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.
Highlights
The ubiquitous nature of sexual reproduction in the tree of life is a key question that is addressed by evolutionary biologists but not yet resolved
We found several lines of evidence to suggest that clonal queens use automictic thelytokous parthenogenesis with central fusion combined with low recombination rates
Comparison of Recombination Rates in Sexual and Clonal Queen Lineages We found that 28 of the 33 microsatellite loci genotyped in worker families produced in sexual queen lineages were dispersed over 11 different linkage groups
Summary
The ubiquitous nature of sexual reproduction in the tree of life is a key question that is addressed by evolutionary biologists but not yet resolved. Several theoretical models have been proposed to highlight the potential evolutionary benefits counteracting this cost of requiring two parents. These models have generated about 20 hypotheses accounting for the long-term advantage of sexual reproduction (reviewed in Kondrashov and Barton and Charlesworth 1998). The short-term advantages of sexual reproduction remain a matter of debate, and asexuality appears to emerge and independently from sexual lineages (Simon et al 2003). There is both theoretical and empirical evidence to suggest that, in specific conditions, asexual populations displace related sexual populations in the short term (Burger 1999; Neiman and Linksvayer 2006; Hoffmann et al 2008). Evol. 28(9):2591–2601. 2011 doi:10.1093/molbev/msr Advance Access publication March 31, 2011
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