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The Interplay of Landscape Features and Social System on the Genetic Structure of a Primate Population: An Agent-Based Simulation Study Using “Tamarins”

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Abstract

Tamarins are small-bodied, forest-dwelling, callitrichines that live in groups containing one to a few adult individuals of each sex. Within these groups, reproduction is usually heavily skewed toward a single dominant male and dominant female, females commonly give birth to cooperatively reared twin offspring, and individuals of both sexes disperse, most often to adjacent groups. Throughout their geographic range, tamarin species are being subject to habitat loss and fragmentation, which may influence their ability to survive and disperse successfully. Here, we use a spatially explicit agent-based population genetics simulation toolkit (GENESYS) to explore the potential effects of social structure and landscape features on the population genetic structure of tamarin primates. We first model the population genetic consequences of tamarin social organization in a homogeneous landscape unconstrained by any barriers to gene flow. We then repeat our analyses using the same social system parameters but in different landscapes that either introduce a barrier to gene flow that restricts dispersal from one half of the model world to the other or divide the world into regions with differing “permeabilities” to dispersal. Our results demonstrate that, in our simulated populations, the social system of tamarins results in the clear and rapid genetic differentiation of social groups within a very short time frame. Over time, the limited dispersal of both males and females leads to a pattern of isolation by distance, as expected from a stepping-stone model of gene flow among groups. Introducing a barrier results in a somewhat more complex pattern: isolation by distance still obtains among social groups within regions on each side of the barrier, but the barrier has a much more significant effect on the structuring of genetic variation, leading to strong genetic differentiation among groups on opposite sides that becomes more pronounced over time. Introducing a region of limited dispersal permeability also results in strong differentiation of groups across that region, even though gene flow throughout the landscape is still possible. Our study demonstrates the utility of the GENESYS toolkit for modeling, in silico, the genetic consequences of many features of the social systems of primates and other group-living animals and for simultaneously exploring the effects of landscape features on spatial genetic structure.

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Acknowledgments

We thank Noah Snyder-Mackler, Lauren Brent, and Amanda Melin for their invitation to participate in the symposium, “Inside the Black Box: The Genetic Basis of Primate Behavior” at the XXIVth Congress of the International Primatological Society in Cancun, Mexico, and to contribute to this special issue of the International Journal of Primatology. A. Di Fiore also thanks Nelly Ménard for the invitation to participate in the SOCIOR Conference (“Social Systems: Demographic and Genetic Issues”) at the Station Biologique de Paimport of the Université de Rennes 1 and Mary Blair for the invitation to participate in the symposium “Landscape Genetics in Primates: New Methods and Applications” at the XXIIIrd Congress of the International Primatological Society in Kyoto, Japan, where early versions of the GENESYS model were first presented. Helpful comments on this study were also provided by Andrew Barr, Kelsey Ellis, Mariah Hopkins, Addison Kemp, and other participants in the 2012–13 Informal Physical Anthropology Seminar group at the University of Texas at Austin. Finally, we especially thank guest editor Amanda Melin and two anonymous reviewers for providing very thoughtful and constructive comments on an earlier version of this manuscript.

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Di Fiore, A., Valencia, L.M. The Interplay of Landscape Features and Social System on the Genetic Structure of a Primate Population: An Agent-Based Simulation Study Using “Tamarins”. Int J Primatol 35, 226–257 (2014). https://doi.org/10.1007/s10764-013-9726-4

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