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What mandrills leave behind: using fecal samples to characterize the major histocompatibility complex in a threatened primate

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Abstract

The major histocompatibility complex (MHC) can be useful in guiding conservation planning because of its influence on immunity, fitness, and reproductive ecology in vertebrates. The mandrill (Mandrillus sphinx) is a threatened primate endemic to central Africa. Considerable research in this species has shown that the MHC is important for disease resistance, mate choice, and reproductive success. However, all previous MHC research in mandrills has focused on an inbred semi-captive population, so their genetic diversity may have been underestimated. Here we expand our current knowledge of mandrill MHC variation by performing next-generation sequencing of non-invasively collected fecal samples from a large wild horde in central Gabon. We observe MHC lineages and alleles shared with other primates, and we uncover 45 putative new class II MHC DRB alleles, including representatives of the DRB9 pseudogene, which has not previously been identified in mandrills. We also document methodological challenges associated with fecal samples in NGS-based MHC research. Even with high read depth, the replicability of alleles from fecal samples was lower than that of tissue samples, and allele assignments are inconsistent between sample types. Further, the common assumption that variants with very high read depth should represent true alleles does not appear to be reliable for fecal samples. Nevertheless, the use of degraded DNA in the present study still enabled significant progress in quantifying immunogenetic diversity and its evolution in wild primates.

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Data availability

Replicability data, MHC allele sequences, consensus MHC allele assignments, and Python scripts will be stored at DataDryad.org. MHC nucleotide and amino acid sequences have also been provided in the Supplementary Material.

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Acknowledgements

We deeply appreciate the aid we received from the staff of the Station d’Etudes des Gorilles et Chimpanzés (SEGC), Gabon, who acted as field guides and assisted in sample collection. We thank the many undergraduate assistants who helped with lab work for this project: Ibraheem Hachem, Justine Davis, Shyla Irthum, Kaleb Hill, Gina Kissee, Claire Melancon, Patrick Hall and Gabrielle Sehon. We also thank the Agence National des Parcs Nationaux (ANPN) and the Centre National de la Recherche Scientifique et Technologique (CENAREST) for research permits No. AR0023/17/MESRSFC/CENAREST/CG/CST/CSAR; AR0036/16/MESRSFC/CENAREST/CG/CST/CSAR and LNP entry permits No. AE17 O 1 6/PR/ANPN/SE/CS/AFKP; AE16025/PR/ANPN/SE/CS/AFKP. We also thank the Audubon Nature Institute for their support.

Funding

We are grateful for the financial support provided by the Freeport McMoran Endowed Chair awarded by the Audubon Nature Institute to Nicola Anthony (University of New Orleans, US), and for support from the University of New Orleans Office of Research (ORSP) (Award #CON000000002361).

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All authors collaboratively conceived of the study topic and design. AW, AGM, and DL collected samples. AW and AGM performed laboratory work, and AW, JL, CvO, and NA planned and performed data analysis. The manuscript was written by AW, with input from all authors.

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Correspondence to Nicola Anthony.

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The authors declare no competing interests.

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Weber, A., Lighten, J., van Oosterhout, C. et al. What mandrills leave behind: using fecal samples to characterize the major histocompatibility complex in a threatened primate. Conserv Genet 25, 533–549 (2024). https://doi.org/10.1007/s10592-023-01587-2

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  • DOI: https://doi.org/10.1007/s10592-023-01587-2

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