Genetic and behavioral correlates of pair living in coppery titi monkeys (Plecturocebus cupreus)
von Sofya Dolotovskaya
Datum der mündl. Prüfung:2020-10-07
Betreuer:Prof. Dr. Eckhard W. Heymann
Gutachter:Prof. Dr. Eckhard W. Heymann
Gutachter:Prof. Dr. Julia Fischer
EnglischThe 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. 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 maintenance in exchange for services provided by males. These services, in addition to the territorial defense, include intensive infant care and protection from predators. The analysis of activity budgets and diet composition in caring adults indicated that after infant birth, females foraged more and consumed more protein-rich food (arthropods) than before. This would probably not be possible if the females had to carry the infants themselves, because arthropod foraging is not well compatible with infant carrying. And indeed, males foraged less and consumed less arthropods when they were carrying infants. In line with these findings, grooming between pair mates was more heavily skewed toward female investment during the period of infant dependency, when male services are most needed. Finally, males provided protection from predators, as their anti-predator behavior was more active than that of females. Altogether, these findings indicate that while females maintain the pair bond, males provide services important to females, namely infant care, protection from predators and territorial defense. In conclusion, this study indicates that three factors are important for maintaining social and genetic monogamy in coppery titis: pair bond, male care and possibilities for unconstrained dispersal. Strong pair bond, supported by contributions of both pair mates, likely limits the opportunities for extra-pair copulations and thus maintains genetic monogamy. Hight level of male care helps to reinforce social and genetic monogamy by freeing the female from the costs of infant carrying. This allows the females to forage more to compensate for the energetic costs of lactation, presumably contributing to their increased fecundity, and also makes the males more attractive to the females. Finally, unconstrained dispersal likely helps to maintain both social and genetic monogamy by preventing deviations from pair-living and keeping the inbreeding at a low level. In sum, these findings demonstrate that not only the components of social system (pair bond and male care) but also habitat characteristics (possibility for unconstrained dispersal) can play important roles in maintaining pair living and promoting genetic monogamy in pair-living species.
Keywords: monogamy, pair-living, titi monkeys, Neotropical primates