Pharaoh ant Monomorium pharaonis queen and workers,©Luigi Pontieri

We study the genetic and behavioral underpinnings of complex social systems in order to understand how these systems function and evolve. We are especially interested in how social interactions affect genetic architecture and trait evolution.

We use social insects, such as the pharaoh ant pictured above, as a study system because they are exemplar social systems and are also well-established models for research in social evolution, behavioral genetics, and collective behavior.

word cloud illustrating common words used in publications

Recent Publications

Linksvayer, T. A., & Wade M. J. (2016).  Theoretical predictions for sociogenomic data: the effects of kin selection and sex-limited expression on the evolution of social insect genomes. Frontiers in Ecology and Evolution. 4, 65. Abstractlinksvayer_and_wade_2016_predictions_for_sociogenomic_data.pdf

Kin selection theory has always been explicitly genetic and has long been invoked to explain the evolution of the sterile worker caste in the social insects. However, sociogenomic studies of the evolution and genomic basis of social insect caste have been largely disconnected from kin selection theory and other related genetic theories of social evolution. Two previous population genetic models make testable predictions for patterns of sequence diversity for genes shaped indirectly by kin selection compared to genes shaped directly by natural selection, but there is some confusion in the literature regarding the predicted effects of kin selection and sex-limited expression on molecular evolution. We review the previous models and then use a simple parental effect model to clarify that the two factors, kin selection and sex-limited expression, are distinct and each has a separate effect on the expected patterns of molecular evolution. We further build on the previous models to show how categories of genes in social insect genomes with diverse combinations of fitness effects (direct, parental, sib, and offspring) and patterns of sex-limitation are predicted to evolve. We discuss how caste- and sex-specific transcriptomic profiling, coupled with population genomic data, can be used to identify different functional categories of genes and subsequently test whether observed patterns of molecular evolution fit theoretical predictions.

Tarpy, D. R., Simone-Finstrom M., & Linksvayer T. A. (2016).  Honey bee colonies regulate queen reproductive traits by controlling which queens survive to adulthood. Insectes Sociaux. 63, 169-174. Abstracttarpy_et_al_2016_insectes_sociaux.pdf

The production of new queens in honey bee colonies is one of the most important determinants of reproductive success, and it involves cooperative behavior among hundreds or thousands of workers. Colony members are generally expected to benefit by optimizing the reproductive traits of prospective replacement queens, but potential conflicts of interest among colony members could result in suboptimal queens. We studied the degree to which colonies regulate adult queen traits by controlling access to developing queens that survived from pupation to adulthood. We also searched for evidence of strong conflict among patrilines by comparing the contribution of patrilines to new queens and new workers, although we found no evidence for the existence of significantly queen-biased patrilines or for any association between patriline contribution to new queens and queen traits. However, adult queens emerging from cells accessible to workers were larger in terms of wet mass and thorax width compared to adult queens emerging from cells that were not accessible to workers. These results suggest that colonies regulate queen quality traits by curtailing low-quality queens from fully developing, which is further evidence that cooperation predominates over potential conflict within honey bee colonies.

Akçay, E., Linksvayer T. A., & Van Cleve J. (2015).  Bridging social evolution theory and emerging empirical approaches to social behavior. Current Opinion in Behavioral Sciences. 6, 59-64. Abstractakcay_et_al_2015_current_opinion.pdf

Spurred on by technological advances, the last several years have seen an explosion of studies of behavioral, genomic, and neurophysiological mechanisms of social behaviors. Yet these empirical studies and the vast amount of data they produce are typically disconnected from well-established social evolution theory. We argue that unlocking the transformative potential of the emerging empirical approaches to social behavior requires new kinds of theoretical approaches that integrate proximate behavioral, genomic, and neurophysiological mechanisms with evolutionary dynamics. We review recent efforts in this direction that show how proximate mechanisms are important for evolutionary dynamics. However, we argue that these frameworks are still too distant from empirical systems to interface with emerging datasets. As an example of improved approaches that can be developed, we focus on the evolution of social gene regulatory networks, and discuss how integrating dynamics of gene regulatory networks with social evolution theory can result in rigorous hypotheses that are testable with sociogenomic data.

