Thelytokous parthenogenesis and its consequences on inbreeding in an ant

Abstract

Thelytokous parthenogenesis, that is, the production of diploid daughters from unfertilized eggs, may involve various cytological mechanisms, each having a different impact on the genetic structure of populations. Here, we determined the cytological mechanism of thelytokous parthenogenesis and its impact on inbreeding in the ant Cataglyphis cursor, a species where queens use both sexual and asexual reproduction to produce, respectively, workers and new queens. It has been suggested that thelytokous parthenogenesis in C. cursor might have been selected for to face high queen mortality and, originally, to allow workers to replace the queen when she passes away. We first determined the mode of thelytokous parthenogenesis by comparing the rate of transition to homozygosity at four highly polymorphic loci to expectations under the different modes of parthenogenesis. Our data show that thelytoky is achieved through automictic parthenogenesis with central fusion. We then estimated the proportion of colonies headed by worker-produced queens in a natural population. We designed a model linking the observed homozygosity in queens to the proportion of queens produced by workers, based on the assumption that (i) parthenogenesis is automictic with central fusion and (ii) queen lineage is asexually produced, resulting in an increase of the inbreeding over generations, whereas workers are sexually produced and therefore not inbred. Our results indicate that more than 60% of the colonies should be headed by a worker-produced queen, suggesting that queen's lifespan is low in this species.

Population genetic structure, worker reproduction and thelytokous parthenogenesis in the desert ant Cataglyphis sabulosa

“…It has been suggested that thelytokous parthenogenesis in C. cursor was selected to counter high queen mortality and to allow workers to replace the queen when she dies (Lenoir et al, 1988). Recent genetic analyses support the assumption that queen replacement is indeed a common phenomenon in this species (Pearcy et al, 2006). Given the level of heterozygosity of the markers and the positive inbreeding coefficient in our study population, these data do not allow us to completely exclude this possibility in C. sabulosa.…”

“…In these species, worker reproduction reportedly occurs in queenless colonies only. In C. cursor, the production of unfertilized diploid eggs has been shown to result from automictic parthenogenesis, with the central fusion of polar nuclei obtained at the end of the gametogenesis (Pearcy et al, 2006). Whether the same mechanism underlies the parthenogenetic production of females by workers of C. sabulosa remains to be verified.…”

Cytogenetic basis of thelytoky in Apis mellifera capensis

“…If recombination has been extensive at meiosis I (typically there are five or more crossover events per chromosome, Wallberg et al 2015), alleles become shuffled between the four pronuclei ) and the genetic outcomes of terminal and central fusion become similar. Loci that are unlinked to the centromere and are heterozygous in the mother will become homozygous in the daughter one third of the time, and the mother's genotype will be retained two thirds of the time (Pearcy et al 2006;Goudie et al 2015). Observations of high levels of heterozygosity in thelytokous Capensis workers have been interpreted as evidence that the fusion is central, with reduced recombination (Moritz and Haberl 1994;Baudry et al 2004).…”

“…If the two pronuclei that fuse are derived from the same secondary oocyte (terminal fusion- Fig. 2), half of the genetic material of the mother is lost in the female offspring, and the individual will be homozygous at all loci (Pearcy et al 2006;Goudie et al 2012;. This kind of fusion is likely to be functionally lethal in honey bees because of the requirement of heterozygosity at the sex locus for normal female development (Beye et al 2003).…”

Evolutionary mysteries in meiosis

“…However, unless meiosis can be entirely bypassed (e.g. as with vegetative reproduction), secondary asexuality is likely to evolve via modification of meiosis, keeping much of the cell signalling and machinery intact ( [65,76,80,81], see also §4). Indeed, detailed cytological and genetic investigations in several asexual species thought to reproduce clonally by mitotic apomixis have uncovered remnants of meiosis [73,[84][85][86].…”