Chemical fingerprints reveal clues to identity, heterozygosity, and relatedness

Pitcher, Benjamin J.; Charrier, Isabelle; Harcourt, Robert

doi:10.1073/pnas.1514278112

Cited by 5 publications

(8 citation statements)

References 20 publications

(20 reference statements)

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“…By contrast, we specifically focused on the skin microbiota for two reasons. First, a previous study of Antarctic fur seal mother–offspring pairs from the same locations uncovered colony‐specific chemical signatures as well as chemical similarities between mothers and their offspring (Stoffel et al, ), suggesting that olfactory cues could be important in mother–offspring recognition (Pitcher, Charrier, & Harcourt, ). Consequently, we wanted to test whether bacterial fermentation mediated by skin microbes could play a role in generating these patterns.…”

Section: Discussionmentioning

confidence: 99%

“…Specifically, the microbial and chemical similarity of mothers and their offspring is consistent with phenotype matching, a mechanism by which the own phenotype or one that is learned early during development is a template used for the recognition of relatives (Blaustein, ). However, to provide conclusive evidence of a link between the skin microbiota, chemical profiles and mother–offspring recognition, it will be necessary to sample microbes and chemical substances from the same individuals (Ezenwa & Williams, ) as well as to demonstrate that fur seal mothers show a preference for the chemical and bacterial profiles of their own offspring relative to those of nonfilial pups (Pitcher et al, ).…”

Section: Discussionmentioning

confidence: 99%

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Fur seal microbiota are shaped by the social and physical environment, show mother–offspring similarities and are associated with host genetic quality

et al. 2019

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Despite an increasing appreciation of the importance of host-microbe interactions in ecological and evolutionary processes, the factors shaping microbial communities in wild populations remain poorly understood. We therefore exploited a natural experiment provided by two adjacent Antarctic fur seal (Arctocephalus gazella) colonies of high and low social density and combined 16S rRNA metabarcoding with microsatellite profiling of mother-offspring pairs to investigate environmental and genetic influences on skin microbial communities. Seal-associated bacterial communities differed profoundly between the two colonies, despite the host populations themselves being genetically undifferentiated. Consistent with the hypothesis that social stress depresses bacterial diversity, we found that microbial alpha diversity was significantly lower in the high-density colony. Seals from one of the colonies that contained a stream also carried a subset of freshwater-associated bacteria, indicative of an influence of the physical environment. Furthermore, mothers and their offspring shared similar microbial communities, in support of the notion that microbes may facilitate mother-offspring recognition. Finally, a significant negative association was found between bacterial diversity and heterozygosity, a measure of host genetic quality. Our study thus reveals a complex interplay between environmental and host genetic effects, while also providing empirical support for the leash model of host control, which posits that bacterial communities are driven not only by bottom-up species interactions, but also by top-down host regulation. Taken together, our findings have broad implications for understanding host-microbe interactions as well as prokaryotic diversity in general. K E Y W O R D SArctocephalus gazella, host control, inbreeding, mother-offspring recognition, pinniped, skin microbiome | 2407 GROSSER Et al. S U PP O RTI N G I N FO R M ATI O N Additional supporting information may be found online in the Supporting Information section at the end of the article. How to cite this article: Grosser S, Sauer J, Paijmans AJ, et al. Fur seal microbiota are shaped by the social and physical environment, show mother-offspring similarities and are associated with host genetic quality.

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Section: Discussionmentioning

confidence: 99%

Section: Discussionmentioning

confidence: 99%

Fur seal microbiota are shaped by the social and physical environment, show mother–offspring similarities and are associated with host genetic quality

et al. 2019

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“…Those analyses remain controversial, however, as unsuitable inference methods have been used, and the true complexity of traits is often ignored (Goldberg and Igić 2008). Pheromones are often highly specific, and are key regulators of offspring and group recognition in mammals (Smadja and Butlin 2009;Pitcher et al 2011Pitcher et al , 2015Rizvanovic et al 2013;Cinková and Policht 2014;Péron et al 2014). Here, we analyze the molecular evolution of a mammalian chemosensory system, examining changes in selection underlying the loss of this complex system throughout the diversification of bats.…”

