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Ongoing Coevolution of Wolbachia and a Widespread Invasive Ant, Anoplolepis gracilipes.

ABSTRACT: While Wolbachia are commonly found among arthropods, intraspecific infection rates can vary substantially across the geographic populations. Here we report nearly 100% prevalence of Wolbachia in the global populations of the yellow crazy ant, Anoplolepis gracilipes. To understand coevolutionary history between Wolbachia and A. gracilipes, we identified single nucleotide polymorphisms (SNPs) in Wolbachia from the ant across 12 geographical regions and compared the phylogeny of SNP-based Wolbachia to patterns of the ant's mitochondrial DNA (mtDNA) variation. Our results revealed a strong concordance between phylogenies of Wolbachia and host mtDNA, providing immediate evidence of co-divergence. Among eight identified SNP loci separating the genetic clusters of Wolbachia, seven loci are located in potential protein-coding genes, three of which being non-synonymous SNPs that may influence gene functions. We found a Wolbachia hypothetical protein gene with signature of positive selection. These findings jointly allow us to characterize Wolbachia-ant coevolution and also raise a question about mechanism(s) underlying maintenance of high prevalence of Wolbachia during the colonization of this invasive ant.

SUBMITTER: Lee CC

PROVIDER: S-EPMC7601630 | biostudies-literature |

REPOSITORIES: biostudies-literature

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Project description: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.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.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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Ongoing Coevolution of Wolbachia and a Widespread Invasive Ant, Anoplolepis gracilipes.

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