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The Evolution of Extreme Polyandry in Social Insects: Insights from Army Ants

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 (N (e)). Excessive multiple mating by queens (polyandry) has been suggested to...

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Autores principales: Barth, Matthias Benjamin, Moritz, Robin Frederik Alexander, Kraus, Frank Bernhard
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Public Library of Science 2014
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4140799/
https://www.ncbi.nlm.nih.gov/pubmed/25144731
http://dx.doi.org/10.1371/journal.pone.0105621
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author Barth, Matthias Benjamin
Moritz, Robin Frederik Alexander
Kraus, Frank Bernhard
author_facet Barth, Matthias Benjamin
Moritz, Robin Frederik Alexander
Kraus, Frank Bernhard
author_sort Barth, Matthias Benjamin
collection PubMed
description 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 (N (e)). 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 N (e). 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.
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spelling pubmed-41407992014-08-25 The Evolution of Extreme Polyandry in Social Insects: Insights from Army Ants Barth, Matthias Benjamin Moritz, Robin Frederik Alexander Kraus, Frank Bernhard PLoS One Research Article 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 (N (e)). 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 N (e). 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. Public Library of Science 2014-08-21 /pmc/articles/PMC4140799/ /pubmed/25144731 http://dx.doi.org/10.1371/journal.pone.0105621 Text en © 2014 Barth et al http://creativecommons.org/licenses/by/4.0/ This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are properly credited.
spellingShingle Research Article
Barth, Matthias Benjamin
Moritz, Robin Frederik Alexander
Kraus, Frank Bernhard
The Evolution of Extreme Polyandry in Social Insects: Insights from Army Ants
title The Evolution of Extreme Polyandry in Social Insects: Insights from Army Ants
title_full The Evolution of Extreme Polyandry in Social Insects: Insights from Army Ants
title_fullStr The Evolution of Extreme Polyandry in Social Insects: Insights from Army Ants
title_full_unstemmed The Evolution of Extreme Polyandry in Social Insects: Insights from Army Ants
title_short The Evolution of Extreme Polyandry in Social Insects: Insights from Army Ants
title_sort evolution of extreme polyandry in social insects: insights from army ants
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4140799/
https://www.ncbi.nlm.nih.gov/pubmed/25144731
http://dx.doi.org/10.1371/journal.pone.0105621
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