Reproductive system, social organization, human disturbance and ecological dominance in native populations of the little fire ant, Wasmannia auropunctata

Abstract

The invasive ant species Wasmannia auropunctata displays both ecologically dominant and non-dominant populations within its native range. Three factors could theoretically explain the ecological dominance of some native populations of W. auropunctata: (i) its clonal reproductive system, through demographic and/or adaptive advantages; (ii) its unicolonial social organization, through lower intraspecific and efficient interspecific competition; (iii) the human disturbance of its native range, through the modification of biotic and abiotic environmental conditions. We used microsatellite markers and behavioural tests to uncover the reproductive modes and social organization of dominant and non-dominant native populations in natural and human-modified habitats. Microsatellite and mtDNA data indicated that dominant and non-dominant native populations (supercolonies as determined by aggression tests) of W. auropunctata did not belong to different evolutionary units. We found that the reproductive system and the social organization are neither necessary nor sufficient to explain W. auropunctata ecological dominance. Dominance rather seems to be set off by unknown ecological factors altered by human activities, as all dominant populations were recorded in human-modified habitats. The clonal reproductive system found in some populations of W. auropunctata may however indirectly contribute to its ecological dominance by allowing the species to expand its environmental niche, through the fixation over time of specific combinations of divergent male and female genotypes. Unicoloniality may rather promote the range expansion of already dominant populations than actually trigger ecological dominance. The W. auropunctata model illustrates the strong impact of human disturbance on species' ecological features and the adaptive potential of clonal reproductive systems.

Androgenesis is a maternal trait in the invasive antWasmannia auropunctata

“…Under the hypothesis that androgenesis is a male trait [11], androgenetic males from clonal populations are expected to produce androgenetic sons regardless of whether their female mates originate from clonal or sexual populations. On the contrary, if androgenesis is a parthenogenetic female trait, as hypothesized in earlier studies [10,17,19], then parthenogenetic females are expected to produce androgenetic sons regardless of whether they were fertilized by males from sexual populations or from other unrelated clonal populations. Finally, we also conducted a population genetic study in natura in a localized geographical zone where clonal and sexual populations live in close proximity, to detect possible natural crosses between reproductive individuals from sexual and clonal populations, and to determine the directionality of androgenesis in wild populations.…”

“…Based on previous genetic studies of populations collected in the field at the same locations [17,20,21], we predicted that four of the collected populations would be sexual and the other five clonal. The mode of reproduction of each population sampled was confirmed a posteriori, by genetic analyses on a subset of reproductive individuals.…”

“…in a human-disturbed habitat), where W. auropunctata populations were expected to be mostly clonal, and for surrounding populations established in the tropical primary forest (i.e. in a natural habitat), where populations were expected to be mostly sexual [17,18] (electronic supplementary material, figure S1). We were particularly interested in assessing whether parthenogenetic queens of natural clonal populations along the forest track could produce androgenetic sons from fathering males originating from surrounding sexual populations.…”

“…DNA was extracted from each individual and genotyped at the same 12 microsatellite loci as above. Population delineation was inferred through behavioural interaction tests between 261 pairs of nests, as described by Foucaud et al [17]. The clonal or sexual mode of reproduction of each queen and male was inferred by visually inspecting individual genotypes and with an in-house program identifying identical multilocus genotypes.…”

“…primary tropical forests), whereas clonal populations are mostly found in disturbed habitats and display invasive characteristics (i.e. high worker and nest densities [17,18]). This suggests that clonal and sexual populations occupy different ecological niches, and that human disturbance commonly drives habitats towards ecological conditions favouring the establishment of invasive clonal populations.…”