Inbreeding Tolerance as a Pre-adapted Trait for Invasion Success in the Invasive Ant Brachyponera chinensis
Pierre Andre Eyer, Kenji Matsuura , Edward L. Vargo , Kazuya Kobayashi , Toshihisa Yashiro , Wataru Suehiro , Chihiro Himuro , Tomoyuki Yokoi , Benoit Guénard , Robert R. Dunn , Kazuki Tsuji
Department of Entomology, Texas A&M University, College Station, TX, USA; Laboratory of Insect Ecology, Kyoto University, Japan ; Department of Entomology, Texas A&M University, College Station, TX, USA ; Laboratory of Insect Ecology, Kyoto University, Japan ; Molecular Ecology, Evolution and Phylogenetics (MEEP) laboratory, The University of Sydney, Australia ; Laboratory of Insect Ecology, Kyoto University, Japan ; Laboratory of Insect Ecology, Kyoto University, Japan ; Laboratory of Conservation Ecology, University of Tsukuba, Japan ; School of Biological Sciences, The University of Hong Kong, SAR ; Department of Applied Ecology, North Carolina State University, Raleigh, NC, USA ; Faculty of Agriculture, University of the Ryukyus, Okinawa, Japan
Introduced populations inevitably experience genetic bottlenecks resulting in inbreeding depression and reduced adaptive potential. In many social insects, this genetic depletion lead to a loss of nestmate recognition and a collapse of colony boundaries, resulting in supercolonies made of interconnected nests with hundreds of queens. This unicolonial structure promotes colony growth, survival and resources monopolization; yet it is considered paradoxical as it reduces relatedness among workers, and thus their indirect fitness. Inbreeding poses additional costs to Hymenoptera due to their genetic sex determination. In this context, it is puzzling how genetically impoverished introduced species circumvent genetic depletion to successfully establish and achieve local dominance in a new environment. Using mitochondrial and microsatellite markers, we show that an introduced population of Brachyponera chinensis in the US has undergone a founder event, reducing its genetic diversity by 40% relative to native Japanese populations. We found an unusually high level of inbreeding in both in the introduced and the native ranges, with queens preferentially mating with related males, together with the reintegration of new queens into their natal nest. Ultimately we show that the bottleneck at the population scale has not affected the genetic diversity or the level of heterozygosity within colonies. We hence report for the first time in an invasive species that inbreeding is not a consequence of the bottleneck, but it is due to sibmating that pre-exists in native populations. This strategy might have pre-adapted this species for invasion as generations of sibmating in native populations may have reduced inbreeding depression through purifying selection of deleterious alleles. In addition, inbreeding prevents the erosion of relatedness associated with high numbers of queens, allowing rapid colony growth, yet preserving workers’ indirect fitness and social cohesion.