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confidence: 99%

“…Pheromones play an important role in social communication and mediate many behaviors critical to fitness, including conspecific recognition, courtship and mating, parental care, territoriality, and even the detection of sick individuals (Fortes-Marco et al 2013;Boillat et al 2015;Martín-Sánchez et al 2015). Pheromones are often highly specific, and are key regulators of offspring and group recognition in mammals (Smadja and Butlin 2009;Pitcher et al 2011Pitcher et al , 2015Rizvanovic et al 2013;Cinková and Policht 2014;Péron et al 2014). With a few exceptions, vomerolfaction is ubiquitous across mammals.…”

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confidence: 99%

Trpc2 pseudogenization dynamics in bats reveal ancestral vomeronasal signaling, then pervasive loss

et al. 2017

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Comparative methods are often used to infer loss or gain of complex phenotypes, but few studies take advantage of genes tightly linked with complex traits to test for shifts in the strength of selection. In mammals, vomerolfaction detects chemical cues mediating many social and reproductive behaviors and is highly conserved, but all bats exhibit degraded vomeronasal structures with the exception of two families (Phyllostomidae and Miniopteridae). These families either regained vomerolfaction after ancestral loss, or there were many independent losses after diversification from an ancestor with functional vomerolfaction. In this study, we use the Transient receptor potential cation channel 2 (Trpc2) as a molecular marker for testing the evolutionary mechanisms of loss and gain of the mammalian vomeronasal system. We sequenced Trpc2 exon 2 in over 100 bat species across 17 of 20 chiropteran families. Most families showed independent pseudogenizing mutations in Trpc2, but the reading frame was highly conserved in phyllostomids and miniopterids. Phylogeny-based simulations suggest loss of function occurred after bat families diverged, and purifying selection in two families has persisted since bats shared a common ancestor. As most bats still display pheromone-mediated behavior, they might detect pheromones through the main olfactory system without using the Trpc2 signaling mechanism.

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“…In the case of species of conservation concern, such differences could therefore impede species recovery even where, for example, conservation measures reduce habitat fragmentation. At a higher taxonomic level, chemical signals may provide effective barriers to hybridization 18 . Olfactory discrimination is therefore potentially fundamental to adaptation and evolution via the maintenance of species boundaries 18 .…”

Section: Introductionmentioning

confidence: 99%

Odour dialects among wild mammals

Kean

Bruford

Russo

et al. 2017

Sci Rep

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Across multiple taxa, population structure and dynamics depend on effective signalling between individuals. Among mammals, chemical communication is arguably the most important sense, underpinning mate choice, parental care, territoriality and even disease transmission. There is a growing body of evidence that odours signal genetic information that may confer considerable benefits including inbreeding avoidance and nepotism. To date, however, there has been no clear evidence that odours encode population-level information in wild mammals. Here we demonstrate for the first time the existence of ‘odour dialects’ in genetically distinct mammalian subpopulations across a large geographical scale. We found that otters, Lutra lutra, from across the United Kingdom possess sex and biogeography-specific odours. Subpopulations with the most distinctive odour profiles are also the most genetically diverse but not the most genetically differentiated. Furthermore, geographic distance between individuals does not explain regional odour differences, refuting other potential explanations such as group odour sharing behaviour. Differences in the language of odours between subpopulations have the potential to affect individual interactions, which could impact reproduction and gene-flow.

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Chemical fingerprints reveal clues to identity, heterozygosity, and relatedness

Cited by 5 publications

References 20 publications

Fur seal microbiota are shaped by the social and physical environment, show mother–offspring similarities and are associated with host genetic quality

Fur seal microbiota are shaped by the social and physical environment, show mother–offspring similarities and are associated with host genetic quality

Trpc2 pseudogenization dynamics in bats reveal ancestral vomeronasal signaling, then pervasive loss

Odour dialects among wild mammals

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