The number of reproductive partners per individual varies markedly across animal mating systems. This variation may be an important determinant of patterns of immunogenetic diversity, particularly at ...Major Histocompatibility Complex (MHC) Class I and II loci. To compare immunogenetic variation in taxa with markedly different mating systems, we used RNAseq-generated data to quantify genotypic diversity in three species of Peromyscine rodents: the monogamous California mouse (Peromyscus californicus) and the polygynandrous deer mouse (P. maniculatus) and brush mouse (P. boylii). By sampling populations of these species from multiple localities in California, we were able to conduct replicated analyses of the relationship between mating system and immunogenetic variation. Across the four localities sampled, diversity at MHC Class I and II genes was consistently higher in the two polygynandrous species. We found no evidence that sampling location (i.e., variation in habitat conditions) contributed to observed differences in MHC variation among populations or species. Collectively, our data indicate that immunogenetic variation in Peromyscine mice is associated with reproductive behavior, rather than geographic locality or habitat type. The consistently greater variability detected in the polygynandrous species examined suggests that balancing selection imposed by behaviorally-mediated pathogen exposure is important in maintaining variation at MHC genes in these animals.
The gut bacterial communities of mammals have profound effects on host fitness, but the processes that generate and maintain gut bacterial diversity remain poorly understood. We mapped compositional ...variation (i.e., β-diversity) in the gut microbiotas of 136 pairs of wild mammalian species living throughout the Americas to assess how the distribution of mammals across geographic space influences the diversification of their gut bacteria. Comparing the gut microbiotas of sympatric and allopatric mammalian populations provided insights into the flow of gut bacteria within and between mammalian communities, revealing that spatial limits on bacterial dispersal promote β-diversity between the gut microbiotas of mammalian species. Each geographic locale displayed a unique gut-microbiota composition that could not be fully explained by the diets and phylogenetic histories of the resident mammalian hosts, indicating that some gut bacteria are geographically restricted. Across the western hemisphere, the compositional overlap between the gut microbiotas of allopatric mammalian populations decayed exponentially with the geographic distance separating the hosts. The relationship between geographic distances among hosts and compositional differences among their gut microbiotas was independent of dietary and phylogenetic divergence among hosts. Within mammalian communities, we observed widespread sharing of gut bacteria between predator–prey host-species pairs, indicating horizontal transfer of gut bacteria through mammalian food chains. Collectively, these results indicate that compositional differences between the gut microbiotas of mammalian taxa are generated and maintained by limits to bacterial dispersal imposed by physical distance between hosts.
•Understanding social evolution requires integration of mechanisms and function.•A general framework for the integration of proximate and ultimate analyses is lacking.•Recent advances enable an ...understanding of the evolution of the mechanistic diversity.•We propose a multidisciplinary framework to analyze the evolution of social behavior.
Social interactions are central to most animals and have a fundamental impact upon the phenotype of an individual. Social behavior (social interactions among conspecifics) represents a central challenge to the integration of the functional and mechanistic bases of complex behavior. Traditionally, studies of proximate and ultimate elements of social behavior have been conducted by distinct groups of researchers, with little communication across perceived disciplinary boundaries. However, recent technological advances, coupled with increased recognition of the substantial variation in mechanisms underlying social interactions, should compel investigators from divergent disciplines to pursue more integrative analyses of social behavior. We propose an integrative conceptual framework intended to guide researchers towards a comprehensive understanding of the evolution and maintenance of mechanisms governing variation in sociality.
