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      Societies Drifting Apart? Behavioural, Genetic and Chemical Differentiation between Supercolonies in the Yellow Crazy Ant Anoplolepis gracilipes

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          Abstract

          Background

          In populations of most social insects, gene flow is maintained through mating between reproductive individuals from different colonies in periodic nuptial flights followed by dispersal of the fertilized foundresses. Some ant species, however, form large polygynous supercolonies, in which mating takes place within the maternal nest (intranidal mating) and fertilized queens disperse within or along the boundary of the supercolony, leading to supercolony growth (colony budding). As a consequence, gene flow is largely confined within supercolonies. Over time, such supercolonies may diverge genetically and, thus, also in recognition cues (cuticular hydrocarbons, CHC's) by a combination of genetic drift and accumulation of colony-specific, neutral mutations.

          Methodology/Principal Findings

          We tested this hypothesis for six supercolonies of the invasive ant Anoplolepis gracilipes in north-east Borneo. Within supercolonies, workers from different nests tolerated each other, were closely related and showed highly similar CHC profiles. Between supercolonies, aggression ranged from tolerance to mortal encounters and was negatively correlated with relatedness and CHC profile similarity. Supercolonies were genetically and chemically distinct, with mutually aggressive supercolony pairs sharing only 33.1%±17.5% (mean ± SD) of their alleles across six microsatellite loci and 73.8%±11.6% of the compounds in their CHC profile. Moreover, the proportion of alleles that differed between supercolony pairs was positively correlated to the proportion of qualitatively different CHC compounds. These qualitatively differing CHC compounds were found across various substance classes including alkanes, alkenes and mono-, di- and trimethyl-branched alkanes.

          Conclusions

          We conclude that positive feedback between genetic, chemical and behavioural traits may further enhance supercolony differentiation through genetic drift and neutral evolution, and may drive colonies towards different evolutionary pathways, possibly including speciation.

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          Most cited references48

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          Arlequin (version 3.0): An integrated software package for population genetics data analysis

          Arlequin ver 3.0 is a software package integrating several basic and advanced methods for population genetics data analysis, like the computation of standard genetic diversity indices, the estimation of allele and haplotype frequencies, tests of departure from linkage equilibrium, departure from selective neutrality and demographic equilibrium, estimation or parameters from past population expansions, and thorough analyses of population subdivision under the AMOVA framework. Arlequin 3 introduces a completely new graphical interface written in C++, a more robust semantic analysis of input files, and two new methods: a Bayesian estimation of gametic phase from multi-locus genotypes, and an estimation of the parameters of an instantaneous spatial expansion from DNA sequence polymorphism. Arlequin can handle several data types like DNA sequences, microsatellite data, or standard multi-locus genotypes. A Windows version of the software is freely available on http://cmpg.unibe.ch/software/arlequin3.
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            Evolution of supercolonies: the Argentine ants of southern Europe.

            Some ants have an extraordinary social organization, called unicoloniality, whereby individuals mix freely among physically separated nests. This type of social organization is not only a key attribute responsible for the ecological domination of these ants, but also an evolutionary paradox and a potential problem for kin selection theory because relatedness between nest mates is effectively zero. The introduction of the Argentine ant in Europe was apparently accompanied by a dramatic loss of inter-nest aggression and the formation of two immense supercolonies (which effectively are two unicolonial populations). Introduced populations experienced only limited loss of genetic diversity at neutral markers, indicating that the breakdown of recognition ability is unlikely to be merely due to a genetic bottleneck. Rather, we suggest that a "genetic cleansing" of recognition cues occurred after introduction. Indeed workers of the same supercolony are never aggressive to each other despite the large geographical distance and considerable genetic differentiation between sampling sites. By contrast, aggression is invariably extremely high between the two supercolonies, indicating that they have become fixed for different recognition alleles. The main supercolony, which ranges over 6,000 km from Italy to the Spanish Atlantic coast, effectively forms the largest cooperative unit ever recorded.
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              A review of ant cuticular hydrocarbons.

              We compared the published cuticular hydrocarbon (CHC) profiles of 78 ant species across 5 subfamilies. Almost 1,000 CHCs have been described for these species, composing 187 distinct homologous series and ten hydrocarbon groups. In descending order of occurrence were: n-alkanes > monomethylalkanes > dimethylalkanes > alkenes > dienes> trimethylalkanes> methylalkenes > methylalkadienes > trienes > tetramethylalkanes. Odd chain lengths and positions of methyl or double bonds at odd carbon numbers were far more numerous than even chain-length compounds or bond positions. Although each species possess its own unique pattern of CHCs, we found no association between CHC profile and phylogeny. The production of the biosynthetically complex compounds (e.g., methyl branched dienes) by the most primitive living ant suggests that the basic genetic architecture required to produce the rich diversity of CHCs was already present prior to their adaptive radiation. Unlike the ubiquitous n-alkanes and monomethylalkanes, there is a huge diversity of species-specific dimethylalkanes that makes them likely candidates for species and nest-mate discrimination signals.
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                Author and article information

                Contributors
                Role: Editor
                Journal
                PLoS One
                plos
                plosone
                PLoS ONE
                Public Library of Science (San Francisco, USA )
                1932-6203
                2010
                22 October 2010
                : 5
                : 10
                : e13581
                Affiliations
                [1 ]Department of Animal Ecology and Tropical Biology, University of Würzburg, Würzburg, Germany
                [2 ]Department of Evolutionary Biology and Animal Ecology, Faculty of Biology, University of Freiburg, Freiburg, Germany
                [3 ]Department of Behavioural Physiology and Sociobiology, University of Würzburg, Würzburg, Germany
                [4 ]Department of Behavioural Biology, University of Osnabrück, Osnabrück, Germany
                Field Museum of Natural History, United States of America
                Author notes

                Conceived and designed the experiments: JD NB TS HF. Performed the experiments: JD TS JB. Analyzed the data: JD NB TS JB HF. Contributed reagents/materials/analysis tools: NB TS HF. Wrote the paper: JD NB TS HF.

                Article
                10-PONE-RA-21011R1
                10.1371/journal.pone.0013581
                2962633
                21042578
                7c5dd78b-cafb-48a5-82dc-39c5c0e67ebc
                Drescher et al. 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 credited.
                History
                : 13 July 2010
                : 30 September 2010
                Page count
                Pages: 8
                Categories
                Research Article
                Ecology/Behavioral Ecology
                Ecology/Evolutionary Ecology
                Ecology/Population Ecology
                Evolutionary Biology/Animal Behavior
                Evolutionary Biology/Evolutionary Ecology

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                Uncategorized

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