No abstract

Nonrecombining genomic variants underlie spectacular social polymorphisms, from bird mating systems to ant social organization. Because these "social supergenes" affect multiple phenotypic traits linked to survival and reproduction, explaining their persistence remains a substantial challenge. Here, we investigate how large nonrecombining genomic variants relate to colony social organization, mating system and dispersal in the Alpine silver ant, Formica selysi. The species has colonies headed by a single queen (monogynous) and colonies headed by multiple queens (polygynous). We confirmed that a supergene with alternate haplotypes-Sm and Sp-underlies this polymorphism in social structure: Females from mature monogynous colonies had the Sm/Sm genotype, while those from polygynous colonies were Sm/Sp and Sp/Sp. Queens heading monogynous colonies were exclusively mated with Sm males. In contrast, queens heading polygynous colonies were mated with Sp males and Sm males. Sm males, which are only produced by monogynous colonies, accounted for 22.9% of the matings with queens from mature polygynous colonies. This asymmetry between social forms in the degree of assortative mating generates unidirectional male-mediated gene flow from the monogynous to the polygynous social form. Biased gene flow was confirmed by a significantly higher number of private alleles in the polygynous social form. Moreover, heterozygous queens were three times as likely as homozygous queens to be multiply mated. This study reveals that the supergene variants jointly affect social organization and multiple components of the mating system that alter the transmission of the variants and thus influence the dynamics of the system.

International audienceAnts figure prominently among the worst invasive species because of their enormous ecological and economic impacts. However, it remains to be investigated which species would be behaviourally dominant when confronted with another invasive ant species, should two species be introduced in the same area. In the future, many regions might have suitable environmental conditions for several invasive ant species, as predicted under climate change scenarios. Here, we explored interactions among several highly invasive ant species, which have been shown to have overlapping suitable areas. The aim of this study was to evaluate the performance in interference competition of seven of the world's worst invasive ant species (Anoplolepis gracilipes, Paratrechina longicornis, Myrmica rubra, Linepithema humile, Lasius neglectus, Wasmannia auropunctata and Pheidole megacephala). We conducted pairwise confrontations, testing the behaviour of each species against each of the six other species (in total 21 dyadic confrontations). We used single worker confrontations and group interactions of 10 versus 10 individuals to establish a dominance hierarchy among these invasive ant species. We discovered two different behavioural strategies among these invasive ants: three species displayed evasive or indifferent behaviour when individuals or groups were confronted (A. gracilipes, Pa. longicornis, M. rubra), while the four remaining species were highly aggressive during encounters and formed a linear dominance hierarchy. These findings contrast with the widespread view that invasive ants form a homogeneous group of species displaying the `invasive syndrome', which includes generally aggressive behaviour. The dominance hierarchy among the four aggressive species may be used to predict the outcome of future competitive interactions under some circumstances. Yet, the existence of several behavioural strategies renders such a prediction less straightforward

Supergenes underlie striking polymorphisms in nature, yet the evolutionary mechanisms by which they arise and persist remain enigmatic. These clusters of linked loci can spread in populations because they captured coadapted alleles or by selfishly distorting the laws of Mendelian inheritance. Here, we show that the supergene haplotype associated with multiple-queen colonies in Alpine silver ants is a maternal effect killer. All eggs from heterozygous queens failed to hatch when they did not inherit this haplotype. Hence, the haplotype specific to multiple-queen colonies is a selfish genetic element that enhances its own transmission by causing developmental arrest of progeny that do not carry it. At the population level, such transmission ratio distortion favors the spread of multiple-queen colonies, to the detriment of the alternative haplotype associated with single-queen colonies. Hence, selfish gene drive by one haplotype will impact the evolutionary dynamics of alternative forms of colony social organization. This killer hidden in a social supergene shows that large nonrecombining genomic regions are prone to cause multifarious effects across levels of biological organization.