Dataset Information

Genetic clusters and sex-biased gene flow in a unicolonial Formica ant.

ABSTRACT: BACKGROUND:Animal societies are diverse, ranging from small family-based groups to extraordinarily large social networks in which many unrelated individuals interact. At the extreme of this continuum, some ant species form unicolonial populations in which workers and queens can move among multiple interconnected nests without eliciting aggression. Although unicoloniality has been mostly studied in invasive ants, it also occurs in some native non-invasive species. Unicoloniality is commonly associated with very high queen number, which may result in levels of relatedness among nestmates being so low as to raise the question of the maintenance of altruism by kin selection in such systems. However, the actual relatedness among cooperating individuals critically depends on effective dispersal and the ensuing pattern of genetic structuring. In order to better understand the evolution of unicoloniality in native non-invasive ants, we investigated the fine-scale population genetic structure and gene flow in three unicolonial populations of the wood ant F. paralugubris. RESULTS:The analysis of geo-referenced microsatellite genotypes and mitochondrial haplotypes revealed the presence of cryptic clusters of genetically-differentiated nests in the three populations of F. paralugubris. Because of this spatial genetic heterogeneity, members of the same clusters were moderately but significantly related. The comparison of nuclear (microsatellite) and mitochondrial differentiation indicated that effective gene flow was male-biased in all populations. CONCLUSION:The three unicolonial populations exhibited male-biased and mostly local gene flow. The high number of queens per nest, exchanges among neighbouring nests and restricted long-distance gene flow resulted in large clusters of genetically similar nests. The positive relatedness among clustermates suggests that kin selection may still contribute to the maintenance of altruism in unicolonial populations if competition occurs among clusters.

SUBMITTER: Holzer B

PROVIDER: S-EPMC2670286 | biostudies-literature | 2009 Mar

REPOSITORIES: biostudies-literature

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Genetic clusters and sex-biased gene flow in a unicolonial Formica ant.

Holzer Barbara B Keller Laurent L Chapuisat Michel M

BMC evolutionary biology 20090331

<h4>Background</h4>Animal societies are diverse, ranging from small family-based groups to extraordinarily large social networks in which many unrelated individuals interact. At the extreme of this continuum, some ant species form unicolonial populations in which workers and queens can move among multiple interconnected nests without eliciting aggression. Although unicoloniality has been mostly studied in invasive ants, it also occurs in some native non-invasive species. Unicoloniality is common ...[more]

PMID: 19335877

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Project description:The evolution of sex-specific phenotypes is an important dimension of diversification and local adaptation. The sex-dependent regulation of gene expression is considered a key genomic mechanism facilitating sex-dependent adaptation. In many species, genes with male-biased expression evolve faster in DNA sequence and expression level than genes with female-biased or sexually monomorphic expression. While positive selection may be responsible for rapid DNA sequence evolution, why expression of male-biased genes also evolves rapidly remains unclear. Beyond sex differences in selection, some aspects of the genetic architecture of gene expression could contribute to the rapid evolution of male-biased gene expression. First, male-biased genes might simply have greater standing genetic variance than female-biased genes. Second, male-biased genes could be less constrained by pleiotropy, either within or between sexes. Here, we evaluate these alternative explanations on an intraspecific scale using a series of quantitative genetic experiments conducted on natural variation in male and female gene expression in the fly Drosophila serrata Male-biased genes had significantly higher genetic variance than female-biased genes and were generally more narrowly expressed across tissues, suggesting lower within-individual pleiotropy. However, consistent with stronger constraints due to between-sex pleiotropy, their between-sex genetic correlations, rMF, were higher than for female-biased genes and more strongly negatively associated with sex bias. Using an extensive clinal dataset, we tested whether sex differences in gene expression divergence among populations have been shaped by pleiotropy. Here too, male-biased gene divergence was more strongly associated with between-sex pleiotropy than was female-biased gene divergence. Systematic differences in genetic variance and pleiotropy may be important factors influencing sex-specific adaptation arising through changes in gene expression.This article is part of the theme issue 'Linking local adaptation with the evolution of sex differences'.

Project description:BACKGROUND:Many insects, including ants, are infected by maternally inherited Wolbachia endosymbiotic bacteria though other secondary endosymbionts have not been reported in ants. It has been suggested that the ability of Wolbachia to invade and remain in an ant population depends on the number of coexisting queens in a colony. We study the genetic and social structure of populations in the ant Formica cinerea which is known to have populations with either monogynous or polygynous colonies. We screen populations for several endosymbiotic bacteria to evaluate the presence of different endosymbionts, possible association between their prevalence and the social structure, and the association between endosymbiont prevalence and genetic differentiation of ant populations. RESULTS:We found three endosymbiotic bacteria; 19% of the nests were infected by Wolbachia, 3.8% by Cardinium and 33% by Serratia. There was significant variation among the populations regarding the proportion of nests infected by Serratia, Wolbachia and the pooled set of all the endosymbionts. Some individuals and colonies carried two of the bacteria, the frequency of double infections agreeing with the random expectation. The proportion of infected ants (individuals or colonies) did not correlate significantly with the population level relatedness values. The difference in the prevalence of Wolbachia between population pairs correlated significantly with the genetic distance (microsatellites) of the populations. CONCLUSIONS:The discovery of several endosymbionts and co-infections by Wolbachia and Cardinium demonstrate the importance of screening several endosymbionts when evaluating their possible effects on social life and queen-worker conflicts over sex allocation. The low prevalence of Wolbachia in F. cinerea departs from the pattern observed in many other Formica ants in which all workers have been infected. It is likely that the strain of Wolbachia in F. cinerea differs from those in other Formica species. The correlation between the difference in Wolbachia prevalence and the pair-wise genetic distance of populations suggests that spreading of the bacteria is restricted by the isolation of the host populations.

Dataset Information

Genetic clusters and sex-biased gene flow in a unicolonial Formica ant.

Publications

Genetic clusters and sex-biased gene flow in a unicolonial Formica ant.

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