Cytogenetic mechanisms of unisexuality in rock lizards

Abstract

Darevskia rock lizards is a unique complex taxa, including more than thirty species, seven of which are parthenogenetic. In mixed populations of Darevskia lizards, tri- and tetraploid forms can be found. The most important issues in the theory of reticulate evolution of Darevskia lizards are the origin of parthenogenetic species and their taxonomic position. However, there is little data on how meiosis proceeds in these species. The present work reports the complex results of cytogenetics in a diploid parthenogenetic species – D. unisexualis. Here we detail the meiotic prophase I progression and the specific features оf mitotic chromosomes organization. The stages of meiosis prophase I were investigated by immunocytochemical analysis of preparations obtained from isolated primary oocytes of D. unisexualis in comparison with maternal species D. raddei nairensis. It has been shown that in D. unisexualis at the leptotene-zygotene stages the axial elements and the synaptonemal complex (SC) form typical “bouquets”. At the pachytene-diplotene stage, 18 autosomal SC-bivalents and thickened asynapted sex Z and w univalents were observed. The presence of SYCP1 protein between the lateral elements of autosomal chromosomes proved the formation of assembled SCs. Comparative genomic hybridization (CGH) on the mitotic metaphase chromosomes of D. unisexualis was carried out using the genomic DNA isolated from the parental species D. raddei nairensis and D. valentini. In the pericentromeric regions of half of the mitotic chromosomes of D. unisexualis, specific regions inherited from maternal species have been found. Following our results, we suggest a model for diploid germ cells formation from diploid oocytes without premeiotic duplication of chromosomes in the oogenesis of diploid parthenogenetic lizards D. unisexualis. Taken as a whole, our findings confirm the hybrid nature of D. unisexualis and shed light on heterozygosity and automixis in diploid parthenogenetic forms.

Mixed‐sex offspring produced via cryptic parthenogenesis in a lizard

“…Altogether, we recorded 194 offspring produced via facultative parthenogenesis (Data S1), which is more than the number of all documented individuals produced via facultative parthenogenesis across all other vertebrates (Booth et al, 2014;Straube et al 2016;Allen, Sanders, & Thomson, 2018). Even the much more accessible mechanism of obligatory parthenogenesis in reptiles-previously assumed not to involve meiosis based on genetic data-had to be reclassified after direct cytological examination (Lutes, Neaves, Baumann, Wiegraebe, & Baumann, 2010), and it is still poorly known in most obligatory parthenogenetic reptiles and can be lineage-specific (Spangenberg, Arakelyan, & Cioffi, 2020). The mechanism of facultative parthenogenesis in vertebrates should be examined by cytogenetic and cytological methods in future.…”

Meiotic synapsis of homeologous chromosomes and mismatch repair protein detection in the parthenogenetic rock lizard Darevskia unisexualis

“…Parthenogenetic species in the genus Darevskia possess hybrid karyotypes of the same ploidy as parental sexual species 2n = 38. Their karyotype combines two parental chromosomal sets with 19 chromosomes, containing the pericentromeric DNA specific for the maternal species and 19 chromosomes with pericentromeric regions specific for the paternal species (Spangenberg et al, 2020; 2020a).…”

“…Previous cytogenetic results in D. unisexualis (Hrazdan population, 2n=38) detailed the hybrid karyotype, which is composed of homeologous chromosomes inherited from the suggested parental species: D. raddei nairensis and D. valentini (Fu et al, 2000; Murphy et al, 2000; Spangenberg et al, 2020). According to the recent study species divergence of D. raddei s.l.…”

“…The only deviation pattern in SC assembly was the lack of synapsis between Z and w sex chromosomes. Heteromorphic sex chromosomes were identified at the pachytene and diplotene stages as completely asynapsed Z and w univalents (Spangenberg et al, 2020). However, these results should not be generalized for all populations of D. unisexualis because occurrence of this species is sporadic with several populations in isolated areas (Arakelyan et al, 2011; Freitas et al, 2016).…”

Independent Evolution of Sex Chromosomes in Eublepharid Geckos, A Lineage with Environmental and Genotypic Sex Determination

“…Amniotes, the clade of vertebrates comprising sauropsids (reptiles and birds) and mammals, demonstrate two major systems of sex determination: the genotypic sex determination (GSD), where the sex is determined by sex-specific genetic factors linked to sex chromosomes, and the environmental sex determination (ESD), where the sex is influenced by environmental factors, most commonly temperature (temperature-dependent sex determination—TSD), during a sensitive period of embryonic development and there are no sex-specific differences in genotypes [ 1 , 2 ]. In addition to sexual reproduction, few reptilian species can reproduce asexually, mostly by hybridogenesis, obligate or facultative parthenogenesis [ 3 , 4 ].…”