Vojvodic, S., Johnson B. R., Harpur B., Kent C., Zayed A., Anderson K. E., & Linksvayer T. A. (2015).  The transcriptomic and evolutionary signature of social interactions regulating honey bee caste development. Ecology and Evolution. DOI: 10.1002/ece3.1720. Abstractvojvodic_et_al-2015-ecology_and_evolution.pdf

The caste fate of developing female honey bee larvae is strictly socially regulated by adult nurse workers. As a result of this social regulation, nurse-expressed genes as well as larval-expressed genes may affect caste expression and evolution. We used a novel transcriptomic approach to identify genes with putative direct and indirect effects on honey bee caste development, and we subsequently studied the relative rates of molecular evolution at these caste-associated genes. We experimentally induced the production of new queens by removing the current colony queen, and we used RNA sequencing to study the gene expression profiles of both developing larvae and their caregiving nurses before and after queen removal. By comparing the gene expression profiles of queen-destined versus worker-destined larvae as well as nurses observed feeding these two types of larvae, we identified larval and nurse genes associated with caste development. Of 950 differentially expressed genes associated with caste, 82% were expressed in larvae with putative direct effects on larval caste, and 18% were expressed in nurses with putative indirect effects on caste. Estimated selection
coefficients suggest that both nurse and larval genes putatively associated with caste are rapidly evolving, especially those genes associated with worker development. Altogether, our results suggest that indirect effect genes play important roles in both the expression and evolution of socially influenced traits such as
caste.

Keller, K., Ishak H. D., Linksvayer T. A., & Mueller U. G. (2015).  Bacterial community composition and diversity in an ancestral ant fungus symbiosis. FEMS Microbiology Ecology. 91, fiv073. Abstract

Editor’s Choice article for issue 91.7 of FEMS Microbiology Ecology

kellner_et_al_2015.pdf

Fungus-farming ants (Hymenoptera: Formicidae, Attini) exhibit some of the most complex microbial symbioses because both macroscopic partners (ants and fungus) are associated with a rich community of microorganisms. The ant and fungal microbiomes are thought to serve important beneficial nutritional and defensive roles in these symbioses. While most recent research has investigated the bacterial communities in the higher attines (e.g., the leaf cutter ant genera Atta and Acromyrmex), which are often associated with antibiotic-producing Actinobacteria, very little is known about the microbial communities in basal lineages, labeled as “lower attines”, which retain the ancestral traits of smaller and more simple societies. In this study we used 16S-amplicon pyrosequencing to characterize bacterial communities of the lower attine ant Mycocepurus smithii among seven sampling sites in central Panama. We discovered that ant and fungus garden associated microbiota were distinct from surrounding soil, but unlike the situation in the derived fungus-gardening ants, which show distinct ant and fungal microbiomes, microbial community structure of the ants and their fungi were similar. Another surprising finding was that the abundance of Actinomycete bacteria was low and instead, these symbioses were characterized by an abundance of Lactobacillus and Pantoea bacteria. Furthermore, our data indicate that Lactobacillus strains are acquired from the environment rather than acquired vertically.

Linksvayer, T. A. (2015).  The molecular and evolutionary genetic implications of being truly social for the social insects. Advances in Insect Physiology. 48, 271-292. Abstractlinksvayer_2015_aip_molecular_and_evolutionary_genetic_implications_of_social_life.pdf

The social complexity that characterizes the eusocial insects strongly affects all aspects
of social insect life, including the molecular and evolutionary genetic basis of social
insect traits. Quantitative genetic theory and empirical approaches have been developed
over the past 60 years specifically to study the genetic implications of social interactions.
Surprisingly, given the obvious biological importance of social interactions in
social insects, this research tradition has been and continues to be widely overlooked
throughout the social insect literature, including in recent sociogenomic studies
focused on understanding the molecular underpinnings of social life. Instead, the overwhelming
majority of social insect genetic research has relied on conventional genetic
approaches developed for solitary organisms focused on the one-to-one association of
an individual's genes to its own traits. I survey social insect studies that conclusively
demonstrate the importance of indirect genetic effects (IGEs), which arise from social
interactions, for social insect trait expression and evolution. I explain why these genetically
based social effects are expected to be ubiquitous in social insects and I explain the
relevance of the IGE framework, originally developed within quantitative genetics, for
molecular genetic studies of social insect traits such as behaviour and caste. I discuss
the problems of ignoring IGEs and relying solely on conventional direct genetic effect
approaches. Finally, I discuss the strong potential of using the IGE approach and other
more systems-level-focused approaches to complement conventional reductionist
approaches in elucidating the genetic basis of social insect trait expression and
evolution.

Mikheyev, A. S., & Linksvayer T. A. (2015).  Genes associated with ant social behavior show distinct transcriptional and evolutionary patterns. eLife. 4, e04775. Abstractmikheyev_and_linksvayer_2015_elife.pdf

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.

Pontieri, L., Vojvodic S., Graham R., Pedersen J. S., & Linksvayer T. A. (2014).  Ant colonies prefer infected over uninfected nest sites. PLoS ONE. 9, e111961. Abstract

Nova Next story discussing Pontieri et al. 2014

New York Times story about waste management mentioning Pontieri et al. 2014

pontierial.2014.plos-onesi.pdf

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.