Mechanisms of symbiont-conferred protection against natural enemies: an ecological and evolutionary framework

https://doi.org/10.1016/j.cois.2014.08.002Get rights and content

Highlights

  • Many vertically-transmitted symbionts protect insect hosts from pathogenic and parasitic natural enemies.

  • Vertically-transmitted symbionts can also alter the ability of insects to vector pathogens and parasites.

  • Protection involves a variety of mechanisms (toxin production, resource competition, activation of host immunity).

  • Mechanisms of protection are influenced by host–symbiont evolutionary history.

  • Mechanisms of protection can influence evolution of host physiological processes.

Many vertically-transmitted microbial symbionts protect their insect hosts from natural enemies, including host-targeted pathogens and parasites, and those vectored by insects to other hosts. Protection is often achieved through production of inhibiting toxins, which is not surprising given that toxin production mediates competition in many environments. Classical models of macroecological interactions, however, demonstrate that interspecific competition can be less direct, and recent research indicates that symbiont-protection can be mediated through exploitation of limiting resources, and through activation of host immune mechanisms that then suppress natural enemies. Available data, though limited, suggest that effects of symbionts on vectored pathogens and parasites, as compared to those that are host-targeted, are more likely to result from symbiont activation of the host immune system. We discuss these different mechanisms in light of their potential impact on the evolution of host physiological processes.

Section snippets

An ecological framework for studying protection

Insects are infected by diverse microorganisms that vary both in their life-history strategies and in their effects on host fitness. Co-infections are common, and of particular interest are interactions between vertically-transmitted microbes (here termed ‘symbionts’) and natural enemies, including host-targeted pathogens and parasites and those vectored by insects to other hosts. Because the fitness of vertically-transmitted symbionts parallels the fitness of their hosts, these symbionts can

How evolution shapes symbiont-conferred protection

In most examples of symbiont-conferred protection, the functional mechanisms underlying protection still need to be identified, which will require a combination of experimental, immunological, genetic and genomic approaches (Box 1). Current examples, however, suggest that symbionts primarily protect insects against host-targeted pathogens either directly through toxin production (Figure 1a) or indirectly through exploitation of shared resources (Figure 1b), while symbionts confer resistance

Consideration of the gut microbiome

In addition to vertically-transmitted symbionts, many insects harbour complex gut microbiomes, and evidence suggests that these too can alter resistance. Mosquitoes, for example, harbour diverse gut flora that influence Plasmodium establishment [10, 11, 12, 51, 52]. A demonstrated relationship between mosquito gut bacterial species complexity and Plasmodium infection appears to be mediated by activation of an immune pathway (IMD) [13, 51, 52]. More recent work identified a gut-inhabiting

Conclusions

The mechanistic basis of symbiont-conferred protection against natural enemies can be complex, involving both direct interactions between microorganisms within hosts and more indirect interactions mediated through host-derived resources and host immune mechanisms (Figure 1). Symbiont-conferred protection can impact both host interactions with their natural enemies and insect vectoring capacity. The same mechanisms of protection can play a role in either case, though the evolutionary framework

References and recommended reading

Papers of particular interest, published within the period of review, have been highlighted as:

  • • of special interest

  • •• of outstanding interest

Acknowledgments

N.M.G. is supported by National Science Foundation grant IOS-1149829. B.J.P. is supported by NSF fellowship DBI-1306387. Special thanks to the participants of the 2014 Keystone Symposium on Mechanisms and Consequences of Invertebrate-Microbe Interactions for stimulating this line of inquiry, and to Angela Douglas for helpful revisions.

References (72)

  • K.M. Oliver et al.

    Facultative bacterial symbionts in aphids confer resistance to parasitic wasps

    Proc Natl Acad Sci U S A

    (2003)
  • J. Wang et al.

    Interactions between mutualist Wigglesworthia and tsetse peptidoglycan recognition protein (PGRP-LB) influence trypanosome transmission

    Proc Natl Acad Sci U S A

    (2009)
  • A. Kliot et al.

    Implication of the bacterial endosymbiont Rickettsia spp. in interactions of the whitefly Bemisia tabaci with tomato yellow leaf curl virus

    J Virol

    (2014)
  • E.O. Jones et al.

    The evolution of host protection by vertically transmitted parasites

    Proc R Soc Lond B Biol Sci

    (2011)
  • C.M. Lively et al.

    Competitive co-existence of vertically and horizontally transmitted parasites

    Evol Ecol Res

    (2005)
  • B.L. Weiss et al.

    Tsetse immune system maturation requires the presence of obligate symbionts in larvae

    PLoS Biol

    (2011)
  • O. Duron et al.

    The diversity of reproductive parasites among arthropods: Wolbachia do not walk alone

    BMC Biol

    (2008)
  • K. Hilgenboecker et al.

    How many species are infected with Wolbachia? A statistical analysis of current data

    FEMS Microbiol Lett

    (2008)
  • R. Zug et al.

    Bad guys turned nice? A critical assessment of Wolbachia mutualisms in arthropod hosts

    Biol Rev Camb Philos Soc

    (2014)
  • J. Ferrari et al.

    Population genetic structure and secondary symbionts in host-associated populations of the pea aphid complex

    Evolution

    (2012)
  • O. Duron et al.

    Arthropods and inherited bacteria: from counting the symbionts to understanding how symbionts count

    BMC Biol

    (2013)
  • K.M. Oliver et al.

    Variation in resistance to parasitism in aphids is due to symbionts not host genotype

    Proc Natl Acad Sci U S A

    (2005)
  • K.M. Oliver et al.

    Bacteriophages encode factors required for protection in a symbiotic mutualism

    Science

    (2009)
  • P.H. Degnan et al.

    Diverse phage-encoded toxins in a protective insect endosymbiont

    Appl Environ Microbiol

    (2008)
  • N.A. Moran et al.

    The players in a mutualistic symbiosis: insects, bacteria, viruses, and virulence genes

    Proc Natl Acad Sci U S A

    (2005)
  • K.M. Oliver et al.

    Defensive symbiosis in the real world-advancing ecological studies of heritable, protective bacteria in aphids and beyond

    Funct Ecol

    (2013)
  • J. Jaenike et al.

    Ecology and evolution of host–parasite associations: mycophagous Drosophila and their parasitic nematodes

    Am Nat

    (2002)
  • J. Jaenike et al.

    Adaptation via symbiosis: recent spread of a Drosophila defensive symbiont

    Science

    (2010)
  • P.T. Hamilton et al.

    Transcriptional responses in a Drosophila defensive symbiosis

    Mol Ecol

    (2013)
  • L.M. Hedges et al.

    Wolbachia and virus protection in insects

    Science

    (2008)
  • L. Teixeira et al.

    The bacterial symbiont Wolbachia induces resistance to RNA viral infections in Drosophila melanogaster

    PLoS Biol

    (2008)
  • J.A. Russell et al.

    Uncovering symbiont-driven genetic diversity across North American pea aphids

    Mol Ecol

    (2013)
  • S.C. Hackett et al.

    Unpredicted impacts of insect endosymbionts on interactions between soil organisms, plants and aphids

    Proc R Soc Lond B Biol Sci

    (2013)
  • G.D.D. Hurst et al.

    The inherited microbiota of arthropods, and their importance in understanding resistance and immunity

  • S.E. Osborne et al.

    Variation in antiviral protection mediated by different Wolbachia strains in Drosophila simulans

    PLoS Pathog

    (2009)
  • E.P. Caragata et al.

    Dietary cholesterol modulates pathogen blocking by Wolbachia

    PLoS Pathog

    (2013)
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