Genetic and Behavioral Correlates of Pair Living in Coppery Titi Monkeys, Plecturocebus Cupreus
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Genetic and behavioral correlates of pair living in coppery titi monkeys (Plecturocebus cupreus) Dissertation for the award of the degree "Doctor of Philosophy" Ph.D. Division of Mathematics and Natural Sciences of the Georg-August-Universität Göttingen within the doctoral program Biodiversity and Ecology of the Georg-August University School of Science (GAUSS) Submitted by Sofya Dolotovskaya From Ufa, Russia Göttingen, 2020 Thesis Committee Prof. Dr. Eckhard W. Heymann, Department of Behavioral Ecology and Sociobiology, German Primate Center, Germany PD Dr. Christian Roos, Primate Genetics Laboratory, German Primate Center, Germany PD Dr. Oliver Schülke, Department of Behavioral Ecology, Johann-Friedrich-Blumenbach- Institute for Zoology & Anthropology, University of Göttingen, Germany Members of the Examination Board Reviewer: Prof. Dr. Eckhard W. Heymann, Department of Behavioral Ecology and Sociobiology, German Primate Center, Germany Second reviewer: Prof. Dr. Julia Fischer, Cognitive Ethology Laboratory, German Primate Center, Germany Further members of the Examination Board PD Dr. Christian Roos, Primate Genetics Laboratory, German Primate Center, Germany PD Dr. Oliver Schülke, Department of Behavioral Ecology, Johann-Friedrich-Blumenbach- Institute for Zoology & Anthropology, University of Göttingen, Germany Prof. Dr. Mark Maraun, Johann-Friedrich-Blumenbach-Institute for Zoology & Anthropology, University of Göttingen, Germany Dr. Sven Bradler, Department of Animal Evolution and Biodiversity, Johann-Friedrich- Blumenbach-Institute for Zoology & Anthropology, University of Göttingen, Germany Date of the oral examination: 7 October 2020 CONTENTS SUMMARY ................................................................................................................................................. 1 CHAPTER 1: GENERAL INTRODUCTION......................................................................................................... 3 1.1. What is “monogamy”: a word on the terminology ...................................................................................... 3 1.2. Why does “monogamy” occur: an overview of hypotheses and comparative studies................................. 4 1.3. Genetic monogamy: ultimate drivers and proximate mechanisms .............................................................. 7 1.4. Thesis aims .................................................................................................................................................. 11 CHAPTER 2: GENERAL METHODS ............................................................................................................... 13 2.1. Biology of titi monkeys................................................................................................................................ 13 2.2. Study site ..................................................................................................................................................... 16 2.3. Study animals and habituation ................................................................................................................... 16 2.4. Data collection: outline ............................................................................................................................... 18 CHAPTER 3: GENETIC MONOGAMY AND MATE CHOICE IN A PAIR-LIVING PRIMATE .................................... 19 CHAPTER 4: WHAT MAKES A PAIR BOND IN A NEOTROPICAL PRIMATE: FEMALE AND MALE CONTRIBUTIONS ................................................................................................................................................................ 42 CHAPTER 5: DO LESS OR EAT MORE: STRATEGIES TO COPE WITH COSTS OF PARENTAL CARE IN A PAIR-LIVING MONKEY .................................................................................................................................................. 56 CHAPTER 6: ACTIVE ANTI-PREDATOR BEHAVIOUR IN RED TITI MONKEYS (Plecturocebus cupreus) ............... 72 CHAPTER 7: GENERAL DISCUSSION ............................................................................................................ 81 7.1. Summary of major findings......................................................................................................................... 81 7.2. Synthesis ..................................................................................................................................................... 83 7.3. Open questions and future research directions .......................................................................................... 98 ACKNOWLEDGEMENTS ........................................................................................................................... 101 REFERENCES ........................................................................................................................................... 103 APPENDIX .............................................................................................................................................. 118 Supplementary information to Chapter 3 ........................................................................................................ 118 Supplementary information to Chapter 4 ........................................................................................................ 126 Supplementary information to Chapter 5 ........................................................................................................ 130 DECLARATION ........................................................................................................................................ 133 Summary SUMMARY The occurrence of monogamy in mammals represents an evolutionary puzzle. Because of reduced parental investment, males are expected to increase their reproductive success by mating with multiple females rather than being committed to one mate. Still, some mammals are socially monogamous, or pair living, and several species are even genetically monogamous. In some pair-living species, “monogamy package” further includes biparental care and pair bonding. To understand why monogamy occurs, it is necessary to examine the relationships between different elements of this package and the factors that influence them. Neotropical titi monkeys of genera Callicebus, Plecturocebus, and Cheracebus are not only socially monogamous, but also have a remarkably high level of male care, where infants are carried almost exclusively by males, and form strong pair bonds, a rare combination among mammals. The aim of this study was to investigate whether this combination is translated into genetic monogamy and which mechanisms help to maintain this social system. To achieve this, I examined mating system and its genetic and behavioral correlates in a wild population of coppery titis, Plecturocebus cupreus, at the Estación Biológica Quebrada Blanco in Peruvian Amazon. I collected fecal samples for genetic analyses from 41 individuals of 14 family groups, including 18 offspring of nine family groups (up to five offspring generations per group). Seven of these groups were also subject to behavioral observations, during which I collected data on social interactions, activity budgets and territorial behaviors of adult males and females (total sampling time 2749 h, focal observation time 384 h, 14 months in total). I showed that coppery titis were mostly genetically monogamous, as paternity analyses based on 18 microsatellite loci found no cases of extra-pair paternity. As the costs of pairing with closely related or incompatible mate can be high in monogamous species, I further examined if mate choice was based on relatedness or heterozygosity. Mating was random with regard to relatedness and heterozygosity. Relatedness between mates in ten observed pairs did not differ from the average relatedness in randomly generated pairs, and heterozygosity of mates was not correlated. Despite the absence of evidence for active inbreeding avoidance via mate choice, pair mates were on average not related (mean r = -0.033). To see if this low relatedness could be explained by natal dispersal, I conducted spatial genetic analysis. No spatial genetic structure was found in either sex, indicating that dispersal was opportunistic, with both sexes migrating over varying distances. These findings suggest that even opportunistic dispersal, as long as it is unconstrained, can generate sufficient genetic diversity in the population to prevent inbreeding. As pair-living species are known to sometimes engage in extra-pair copulations to minimize inbreeding, the sufficient genetic diversity can help to maintain genetic monogamy by rendering these extra-pair copulations unnecessary. 1 Summary At our study site, unconstrained dispersal was likely facilitated by the relatively low population density in undisturbed habitat. To investigate behavioral mechanisms of monogamy maintenance, I examined female and male contributions to the pair bond, territorial defense, and infant care. Females were found to contribute more than males to the maintenance of proximity and affiliation within pairs. They groomed males more than vice versa and made most of the approaches and leaves within pairs. Males, on the other hand, contributed more than females to the territorial defense, participating in the intergroup encounters more often and more actively. These findings are consistent with the concept of a pair bond as an exchange of services, where females contribute to proximity and affiliation