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Pontieri, L., Schmidt A. M., Singh R., Pedersen J. S., & Linksvayer T. A. (2017).  Artificial selection on ant female caste ratio uncovers a link between female-biased sex ratios and infection by Wolbachia endosymbionts. Journal of Evolutionary Biology. 30, 225-234. Abstract

Social insect sex and caste ratios are well-studied targets of evolutionary conflicts, but the heritable factors affecting these traits remain unknown. To elucidate these factors, we carried out a short-term artificial selection study on female caste ratio in the ant Monomorium pharaonis. Across three generations of bidirectional selection, we observed no response for caste ratio, but sex ratios rapidly became more female-biased in the two replicate high selection lines and less female-biased in the two replicate low selection lines. We hypothesized that this rapid divergence for sex ratio was caused by changes in the frequency of infection by the heritable bacterial endosymbiont Wolbachia, because the initial breeding stock varied for Wolbachia infection, and Wolbachia is known to cause female-biased sex ratios in other insects. Consistent with this hypothesis, the proportions of Wolbachia-infected colonies in the selection lines changed rapidly, mirroring the sex ratio changes. Moreover, the estimated effect of Wolbachia on sex ratio (~13% female bias) was similar in colonies before and during artificial selection, indicating that this Wolbachia effect is likely independent of the effects of artificial selection on other heritable factors. Our study provides evidence for the first case of endosymbiont sex ratio manipulation in a social insect.

Warner, M. R., Mikheyev A. S., & Linksvayer T. A. (2017).  Genomic signature of kin selection in an ant with obligately sterile workers. Molecular Biology and Evolution. AbstractWebsite

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 showed relaxed adaptive evolution compared to 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 showed relaxed selection. Our study identifies a putative genomic signature of kin selection and helps to integrate emerging sociogenomic data with longstanding social evolution theory.

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.

Warner, M. R., Kovaka K., & Linksvayer T. A. (2016).  Late-instar ant worker larvae play a prominent role in colony-level caste regulation. Insectes Sociaux. doi:10.1007/s00040-016-0501-3, Abstract

The success of social insect societies is often attributed to an efficient reproductive division of labor between queen and worker castes. At the group level, social insect colonies must decide both the timing and amount of resources to allocate to each caste. Queen production is typically restricted by factors such as season or the presence of fertile queens in colonies. In the absence of such inhibition, the relative production of new queens versus workers varies between and is regulated by colonies. Here, we investigate social regulation of caste in the ant Monomorium pharaonis through a series of experiments manipulating the environment in which developing larvae are reared. The number of new queens produced depended strongly on diet as well as the number of late-instar worker larvae in the colony at the time of caste regulation. Given that these late-instar larvae are known to process solid protein for the rest of the colony, their stimulatory effect on queen production is likely a result of their contribution to a colony’s nutrient assimilation. Our results emphasize the need to consider late-instar larvae as critical social players and effectors of colony regulatory dynamics.

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.

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


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.

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.

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.

Jasper, W. C., Linksvayer T. A., Atallah J., Friedman D., Chiu J. C., & Johnson B. R. (2015).  Large scale coding sequence change underlies the evolution of post-developmental novelty in honey bees. Molecular Biology and Evolution. 32, 334-346. Abstract


Whether coding or regulatory sequence change is more important to the evolution of phenotypic novelty is one of biology's major unresolved questions. The field of evo-devo has shown that in early development changes to regulatory regions are the dominant mode of genetic change, but whether this extends to the evolution of novel phenotypes in the adult organism is unclear. Here we conduct ten RNA-Seq experiments across both novel and conserved tissues in the honey bee to determine to what extent post-developmental novelty is based on changes to the coding regions of genes. We make several discoveries. First, we show that with respect to novel physiological functions in the adult animal, positively selected tissue-specific genes of high expression underlie novelty by conferring specialized cellular functions. Such genes are often, but not always taxonomically restricted genes (TRGs). We further show that positively selected genes, whether TRGs or conserved genes, are the least connected genes within gene expression networks. Overall, this work suggests that the evo-devo paradigm is limited, and that the evolution of novelty, post-development, follows additional rules. Specifically, evo-devo stresses that high network connectedness (repeated use of the same gene in many contexts) constrains coding sequence change as it would lead to negative pleiotropic effects. Here we show that in the adult animal, the converse is true: genes with low network connectedness (TRGs and tissue-specific conserved genes) underlie novel phenotypes by rapidly changing coding sequence to perform new specialized functions.

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

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

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


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.

Linksvayer, T. A. (2014).  Eusociality. (Losos, J., Ed.).Oxford Bibliographies in Evolutionary Biology. , New York: Oxford University Press Abstract


Linksvayer, T. A. (2014).  Survival of the fittest group. Nature. doi:10.1038/nature13755.

News & Views on Pruitt and Goodnight 2014,

Kellner, K., Fernandez-Marin H., Ishak H. D., Sen R., Linksvayer T. A., & Mueller U. G. (2013).  Co-evolutionary patterns and diversification of ant-fungus associations in the asexual fungus-farming ant Mycocepurus smithii in Panama. Journal of Evolutionary Biology. 26, 1353-1362. Abstractkellner_et_al_2013_co-evolutionary_patterns_ant_fungus.pdf

Partner fidelity through vertical symbiont transmission is thought to be the primary mechanism stabilizing cooperation in the mutualism between fungus-farming (attine) ants and their cultivated fungal symbionts. An alternate or additional mechanism could be adaptive partner or symbiont choice mediating horizontal cultivar transmission or de novo domestication of free-living fungi. Using microsatellite genotyping for the attine ant Mycocepurus smithii and ITS rDNA sequencing for fungal cultivars, we provide the first detailed population genetic analysis of local ant-fungus associations to test for the relative importance of vertical vs. horizontal transmission in a single attine species. M.smithii is the only known asexual attine ant, and it is furthermore exceptional because it cultivates a far greater cultivar diversity than any other attine ant. Cultivar switching could permit the ants to re-acquire cultivars after garden loss, to purge inferior cultivars that are locally mal-adapted or that accumulated deleterious mutations under long-term asexuality. Compared to other attine ants, symbiont choice and local adaptation of ant-fungus combinations may play a more important role than partner-fidelity feedback in the co-evolutionary process of M.smithii and its fungal symbionts.

