Evolution of parthenogenetic reproduction in Caucasian rock lizards: A review.

Despite numerous works devoted to hybrid origin of parthenogenesis in reptiles, the causes of hybridization between different species, resulting in the origin of parthenogenetic forms, remain uncertain. Recent studies demonstrate that sexual species considered parental to parthenogenetic rock lizards (Darevskia spp.) avoid interspecific mating in the secondary overlap areas. A specific combination of environmental factors during last glaciation period was critical for ectotherms, which led to a change in their distribution and sex ratio. Biased population structure (e.g., male bias) and limited available distributional range favored the deviation of reproductive behavior when species switched to interspecific mates. To date, at least 7 diploid parthenogenetic species of rock lizards (Darevskia, Lacertidae) originated through interspecific hybridization in the past. The cytogenetic specifics of meiosis, in particular the weak checkpoints of prophase I, may have allowed the formation of hybrid karyotypes in rock lizards. Hybridization and polyploidization are 2 important evolutionary forces in the genus Darevskia. At present, throughout backcrossing between parthenogenetic and parental species, the triploid and tetraploid hybrid individuals appear annually, but no triploid species found among Darevskia spp. on current stage of evolution. The speciation by hybridization with the long-term stage of diploid parthenogenetic species, non-distorted meiosis, together with the high ecological plasticity of Caucasian rock lizards provide us with a new model for considering the pathways and persistence of the evolution of parthenogenesis in vertebrates.

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

Parthenogenetic species of Caucasian rock lizards of the genus Darevksia are important evidence for reticulate evolution and speciation by hybridization in vertebrates. Female-only lineages formed through interspecific hybridization have been discovered in many groups. Nevertheless, critical mechanisms of oogenesis and specifics of meiosis that provide long-term stability of parthenogenetic species are still unknown. Here we report cytogenetic characteristics of somatic karyotypes and meiotic prophase I nuclei in the diploid parthenogenetic species Darevskia unisexualis from the new population "Keti" in Armenia which contains an odd number of chromosomes 2n = 37, instead of the usual 2n = 38. We revealed 36 acrocentric chromosomes and a single metacentric autosomal chromosome, resulting from Robertsonian translocation. Comparative genomic hybridization revealed that chromosome fusion occurred between two chromosomes inherited from the maternal species, similar to another parthenogenetic species D. rostombekowi. To trace the chromosome behaviour in meiosis, we performed an immunocytochemical study of primary oocytes' spread nuclei and studied chromosome synapsis during meiotic prophase I in D. unisexualis based on analysis of synaptonemal complexes (SCs). We found meiotic SC-trivalent composed of one metacentric and two acrocentric chromosomes. We confirmed that the SC was assembled between homeologous chromosomes inherited from two parental species. Immunostaining of the pachytene and diplotene nuclei revealed a mismatch repair protein MLH1 loaded to all autosomal SC bivalents. Possible mechanisms of meiotic recombination between homeologous chromosomes are discussed.

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

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.

The role of hybridisation in the origin and evolutionary persistence of vertebrate parthenogens: a case study of Darevskia lizards.

Obligate parthenogenesis is found in only 0.1% of the vertebrate species, is thought to be relatively short lived and is typically of hybrid origin. However, neither the evolutionary persistence of asexuality in vertebrates, nor the conditions that allow the generation of new parthenogenetic lineages are currently well understood. It has been proposed that vertebrate parthenogenetic lineages arise from hybridisation between two divergent taxa within a specific range of phylogenetic distances (the 'Balance Hypothesis'). Moreover, parthenogenetic species often maintain a certain level of hybridisation with their closest sexual relatives, potentially generating new polyploid hybrid lineages. Here we address the role of hybridisation in the origin and evolutionary lifespan of vertebrate parthenogens. We use a set of microsatellite markers to characterise the origins of parthenogens in the lizard genus Darevskia, to study the distinctiveness of sexual and asexual taxa currently in sympatry, and to analyse the evolutionary consequences of interspecific hybridisation between asexual females and sexual males. We find that parthenogens result from multiple past hybridisation events between species from specific lineages over a range of phylogenetic distances. This suggests that the Balance Hypothesis needs to allow for lineage-specific effects, as envisaged in the Phylogenetic Constraint Hypothesis. Our results show recurrent backcrossing between sexual and parthenogenic Darevskia but neither gene flow nor formation of new asexual lineages. We suggest that, along with their demographic advantage, parthenogens gain additional leverage to outcompete sexuals in nature when the retention of sexual reproductive machinery allows backcrossing with their sexual ancestors.

Reticulate Evolution of the Rock Lizards: Meiotic Chromosome Dynamics and Spermatogenesis in Diploid and Triploid Males of the Genus Darevskia.

Knowing whether triploid hybrids resulting from natural hybridization of parthenogenetic and bisexual species are fertile is crucial for understanding the mechanisms of reticulate evolution in rock lizards. Here, using males of the bisexual diploid rock lizard species Darevskia raddei nairensis and Darevskia valentini and a triploid hybrid male Darevskia unisexualis × Darevskia valentini, we performed karyotyping and comparative immunocytochemistry of chromosome synapsis and investigated the distribution of RAD51 and MLH1 foci in spread spermatocyte nuclei in meiotic prophase I. Three chromosome sets were found to occur in cell nuclei in the D. unisexualis × D. valentini hybrid, two originating from a parthenogenetic D. unisexualis female and one from the D. valentini male. Despite this distorted chromosome synapsis and incomplete double-strand breaks repair in meiotic prophase I, the number of mismatch repair foci in the triploid hybrid was enough to pass through both meiotic divisions. The defects in synapsis and repair did not arrest meiosis or spermatogenesis. Numerous abnormal mature spermatids were observed in the testes of the studied hybrid.