Sex and Clonality in the Little Fire Ant

Abstract

Reproduction systems are controlling the creation of new genetic variants as well as how natural selection can operate on these variants. Therefore, they had historically been one of the main foci of evolutionary biology studies. The little fire ant, Wasmannia auropunctata, has been found to display an extraordinary reproduction system, in which both males and female queens are produced clonally. So far, native sexual populations of W. auropunctata have not been identified. Our goals were to identify such sexual populations and investigate the origins of female parthenogenesis and male clonality. Using mitochondrial DNA and microsatellite markers in 17 native populations, we found that traditional sexual populations occurred in W. auropunctata and are likely the recent source of neighboring clonal populations. Queen parthenogenesis has probably evolved several times through mutational events. Male clonality is tightly linked to queen parthenogenesis and thus appears to be female controlled. Its origin could be accounted for by 2 mutually exclusive hypotheses: either by the expected coevolution of the 2 sexes (i.e., a variant of the maternal genome elimination hypothesis) or by a shared mechanistic origin (i.e., by the production of anucleate ovules by parthenogenetic queens). Our results also show that W. auropunctata males and females do not form separate evolutionary units and are unlikely to be engaged in an all-out battle of sexes. This work opens up new perspectives for studies on the adaptive significance and evolutionary stability of mixed sexual and clonal reproduction systems in living organisms.

Androgenesis: where males hijack eggs to clone themselves

“…It is possible that sexual reproduction between queens and males (which usually generates workers) generates males if the queen's genome is successfully eliminated from the eggs [9]. Alternatively, it has been suggested that queens of at least one species (W. auropunctata) produce a small proportion of eggs that are non-nucleate (similar to the mechanism in Cupressus), and that these non-nucleate eggs give rise to androgenetic males if fertilized by sperm [51]. Given that queens of most ant species are highly fecund, the costs of producing non-nucleate eggs may be negligible if their number is low.…”

“…In the little fire ant, W. auropunctata, workers arise sexually, queens arise by thelytoky, and males arise androgenetically [9,11,51]. It is tempting to regard this situation as a classic evolutionary arms race in which males retaliate against the absence rstb.royalsocietypublishing.org Phil.…”

Androgenesis is a maternal trait in the invasive antWasmannia auropunctata

“…In W. auropunctata, this unusual mating system is not induced by any of the most common endosymbiotic manipulators [15] and appears instead to be genetically determined [16]. Foucaud et al [10] demonstrated that W. auropunctata populations displaying a parthenogenesis-androgenesis system (hereafter referred to as 'clonal' populations, for simplicity) have recurrently emerged from ancestral classical haplo-diploid sexual populations (hereafter referred to as 'sexual' populations), in which females (i.e. queens and sterile workers) develop from diploid fertilized eggs and males develop from haploid unfertilized eggs (arrhenotoky).…”

“…Androgenesis has traditionally been regarded as a male trait, giving to androgenetic males a substantial fitness advantage over their sexually reproducing relatives [5]. Androgenesis has, to date, been identified as the main form of reproduction in a very small number of species from four distinct taxa: the hermaphrodite Saharan cypress tree Cupressus dupreziana [6], four hermaphrodite species of freshwater clams from the genus Corbicula [7], a hybrid complex of Bacillus stick insects [8,9], and three haplo-diploid ant species: Wasmannia auropunctata [10,11], Vollenhovia emeryi [12] and Paratrechina longicornis [13].…”

“…queens) reproduce via parthenogenesis and workers (i.e. sterile individuals) are produced by sexual reproduction [10,12,13]. In W. auropunctata, this unusual mating system is not induced by any of the most common endosymbiotic manipulators [15] and appears instead to be genetically determined [16].…”