Genotypic similarities among the parthenogenetic Darevskia rock lizards with different hybrid origins

Abstract

Background The majority of parthenogenetic vertebrates derive from hybridization between sexually reproducing species, but the exact number of hybridization events ancestral to currently extant clonal lineages is difficult to determine. Usually, we do not know whether the parental species are able to contribute their genes to the parthenogenetic vertebrate lineages after the initial hybridization. In this paper, we address the hypothesis, whether some genotypes of seven phenotypically distinct parthenogenetic rock lizards (genus Darevskia) could have resulted from back-crosses of parthenogens with their presumed parental species. We also tried to identify, as precise as possible, the ancestral populations of all seven parthenogens. Results We analysed partial mtDNA sequences and microsatellite genotypes of all seven parthenogens and their presumed ansectral species, sampled across the entire geographic range of parthenogenesis in this group. Our results confirm the previous designation of the parental species, but further specify the maternal populations that are likely ancestral to different parthenogenetic lineages. Contrary to the expectation of independent hybrid origins of the unisexual taxa, we found that genotypes at multiple loci were shared frequently between different parthenogenetic species. The highest proportions of shared genotypes were detected between (i) D. sapphirina and D. bendimahiensis and (ii) D. dahli and D. armeniaca, and less often between other parthenogens. In case (ii), genotypes at the remaining loci were notably distinct. Conclusions We suggest that both observations (i-ii) can be explained by two parthenogenetic forms tracing their origin to a single initial hybridization event. In case (ii), however, occasional gene exchange between the unisexual and the parental bisexual species could have taken place after the onset of parthenogenetic reproduction. Indeed, backcrossed polyploid hybrids are relatively frequent in Darevskia, although no direct evidence of recent gene flow has been previously documented. Our results further suggest that parthenogens are losing heterozygosity as a result of allelic conversion, hence their fitness is expected to decline over time as genetic diversity declines. Backcrosses with the parental species could be a rescue mechanism which might prevent this decline, and therefore increase the persistance of unisexual forms.

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

“…Thus, the main question, in this case, is the age of each parthenogenetic form of rock lizards and the possibility of the repeated evolution of hybrid parthenogenetic lineages in the Darevskia genus. Possible sporadic hybridizations of the parthenogenetic forms, with males of the sexual parental species, also cannot be excluded (Brunes et al, 2019; Tarkhnishvili et al, 2017; Tarkhnishvili et al, 2020). Second variant: CO between the homeologous chromosomes in D. unisexualis is suppressed.…”

“…Different female‐only populations could accumulate genetic changes independently of each other. Backcrosses with the parental species are considered as possible rescue mechanisms which might increase the persistence of parthenogenetic forms (Tarkhnishvili et al, 2020).…”

Sex chromosomes in meiotic, hemiclonal, clonal and polyploid hybrid vertebrates: along the ‘extended speciation continuum'

“…Only certain combinations of inter-clade hybridizations of bisexual species ( caucasica clade and rudis clade) led to diploid parthenogenetic lineages, despite numerous records of natural within-clade hybridizations [295]. The ancestral clades show deep divergences (discussed by Avise [46]) and possibly can all be traced back to a few initial hybridization events [39], seemingly supporting the ‘rare formation hypothesis' (see §3(a)). Murphy et al [289] proposed sex chromosomes to play key roles in the formation of unisexual Darevskia , which like most lacertid lizards [303] feature female heterogamety (ZW).…”

“…Discussing the balance hypothesis, Stöck et al ([ 148 ], supported by [ 149 , 150 ]), also emphasized that ‘asexual' vertebrates are very rarely formed (e.g. 0.5% of reptile species [ 39 , 151 , 152 ]) since both sufficient divergence and generally complex genetic preconditions are necessary to naturally produce viable and fertile clonal genomes and phenotypes (‘rare formation hypothesis' [ 148 ]).…”

“…The Caucasian parthenogenetic lacertid Darevskia present allo-diploid hybrids ( figure 1 ) [ 299 – 301 ], with known hybrid compositions [ 39 , 294 , 302 ]. Only certain combinations of inter-clade hybridizations of bisexual species ( caucasica clade and rudis clade) led to diploid parthenogenetic lineages, despite numerous records of natural within-clade hybridizations [ 295 ].…”