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Gut microbiota and kin recognition

2013, Trends in Ecology & Evolution

TREE-1630; No. of Pages 2 Spotlight Gut microbiota and kin recognition Anne Lizé, Raegan McKay, and Zenobia Lewis Evolution, Ecology and Behavior, Institute of Integrative Biology, University of Liverpool, Crown Street, Liverpool, L69 7ZB, UK The animal gut contains a large reservoir of symbionts. Whilst these microbes have obvious physiological functions in, for example, digestion and immune defence, they can also affect their host’s behavior. Increasing evidence suggests that gut microbiota alters the scent of an individual, thereby affecting mate choice and kin recognition. Diversity and specificity of gut microbiota The animal gut contains a large reservoir of symbionts, and whilst having obvious physiological functions in digestion and immune defence, gut microbes can affect many aspects of host behavior [1]. Recent studies highlight the importance of gut microbiota on the evolution of mate preferences (e.g., [2]), while others demonstrate that social behaviors can alter gut microbiota communities [3]. Here, we extend a hypothesis first coined in the 1970s that gut microbiota alter the scent of mammals [1,4] and could thus play a key role in kin recognition. While this hypothesis has been examined most extensively in mammals, it is likely to also be important in social insects. New technologies such as high-throughput sequencing have recently led to significant advances, which allow us to further our understanding of the influence of gut communities or specific bacteria on animal communication. The diversity and specificity of gut microbiota communities is altered by host genotype, and environmental factors such as diet, geography, temperature, and social interactions. Under laboratory conditions, reciprocal transplantation of gut microbiota between germ-free mice and zebrafish, led transplanted communities to adjust to their natural host microbiota through host selective processes [5]. Self-adjustment of gut microbiota community composition has also been demonstrated in the parasitoid wasp Nasonia sp. [6]. While gut microbiota specificity is at least partly determined by host phylogeny, the diversity of the microbial community is also influenced by host environment and diet (e.g., in humans [7], and insects [3]). Gut microbiota is important for mate preferences and sociality through pheromone alterations Recent evidence suggests that ecological divergence of host populations is accompanied by changes in their associated bacterial communities, and these themselves could play a role in driving mate preferences [6]. In the fruit fly Drosophila melanogaster divergent gut bacterial communities are associated with differences in cuticular hydrocarbon (CHC) profiles, also known as sex pheromones. CHCs are used in chemical communication between individuals in Corresponding author: Lizé, A. ([email protected]). many insects, and flies have been shown to express a marked preference for mating with individuals presenting similar CHC, and thus gut bacterial, profiles [2]. Gut microbiota can alter sex pheromones either by bacterialspecific molecules acting as sex attractants, or by bacterialinduced effects on nuclear genes that code for sex pheromones [6]. Pheromones are also important for social species, providing labels for intra-group recognition. Social living enhances similarity of microbiota (i.e., microbiota shared by related individuals), through providing a continual flux of symbionts from related individuals such as nestmates in insects, as opposed to from the environment and/or random individuals. Studies suggest that relatives raised in a common environment harbor more similar bacterial communities than non-relatives or relatives raised in different environments [7,8]. In addition, evidence of co-evolution between gut bacteria and their host confirms the importance of similarity in gut bacteria communities within social groups. For example, vertically transmitted microbiomes co-diverged alongside their host in social bees, but not in solitary bees [3]. In the social bees, co-adaptation is sufficient to provide resistance to gut pathogens, but group-living is essential for the successful establishment of protective microbiota [3]. Gut microbiota is implicated in nestmate recognition The sharing of gut microbiota in socially living organisms suggests that nest mate identity can be inferred from microbiome constitution in social species, as in termites [9]. Nestmate recognition is the process whereby an individual differentiates between individuals belonging to their own versus an alien colony. Nestmate recognition often results in the discrimination of kin from non-kin, but while kin recognition is the assessment of the degree of relatedness between two individuals, nestmate recognition is a binary recognition process of group members. Nestmate recognition involves the matching of a label, for example, the chemical profile containing nestmate cues, with a template such as the mental representation of the colony individual odor stored in the memory, and depending on the similarity between the two, a conspecific will be accepted or rejected. The expression of the label can be influenced by multiple sources, which can be heritable, or derived from the environment, for example, food or nest material. Both heritably and environmentally determined labels can theoretically be altered by changes in the gut microbiota. For example, termite-microbiota co-adaptation aiding in wood digestion must be inherited from generation to generation even if the gut microbiota is horizontally transmitted from individuals to others in a colony through 1 TREE-1630; No. of Pages 2 Spotlight coprophagy. Any alteration of the gut microbiota is hence supposed to alter the co-adapted equilibrium between termites and their gut helpers. In the same way, the environment or food consumed earlier in life could also affect individual odors. Gut microbiota might play a role in kin recognition Kin recognition, the cognitive process by which animals distinguish kin and non-kin is an important biological property because the ability to recognize one’s relatives provides a mechanism allowing both the emergence of altruism and sociality. The cues that are correlated with kinship often elicit differences in behavioral responses that an individual expresses toward kin compared to non-kin, a process called kin discrimination. For example, females of the pre-social wasp Goniozus legneri are capable of direct kin recognition of full sisters without any prior experience of related individuals. Moreover, these parasitoid females treat unrelated females as related ones provided they have developed and fed on the same host during development, suggesting that females that have co-developed share an environmentally-induced label even when they are nonrelated [10]. The body of literature on kin recognition is large and diverse, both in vertebrates and invertebrates, but it often describes the process without specifying the mechanism used by related individuals to recognize each other. Here we propose that individual scent might vary according to their gut microbial community, which could be a powerful cue in kin recognition processes. Gut microbiota has recently been recognized as a potential important driver of speciation through species recognition [6]. We propose that recent advances in molecular technologies provide an excellent opportunity to test the hypothesis, first developed almost forty years ago, that gut microbiota could be functionally important for processes of nestmate and kin recognition. Until now, most of the current evidence that animals share similar gut microbiota comes from characterizing bacterial communities via 16S rRNA analyses (e.g., [8]). While such studies suggest that human and other mammalian siblings raised in a similar environment exhibit 2 Trends in Ecology and Evolution xxx xxxx, Vol. xxx, No. x more similar bacterial communities, to date there is no evidence that this will in turn affect recognition between individuals. Hence, the use of metagenomic data generated via high-throughput sequencing, which is now time and cost effective, is an important avenue of study, which should reveal the metabolic products of kin-based bacterial communities that may contribute to recognition cues. Empirical examination of the role of gut microbiota in kin and nestmate recognition, coupled with metagenomic analysis of bacterial products across a wide range of solitary and social species, will allow us to determine the implications of gut microbiota for social evolution. Acknowledgments The authors are grateful to one anonymous reviewer, Paul Craze, and Gregory D.D. Hurst for critical reading and comments of the manuscript. 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(2011) Unravelling the effects of the environment and host genotype on the gut microbiome. Nat. Rev. Microbiol. 9, 279–290 8 Yatsunenko, T. et al. (2012) Human gut microbiome viewed across age and geography. Nature 466, 222–228 9 Minkley, N. et al. (2006) Nest specificity of the bacterial community in termite guts (Hodotermes mossambicus). Ins. Soc. 53, 339–344 10 Lizé, A. et al. (2012) Two components of kin recognition influence parasitoid aggression in resource competition. Anim. Behav. 83, 793–799 0169-5347/$ – see front matter ß 2012 Elsevier Ltd. All rights reserved. http://dx.doi.org/10.1016/j.tree.2012.10.013 Trends in Ecology and Evolution xx (2012) 1–2