Holman, L., van Zweden J. S., Linksvayer T. A., & d'Ettorre P. (2013).  Crozier's paradox revisited: maintenance of genetic recognition systems by disassortative mating. BMC Evolutionary Biology. 13, 211. Abstractholman_et_al_2013_croziers_paradox_revisited.pdf

Background: Organisms 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.Results: Here, 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.Conclusions: Our 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.

Holman, L., Linksvayer T. A., & d'Ettorre P. (2013).  Genetic constraints on dishonesty and caste dimorphism in an ant. American Naturalist. 181, 161-170. Abstractholman_et_al_2013_genetic_constraints_on_dishonesty.pdfWebsite

The ultimate causes of honest signaling remain a subject of debate, with questions remaining over the relative importance of costs and constraints. Signal costs may make dishonesty prohibitively expensive, while genetic constraints could make it impossible. We investigated honest signaling using full-sib analysis and parent-offspring regression in the ant Lasius niger, in which queens produce a cuticular hydrocarbon-based pheromone that signals fertility and inhibits worker reproduction and aggression. We found multiple lines of evidence that cuticular hydrocarbon production is genetically correlated with oogenesis and that the queen pheromone 3-methylhentriacontane and other 3-methylalkanes have strong genetic links with fertility relative to other cuticular hydrocarbons. These genetic correlations may maintain honesty in the face of directional selection on signaling and explain the putatively widespread use of cuticular hydrocarbons in fertility signaling across the social insects. We also found evidence for a positive genetic correlation for fertility between the castes; that is, the most fertile queens produced especially fertile workers. These results highlight that intercaste genetic correlations could constrain the evolution of queen-worker dimorphism, such that worker reproduction may sometimes reflect a nonadaptive "caste load" rather than positively selected cheating.

Linksvayer, T. A., Busch J. W., & Smith C. R. (2013).  Social supergenes of superorganisms: Do supergenes play important roles in social evolution?. Bioessays. 35, 683-689. AbstractWebsite

We suggest that supergenes, groups of co-inherited loci, may be involved in a range of intriguing genetic and evolutionary phenomena in insect societies, and may play broad roles in the evolution of cooperation and conflict. Supergenes are central in the evolution of an array of traits including self-incompatibility, mimicry, and sex chromosomes. Recently, researchers identified a large supergene, described as a social chromosome, which controls social organization in the fire ant. This system was previously considered to be a remarkable example of a single gene affecting a complex social trait. We describe how selection may commonly favor reduced recombination and the formation of supergenes for social traits, and once formed, supergenes may strongly influence further evolutionary dynamics within and between lineages. The evolution of supergenes, and even wholly non-recombining genomes, may be particularly common in systems in which genetically distinct lineages can form mutually reinforcing socially parasitic relationships.

Linksvayer, T. A., Fewell J. H., Gadau J., & Laubichler M. D. (2012).  Developmental evolution in social insects: regulatory networks from genes to societies. Journal of Experimental Zoology Part B-Molecular and Developmental Evolution. 318B, 159-169. Abstractlinksvayer_et_al_2012_jez_developmental_evolution_in_social_insects_color.pdf

The evolution and development of complex phenotypes in social insect colonies, such as queenworker dimorphism or division of labor, can, in our opinion, only be fully understood within an expanded mechanistic framework of Developmental Evolution. Conversely, social insects offer a fertile research area in which fundamental questions of Developmental Evolution can be addressed empirically. We review the concept of gene regulatory networks (GRNs) that aims to fully describe the battery of interacting genomic modules that are differentially expressed during the development of individual organisms. We discuss how distinct types of network models have been used to study different levels of biological organization in social insects, from GRNs to social networks. We propose that these hierarchical networks spanning different organizational levels from genes to societies should be integrated and incorporated into full GRN models to elucidate the evolutionary and developmental mechanisms underlying social insect phenotypes. Finally, we discuss prospects and approaches to achieve such an integration. J. Exp. Zool. (Mol. Dev. Evol.) 318:159169, 2012. (c) 2012 Wiley Periodicals, Inc.

Linksvayer, T. A., Kaftanoglu O., Akyol E., Blatch S., Amdam G. V., & Page R. E. (2012).  Larval and nurse worker control of developmental plasticity and the evolution of honey bee queen-worker dimorphism (vol 24, pg 1939, 2011). Journal of Evolutionary Biology. 25, 416-416. Abstractlinksvayer_et_al_2011_jeb_corrected.pdf

small correction of figure caption for Linksvayer et al. 2011

Wang, Y., Kocher S. D., Linksvayer T. A., Grozinger C. M., Page R. E., & Amdam G. V. (2012).  Regulation of behaviorally associated gene networks in worker honey bee ovaries. Journal of Experimental Biology. 215, 124-134. Abstractwang_et_al_2011_j_exp_biol.pdf

Several lines of evidence support genetic links between ovary size and division of labor in worker honey bees. However, it is largely unknown how ovaries influence behavior. To address this question, we first performed transcriptional profiling on worker ovaries from two genotypes that differ in social behavior and ovary size. Then, we contrasted the differentially expressed ovarian genes with six sets of available brain transcriptomes. Finally, we probed behavior-related candidate gene networks in wild-type ovaries of different sizes. We found differential expression in 2151 ovarian transcripts in these artificially selected honey bee strains, corresponding to approximately 20.3% of the predicted gene set of honey bees. Differences in gene expression overlapped significantly with changes in the brain transcriptomes. Differentially expressed genes were associated with neural signal transmission (tyramine receptor, TYR) and ecdysteroid signaling; two independently tested nuclear hormone receptors (HR46 and ftz-f1) were also significantly correlated with ovary size in wild-type bees. We suggest that the correspondence between ovary and brain transcriptomes identified here indicates systemic regulatory networks among hormones (juvenile hormone and ecdysteroids), pheromones (queen mandibular pheromone), reproductive organs and nervous tissues in worker honey bees. Furthermore, robust correlations between ovary size and neural-and endocrine response genes are consistent with the hypothesized roles of the ovaries in honey bee behavioral regulation.

