Elsevier

Biological Conservation

Volume 250, October 2020, 108695
Biological Conservation

Perspective
Microbiomes are integral to conservation of parasitic arthropods

https://doi.org/10.1016/j.biocon.2020.108695Get rights and content

Highlights

  • Parasitic arthropods are expected to suffer high extinction due to climate change.

  • Parasites depend on microbes for access to and their function within suitable habitat.

  • Environmental alteration of microbiomes may decrease suitable habitat for parasites.

  • Successful parasite conservation will depend on knowledge of parasite microbiomes.

Abstract

Parasitic arthropods have not typically been included in conservation and management strategies, possibly because the most well-known blood-feeding arthropods are associated with human and livestock disease. However, the vast majority of parasitic arthropods pose no threat to human health and instead contribute to the overall stability of communities to which they belong. The loss of parasitic arthropod biodiversity likely has repercussions for host health, population density, and community structure. The need for parasitic arthropod conservation is urgent given they represent the majority of parasitic animal biodiversity and environmental change is expected to pose a significant threat to their survival. We urge that microbial associations of host–parasitic arthropod assemblages be considered in conservation efforts. Parasitic arthropods are dependent on their microbial associates for development, nutrient acquisition, immune function, and reproduction. The microbiome also mediates the interactions between a parasitic arthropod and a host, and the role of a parasitic arthropod in vectoring pathogens to its host. The microbiome may therefore represent a “weak link” that increases the susceptibility of parasitic arthropods to environmental change. Fundamental knowledge is missing, precluding assessment of this complex association between microbes and parasitic arthropods. We highlight broad areas of future research that focus on building primary knowledge, developing experimental protocols and novel statistics, and leveraging new techniques to increase the resolution at which we can examine microbial communities of parasites. Conservation of parasitic arthropods that accounts for microbiota will likely be more effective at maintaining parasite biodiversity and at controlling arthropod-vectored disease emergence.

Introduction

Though often overlooked, global parasite biodiversity is threatened by environmental change and declining host biodiversity (Gómez et al., 2012; Rocha et al., 2016; Carlson et al., 2017). Indeed, all species are hosts for parasitic organisms, supporting a remarkable diversity of parasitic species, and the loss of these parasite species from ecosystems may have unforeseen negative consequences (Gómez et al., 2012; Stringer and Linklater, 2014; Wood and Johnson, 2015; Dougherty et al., 2016). Climate change-induced habitat alteration alone is expected to cause a global loss of 5–10% of parasite diversity by 2070, with ectoparasites experiencing greater extinction risk than endoparasites (Carlson et al., 2017). Parasites with high host specificity, a complex life cycle, or narrow environmental preferences will be impacted most severely (Cizauskas et al., 2017). As arthropods comprise the majority of classified animal life on earth (Giribet and Edgecombe, 2012) and the majority of parasitic animals are arthropods (Weinstein and Kuris, 2016), extinction of parasitic arthropod species represents a significant threat to biodiversity.

Parasites are most commonly viewed as hurdles along the path towards conservation of free-living host species, rather than the target of conservation efforts themselves (Stringer and Linklater, 2014; Dougherty et al., 2016). However, increasing evidence shows that parasites contribute to healthy host immune response, host population regeneration, ecological network stability, and nutrient cycling (Gómez et al., 2012; Hatcher et al., 2012; Wood and Johnson, 2015; Dougherty et al., 2016). For example, in humans, infection with some helminth parasites modulates the immune response and eases the effects of autoimmune diseases, like Crohn's disease and multiple sclerosis (Summers et al., 2005; Correale and Farez, 2007; Maizels, 2019). Mussels parasitized by endoliths are better able to survive bouts of extreme heat stress than non-infected individuals (Zardi et al., 2016). The trematode Cryptocotyle lingua (Plagiorchiida; Heterophyidae) decreases grazing rate of the common periwinkle snail (Littorina littorea), allowing greater macroalgae abundance for other marine herbivores (Wood et al., 2007). While parasites by definition harm their hosts to varying degrees, the net effect on populations and communities can be beneficial through the ecological functions they contribute.

A community of organisms is more than what meets the eye. If we follow the concept of the holobiont, where an individual organism is actually a composite of itself and associated microbes, and extend it to the scale of communities, then a community is a reflection of the millions of microscopic interactions that occur between the macro and microorganisms occupying a shared space. Even the interactions between hosts and parasites in a community, which are seemingly governed by their own evolutionary associations, are impacted by microorganisms (Dheilly, 2014; Kemen, 2014; Dheilly et al., 2015). The role of parasitic arthropods as hosts of microbes, vectors of microbes, and drivers of free-living host–microbe interactions has not been examined in the context of parasite conservation. Microbes are necessary to the development, immune response, and reproduction of parasitic arthropods (Engel and Moran, 2013; Narasimhan and Fikrig, 2015; Contreras-Garduño et al., 2016) and must be considered an integral part of efforts to stem global biodiversity loss.

