Elucidating the Evolutionary Consequences of Sociality Through Genome-wide Analyses of Social and Solitary Mammals

Social affiliation and group living are seminal aspects of some of the most exciting and intensely studied topics in behavioral biology, from the field of human psychopathology to investigations of cooperation and reproductive skew in animal societies. Understanding how and why sociality evolves as an alternative to the much more common trait of solitary living has long been a topic of special interest among biologists, particularly in light of evidence that group living can impose a number of costs (e.g., increased exposure to pathogens or increased resource competition) that can negatively impact direct fitness. It is hypothesized that sociality only evolves when the benefits associated with cooperation outweigh the costs of competition. Social animals are therefore likely exposed to a unique set of evolutionary pressures as a result of the distinct costs and benefits inherent to their gregarious lifestyles, and social animals should consequently exhibit adaptations that specifically counterbalance the costs associated with sociality. For my dissertation, I set out to explore the evolutionary consequences of sociality by investigating patterns of genomic variation and change in social and solitary animals from a population-level and a broad, comparative perspective, respectively.The first two chapters of my dissertation serve as a comparative case study on the impacts of sociality on population structure in a novel rodent system. I present population-level genomic data from two species of pebble-mound mice (genus Pseudomys, family Muridae) endemic to mainland Australia: the solitary Queensland pebble-mound mouse (P. patrius) and the social Ngadji (P. chapmani). Like other pebble-mound mice, these focal species construct large aggregations of pebbles over their subterranean burrows that, although not necessary for survival, are required by females for mating. As a result of their distinct social systems, these closely related and ecologically similar congeners serve as compelling point of comparison. By characterizing patterns of genomic variation within each of these species, I demonstrate differences in population structure between the two species, particularly in relationship to pebble-mounds and kinship. In Chapter 1, I demonstrate that the Queensland pebble-mound mouse exhibits significant evidence of kin structure despite being solitary. In this particular case, kin structure seems to arise as a result of the spatially fixed resources (i.e., pebble-mounds) sought out by females. Because affiliations among close kin are very typical of social animals, these findings raise questions about how social and solitary animals might aggregate differently. These questions are then addressed in Chapter 2, where I demonstrate that the social Ngadji also exhibits kin stratification around pebble-mounds, but on a much broader scale than in the Queensland pebble-mound mouse. Beyond describing the molecular ecology of these two non-model species, this work demonstrates that population-level studies that utilize comparative frameworks of closely related and ecologically similar species can provide insights into the impacts of sociality on dispersal and mating system that might inform future studies on the ecological conditions and behavioral mechanisms underlying group living.Whereas the first two chapters consider the impacts of social system on general, population-level processes, the final chapter tests an explicit hypothesis about the evolutionary consequences of sociality on a broader comparative scale. Of all the proposed costs associated with group living, increased exposure to pathogens may be one of the most important: not only are pathogen exposure and disease susceptibility are two of the greatest influences on an individual’s reproductive success, but communicable diseases are known to thrive in communities characterized by group living and high rates of conspecific interaction. However, attempts to explicitly demonstrate the putative immunological consequences of sociality have historically proven difficult. For example, consider two ecologically similar species that share recent common ancestry but demonstrate distinct social organizations. One might attempt to characterize differences in immune pressures by measuring differences in pathogen exposure or parasite loads between the two species. However, divergence among species generally leads to divergence among their respective pathogens and parasites, such that measures of pathogen or parasite loads may become entirely incomparable between the two species. Similarly, this approach assumes that no adaptations (physiological, behavioral, or otherwise) have arisen since the divergence of the two species that might counteract their respective immune pressures. Rather than attempting to quantify the extent of immune-related evolutionary pressures by assessing pathogen or parasite prevalence, Chapter 3 characterizes the relative pathogen-mediated pressure acting on social and solitary species by assessing positive selection in immune orthologues from nine species across three divergent mammal lineages. These analyses demonstrate that relatively social and solitary mammals experience distinct evolutionary pressures, with group-living species experiencing faster rates of evolution at immune loci. When considered in conjunction with candidate loci studies in more limited taxonomic comparisons, these findings suggest that increased immune burden is one of the more common costs associated with sociality