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The evolution of extreme polyandry in social insects: insights from army ants.

ABSTRACT: The unique nomadic life-history pattern of army ants (army ant adaptive syndrome), including obligate colony fission and strongly male-biased sex-ratios, makes army ants prone to heavily reduced effective population sizes (Ne). Excessive multiple mating by queens (polyandry) has been suggested to compensate these negative effects by increasing genetic variance in colonies and populations. However, the combined effects and evolutionary consequences of polyandry and army ant life history on genetic colony and population structure have only been studied in a few selected species. Here we provide new genetic data on paternity frequencies, colony structure and paternity skew for the five Neotropical army ants Eciton mexicanum, E. vagans, Labidus coecus, L. praedator and Nomamyrmex esenbeckii; and compare those data among a total of nine army ant species (including literature data). The number of effective matings per queen ranged from about 6 up to 25 in our tested species, and we show that such extreme polyandry is in two ways highly adaptive. First, given the detected low intracolonial relatedness and population differentiation extreme polyandry may counteract inbreeding and low Ne. Second, as indicated by a negative correlation of paternity frequency and paternity skew, queens maximize intracolonial genotypic variance by increasingly equalizing paternity shares with higher numbers of sires. Thus, extreme polyandry is not only an integral part of the army ant syndrome, but generally adaptive in social insects by improving genetic variance, even at the high end spectrum of mating frequencies.

SUBMITTER: Barth MB

PROVIDER: S-EPMC4140799 | biostudies-literature | 2014

REPOSITORIES: biostudies-literature

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The evolution of extreme polyandry in social insects: insights from army ants.

Barth Matthias Benjamin MB Moritz Robin Frederik Alexander RF Kraus Frank Bernhard FB

PloS one 20140821 8

The unique nomadic life-history pattern of army ants (army ant adaptive syndrome), including obligate colony fission and strongly male-biased sex-ratios, makes army ants prone to heavily reduced effective population sizes (Ne). Excessive multiple mating by queens (polyandry) has been suggested to compensate these negative effects by increasing genetic variance in colonies and populations. However, the combined effects and evolutionary consequences of polyandry and army ant life history on geneti ...[more]

PMID: 25144731

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Project description:BackgroundArmy ants are dominant invertebrate predators in tropical and subtropical terrestrial ecosystems. Their close relatives within the dorylomorph group of ants are also highly specialized predators, although much less is known about their biology. We analyzed molecular data generated from 11 nuclear genes to infer a phylogeny for the major dorylomorph lineages, and incorporated fossil evidence to infer divergence times under a relaxed molecular clock.ResultsBecause our results indicate that one subfamily and several genera of dorylomorphs are non-monophyletic, we propose to subsume the six previous dorylomorph subfamilies into a single subfamily, Dorylinae. We find the monophyly of Dorylinae to be strongly supported and estimate the crown age of the group at 87 (74-101) million years. Our phylogenetic analyses provide only weak support for army ant monophyly and also call into question a previous hypothesis that army ants underwent a fundamental split into New World and Old World lineages. Outside the army ants, our phylogeny reveals for the first time many old, distinct lineages in the Dorylinae. The genus Cerapachys is shown to be non-monophyletic and comprised of multiple lineages scattered across the Dorylinae tree. We recover, with strong support, novel relationships among these Cerapachys-like clades and other doryline genera, but divergences in the deepest parts of the tree are not well resolved. We find the genus Sphinctomyrmex, characterized by distinctive abdominal constrictions, to consist of two separate lineages with convergent morphologies, one inhabiting the Old World and the other the New World tropics.ConclusionsWhile we obtain good resolution in many parts of the Dorylinae phylogeny, relationships deep in the tree remain unresolved, with major lineages joining each other in various ways depending upon the analytical method employed, but always with short internodes. This may be indicative of rapid radiation in the early history of the Dorylinae, but additional molecular data and more complete species sampling are needed for confirmation. Our phylogeny now provides a basic framework for comparative biological analyses, but much additional study on the behavior and morphology of doryline species is needed, especially investigations directed at the non-army ant taxa.

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The evolution of extreme polyandry in social insects: insights from army ants.

Publications

The evolution of extreme polyandry in social insects: insights from army ants.

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