Genetic variation at MHC class II loci influences both olfactory signals and scent discrimination in ring-tailed lemurs

Abstract

Background Diversity at the Major Histocompatibility Complex (MHC) is critical to health and fitness, such that MHC genotype may predict an individual’s quality or compatibility as a competitor, ally, or mate. Moreover, because MHC products can influence the components of bodily secretions, an individual’s body odors may signal its MHC composition and influence partner identification or mate choice. Here, we investigated MHC-based signaling and recipient sensitivity by testing for odor-gene covariance and behavioral discrimination of MHC diversity and pairwise dissimilarity in a strepsirrhine primate, the ring-tailed lemur ( Lemur catta ). Methods First, we coupled genotyping of the MHC class II gene, DRB, with gas chromatography-mass spectrometry of genital gland secretions to investigate if functional genetic diversity is signaled by the chemical diversity of lemur scent secretions. We also assessed if the chemical similarity between individuals correlated with their MHC-DRB similarity. Next, we assessed if lemurs discriminated this chemically encoded, genetic information in opposite-sex conspecifics. Results We found that both sexes signaled overall MHC-DRB diversity and pairwise MHC-DRB similarity via genital secretions, but in a sex- and season-dependent manner. Additionally, the sexes discriminated absolute and relative MHC-DRB diversity in the genital odors of opposite-sex conspecifics, suggesting that lemur genital odors function to advertise genetic quality. Conclusions In summary, genital odors of ring-tailed lemurs provide honest information about an individual’s absolute and relative MHC quality. Complementing evidence in humans and Old World monkeys, we suggest that reliance on scent signals to communicate MHC quality may be important across the primate lineage. Electronic supplementary material The online version of this article (10.1186/s12862-019-1486-0) contains supplementary material, which is available to authorized users.

Feather chemicals contain information about the major histocompatibility complex in a highly scented seabird

“…In addition to only finding support for gene–odour covariance in certain dyads of individuals, the effect sizes associated with our positive findings were small. Both of these results are consistent with other studies from mammals and birds, which found similar effect sizes and often only detected relationships in certain dyads [26,33,34,62]. The diverse array of factors that affect chemical profiles may explain these findings.…”

“…Vertebrate chemical profiles change seasonally and may only reflect genetic markers during the breeding season [26,66,67]. The absence of genetic information in chemical profiles during the non-breeding season might be explained by energetic costs associated with producing chemical secretions [67,68], although there is currently limited support for this idea in birds [69].…”

Infection threat shapes our social instincts

“…The MHC marks the scent of urine (both in mice and in humans: Eggert et al 1999) and is quite likely to affect the odor of one's breath, sweat, and genitals as well (Wobst 1999;Aksenov et al 2012;Grogan 2019). It can also alter the menagerie of microbes individuals carry around (Khan et al 2019), and thus the aromatic gases such microbes give off (Rudden et al 2020).…”

Design, delivery and perception of condition-dependent chemical signals in strepsirrhine primates: implications for human olfactory communication

“…Genotyping the MHC-DRB in a large number of wild and captive lemurs showed that captive animals have reduced allelic diversity [174]. Nevertheless, their allelic diversity relates significantly to the chemical richness of their genital signals and to the responsiveness of conspecifics encountering their scents for the first time [104]. For example, males that have the most MHC-DRB supertypes also have the greatest chemical richness in their genital secretions-attributes that are detectable by female recipients, who associate most often with the scent of MHC-DRB dissimilar males.…”

“…They also advertise pairwise kinship or MHC-DRB similarity. Such odour-gene relationships in both sexes facilitate prioritization of agonistic or nepotistic interactions, as well as compatible mate attraction and inbreeding avoidance to increase the immunocompetence of offspring [52,53,[102][103][104]-findings that are functionally relevant to humans and other primates [150,[175][176][177].…”