Anderson, K. E., Wheeler D. E., Yang K., & Linksvayer T. A. (2011).  Dynamics of an ant-ant obligate mutualism: colony growth, density dependence and frequency dependence. Molecular Ecology. 20, 1781-1793., Number 8 Abstractanderson_et_al._2011_molecol.pdf

In insect societies, worker vs. queen development (reproductive caste) is typically governed by environmental factors, but many Pogonomyrmex seed-harvester ants exhibit strict genetic caste determination, resulting in an obligate mutualism between two reproductively isolated lineages. Same-lineage matings produce fertile queens while alternate-lineage matings produce sterile workers. Because new virgin queens mate randomly with multiple males of each lineage type, and both worker and queen phenotypes are required for colony growth and future reproduction, fitness is influenced by the relative frequency of each lineage involved in the mutualistic breeding system. While models based solely on frequency-dependent selection predict the convergence of lineage frequencies towards equal (0.5/0.5), we surveyed the lineage ratios of 49 systems across the range of the mutualism and found that the global lineage frequency differed significantly from equal. Multiple regression analysis of our system survey data revealed that the density and relative frequency of one lineage decreases at lower elevations, while the frequency of the alternate lineage increases with total colony density. While the production of the first worker cohort is largely frequency dependent, relying on the random acquisition of worker-biased sperm stores, subsequent colony growth is independent of lineage frequency. We provide a simulation model showing that a net ecological advantage held by one lineage can lead to the maintenance of stable but asymmetric lineage frequencies. Collectively, these findings suggest that a combination of frequency-dependent and frequency-independent mechanisms can generate many different localized and independently evolving system equilibria.

Rueppell, O., Metheny J. D., Linksvayer T., Fondrk M. K., Page R. E., & Amdam G. V. (2011).  Genetic architecture of ovary size and asymmetry in European honeybee workers. Heredity. 106, 894-903. Abstractrueppell_et_al_2011_heredity.pdf

The molecular basis of complex traits is increasingly understood but a remaining challenge is to identify their co-regulation and inter-dependence. Pollen hoarding (pln) in honeybees is a complex trait associated with a well-characterized suite of linked behavioral and physiological traits. In European honeybee stocks bidirectionally selected for pln, worker (sterile helper) ovary size is pleiotropically affected by quantitative trait loci that were initially identified for their effect on foraging behavior. To gain a better understanding of the genetic architecture of worker ovary size in this model system, we analyzed a series of crosses between the selected strains. The crossing results were heterogeneous and suggested non-additive effects. Three significant and three suggestive quantitative trait loci of relatively large effect sizes were found in two reciprocal backcrosses. These loci are not located in genome regions of known effects on foraging behavior but contain several interesting candidate genes that may specifically affect worker-ovary size. Thus, the genetic architecture of this life history syndrome may be comprised of pleiotropic, central regulators that influence several linked traits and other genetic factors that may be downstream and trait specific. Heredity (2011) 106, 894-903; doi:10.1038/hdy.2010.138; published online 3 November 2010

Abbot, P., Abe J., Alcock J., Alizon S., Alpedrinha J. A. C., Andersson M., et al. (2011).  Inclusive fitness theory and eusociality. Nature. 471, E1-E4., Number 7339 Abstractabbot_etal_nature_2011.pdf


Van Dyken, J. D., Linksvayer T. A., & Wade M. J. (2011).  Kin selection-mutation balance: a model for the origin, maintenance, and consequences of social cheating. American Naturalist. 177, 288-300., Number 3 Abstractvan_dyken_et_al_2011_kin_selection-mutation_balance_am_nat.pdf

Social conflict, in the form of intraspecific selfish "cheating," has been observed in a number of natural systems. However, a formal, evolutionary genetic theory of social cheating that provides an explanatory, predictive framework for these observations is lacking. Here we derive the kin selection mutation balance, which provides an evolutionary null hypothesis for the statics and dynamics of cheating. When social interactions have linear fitness effects and Hamilton's rule is satisfied, selection is never strong enough to eliminate recurrent cheater mutants from a population, but cheater lineages are transient and do not invade. Instead, cheating lineages are eliminated by kin selection but are constantly reintroduced by mutation, maintaining a stable equilibrium frequency of cheaters. The presence of cheaters at equilibrium creates a "cheater load" that selects for mechanisms of cheater control, such as policing. We find that increasing relatedness reduces the cheater load more efficiently than does policing the costs and benefits of cooperation. Our results provide new insight into the effects of genetic systems, mating systems, ecology, and patterns of sex-limited expression on social evolution. We offer an explanation for the widespread cheater/altruist polymorphism found in nature and suggest that the common fear of conflict-induced social collapse is unwarranted.

