Genetically based social communication in an inbred group-living wild mammal

Chemical communication is the oldest and most widespread form of communication in the animal kingdom and its applications are manifold. Assessing relatedness and genetic quality in conspecifics through odor is one such purpose and it can increase an individual’s fitness. However, the mechanisms of how genetic composition can reliably be translated into odor as well as the specific genes involved in signaling genetic quality and relatedness are still up for debate. A promising candidate for signaling genetic composition through odor is the major histocompatibility complex (MHC), which is shared by virtually all jawed vertebrates, exhibits the necessary polymorphism and, due to its central role in the adaptive immune response, has the potential to act on the odor of an individual both directly and indirectly. In this thesis, I intend to investigate the genetic basis of chemical communication in a social mammal, the banded mongoose. Banded mongooses are prolific scent markers that use secretions from different organs to communicate both within and between groups, as well as intra- and intersexually. Their exceptional breeding system, cooperative behavior and inbreeding levels make them the ideal target for investigating the effects of the MHC on fitness and its potential involvement in chemical communication. I used high throughput sequencing to characterize both classes of the MHC in a large sample of the banded mongoose population inhabiting Queen Elizabeth National Park, Uganda. This analysis revealed historical selection maintaining diversity comparable to other species of the same conservation status, despite frequent inbreeding, as well as trans-species polymorphism. I then combined the genetic data on individual MHC diversity with long-term life history data collected over more than 25 years to investigate current selection acting on the MHC. This analysis revealed sex-specific effects of MHC diversity on fitness, particularly lifetime reproductive success. Interestingly, the effect of MHC diversity on lifetime reproductive success was positive for males, while females displayed the opposite relationship. The resulting sexual conflict over MHC diversity appeared to be unresolved, as MHC diversity did not differ between the sexes. Next, I investigated if MHC composition, either measured as diversity or similarity, as well as relatedness in unfamiliar individuals are broadcasted and perceived via odor, causing individuals to respond accordingly. Indeed, banded mongooses responded to relatedness and MHC diversity in unfamiliar conspecifics, increasing their response with decreasing relatedness and MHC diversity. Histological analysis helped characterize the anal gland, which is used for scent marking, and provided information necessary to interpret potential pathways of interaction between the MHC and microbiota in generating odors within the gland. Moreover, histology revealed a yet undescribed cheek scent gland that produces lipid-rich secretion potentially used for scent marking. The results furthermore hint to the possibility of scent rubbing in banded mongooses, aimed at taking up scents instead of depositing them, potentially to facilitate cooperative behavior. Finally, I performed a systematic review of the current literature on interactions between the MHC, microbiota and odor, summarized potential relationships and the evidence for them and pointed out gaps in the literature. Combined with a review of the immunological literature, it provides background information on potential mechanisms of interaction between the MHC and microbiota and gives recommendations for designing studies that effectively tackle the open questions in the field. Overall, this thesis provides missing information on banded mongooses and thereby poses an ideal starting point for further studies on the role of the MHC in social communication, fitness and infection as well as scent marking and scent rubbing. These findings can stimulate further research on this fascinating study system as well as other species, and the application of multifaceted approaches needed to unravel the complex interplay between the MHC, microbiota and odor, and their roles in chemical communication.

Level thesis:degree_level

thesis.doctoral

Grantor dc:publisher

Universität Bielefeld

Year

2025

Author dc:creator

• Schubert, Nadine

Repository record source_url

https://pub.uni-bielefeld.de/record/3005703

OAI identifier oai:identifier

oai:pub.uni-bielefeld.de:3005703