Here, we provide a brief review of the importance of microbes to parasitic arthropods and outline areas of future research necessary to preserving parasitic arthropod biodiversity. Weinstein and Kuris (2016) define a parasite as a consumer that feeds on a maximum of one host individual during at least one life stage. We build on this definition to also include organisms that obligately feed on a single host species, regardless of the number of individuals, during at least one life stage. This definition excludes some micropredators like mosquitoes and tsetse flies, but includes others like louse flies, bat flies, and fish mites. Our current knowledge is biased towards insect parasites in the Order Diptera and arachnid parasites in the Subclass Acari, the two clades that contain the majority of parasitic arthropods (Weinstein and Kuris, 2016) and are therefore the focus of this review. However, we encourage the scientific community to investigate the role of microbes in the biology and ecology of other parasitic arthropods (c.f. Agany et al., 2020).

Section snippets

Parasite microbiomes are central to parasite health and reproduction

The microbiome is composed of archaea, bacteria, fungi, protozoa, and viruses. The sources of microbes found within parasites are not completely known, but likely include the broader environmental microbiome, the host microbiome, and the microbiomes of other parasite individuals within the same population (Fig. 1A). Primary and secondary bacterial symbionts share close evolutionary histories with their hosts and are typically maternally inherited (Moran et al., 2008). These bacteria provision

The link between host and parasite microbiomes and parasitic arthropod conservation

We cannot fully address projected parasite biodiversity loss without accounting for the multidimensional nature of hosts, parasitic arthropods, and the microbes that mediate their interactions. Microbiome perturbations may effectively limit the suitable habitat for parasitic arthropods, putting them at greater risk of extinction in the face of environmental change. Suitable “habitat” for parasitic arthropods encompasses both the host and broader environment where the host lives. The link

Directions for future conservation efforts

Conservation strategies targeting free-living arthropod species are broadly used to improve agricultural and natural landscapes, and to prevent arthropod biodiversity loss (Lattin, 1993; Hartley et al., 2007; Gaspar et al., 2011; Sebek et al., 2016; Mader et al., 2017). For example, many species of butterflies and moths have had or continue to have their populations supplemented by captive breeding programs to counteract declines caused by climate change and habitat loss (Ngoka et al., 2007;

Conclusion

Parasitic arthropod microbiomes offer opportunities for future research with implications for community ecology and evolutionary biology, conservation of global biodiversity, and disease ecology of pathogens relevant to human health, livestock, crops, and wildlife. The microbiome mediates the development, health, and reproduction of parasitic arthropods as well as the interactions of parasitic arthropods with the outside world. Through this interdependence, microbiomes must be a primary

Declaration of competing interest

The authors have no conflicts to declare.

Acknowledgments

Thank you to Dr. Skylar Hopkins and Dr. Colin Carlson for organizing this special issue on parasite conservation and inviting us to participate. Thank you to Dr. Kayce Bell for recommending us to the organizers. Thank you to three reviewers whose insights greatly improved the manuscript. We acknowledge the use of PhyloPic silhouettes for Fig. 1, which were created by Matt Crook (Gammaproteobacteria; https://creativecommons.org/licenses/by/3.0/), Tracy Heath (Querqus), Anne-Caroline Heintz

References (126)

  • C.C. Nice et al.

    An unseen foe in arthropod conservation efforts: the case of Wolbachia infections in the Karner blue butterfly

    Biol. Conserv.

    (2009)
  • F. Renoz et al.

    Evolutionary responses of mutualistic insect-bacterial symbioses in a world of fluctuating temperatures

    Curr Opin Insect Sci

    (2019)
  • N.M. Abraham et al.

    Pathogen-mediated manipulation of arthropod microbiota to promote infection

    Proc. Natl. Acad. Sci. U. S. A.

    (2017)
  • D.D.M. Agany et al.

    Microbiome differences etween human head and body lice ecotypes revealed by 16S rRNA gene amplicon sequencing

    J. Parasitol.

    (2020)
  • M. Alejandra Perotti et al.

    Endosymbionts of lice

  • S. Altizer et al.

    Food for contagion: synthesis and future directions for studying host-parasite responses to resource shifts in anthropogenic environments

    Philos. Trans. R. Soc. Lond. Ser. B Biol. Sci.

    (2018)
  • K.R. Amato et al.

    Habitat degradation impacts black howler monkey (Alouatta pigra) gastrointestinal microbiomes

    ISME J.

    (2013)
  • K. Anantharaman et al.

    Thousands of microbial genomes shed light on interconnected biogeochemical processes in an aquifer system

    Nat. Commun.

    (2016)
  • C.B. Beard et al.

    Bacterial symbionts of the triatominae and their potential use in control of Chagas disease transmission

    Annu. Rev. Entomol.

    (2002)
  • C.G. Becker et al.

    Land cover and forest connectivity alter the interactions among host, pathogen and skin microbiome

    Proc. Biol. Sci.

    (2017)
  • M. Ben-Yosef et al.

    Host-specific associations affect the microbiome of Philornis downsi, an introduced parasite to the Galápagos Islands

    Mol. Ecol.

    (2017)
  • P.C. Blainey

    The future is now: single-cell genomics of bacteria and archaea

    FEMS Microbiol. Rev.

    (2013)
  • S.I. Bonnet et al.

