Meiotic Recombination Dramatically Decreased in Thelytokous Queens of the Little Fire Ant and Their Sexually Produced Workers

Abstract

The little fire ant, Wasmannia auropunctata, displays a peculiar breeding system polymorphism. Classical haplo-diploid sexual reproduction between reproductive individuals occurs in some populations, whereas, in others, queens and males reproduce clonally. Workers are produced sexually and are sterile in both clonal and sexual populations. The evolutionary fate of the clonal lineages depends strongly on the underlying mechanisms allowing reproductive individuals to transmit their genomes to subsequent generations. We used several queen-offspring data sets to estimate the rate of transition from heterozygosity to homozygosity associated with recombination events at 33 microsatellite loci in thelytokous parthenogenetic queen lineages and compared these rates with theoretical expectations under various parthenogenesis mechanisms. We then used sexually produced worker families to define linkage groups for these 33 loci and to compare meiotic recombination rates in sexual and parthenogenetic queens. Our results demonstrate that queens from clonal populations reproduce by automictic parthenogenesis with central fusion. These same parthenogenetic queens produce normally segregating meiotic oocytes for workers, which display much lower rates of recombination (by a factor of 45) than workers produced by sexual queens. These low recombination rates also concern the parthenogenetic production of queen offspring, as indicated by the very low rates of transition from heterozygosity to homozygosity observed (from 0% to 2.8%). We suggest that the combination of automixis with central fusion and a major decrease in recombination rates allows clonal queens to benefit from thelytoky while avoiding the potential inbreeding depression resulting from the loss of heterozygosity during automixis. In sterile workers, the strong decrease of recombination rates may also facilitate the conservation over time of some coadapted allelic interactions within chromosomes that might confer an adaptive advantage in habitats disturbed by human activity, where clonal populations of W. auropunctata are mostly found.

Cryptic sexual populations account for genetic diversity and ecological success in a widely distributed, asexual fungus-growing ant

“…Population-genetic studies of some species revealed a diversity of highly complex genetic systems, including different cytogenetic mechanisms used to produce workers and queens, facultative sexual reproduction, and clonal male lineages (23)(24)(25)(26)(27). Asexual eusocial Hymenoptera produce diploid offspring via meiotic parthenogenesis, or automixis, in which a limited amount of genetic variability is generated through fusion of sister nuclei (28)(29)(30)(31). In contrast, mitotic parthenogenesis, or apomixis, in which offspring are genetic clones of their mothers, has not been demonstrated unambiguously in social insects.…”

Androgenesis is a maternal trait in the invasive antWasmannia auropunctata

“…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.…”

Uncovering Cryptic Asexuality in Daphnia magna by RAD Sequencing

“…Examples are many fungal species, including yeast, in which central fusion during within-tetrad mating (= automixis) is assured by a mating type locus (unless there is a mating type switch or recombination between the centromere and the mating type locus) (Antonovics and Abrams 2004). Another example comes from several social insects, which can reproduce parthenogenetically by central fusion, and, additionally, show very low rates of crossover within the chromosomes (Baudry et al 2004;Oldroyd et al 2008;Rey et al 2011). With very low recombination rates, central fusion effectively approaches clonality because central fusion assures that parental heterozygosity is retained at the centromeres, and low rates of crossover result only in a slow decay of heterozygosity in the centromere-distal regions.…”