SOCIAL EVOLUTION IN ANTS: DIRECT AND INDIRECT GENETIC EFFECTS

Thesis (PhD) - Indiana University, Ecology and Evolutionary Biology, 2005When social interactions occur, the phenotype of an individual can be influenced both directly by its own genes and indirectly by genes expressed in social partners. Eusocial insect colonies are notable for extensive behavioral interactions among larval, worker, and queen nestmates. In particular, developing larvae are reliant on care provided by workers and queens. Social insect phenotypes are thus affected by zygotic genes expressed during development (direct genetic effects), genes expressed in care-giving adult workers (sibsocial genetic effects), and genes expressed in queens (maternal genetic effects). The purpose of this dissertation was to incorporate this complexity into models of social insect evolution and to empirically study the evolutionary importance of direct and indirect genetic effects on ant phenotypes. The first chapter reviews existing models for the evolutionary origin and maintenance of eusociality in social insects and proposes a new model incorporating both direct and indirect genetic effects. The second chapter uses a quantitative genetic approach to estimate variation for direct and indirect genetic effects on worker, gyne, and male mass, caste ratio, and sex ratio within a population of the ant Temnothorax curvispinosus. There was genetic variation for direct, maternal, and sibsocial effects for all traits, suggesting that larval, queen, and worker influences on mass, caste ratio, and sex ratio can respond to selection. However, there was also evidence for negative genetic correlations between each effect, demonstrating a potential constraint to the independent evolution of these effects. The third chapter uses the same ant colonies to study the effects of experimental queen removal and manipulation of relatedness among workers and larvae on mean colony worker, gyne, and male mass, caste ratio, and sex ratio. The fourth chapter examines the contribution of direct and sibsocial genetic effects to phenotypic differences between three Temnothorax species. The results demonstrate that among-species differences are influenced by the interaction of genes expressed in developing larvae and care-giving workers. Overall, this dissertation demonstrates the evolutionary importance of both direct and indirect genetic effects to social insect phenotypes

Ant Species Differences Determined by Epistasis between Brood and Worker Genomes

Epistasis arising from physiological interactions between gene products often contributes to species differences, particularly those involved in reproductive isolation. In social organisms, phenotypes are influenced by the genotypes of multiple interacting individuals. In theory, social interactions can give rise to an additional type of epistasis between the genomes of social partners that can contribute to species differences. Using a full-factorial cross-fostering design with three species of closely related Temnothorax ants, I found that adult worker size was determined by an interaction between the genotypes of developing brood and care-giving workers, i.e. intergenomic epistasis. Such intergenomic social epistasis provides a strong signature of coevolution between social partners. These results demonstrate that just as physiologically interacting genes coevolve, diverge, and contribute to species differences, so do socially interacting genes. Coevolution and conflict between social partners, especially relatives such as parents and offspring, has long been recognized as having widespread evolutionary effects. This coevolutionary process may often result in coevolved socially-interacting gene complexes that contribute to species differences

Genes associated with ant social behavior show distinct transcriptional and evolutionary patterns

Studies of the genetic basis and evolution of complex social behavior emphasize either conserved or novel genes. To begin to reconcile these perspectives, we studied how the evolutionary conservation of genes associated with social behavior depends on regulatory context, and whether genes associated with social behavior exist in distinct regulatory and evolutionary contexts. We identified modules of co-expressed genes associated with age-based division of labor between nurses and foragers in the ant Monomorium pharaonis, and we studied the relationship between molecular evolution, connectivity, and expression. Highly connected and expressed genes were more evolutionarily conserved, as expected. However, compared to the rest of the genome, forager-upregulated genes were much more highly connected and conserved, while nurse-upregulated genes were less connected and more evolutionarily labile. Our results indicate that the genetic architecture of social behavior includes both highly connected and conserved components as well as loosely connected and evolutionarily labile components.It was funded by University of Pennsylvania with grant name: University Research Foundation grant

Ant colonies prefer infected over uninfected nest sites

During colony relocation, the selection of a new nest involves exploration and assessment of potential sites followed by colony movement on the basis of a collective decision making process. Hygiene and pathogen load of the potential nest sites are factors worker scouts might evaluate, given the high risk of epidemics in group-living animals. Choosing nest sites free of pathogens is hypothesized to be highly efficient in invasive ants as each of their introduced populations is often an open network of nests exchanging individuals (unicolonial) with frequent relocation into new nest sites and low genetic diversity, likely making these species particularly vulnerable to parasites and diseases. We investigated the nest site preference of the invasive pharaoh ant, Monomorium pharaonis, through binary choice tests between three nest types: nests containing dead nestmates overgrown with sporulating mycelium of the entomopathogenic fungus Metarhizium brunneum (infected nests), nests containing nestmates killed by freezing (uninfected nests), and empty nests. In contrast to the expectation pharaoh ant colonies preferentially (84%) moved into the infected nest when presented with the choice of an infected and an uninfected nest. The ants had an intermediate preference for empty nests. Pharaoh ants display an overall preference for infected nests during colony relocation. While we cannot rule out that the ants are actually manipulated by the pathogen, we propose that this preference might be an adaptive strategy by the host to "immunize" the colony against future exposure to the same pathogenic fungus