Linksvayer, T. A., Kaftanoglu O., Akyol E., Blatch S., Amdam G. V., & Page R. E. (2011).  Larval and nurse worker control of developmental plasticity and the evolution of honey bee queen-worker dimorphism. Journal of Evolutionary Biology. 24, 1939-1948. Abstractlinksvayer_et_al_2011_jeb_corrected.pdf

Social evolution in honey bees has produced strong queen-worker dimorphism for plastic traits that depend on larval nutrition. The honey bee developmental programme includes both larval components that determine plastic growth responses to larval nutrition and nurse components that regulate larval nutrition. We studied how these two components contribute to variation in worker and queen body size and ovary size for two pairs of honey bee lineages that show similar differences in worker body-ovary size allometry but have diverged over different evolutionary timescales. Our results indicate that the lineages have diverged for both nurse and larval developmental components, that rapid changes in worker body-ovary size allometry may disrupt queen development and that queen-worker dimorphism arises mainly from discrete nurse-provided nutritional environments, not from a developmental switch that converts variable nutritional environments into discrete phenotypes. Both larval and nurse components have likely contributed to the evolution of queen-worker dimorphism.

Schmidt, A. M., Linksvayer T. A., Boomsma J. J., & Pedersen J. S. (2011).  No benefit in diversity? The effect of genetic variation on survival and disease resistance in a polygynous social insect. Ecological Entomology. 36, 751-759. Abstractschmidt_et_al_2011_ecol_entomol.pdf

1. Multiple mating by queens has been shown to enhance disease resistance in insect societies, because higher genetic diversity among nestmates improves collective immune defences or offers a certain level of herd immunity. However, it has remained ambiguous whether polygynous societies with large numbers of queens also benefit from increased genetic diversity.2. We used one of the very few ant species that can be reared across generations, the pharaoh ant, Monomorium pharaonis Linnaeus, to create experimental colonies with two types of enhanced genetic diversity: (i) mixed workers from three divergent inbred lineages representing the 'polygyny-equivalent' of multiple mating by queens (i. e. increased between-worker variation); and (ii) uniform workers whose overall heterozygosity was increased by two subsequent generations of crossing between the same divergent inbred lineages (i. e. increased within-worker variation).3. We found significant differences in worker survival among the three inbred lineages, with exposure to conidiospores of the fungal pathogen Beauveria bassiana causing significant mortality to the workers independently of their diversity type. Increased diversity did not improve the resistance to Beauveria.4. Enhanced heterozygosity colonies had worker survival rates similar to the most resistant inbred lineage, whereas colonies with mixed workers from the three inbred lineages had lower worker and larval survival. Workers did not show any infection-avoidance behaviour.5. Average larval survival appeared unaffected by the presence of conidiospores. It benefitted from increased heterozygosity but was reduced in mixed colonies independent of infection. This suggests that negative, but cryptic social interactions in mixed colonies may affect overall survival.6. The present results do not provide evidence for or against a link between increased genetic variation and increased disease resistance in pharaoh ants, but show that colonies differ considerably in general survival. Thus, increasing the genetic diversity of pharaoh ant colonies may not provide survival advantages in the face of pathogen exposure, and polygyny and polyandry may not be directly comparable mechanisms for creating adaptive resistance towards pathogens.

Schmidt, A. M., Linksvayer T. A., Boomsma J. J., & Pedersen J. S. (2011).  Queen-worker caste ratio depends on colony size in the pharaoh ant (Monomorium pharaonis). Insectes Sociaux. 58, 139-144., Number 2 Abstractschmidtal.2011_insectsoc_reprint.pdf

The success of an ant colony depends on the simultaneous presence of reproducing queens and non-reproducing workers in a ratio that will maximize colony growth and reproduction. Despite its presumably crucial role, queen-worker caste ratios (the ratio of adult queens to workers) and the factors affecting this variable remain scarcely studied. Maintaining polygynous pharaoh ant (Monomorium pharaonis) colonies in the laboratory has provided us with the opportunity to experimentally manipulate colony size, one of the key factors that can be expected to affect colony level queen-worker caste ratios and body size of eclosing workers, gynes and males. We found that smaller colonies produced more new queens relative to workers, and that these queens and workers both tended to be larger. However, colony size had no effect on the size of males or on the sex ratio of the individuals reared. Furthermore, for the first time in a social insect, we confirmed the general life history prediction by Smith and Fretwell (Am Nat 108:499-506, 1974) that offspring number varies more than offspring size. Our findings document a high level of plasticity in energy allocation toward female castes and suggest that polygynous species with budding colonies may adaptively adjust caste ratios to ensure rapid growth.

Kaftanoglu, O., Linksvayer T. A., & Page R. E. (2011).  Rearing honey bees, Apis mellifera, in vitro 1: Effects of sugar concentrations on survival and development. Journal of Insect Science. 11, 96. Abstractkaftanoglu_et_al_2011_j_insect_science_in_vitro.pdf

A new method for rearing honey bees, Apis mellifera L. (Hymenoptera: Apidae), in vitro was developed and the effects of sugar concentrations on survival and development were studied. Seven different glucose (G) and fructose (F) compositions (0%G+0%F, 3%G+3%F, 6%G+6%F, 12%G+12%F, 0%G+12%F, 12%G+0%F, and 4%G+8%F) were tested. Larvae were able to grow to the post defecation stage without addition of sugars (Diet 1), but they were not able to metamorphose and pupate. Adults were reared from diets 2-7. The average larval survival, prepupal larval weights, adult weights, and ovariole numbers were affected significantly due to the sugar compositions in the diets. High sugar concentrations (12%G+12%F) increased the number of queens and intercastes.

van Zweden, J. S., Brask J. B., Christensen J. H., Boomsma J. J., Linksvayer T. A., & d'Ettorre P. (2010).  Blending of heritable recognition cues among ant nestmates creates distinct colony gestalt odours but prevents within-colony nepotism. Journal of Evolutionary Biology. 23, 1498-1508. Abstractvan_zweden_et_al_2010_jeb_blending_of_heritable_recognition_cues.pdf