Catastrophic events can significantly impact the demographic processes that shape natural populations of organisms. However, linking the outcomes of such events to specific demographic parameters is ...often challenging due to a lack of detailed pre-event data. The eruption of the Puyehue-Cordon Caulle volcanic complex on 4 June 2011 had profound consequences for the biota of southwestern Argentina. Our long-term behavioral, ecological, and demographic studies of two species of tuco-tucos (Ctenomys sociabilis and C. haigi) that occur in the region most heavily impacted by ash fall from the eruption provided an unusual opportunity to assess the effects of this event on natural populations of mammals. The post-eruption density of the study population for each species was markedly reduced compared to pre-eruption values, with the relative magnitude of this reduction being greater for the group-living C. sociabilis. The more extensive data set for this species indicated that ash fall from the eruption altered the food resources available to these animals; differences in pre- and post-eruption stable isotope signatures for fur samples from C. sociabilis were consistent with observed changes in vegetation. Per capita female reproductive success was also reduced in this species during the first breeding season following the eruption. Based on our detailed demographic records for C. sociabilis, neither survival of yearling females from 2010 to 2011 nor the percentage of unmarked females in the study population in 2011 differed from pre-eruption values. Instead, the post-eruption decrease in population density for C. sociabilis appeared to reflect reduced within-population recruitment of juvenile females to the 2011 breeding population. Although the eruption did not result in the local extinction of either study population, the demographic consequences detected are likely to have impacted the effective sizes of these populations, creating important opportunities to link specific demographic parameters to previously reported decreases in genetic variability detected after this significant natural event.
Competition among males for access to reproductive opportunities is a central tenet of behavioural biology that has critical implications for studies of mating systems, sexual selection and the ...evolution of numerous phenotypic traits. Given the expectation that males should compete vigorously for access to females, it may at first seem paradoxical that males in some species cooperate to reproduce, often resulting in the apparent sacrifice of direct fitness by some members of these cooperative partnerships. Because this form of cooperation lies at the interface between natural, sexual and kin selection, studies of the adaptive consequences of male reproductive cooperation may yield important insights into how complex and sometimes conflicting selective pressures shape individual behaviour. Here, we define and review examples of reproductive cooperation among male animals. We take an integrative approach to reviewing the potential causes of male–male cooperation, including potential adaptive hypotheses, ecological correlates, phylogenetic patterns and physiological mechanisms. The impact of male reproductive cooperation on sexual selection theory is also discussed. We conclude by outlining several important directions for future research, including efforts to improve understanding of the ecological and demographic contexts in which male reproductive cooperation occurs. Collectively, such analyses promise to improve our understanding of multiple fundamental concepts in evolutionary biology.
•Cooperation between males in reproductive contexts is an underappreciated and puzzling behaviour.•We define male–male cooperation in reproduction and identify different types of behaviours.•We list species where males engage in cooperative reproduction and describe taxonomic patterns.•We outline potential causes, from proximate to ultimate, associated with this cooperation.•Challenges and opportunities for the development of sexual selection theory are discussed.
The manner in which individual life history traits respond to the environment and to each other, and how these traits combine to form overall patterns of life history variation, remains poorly ...characterized in wild populations. We monitored breeding Dark-eyed Juncos (Junco hyemalis) across a 700-m elevational range. We compared breeding season length, temporal patterns of breeding activity, adult body size, clutch size, brood size, nestling quality, and nest mortality among elevations. We also compared environmental measures across the studied elevations to determine whether abiotic factors explained life history trait variation. We used 12 microsatellite loci to test for genetic differentiation in populations at different elevations. Finally, we constructed a computer simulation to evaluate the combined effects of observed variation in life history traits. We found differences among elevations in breeding season length and in patterns of reproductive timing, which did not match each other and which were not explained solely by abiotic factors. We found no differences among elevations in adult body size, clutch size, brood size, or nestling quality. Nest mortality increased significantly with elevation. Genetic differentiation was too low to define distinct subpopulations. The simulation suggested that differences in mortality, in combination with differences in breeding season length, contributed to substantial differences in reproductive success among elevations. Thus, although individual life history traits showed little evidence of variation in response to the environment or to each other and little genetic differentiation, variation in breeding season length and in nest mortality were potential drivers of substantial elevational variation in overall life history in this system. These results demonstrate that individual life history traits may vary substantially in their patterns of variation, and that some life history traits may have disproportionate effects on overall life history.
