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

Abstract

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.

Extraordinary centromeres: differences in the meiotic chromosomes of two rock lizards speciesDarevskia portschinskiiandDarevskia raddei

“…1 and 3), and were comparable to the results of our previous study of two other bisexual species, D. raddei nairensis and D. valentini (Spangenberg et al, 2017). For example, the absence of a classical leptotene stage with long threads (presynaptic stage with completely formed chromosome axial elements) is a common feature among all four rock lizards species studied by us to date.…”

“…The rock lizards-specific features of the prophase I stages were described before (Spangenberg et al, 2017). Early presynaptic stages criteria for leptotene: multiple fragments of unpaired axial elements, and for the zygotene: long partially synapsed axial elements, «bouquet» formation (telomere clustering at zygotene), no signs of desynapsis in telomere regions, no MLH1-protein foci.…”

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

“…However, Arakelyan et al [ 62 ] showed the presence of mature gonads in some triploid females and males, similar to earlier described for Cnemidophorus [ 84 ]. Spangenberg et al [ 63 ] showed that defects in chromosome synapsis of triploid hybrid male D. unisexualis x D. valentini did not block meiosis, although the 281 spermatozoa studied in their paper all showed some developmental defects. In conclusion, backcrossing of parthenogenetic Darevskia with their presumed paternal species is documented, although definitive evidence of fertile F1 is still absent.…”

“…Although the possibility of ongoing gene flow from a parental species into the parthenogenetic forms of reptiles is usually not considered, it can not be excluded completely [ 24 ]. Darevsky and Kulikova [ 58 ] mentioned the presence of hybrids between parthenogenetic D. armeniaca and sexually reproducing D. valentini ; all of them were triploid, and females were sterile [ 58 – 60 ], although later some triploids with fully developed gonads were found [ 61 – 63 ]. Freitas et al [ 37 ] genotyped multiple triploid individuals in sympatric populations of D. valentini, D. armeniaca, and D. unisexualis , but ruled out gene introgression from the presumed paternal species into parthenogenetic lineages.…”

Comparing developmental stability in unisexual and bisexual rock lizards of the genusDarevskia

“…We may speculate that even if detrimental consequences of hybridity or parthenogenesis occur in Darevskia lizards, the parthenogens survive due to a production of offspring viable enough to pass through the hard selection and/or that the phase of potential genetic decay has not yet come to pass. Recent findings even suggest that parthenogenetic lineages of Darevskia lizards may switch back to sexual reproduction and escape from the potential evolutionary dead-end (Danielyan et al, 2008;Spangenberg et al, 2017), therefore, there is a little evidence for their hypothetically "poorer" quality. Nonetheless, what is valid for Darevskia lizards does not have to be valid universally.…”