The evolution of sociality is facilitated by the recognition of close kin, but if kin recognition is too accurate, nepotistic behaviour within societies can dissolve social cohesion. In social insects, cuticular hydrocarbons act as nestmate recognition cues and are usually mixed among colony members to create a Gestalt odour. Although earlier studies have established that hydrocarbon profiles are influenced by heritable factors, transfer among nestmates and additional environmental factors, no studies have quantified these relative contributions for separate compounds. Here, we use the ant Formica rufibarbis in a cross-fostering design to test the degree to which hydrocarbons are heritably synthesized by young workers and transferred by their foster workers. Bioassays show that nestmate recognition has a significant heritable component. Multivariate quantitative analyses based on 38 hydrocarbons reveal that a subset of branched alkanes are heritably synthesized, but that these are also extensively transferred among nestmates. In contrast, especially linear alkanes are less heritable and little transferred; these are therefore unlikely to act as cues that allow within-colony nepotistic discrimination or as nestmate recognition cues. These results indicate that heritable compounds are suitable for establishing a genetic Gestalt for efficient nestmate recognition, but that recognition cues within colonies are insufficiently distinct to allow nepotistic kin discrimination.

Johnson, B. R., & Linksvayer T. A. (2010).  Deconstructing the Superorganism: Social Physiology, Groundplans, and Sociogenomics. Quarterly Review of Biology. 85, 57-79., Number 1 Abstractjohnson_and_linksvayer_2010.pdf

Our understanding of insect societies is rapidly expanding due to an emphasis on integrative approaches. Emerging tools enabling the molecular dissection of social behavior, together with novel hypotheses for the evolution of eusociality, are emblematic of this progress. However, an obstacle to a truly integrative approach remains, as social physiology-the basis of group-level coordination-has generally been neglected by geneticists. In this paper, we begin a synthesis of these fields by first reviewing three classes of social insect organization that mark major transitions in increasing social complexity. We then develop an expansion of the superorganism concept in order to place eusociality into a broad evolutionary context, and we also interpret current molecular and genetic work on the evolution of eusociality. The groundplan hypothesis proposes that eusociality arose via simple changes in the regulation of ancestral gene sets affecting reproductive physiology and behavior, and we argue that this hypothesis is explanatory for the evolution of division of labor (social anatomy) but not for the regulatory systems that ensure group-level coordination of action (social physiology), which we propose is dependent on previously unrelated traits that are brought together into novel genetic networks. We conclude with a review of recent work in sociogenomics that supports our hypotheses.

Wade, M. J., Wilson D. S., Goodnight C., Taylor D., Bar-Yam Y., de Aguiar M. A. M., Stacey B., Werfel J., Hoelzer G. A., Brodie E. D., Fields P., Breden F., Linksvayer T. A., Fletcher J. A., Richerson P. J., Bever J. D., Van Dyken J. D., & Zee P. (2010).  Multilevel and kin selection in a connected world. Nature. 463, E8-E9., Number 7283


Linksvayer, T. A. (2010).  Subsociality and the evolution of eusociality. (Breed, M., Moore, J., Ed.).Encylopedia of Animal Behavior. : Academic Press Abstractlinksvayer_2010_subsociality_chapter_00359.pdf


Moorad, J. A., & Linksvayer T. A. (2010).  Levels of selection on threshold characters (vol 179, pg 899, 2008). Genetics. 185, 706-706., Number 2 Abstract


Kaftanoglu, O., Linksvayer T. A., & Page R. E. (2010).  Rearing honey bees (Apis mellifera L.) in vitro: effects of feeding intervals on survival and development. Journal of Apicultural Research. 49, 311-317., Number 4 Abstract


A new and simple technique was developed to rear honey bees (Apis mellifera L.) in vitro. One day old larvae were grafted into Petri dishes and fed a basic diet at six different time intervals. There were no differences in the larval weights, survival rates or ovariole numbers of the bees among the groups that were fed at different intervals, but they were heavier and had larger ovaries than hive reared bees. It was shown that honey bees can be reared in vitro without replenishing their food daily. This simple mass provisioning technique reduces the labour involved, and enables the researcher to raise large number of bees in vitro.

Linksvayer, T. A., & Wade M. J. (2009).  Genes with social effects are expected to harbor more sequence variation within and between species. Evolution. 63, 1685-1696., Number 7 Abstractlinksvayer_and_wade_2009_evolution_genes_with_social_effects.pdf

The equilibrium sequence diversity of genes within a population and the rate of sequence divergence between populations or species depends on a variety of factors, including expression pattern, mutation rate, nature of selection, random drift, and mating system. Here, we extend population genetic theory developed for maternal-effect genes to predict the equilibrium polymorphism within species and sequence divergence among species for genes with social effects on fitness. We show how the fitness effects of genes, mating system, and genetic system affect predicted gene polymorphism. We find that, because genes with indirect social effects on fitness effectively experience weaker selection, they are expected to harbor higher levels of polymorphism relative to genes with direct fitness effects. The relative increase in polymorphism is proportional to the inverse of the genetic relatedness between individuals expressing the gene and their social partners that experience the fitness effects of the gene. We find a similar pattern of more rapid divergence between populations or species for genes with indirect social effects relative to genes with direct effects. We focus our discussion on the social insects, organisms with diverse indirect genetic effects, mating and genetic systems, and we suggest specific examples for testing our predictions with emerging sociogenomic tools.

