Chemical fingerprints encode mother–offspring similarity, colony membership, relatedness, and genetic quality in fur seals

Abstract

Chemical communication underpins virtually all aspects of vertebrate social life, yet remains poorly understood because of its highly complex mechanistic basis. We therefore used chemical fingerprinting of skin swabs and genetic analysis to explore the chemical cues that may underlie mother-offspring recognition in colonially breeding Antarctic fur seals. By sampling mother-offspring pairs from two different colonies, using a variety of statistical approaches and genotyping a large panel of microsatellite loci, we show that colony membership, mother-offspring similarity, heterozygosity, and genetic relatedness are all chemically encoded. Moreover, chemical similarity between mothers and offspring reflects a combination of genetic and environmental influences, the former partly encoded by substances resembling known pheromones. Our findings reveal the diversity of information contained within chemical fingerprints and have implications for understanding mother-offspring communication, kin recognition, and mate choice. Olfaction in particular is fundamental to animal communication, mediating social interactions as varied as territorial behavior, kin recognition, and mate choice (1). Metabolomic tools, such as gas chromatography-mass spectrometry (GC-MS) have made it possible to generate individual-specific chemical "fingerprints." By separating compounds and quantifying their relative abundances, these fingerprints provide a wealth of information, even though not all compounds can necessarily be identified. Both volatile and contact cues are potentially hidden within the extreme complexity of chemical profiles, which is why a mechanistic understanding of chemical communication is still lacking in natural vertebrate populations (2).In particular, "surprisingly little progress" has been made in understanding the link between vertebrate chemical fingerprints and genotype (2). Experimental studies have shown that females of several species are capable of discriminating potential partners based on olfactory cues (3-5). However, very few studies have demonstrated a convincing link between the molecular composition of chemical fingerprints and genetic traits, such as heterozygosity (a measure of genetic quality) and relatedness (6-9). These studies were almost exclusively conducted on a captive population of lemurs, a species known for its conspicuous use of scent marking.A functional understanding of how genotype is chemically encoded also requires knowledge of how many and which types of substances are involved. This is challenging because, especially in natural populations, an individual's mixture of surface chemicals is not only the product of its genotype but may also be mediated by hormones, the microbial flora, body condition, and environmental factors (2). Thus, analyses based on overall chemical fingerprints may overlook subtle genetic signatures and make little if any headway toward identifying the specific substances involved. A second less-appreciated problem is that the modest panels of around 10-15 microsat...

Born blonde: a recessive loss‐of‐function mutation in the melanocortin 1 receptor is associated with cream coat coloration in Antarctic fur seals

“…In support of previous studies of the breeding population of fur seals at South Georgia (e.g., Hoffman et al., 2011; Stoffel et al. 2015), Bayesian cluster analysis yielded a best clustering solution of K  =   1. With such a large number of loci, this finding allows us to rule out the possibility that cream‐colored individuals are genetically divergent from wild‐type individuals and thus lends further support to the notion that the S291F substitution causes hypopigmentation.…”

Chemical fingerprints reveal clues to identity, heterozygosity, and relatedness

“…Females show active mate choice, preferring males that are heterozygous and unrelated, but the mechanism by which this is achieved has remained elusive (16). Stoffel et al (9) propose that chemical fingerprints may be involved in female mate choice, but they were hampered by a lack of male sampling. This raises the exciting possibility that by investigating male chemical fingerprints and undertaking an experimental assessment of female preferences for chemical signals linked to heterozygosity, an understanding of the mechanism underlying mate selection may finally be within our grasp.…”

“…In the face of multiple species range changes and increased interspecific interactions, understanding barriers to hybridization is ever more important (19). The link between genotype and chemical fingerprints identified by Stoffel et al (9) opens a new avenue of investigation into the possible role of chemical information in the maintenance of species boundaries.…”

“…Increasing sophistication of statistical analyses supported by large panels of economically derived markers is opening up entire new avenues of study. In the near future, identifying parts of the genome under divergent selection may prove even more powerful in detecting subtle underlying processes resulting from adaptive genetic variation (20) than the application of large numbers of neutral markers such as those applied in Stoffel et al (9).…”

“…However, perhaps due to both the complexity of working with natural vertebrate populations and the complexity of vertebrate scents, the mechanistic basis of chemical communication has received little study (8). In PNAS, Stoffel et al (9) provide an important advance in the understanding of chemical communication in wild mammals. They compared genetic similarity and the chemical profiles of Antarctic fur seals in two colonies.…”