Abstract

BackgroundIn 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 FindingsWe 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.ConclusionsWe 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.

Highlights

  • In most social insect species, a colony is a closed family unit that contains a queen and her daughter workers [1]

  • 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

  • Some tramp ant species such as Linepithema humile [2], Pheidole megacephala [3], Wasmannia auropunctata [4], Lasius neglectus [5] or Anoplolepis gracilipes [6] share a similar set of strategies: They form large polydomous, highly polygynous supercolonies, within which aggression is absent and individuals move freely between nests [7]

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Summary

Introduction

In most social insect species, a colony is a closed family unit that contains a queen and her daughter workers [1]. As a consequence of this strategy, gene flow among colonies is maintained within the population Social insects such as ants, show a large variety in social organization, reproductive systems, mating behaviour and dispersal modes. 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. 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). Over time, such supercolonies may diverge genetically and, in recognition cues (cuticular hydrocarbons, CHC’s) by a combination of genetic drift and accumulation of colony-specific, neutral mutations

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