Linksvayer, T. A., Fondrk M. K., & Page R. E. (2009).  Honeybee social regulatory networks are shaped by colony-level selection. American Naturalist. 173, E99-E107. Abstractlinksvayer_et_al_2009_amnat_honey_bee_social_regulatory_networks.pdf

Social interactions pervade all aspects of life in the social insects. Networks of interacting nestmates enable the maintenance of colony homeostasis and regulation of brood development. Artificial colony-level selection on the amount of pollen stored in honeybee colonies has produced high- and low-pollen-hoarding strains that have been used as a model system to study the genetic and physiological basis of differences in forager behavior that contribute to colony-level differences in pollen hoarding. Here we extend this model system using an interacting-phenotypes approach that explicitly studies genetic components arising from social interactions. High- and low-pollen-hoarding-strain larvae were reared in hives with high- or low-strain older larvae and high- or low-strain adult workers. The ovariole number and dry mass of focal individuals depended on interactions between the genotypes of the focal individuals and their brood and adult worker nestmates. These results show that trait expression by individual honeybee workers is modulated by the genotypic composition of the colony, indicating that individual-level phenotypes are properties of the composite "sociogenome." Thus, colony-level selection has produced strains with distinct combinations of socially interacting genes, which make up the social networks that regulate development and expressed phenotypes.

Linksvayer, T. A., Rueppell O., Siegel A., Kaftanoglu O., Page R. E., & Amdam G. V. (2009).  The genetic basis of transgressive ovary size in honeybee workers. Genetics. 183, 693-707., Number 2 Abstract


Ovarioles are the functional unit of the female insect reproductive organs and the number of ovarioles per ovary strongly influences egg-laying rate and fecundity. Social evolution in the honeybee (Apis mellifera) has resulted ill queens with 200-360 total ovarioles and workers with usually 20 or less. In addition, variation in ovariole number among workers relates to worker sensory tuning, foraging behavior, and the ability to lay unfertilized male-destined eggs. To study the genetic architecture of worker ovariole number, we performed a series of crosses between Africanized and European bees that differ ill worker ovariole number. Unexpectedly, these crosses produced transgressive worker phenotypes with extreme ovariole numbers that were sensitive to the social environment. We used a new selective pooled DNA interval mapping approach with two Africanized backcrosses to identify quantitative trait loci (QTL) underlying the transgressive ovary phenotype. We identified one QTL on chromosome 11 and found some evidence for another QTL oil chromosome 2. Both QTL regions contain plausible functional candidate genes. The ovariole number of foragers was correlated with the sugar concentration of collected nectar, supporting previous studies showing a link between worker physiology and foraging behavior. We discuss how the phenotype of extreme worker ovariole numbers and the underlying genetic factors we identified could be linked to the development of queen traits.

Anderson, K. E., Smith C. R., Linksvayer T. A., Mott B. M., Gadau J., & Fewell J. H. (2009).  Modeling the maintenance of a dependent lineage system: the influence of positive frequency-dependent selection on sex ratio. Evolution. 63, 2142-2152., Number 8 Abstract


In insect societies, worker versus queen development (reproductive caste) is typically governed by environmental factors, but some Pogonomyrmex seed-harvester ants exhibit strict genetic caste determination, resulting in an obligate mutualism between two reproductively isolated lineages. Queens mate randomly with multiple males from each lineage and intralineage crosses produce new queens, whereas interlineage crosses produce workers. Early colony survival is negatively frequency dependent; when lineage frequencies are unequal, queens from the rarer lineage benefit because they acquire more interlineage sperm, and produce more workers. Here we examine theoretically and empirically the effect of relative lineage frequency on sex ratio. We predict that the ratio of inter- to intralineage sperm acquired by queens of each lineage will affect the sex ratio produced at colony maturity. Consistent with model predictions, we found that gyne production in mature colonies was positively frequency dependent, increasing significantly with increasing lineage frequency across 15 populations. Unequal lineage frequencies are common and likely maintained by a complex interplay between an ecological advantage specific to one lineage, and opposing frequency-dependent selection pressures experienced throughout the colonies life-cycle; rare lineage colonies benefit during early colony growth, and common lineage colonies benefit at reproductive maturity.

Page Jr, R. E., Linksvayer T. A., & Amdam G. V. (2009).  Social life from solitary regulatory networks: a new paradigm for insect sociality. (Gadau, J., Fewell, J. H., Ed.).Organization of Insect Societies: From Genomes to Socio-complexity. , Cambridge, Massachusetts: Harvard University Press Abstract


Linksvayer, T. A., & Janssen M. A. (2009).  Traits underlying the capacity of ant colonies to adapt to disturbance and stress regimes. Systems Research and Behavioral Science. 26, 315-329., Number 3 Abstract


How do groups of social agents organize themselves to cope with stress and disturbances? We address this question by looking at ant colonies. We review the suites of traits that allow ant species to adapt to different disturbance and stress regimes, and changes in these regimes. Low temperatures and low nest site and food resource availability are important stresses that affect ant abundance and distribution. Large-scale habitat disturbances, such as fire, grazing and mining, and small-scale disturbances that more directly affect individual colonies, such as predation, parasitism and disease, also affect ant abundance and distribution. We use functional groups to study the social and individual traits underlying different responses to temperature stress, large-scale habitat disturbance and competition from other ants. Specific individual and colony traits, such as colony size, queen number and worker specialization, seem to underlie adaptation to various stress and disturbance regimes. Copyright (c) 2008 John Wiley & Sons, Ltd.