Genomic Signature of Kin Selection in an Ant with Obligately Sterile Workers

Kin selection is thought to drive the evolution of cooperation and conflict, but the specific genes and genome-wide patterns shaped by kin selection are unknown. We identified thousands of genes associated with the sterile ant worker caste, the archetype of an altruistic phenotype shaped by kin selection, and then used population and comparative genomic approaches to study patterns of molecular evolution at these genes. Consistent with population genetic theoretical predictions, worker-upregulated genes experienced reduced selection compared with genes upregulated in reproductive castes. Worker-upregulated genes included more taxonomically restricted genes, indicating that the worker caste has recruited more novel genes, yet these genes also experienced reduced selection. Our study identifies a putative genomic signature of kin selection and helps to integrate emerging sociogenomic data with longstanding social evolution theory

Transcriptomic basis and evolution of the ant nurse-larval social interactome

Development is often strongly regulated by interactions among close relatives, but the underlying molecular mechanisms are largely unknown. In eusocial insects, interactions between caregiving worker nurses and larvae regulate larval development and resultant adult phenotypes. Here, we begin to characterize the social interactome regulating ant larval development by collecting and sequencing the transcriptomes of interacting nurses and larvae across time. We find that the majority of nurse and larval transcriptomes exhibit parallel expression dynamics across larval development. We leverage this widespread nurse-larva gene co-expression to infer putative social gene regulatory networks acting between nurses and larvae. Genes with the strongest inferred social effects tend to be peripheral elements of within-tissue regulatory networks and are often known to encode secreted proteins. This includes interesting candidates such as the nurse-expressed giant-lens, which may influence larval epidermal growth factor signaling, a pathway known to influence various aspects of insect development. Finally, we find that genes with the strongest signatures of social regulation tend to experience relaxed selective constraint and are evolutionarily young. Overall, our study provides a first glimpse into the molecular and evolutionary features of the social mechanisms that regulate all aspects of social life

Genomic Signature of Kin Selection in an Ant with Obligately Sterile Workers

Kin selection is thought to drive the evolution of cooperation and conflict, but the specific genes and genome-wide patterns shaped by kin selection are unknown. We identified thousands of genes associated with the sterile ant worker caste, the archetype of an altruistic phenotype shaped by kin selection, and then used population and comparative genomic approaches to study patterns of molecular evolution at these genes. Consistent with population genetic theoretical predictions, worker-upregulated genes experienced reduced selection compared with genes upregulated in reproductive castes. Worker-upregulated genes included more taxonomically restricted genes, indicating that the worker caste has recruited more novel genes, yet these genes also experienced reduced selection. Our study identifies a putative genomic signature of kin selection and helps to integrate emerging sociogenomic data with longstanding social evolution theory

Crozier’s paradox revisited: maintenance of genetic recognition systems by disassortative mating

BackgroundOrganisms are predicted to behave more favourably towards relatives, and kin-biased cooperation has been found in all domains of life from bacteria to vertebrates. Cooperation based on genetic recognition cues is paradoxical because it disproportionately benefits individuals with common phenotypes, which should erode the required cue polymorphism. Theoretical models suggest that many recognition loci likely have some secondary function that is subject to diversifying selection, keeping them variable.ResultsHere, we use individual-based simulations to investigate the hypothesis that the dual use of recognition cues to facilitate social behaviour and disassortative mating (e.g. for inbreeding avoidance) can maintain cue diversity over evolutionary time. Our model shows that when organisms mate disassortatively with respect to their recognition cues, cooperation and recognition locus diversity can persist at high values, especially when outcrossed matings produce more surviving offspring. Mating system affects cue diversity via at least four distinct mechanisms, and its effects interact with other parameters such as population structure. Also, the attrition of cue diversity is less rapid when cooperation does not require an exact cue match. Using a literature review, we show that there is abundant empirical evidence that heritable recognition cues are simultaneously used in social and sexual behaviour.ConclusionsOur models show that mate choice is one possible resolution of the paradox of genetic kin recognition, and the literature review suggests that genetic recognition cues simultaneously inform assortative cooperation and disassortative mating in a large range of taxa. However, direct evidence is scant and there is substantial scope for future work

Ant Colonies Prefer Infected over Uninfected Nest Sites

During colony relocation, the selection of a new nest involves exploration and assessment of potential sites followed by colony movement on the basis of a collective decision making process. Hygiene and pathogen load of the potential nest sites are factors worker scouts might evaluate, given the high risk of epidemics in group-living animals. Choosing nest sites free of pathogens is hypothesized to be highly efficient in invasive ants as each of their introduced populations is often an open network of nests exchanging individuals (unicolonial) with frequent relocation into new nest sites and low genetic diversity, likely making these species particularly vulnerable to parasites and diseases. We investigated the nest site preference of the invasive pharaoh ant, Monomorium pharaonis, through binary choice tests between three nest types: nests containing dead nestmates overgrown with sporulating mycelium of the entomopathogenic fungus Metarhizium brunneum (infected nests), nests containing nestmates killed by freezing (uninfected nests), and empty nests. In contrast to the expectation pharaoh ant colonies preferentially (84%) moved into the infected nest when presented with the choice of an infected and an uninfected nest. The ants had an intermediate preference for empty nests. Pharaoh ants display an overall preference for infected nests during colony relocation. While we cannot rule out that the ants are actually manipulated by the pathogen, we propose that this preference might be an adaptive strategy by the host to “immunize” the colony against future exposure to the same pathogenic fungus