Identifying the factors that favor group living is central to studies of animal social behavior. One demographic parameter that is expected to substantially shape spatial and social relationships is ...population density. Specifically, high population densities may favor group living by constraining opportunities to live alone. In contrast, low densities may allow individuals to spread out within the habitat, leading to a reduction in the prevalence or size of social groups. Abrupt changes in density following natural catastrophic events provide important opportunities to evaluate the effects of population density on patterns of spatial and social organization. As part of long-term studies of the behavioral ecology of a population of highland tuco-tucos (Ctenomys opimus) at Monumento Natural Laguna de los Pozuelos, Jujuy Province, Argentina, we monitored the demographic and behavioral consequences of a flood that inundated our study site during December 2012. Unlike most species of Ctenomys studied to date, highland tuco-tucos are group living, meaning that multiple adults share burrow systems and nest sites. Despite a post-flood reduction in population density of ~75%, animals present on the study site during the 2013 breeding season continued to live in multi-adult social units (groups). No differences between pre- and post-flood home range sizes were detected and although between-unit spatial overlap was reduced in 2013, overlap within social units did not differ from that in pre-flood years. Animals assigned to the same social unit in 2013 had not lived together during 2012, indicating that post-flood groups were not simply the remnants of those present prior to the flood. Collectively, these findings indicate that group living in highland tuco-tucos is not driven by the density of conspecifics in the habitat. In addition to enhancing understanding of the adaptive bases for group living in Ctenomys, our analyses underscore the power of catastrophic events to generate insights into fundamental aspects of social behavior.
As more species undergo range shifts in response to climate change, it is increasingly important to understand the factors that determine an organism’s realized niche. Physiological limits imposed by ...abiotic factors constrain the distributions of many species. Because glucocorticoids are essential to the maintenance of physiological homeostasis, identifying glucocorticoid–environment relationships may generate critical insights into both limits on species distributions and potential responses to environmental change. We explored relationships between variability in baseline glucocorticoids and sensitivity to environmental conditions in two chipmunk species characterized by divergent patterns of spatial, genetic, and morphological change over the past century. Specifically, we investigated whether the alpine chipmunk (Tamias alpinus), which has undergone pronounced changes, displays greater glucocorticoid sensitivity to environmental parameters than the lodgepole chipmunk (T. speciosus), which has exhibited little change over the same interval. From 2013 to 2015, we collected environmental data and fecal glucocorticoid metabolite (FGM) samples from these species. Using generalized linear mixed models and a model averaging approach, we examined the impacts of environmental and individual phenotypic parameters on FGMs. We found pronounced interspecific differences, with environmental parameters being better predictors of FGMs in T. alpinus. FGMs in this species were particularly elevated in less climatically suitable habitats and in areas with higher maximum daily temperatures. Individual phenotypic traits were not predictive of FGMs in T. alpinus, although they were highly predictive for T. speciosus. Collectively, these findings support the hypothesis that T. alpinus is more sensitive to environmental change. More generally, our results suggest that both phenotypic attributes and environmental conditions contribute to FGM responses but that the relative contributions of these factors differ among taxa, including among closely related species. Finally, our analyses underscore the value of glucocorticoids as bioindicators of sensitivity to environmental change in species for which the factors affecting stress physiology have been assessed.
Elucidating the genetic mechanisms that underlie complex adaptive phenotypes is a central problem in evolutionary biology. For behavioral biologists, the ability to link variation in gene expression ...to the occurrence of specific behavioral traits has long been a largely unobtainable goal. Social interactions with conspecifics represent a fundamental component of the behavior of most animal species. Although several studies of mammals have attempted to uncover the genetic bases for social relationships using a candidate gene approach, none have attempted more comprehensive, transcriptome-based analyses using high throughout sequencing. As a first step toward improved understanding of the genetic underpinnings of mammalian sociality, we generated a reference transcriptome for the colonial tuco-tuco (Ctenomys sociabilis), a social species of subterranean rodent that is endemic to southwestern Argentina. Specifically, we analyzed over 500 million Illumina sequencing reads derived from the hippocampi of 10 colonial tuco-tucos housed in captivity under a variety of social conditions. The resulting reference transcriptome provides a critical tool for future studies aimed at exploring relationships between social environment and gene expression in this non-model species of social mammal.
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