    The tick microbiome: why non-pathogenic microorganisms matter in tick biology and pathogen transmission

    Front. Cell. Infect. Microbiol.

    (2017)
  • B.M. Boyd et al.

    Genome sequence of Candidatus Riesia pediculischaeffi, endosymbiont of chimpanzee lice, and genomic comparison of recently acquired endosymbionts from human and chimpanzee lice

    G3

    (2014)
  • A.T. Busby et al.

    Expression of heat shock proteins and subolesin affects stress responses, Anaplasma phagocytophilum infection and questing behaviour in the tick, Ixodes scapularis

    Med. Vet. Entomol.

    (2012)
  • H.J. Carius et al.

    Genetic variation in a host-parasite association: potential for coevolution and frequency-dependent selection

    Evolution

    (2001)
  • C.J. Carlson et al.

    Parasite biodiversity faces extinction and redistribution in a changing climate

    Sci. Adv.

    (2017)
  • K. Chaisiri et al.

    Symbiosis in an overlooked microcosm: a systematic review of the bacterial flora of mites

    Parasitology

    (2015)
  • C.A. Cizauskas et al.

    Parasite vulnerability to climate change: an evidence-based functional trait approach

    R. Soc. Open Sci.

    (2017)
  • J. Contreras-Garduño et al.

    Insect immune priming: ecology and experimental evidences

    Ecol. Entomol.

    (2016)
  • C. Corbin et al.

    Heritable symbionts in a world of varying temperature

    Heredity

    (2017)
  • J. Correale et al.

    Association between parasite infection and immune responses in multiple sclerosis

    Ann. Neurol.

    (2007)
  • N.M. Dheilly

    Holobiont–holobiont interactions: redefining host–parasite interactions

    PLoS Pathog.

    (2014)
  • N.M. Dheilly et al.

    Parasite Microbiome Project: systematic investigation of microbiome dynamics within and across parasite-host interactions

    mSystems

    (2017)
  • N.M. Dheilly et al.

    Parasite microbiome project: grand challenges

    PLoS Pathog.

    (2019)
  • E.R. Dougherty et al.

    Paradigms for parasite conservation

    Conserv. Biol.

    (2016)
  • A.E. Douglas

    The microbial dimension in insect nutritional ecology

    Funct. Ecol.

    (2009)
  • P. Engel et al.

    The gut microbiota of insects - diversity in structure and function

    FEMS Microbiol. Rev.

    (2013)
  • H. Feldhaar

    Bacterial symbionts as mediators of ecologically important traits of insect hosts

    Ecol. Entomol.

    (2011)
  • L.V. Ferguson et al.

    Seasonal shifts in the insect gut microbiome are concurrent with changes in cold tolerance and immunity

    Funct. Ecol.

    (2018)
  • N.M. Fountain-Jones et al.

    Towards an eco-phylogenetic framework for infectious disease ecology: eco-phylogenetics and disease ecology

    Biol. Rev.

    (2018)
  • T. Fukami

    Historical contingency in community assembly: integrating niches, species pools, and priority effects

    Annu. Rev. Ecol. Evol. Syst.

    (2015)
  • T. Gardiner et al.

    Introductions of two insect species threatened by sea-level rise in Essex, United Kingdom: Fisher’s estuarine moth Gortyna borelii lunata (Lepidoptera: Noctuidae) and mottled grasshopper Myrmeleotettix maculatus (Orthoptera: Acrididae)

    Int. Zoo Yb.

    (2017)
  • C. Gaspar et al.

    Selection of priority areas for arthropod conservation in the Azores archipelago

    J. Insect Conserv.

    (2011)
  • A. Ghosh et al.

    Captive Rearing of Papilio polymnestor and Chilasa clytia Butterflies in the Campus of Jahangirnagar University

    (2019)
  • C.M. Gibson et al.

    Extraordinarily widespread and fantastically complex: comparative biology of endosymbiotic bacterial and fungal mutualists of insects

    Ecol. Lett.

    (2010)
  • G. Giribet et al.

    Reevaluating the arthropod tree of life

    Annu. Rev. Entomol.

    (2012)
  • A. Gómez et al.

    Parasite conservation, conservation medicine, and ecosystem health

  • R. Gross et al.

    Immunity and symbiosis

    Mol. Microbiol.

    (2009)
  • F. Gutzwiller et al.

    Correlation between the green-island phenotype and Wolbachia infections during the evolutionary diversification of Gracillariidae leaf-mining moths

    Ecol. Evol.

    (2015)
  • Cited by (4)

    • The ecological significance of arthropod vectors of plant, animal, and human pathogens

      2022, Trends in Parasitology
      Citation Excerpt :

      The microbiome of hematophagous vectors also has critical roles in interactions with the vertebrate hosts, as well as in the transmission of pathogens [56]. The extent of the ecological roles conferred by the microbiome is only beginning to be revealed, and gaps remain in our understanding of the microbiome-mediated consequences of vector suppression on ecosystem functioning [57]. Resources at breeding sites of dipteran vectors are generally limiting, and intraspecific resource competition can drive population dynamics.

    View full text