Moorad, J. A., & Linksvayer T. A. (2008).  Levels of selection on threshold characters. Genetics. 179, 899-905., Number 2 Abstractmoorad_and_linksvayer_2008_genetics_threshold_traits.pdf

Threshold models are useful for understanding the evolution of dimorphic traits with polygenic bases. Selection for threshold characters on individuals is expected to be frequency dependent because of the peculiar way that selection views underlying genetic and environmental factors. Selection among individuals is inefficient because individual phenotypes fall into only two discrete categories that map imperfectly to the underlying genes. Incidence, however, can be continuously distributed among groups, making among-group selection relatively more efficient. Differently put, the group-mean phenotype can be a better predictor of an individual's genotype than that individual's own phenotype. Because evolution in group-structured populations is governed by the balance of selection within and between groups, we can expect threshold traits to evolve in fundamentally different ways when group mean fitness is a function of morph frequency. We extend the theory of selection on threshold traits to include group selection using contextual analysis. For the simple case of linear group-fitness functions, we show that the group-level component of selection, like the individual-level component, is frequency dependent. However, the conditions that determine which component dominates when levels of selection are in conflict (as described by Hamilton's rule) are not frequency dependent. Thus, enhanced group selection is not an inherent property of threshold characters. Nevertheless, we show that predicting the effects of multiple levels of selection on dimorphic traits requires special considerations of the threshold model.

Linksvayer, T. A. (2008).  Queen-worker-brood coadaptation rather than conflict may drive colony resource allocation in the ant Temnothorax curvispinosus. Behavioral Ecology and Sociobiology. 62, 647-657., Number 5 Abstractlinksvayer_2008_bes_queen-worker-brood_coadaptation.pdf

Conflicts of interest among genetically heterogeneous nestmates in social insect colonies have been emphasized as driving colony resource allocation. However, potential intracolonial conflicts may not actually be realized so that resource allocation could be shaped primarily by among-colony selection that maximizes colony productivity. To elucidate the causal basis of patterns of resource allocation, I experimentally manipulated three fundamental aspects of colony social structure (relatedness among workers, relatedness among larvae, and queen presence) in the ant Temnothorax curvispinosus and measured effects on colony resource allocation to new workers, gynes, and males. The experimental manipulations had widespread effects on patterns of colony resource allocation, but there was little evidence for realized conflicts over the sex ratio and caste ratio. Decreasing nestmate relatedness caused decreased colony productivity, suggesting that more closely related nestmates have more favorably interacting phenotypes. Together, these results suggest that resource allocation in T. curvispinosus may be shaped more by among-colony selection than intracolonial conflict, leading to queen worker-brood coadaptation.

Anderson, K. E., Linksvayer T. A., & Smith C. R. (2008).  The causes and consequences of genetic caste determination in ants (Hymenoptera: Formicidae). Myrmecological News. 11, 119-132. Abstract


Linksvayer, T. A. (2007).  Ant species differences determined by epistasis between brood and worker genomes. PLoS ONE. 2, , Number 10 Abstractlinksvayer_2007_plos_one_interspecific_differences_and_intergenomic_epsistasis.pdf

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.

Neiman, M., & Linksvayer T. A. (2006).  The conversion of variance and the evolutionary potential of restricted recombination. Heredity. 96, 111-121., Number 2 Abstractneiman_and_linksvayer_2006.pdf

Genetic recombination is usually considered to facilitate adaptive evolution. However, recombination prevents the reliable cotransmission of interacting gene combinations and can disrupt complexes of coadapted genes. If interactions between genes have important fitness effects, restricted recombination may lead to evolutionary responses that are different from those predicted from a purely additive model and could even aid adaptation. Theory and data have demonstrated that phenomena that limit the effectiveness of recombination via increasing homozygosity, such as inbreeding and population subdivision and bottlenecks, can temporarily increase the additive genetic variance available to these populations. This effect has been attributed to the conversion of nonadditive to additive genetic variance. Analogously, phenomena such as chromosomal inversions and apomictic parthenogenesis that physically restrict recombination in part or all of the genome may also result in a release of additive variance. Here, we review and synthesize literature concerning the evolutionary potential of populations with effectively or physically restricted recombination. Our goal is to emphasize the common theme of increased short-term access to additive genetic variance in all of these situations and to motivate research directed towards a more complete characterization of the relevance of the conversion of variance to the evolutionary process.

Linksvayer, T. A. (2006).  Direct, maternal, and sibsocial genetic effects on individual and colony traits in an ant. Evolution. 60, 2552-2561., Number 12 Abstractlinksvayer_2006_evolution__direct_maternal_sibsocial_genetic_effects_in_an_ant.pdf

When social interactions occur, the phenotype of an individual is influenced directly by its own genes (direct genetic effects) but also indirectly by genes expressed in social partners (indirect genetic effects). Social insect colonies are characterized by extensive behavioral interactions among workers, brood, and queens so that indirect genetic effects are particularly relevant. I used a series of experimental manipulations to disentangle the contribution of direct effects, maternal (queen) effects, and sibsocial (worker) effects to variation for worker, gyne, and male mass; caste ratio; and sex ratio in the ant Temnothorax curvispinosus. The results indicate genetic variance for direct, maternal, and sibsocial effects for all traits, except for male mass there was no significant maternal variance, and for sex ratio the variance for direct effects was not separable from maternal variance for the primary sex ratio. Estimates of genetic correlations between direct, maternal, and sibsocial effects were generally negative, indicating that these effects may not evolve independently. These results have broad implications for social insect evolution. For example, the genetic architecture underlying social insect traits may constrain the realization of evolutionary conflicts between social partners.

