Elsevier

Hormones and Behavior

Volume 88, February 2017, Pages 112-121
Hormones and Behavior

Review article
Ecoimmunology and microbial ecology: Contributions to avian behavior, physiology, and life history

https://doi.org/10.1016/j.yhbeh.2016.12.003Get rights and content

Highlights

  • Life phases vary in their microbial exposure.

  • Early life microbial defense relies on parental modulation of immunity and microbes.

  • Congregating conspecifics, movement into new habitats, and molt increase microbial risk.

  • Use of –omics will reveal the effects of microbes on life history, immunity, and diet niche.

Abstract

Bacteria have had a fundamental impact on vertebrate evolution not only by affecting the evolution of the immune system, but also generating complex interactions with behavior and physiology. Advances in molecular techniques have started to reveal the intricate ways in which bacteria and vertebrates have coevolved. Here, we focus on birds as an example system for understanding the fundamental impact bacteria have had on the evolution of avian immune defenses, behavior, physiology, reproduction and life histories. The avian egg has multiple characteristics that have evolved to enable effective defense against pathogenic attack. Microbial risk of pathogenic infection is hypothesized to vary with life stage, with early life risk being maximal at either hatching or fledging. For adult birds, microbial infection risk is also proposed to vary with habitat and life stage, with molt inducing a period of increased vulnerability. Bacteria not only play an important role in shaping the immune system as well as trade-offs with other physiological systems, but also for determining digestive efficiency and nutrient uptake. The relevance of avian microbiomes for avian ecology, physiology and behavior is highly topical and will likely impact on our understanding of avian welfare, conservation, captive breeding as well as for our understanding of the nature of host-microbe coevolution.

Section snippets

Introduction: microbial ecology, immune defense, and co-evolution

Ever since birds first appeared in the Mesozoic era (Benson et al., 2014), they have coexisted with microbes, potentially coevolving with avian ontogeny, behavior, physiology and immune function. There is even a growing literature to suggest that microbes were instrumental in determining early feather coloration and structure (Carney et al., 2012, Moyer et al., 2014). To put the importance of microbes into perspective: the microbial community inhabiting the human gut (1014cells) is estimated to

Eggs and embryos

Eggs and embryos are associated with microbe communities present in nests, as well as on the skin, feathers and feces of parents. Birds utilize a wide variety of different nesting materials including with potentially distinct microbial communities and some materials may even have antimicrobial characteristics. Feathers have been proposed to have antimicrobial characteristics and can prevent or manipulate microbial colonization (Peralta-Sanchez et al., 2012, Ruiz-Castellano et al., 2016, Shawkey

Nestlings and juveniles

Bacterial nest densities and assemblages (Berger et al., 2003) are hypothesized to play an important role in determining nestling growth and development. Siblings share more similar bacterial assemblage composition than would be expected by chance, demonstrating the potential role of the nest environment in shaping immune development (Brandl et al., 2014). To understand relationships between nestling immune function and bacteria, it is important to understand how immune function development

Adult phases

Adult microbial exposure is hypothesized to be a function of species' ecology, behavior and life history strategy which interact to produce variation in the relative risk of pathogenic microbe exposure (Fig. 2). Both comparative studies and manipulative experiments that alter the microbial exposure of birds at various stages of their life history could reveal the nature of physiological trade-offs that might be relevant in mediating the cost of bacterial defense. For example, Evans et al. (2016)

Microbial biogeography

Global microbe diversity and density are predicted to follow latitudinal diversity trends (Fuhrman et al., 2008, Stephens et al., 2016) but biogeography of microorganisms is complicated by host associations (e.g. Altizer et al., 2007, Huang et al., 2015, O'Dwyer et al., 2012) and a release from some of the biogeographical processes that shape macroorganism diversity and distribution (Horner-Devine et al., 2007, Martiny et al., 2006). Within high latitude zones temperature predicts pathogen

Conclusion: key questions and techniques

Much remains to be revealed about the influence of microbes on avian immunology, endocrinology, and behavior. Here, we present the key questions to be pursued in avian microbial ecology if we are to understand this neglected influence on life history evolution.

Author contributions statement

JKE wrote the first draft of the Eggs and Embryos and Nestlings and Juveniles sections. BA wrote the first draft of the Adult Phases section. KLB and BA jointly wrote the Ecological Considerations sections. JKE and KCK developed Fig. 1. BA and KLB developed Fig. 2. JKE and BA jointly wrote the Introduction and Conclusion sections. KLB, SG, and KCK revised the subsequent manuscript drafts.

Acknowledgements

We wish to thank the editors of the special issue for the invitation to submit our review.

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