Inbreeding tolerance as a pre‐adapted trait for invasion success in the invasive ant Brachyponera chinensis

Abstract

Identifying traits that facilitate species introductions and successful invasions of ecosystems represents a key issue in ecology. Following their establishment into new environments, many non‐native species exhibit phenotypic plasticity with post‐introduction changes in behaviour, morphology or life history traits that allow them to overcome the presumed loss of genetic diversity resulting in inbreeding and reduced adaptive potential. Here, we present a unique strategy in the invasive ant Brachyponera chinensis (Emery), in which inbreeding tolerance is a pre‐adapted trait for invasion success, allowing this ant to cope with genetic depletion following a genetic bottleneck. We report for the first time that inbreeding is not a consequence of the founder effect following introduction, but it is due to mating between sister queens and their brothers that pre‐exists in native populations which may have helped it circumvent the cost of invasion. We show that a genetic bottleneck does not affect the genetic diversity or the level of heterozygosity within colonies and suggest that generations of sib‐mating in native populations may have reduced inbreeding depression through purifying selection of deleterious alleles. This work highlights how a unique life history may pre‐adapt some species for biological invasions.

Population and colony structure of an ant with territorial males, Cardiocondyla venustula

“…In contrast to honeybees and presumably also other social Hymenoptera [53], Cardiocondyla does not exhibit single-locus complementary sex determination and inbreeding therefore does not lead to the production of non-viable or sterile diploid males. Resistance towards inbreeding and genetic impoverishment has previously been suggested to facilitate the successful establishment of small propagules in novel environments [16,[54][55][56][57], and our study again highlights that sib-mating in Cardiocondyla is not a consequence but a precondition of invasiveness (see also [58]).…”

The underdog invader: Breeding system and colony genetic structure of the dark rover ant (Brachymyrmex patagonicus Mayr)

“…This unorthodox strategy circumvents the costs of inbreeding within bottlenecked populations, therefore acting as a pre-adaptive trait to invasion (Pearcy et al, 2011). In the Asian needle ant Brachyponera chinensis, the genetic diversity and level of heterozygosity within introduced colonies are similar to those observed in the native range, despite the severe bottleneck experienced by the introduced population (Eyer, Matsuura, et al, 2018). In this species, inbreeding does not result from the founder effect, but rather due to sibmating pre-existing in the native range.…”

“…To date, the combination of polygyny, colony budding dispersal, and unicolonial structure has been described in many invasive ants species, including the most widespread and destructive ones (reviewed in Holway et al, 2002), such as L. humile (Giraud et al, 2002), Lasius neglectus (Cremer, Ugelvig, & Drijfhout, 2008), Wasmannia auropunctata (Fournier et al, 2005), P. megacephala (Fournier et al, 2009), Monomorium pharaonis (Buczkowski & Bennett, 2009;Schmidt, d'Ettorre, & Pedersen, 2010), M. floricola (Wetterer, 2010), A. gracilipes (Thomas et al, 2010), N. fulva (Eyer, McDowell, et al, 2018), Tapinoma melanocephalum (Zheng, Yang, Zeng, Vargo, & Xu, 2018), and the polygyne form of Solenopsis invicta (Fletcher, Blum, Whitt, & Temple, 1980). Interestingly, these strategies have also been reported in a lesser extend in the invasive ant Brachyponera chinensis (Eyer, Matsuura, et al, 2018), in the tramp ant species of the genus Cardiocondyla (Heinze, Cremer, Eckl, & Schrempf, 2006) and in introduced populations of the termite Reticulitermes urbis (Leniaud, Pichon, Uva, & Bagnères, 2009).…”

Drone aggregation behavior in the social wasp Vespula germanica (Hymenoptera: Vespidae): Effect of kinship and density

“…A better understanding of the factors that regulate the conformation of V. germanica leks could contribute to explain some of the drivers that lead to the invasion success observed in some yellow jacket species. When invasive species arrive to new territories, genetic homogeneity is expected until the arrival of new propagules 40 . This leads to hypothesis that on one hand female V. germanica reproductives would have high tolerance to mate with close relatives (as suggested by Goodisman et al 2002) thus favoring the establishment of the species in the arrival phase when a high proportion of sibling drones are the only alternative to mate.…”