Linksvayer, T. A., Wade M. J., & Gordon D. M. (2006).  Genetic caste determination in harvester ants: Possible origin and maintenance by cyto-nuclear epistasis. Ecology. 87, 2185-2193., Number 9 Abstract


While reproductive caste in eusocial insects is usually determined by environmental factors, in some populations of the harvester ants, Pogonomyrmex barbatus and P. rugosus, caste has been shown to have a strong genetic component. This system of genetic caste determination (GCD) is characterized by between-caste nuclear variation and high levels of mitochondrial haplotype variation between alternative maternal lineages. Two previous genetic models, involving a single nuclear caste-determining locus or interactions between two nuclear loci, respectively, have been proposed to explain the GCD system. We propose a new model based on interactions between nuclear and mitochondrial genes that can better explain the co-maintenance of distinct nuclear and mitochondrial lineages. In our model, females with coevolved cyto-nuclear gene complexes, derived from intra-lineage mating, develop into gynes, while females with disrupted cyto-nuclear complexes, derived from inter-lineage mating, develop into workers. Both haplodiploidy and inbreeding facilitate the buildup of such coevolved cyto-nuclear complexes within lineages. In addition, the opportunity for both intra-lineage and inter-lineage mating in polyandrous populations facilitates the accumulation of gyne-biasing genes. This model may also help to explain the evolution of workerless social parasites. We discuss similarities of GCD and cytoplasmic male sterility in plants and how worker production of males would affect the stability of GCD. Finally, we propose experiments and observations that might help resolve the origin and maintenance of this unusual system of caste determination.

Steiner, F. M., Schlick-Steiner B. C., Konrad H., Linksvayer T. A., Quek S. P., Christian E., Stauffer C., & Buschinger A. (2006).  Phylogeny and evolutionary history of queen polymorphic Myrmecina ants (Hymenoptera : Formicidae). European Journal of Entomology. 103, 619-626., Number 3 Abstract


The phylogenetic relationships in the myrmicine ant genus Myrmecina were analyzed using 1,281 bp of the mitochondrial cytochrome c oxidase I gene. Intermorphic queens observed in M. graminicola (Europe), M nipponica (Japan), M americana (North America; reported for the first time) and M sp. A (Java) were reconstructed as an ancestral trait in this genus. Molecular-clock-based age estimates suggest that queen polymorphism evolved in Myrmecina at the latest during the Miocene. In terms of bio-geographical regions, the inferred chronological order of divergence is: (oriental, (nearctic, (western palearctic, eastern palearetic))).

Linksvayer, T. A., & Wade M. J. (2005).  The evolutionary origin and elaboration of sociality in the aculeate Hymenoptera: Maternal effects, sib-social effects, and heterochrony. Quarterly Review of Biology. 80, 317-336., Number 3 Abstractlinksvayer_and_wade_2005_qrb_evolution_of_sociality.pdf

We discuss the evolutionary origin and elaboration of sociality using an indirect genetic effects perspective. Indirect genetic effects models simultaneously consider zygotic genes, genes expressed in social partners (especially mothers and siblings), and the interactions between them. Incorporation of these diverse genetic effects should lead to more realistic models of social evolution. We first review haplodiploidy as a factor that promotes the evolution of eusociality. Social insect biologists have doubted the importance of relatedness asymmetry caused by hoplodiploidy and focused on other predisposing factors such as maternal care. However, indirect effects theory shows that maternal care evolves more readily in haplodiploids, especially with inbreeding and despite multiple mating. Because extended maternal care is believed to be a precondition for the evolution of eusociality, the evolutionary bias towards maternal care in haplodiploids may result in a further bias towards eusocialily in these groups. Next, we compare kin selection and parental manipulation and then briefly review additional hypotheses for the evolutionary origin of eusociality. We present a verbal model for the evolutionary origin and elaboration of sib-social care from maternal care based on the modification of the timing of expression of maternal care behaviors. Specifically, heterochrony genes cause maternal care behaviors to be expressed prereproductively towards siblings instead of postreproductively towards offspring. Our review demonstrates that both maternal effect genes (expressed in a parental manipulation manner) and direct effect zygotic genes (expressed in an offspring control manner) are likely involved in the evolution of eusociality. We conclude by describing theoretical and empirical advances with indirect genetic effects and sociogenomics, and me provide specific quantitative genetic and genomic predictions from our heterochrony model for the evolutionary origin and elaboration of eusociality.

Linksvayer, T. A., McCall A. C., Jensen R. M., Marshall C. M., Miner J. W., & McKone M. J. (2002).  The function of hitchhiking behavior in the leaf-cutting ant Atta cephalotes. Biotropica. 34, 93-100., Number 1 Abstractlinksvayer_et_al_2002_biotropica_function_of_hitchhiking.pdf

In some leaf-cutting ant species, minim workers ride on the fragments of leaves as they are carried back to the nest from the cutting site. There is convincing evidence that these "hitchhikers" can protect the leaf carriers from attack by phorid (Diptera: Phoridae) parasitoids, but we consider the possibility of other functions for the hitchhiking behavior. It has been hypothesized that the hitchhikers (1) feed on leaf sap from the edges of the cut leaves; (2) ride back to the nest to save energy; (3) get caught on the fragments as they are cut, and hitchhike because they cannot (or will not) get off; and (4) begin the process of preparing the leaf to enter the fungal gardens in the nest, perhaps by removing microbial contaminants. We observed hitchhikers of Atra cephalotes in 14 nests at the La Selva Biological Station in Costa Rica. There was no difference in the proportion of leaf carriers with hitchhikers between day and night. Because the nests we observed were largely nocturnal, more than 90 percent of the hitchhiking occurred at night. The phorid parasitoids are usually considered to be diurnal, so the preponderance of nocturnal hitchhiking suggests other functions in addition to parasitoid defense. Hitchhikers spent more time in the defensive head-up posture during the day, but spent more time in the head-down posture at night. The head-down posture may indicate cleaning or other leaf preparation. The hitchhikers were never observed feeding on sap. Hitchhikers frequently got onto and off of the fragments, and so they were not "marooned." Few hitchhikers rode all the way back to the nest and were often moving on the leaf fragment; these observations make the energy conservation hypothesis less likely, although we cannot reject it. We conclude that parasitoid defense is an important function of hitchhiking but also that there are probably other functions when parasitoids are absent. Based on available data, the most likely possibility is preparation of the leaf fragment before it enters the nest.