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Multi-scale predictors of parasite risk in wild male savanna baboons (Papio cynocephalus)

  • Bobby HabigEmail author
  • David A. W. A. M. Jansen
  • Mercy Y. Akinyi
  • Laurence R. Gesquiere
  • Susan C. Alberts
  • Elizabeth A. Archie
Original Article

Abstract

Several factors are thought to shape male parasite risk in polygynous and polygynandrous mammals, including male-male competition, investment in potentially immunosuppressive hormones, and dispersal. Parasitism is also driven by processes occurring at larger scales, including host social groups and populations. To date, studies that test parasite-related costs of male behavior at all three scales—individual hosts, social groups, and the host population—remain rare. To fill this gap, we investigated multi-scale predictors of helminth parasitism in 97 male savanna baboons (Papio cynocephalus) living in the Amboseli ecosystem in Kenya over a 5-year span. Controlling for multi-scale processes, we found that many of the classic indicators of male mating effort—high dominance rank, testosterone, and glucocorticoids—did not predict helminth infection risk. However, we identified two parasite-related costs associated with male behavior: (i) socially connected males exhibited higher Trichuris trichiura egg counts and greater parasite species richness than socially isolated males and (ii) males with stable group residency exhibited higher parasite species richness than males who frequently dispersed to new social groups. At the population level, males harbored more parasites following periods of drought than rainfall. Lastly, parasites exhibited positive covariance suggesting that infection risk increases if a host already harbors one or more parasite taxa. These results indicate that multi-scale processes are important in driving male parasite risk and that some aspects of male behavior are costly. Together, our results provide an unusually holistic perspective on the drivers of parasite risk in the context of male behaviors and life histories.

Significance statement

Infection by gastrointestinal helminths can have major consequences for host fitness, especially in the context of male mating effort. Multi-scale processes—from the host to its social group and population—are important for understanding key drivers of parasitism. We leveraged long-term data from one of the longest running behavioral ecology studies of a wild primate population in the world, the well-studied Amboseli baboon population in Kenya. We found that traditional indicators of male mating effort (attaining high dominance rank, high testosterone and glucocorticoids) did not predict parasitism. However, male social connectedness to females, competitive group demography, and harsh weather were all associated with higher parasitism. Because socially connected males faced the highest parasite risk, males may face a tradeoff between male-female relationships and parasitism. Our results show how processes at multiple scales contribute to variation in male parasite risk.

Keywords

Dominance rank Glucocorticoids Papio cynocephalus Parasitism Social connectedness Testosterone 

Notes

Acknowledgments

We gratefully acknowledge Kenya Wildlife Services, Institute of Primate Research, National Museums of Kenya, National Council for Science and Technology, and members of the Amboseli-Longido pastoralist communities for their cooperation and assistance. We are grateful to Jeanne Altmann for her leadership and collaboration in producing behavioral and demographic data on the Amboseli baboons. The ABRP field team (R.S. Mututua, S. Sayialel, and J.K. Warutere) provided expert assistance with data collection; T. Wango and V. Oudo provided assistance with fecal sample processing. We also thank N. Learn, J. Gordon, and K. Pinc for database design and management. For a complete set of acknowledgments of funding sources, logistical assistance, and data collection and management, please visit http://amboselibaboons.nd.edu/acknowledgements/. We would also like to thank David P. Watts, Justin Wilcox, and an anonymous reviewer for providing commentary on previous drafts of this manuscript.

Funding information

This research was supported by the National Science Foundation and the National Institute on Aging, currently through NSF IOS 1456832 and through NIH R01AG053330, R01HD088558, and P01AG031719.

Compliance with ethical standards

Ethical standards

All applicable international, national, and/or institutional guidelines for the care and use of animals were followed. All protocols were approved by the Institutional Animal Care and Use Committees at Duke University (A0840903) and the University of Notre Dame (13-11-1352).

Conflict of interest

The authors declare that they have no conflict of interest.

Supplementary material

265_2019_2748_MOESM1_ESM.docx (42 kb)
ESM 1 (DOCX 42 kb)

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Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2019

Authors and Affiliations

  1. 1.Department of Biological SciencesUniversity of Notre DameNotre DameUSA
  2. 2.Department of Biology, Queens CollegeCity University of New YorkNew YorkUSA
  3. 3.Departments of Biology and Evolutionary AnthropologyDuke UniversityDurhamUSA
  4. 4.Institute of Primate ResearchNational Museums of KenyaNairobiKenya

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