing for rapid reprogramming of duplicated Treh during evolution. Our results suggest that gene duplication of Treh and subsequent functional diversification could increase the survival rate of lepidopteran insects through various regulations of intracellular trehalose levels, facilitating their adaptation to diverse habitats. This study provides evidence regarding the mechanism by which gene family expansion can contribute to species adaptation through gene duplication and subsequent functional diversification.

  • Cohabitation and roommate bias of symbiotic bacteria in insect hosts
    Mol. Ecol. (IF 5.855) Pub Date : 2019-11-22
    Sharon E. Zytynska

    Symbiotic interactions between insects and bacteria have long fascinated ecologists. Aphids have emerged as the model system on which to study the effect of endosymbiotic bacteria on their hosts. Aphid‐symbiont interactions are ecologically interesting as aphids host multiple secondary symbionts that can provide broad benefits, such as protection against heat stress or specialist natural enemies (parasitic wasps and entomopathogenic fungi). There are nine common aphid secondary symbionts and individual aphids host on average 1–2 symbionts. A cost‐benefit trade‐off for hosting symbionts is thought to explain why not all aphids host every possible symbiont in a population. Both positive and negative associations between various symbionts occur, and this could happen due to increased costs when cohosting certain combinations or as a consequence of competitive interactions between the symbionts within a host. In this issue of Molecular Ecology, Mathé‐Hubert, Kaech, Hertaeg, Jaenike, and Vorburger (2019) use data on the symbiont status of field‐collected aphids to inform a model on the evolution of symbiont co‐occurrence. They vary the effective female population size as well as the rate of horizontal and maternal transmission to infer the relative impact of symbiont‐symbiont interactions versus random drift. Additional data analysis revisits an association between two symbionts in a fruit fly species using a long‐term data set to highlight that such interactions are not limited to aphids.

  • DNA barcodes expose unexpected diversity in Canadian mites
    Mol. Ecol. (IF 5.855) Pub Date : 2019-11-22
    Monica R. Young, Heather C. Proctor, Jeremy R. deWaard, Paul D. N. Hebert

    Mites (Arachnida: Acariformes, Parasitiformes) are the most abundant and species‐rich group of arthropods in soil, but are also diverse in freshwater habitats, on plants, and as symbionts of larger animals. However, assessment of their diversity has been impeded by their small size and often cryptic morphology. As a consequence, published estimates of their species richness span more than two orders of magnitude (0.4–114 million). In this study we employ DNA barcoding and the Barcode Index Number (BIN) system to investigate mite diversity at over 1,800 sites across Canada, primarily from soil and litter habitats with smaller contributions from freshwater, plants, and animal hosts. Barcodes from 73,394 specimens revealed 7,077 BINs with representatives from all four orders (Ixodida, Mesostigmata, Sarcoptiformes, Trombidiformes) and 60% (186) of the known families. The BIN total is 2.4 times the number of species previously recorded from Canada (2,999), reflecting the unexpectedly high richness of several families. Richness projections suggest that more than 28,000 BINs occur at the sampled locations, indicating that the Canadian mite fauna almost certainly includes more than 30,000 species—a total similar to that for the most diverse insect order in Canada, Diptera. This unexpected diversity was partitioned into highly dissimilar, spatially‐structured assemblages that likely reflect dispersal limitation and environmental heterogeneity. Further sampling of a greater diversity of habitats will refine understanding of mite diversity in Canada, but similar analyses in other geographic regions will be essential to ascertain their diversity at a global scale.

  • The complex evolutionary history of apricots: Species divergence, gene flow and multiple domestication events
    Mol. Ecol. (IF 5.855) Pub Date : 2019-11-22
    Shuo Liu, Amandine Cornille, Stéphane Decroocq, David Tricon, Aurélie Chague, Jean‐Philippe Eyquard, Wei‐Sheng Liu, Tatiana Giraud, Véronique Decroocq

    Domestication is an excellent model to study diversification and this evolutionary process can be different in perennial plants, such as fruit trees, compared to annual crops. Here, we inferred the history of wild apricot species divergence and of apricot domestication history across Eurasia, with a special focus on Central and Eastern Asia, based on microsatellite markers and approximate Bayesian computation. We significantly extended our previous sampling of apricots in Europe and Central Asia towards Eastern Asia, resulting in a total sample of 271 cultivated samples and 306 wild apricots across Eurasia, mainly Prunus armeniaca and Prunus sibirica, with some Prunus mume and Prunus mandshurica. We recovered wild Chinese species as genetically differentiated clusters, with P. sibirica being divided into two clusters, one possibly resulting from hybridization with P. armeniaca. Central Asia also appeared as a diversification centre of wild apricots. We further revealed at least three domestication events, without bottlenecks, that gave rise to European, Southern Central Asian and Chinese cultivated apricots, with ancient gene flow among them. The domestication event in China possibly resulted from ancient hybridization between wild populations from Central and Eastern Asia. We also detected extensive footprints of recent admixture in all groups of cultivated apricots. Our results thus show that apricot is an excellent model for studying speciation and domestication in long‐lived perennial fruit trees.

Contents have been reproduced by permission of the publishers.
上海纽约大学William Glover