Parthenogenesis in Darevskia lizards: A rare outcome of common hybridization, not a common outcome of rare hybridization

Abstract

Hybridization is a common evolutionary process with multiple possible outcomes. In vertebrates, interspecific hybridization has repeatedly generated parthenogenetic hybrid species. However, it is unknown whether the generation of parthenogenetic hybrids is a rare outcome of frequent hybridization between sexual species within a genus or the typical outcome of rare hybridization events. Darevskia is a genus of rock lizards with both hybrid parthenogenetic and sexual species. Using capture sequencing, we estimate phylogenetic relationships and gene flow among the sexual species, to determine how introgressive hybridization relates to the origins of parthenogenetic hybrids. We find evidence for widespread hybridization with gene flow, both between recently diverged species and deep branches. Surprisingly, we find no signal of gene flow between parental species of the parthenogenetic hybrids, suggesting that the parental pairs were either reproductively or geographically isolated early in their divergence. The generation of parthenogenetic hybrids in Darevskia is, then, a rare outcome of the total occurrence of hybridization within the genus, but the typical outcome when specific species pairs hybridize. Our results question the conventional view that parthenogenetic lineages are generated by hybridization in a window of divergence. Instead, they suggest that some lineages possess specific properties that underpin successful parthenogenetic reproduction.

Premeiotic endoreplication is the mechanism of obligate parthenogenesis in rock lizards of the genusDarevskia

“…The apparent variability of mechanisms in the obligate parthenogens of the hybrid origin, based on the information available at the time in parthenogenetic Aspidoscelis and Darevskia lizards, led to the conclusion that "the mechanisms of meiosis in vertebrate parthenogens may not conform to a one-size-fits-all scenario" (Freitas et al, 2022). However, it seems that we need to revise this view: while terminal fusion and postmeiotic doubling connected with the loss of heterozygosity seem to be the mechanism of facultative parthenogenesis (Booth et al, 2012(Booth et al, , 2014Booth and Schuett, 2016;Kratochvíl et al, 2020;Ho et al, 2023), only premeiotic endoreplication is now known in obligate parthenogenetic vertebrates of hybrid origin.…”

Absence of female preference and the origin of a unisexual species, the Amazon molly (Poecilia formosa)

“…Using the Amazon molly (Poecilia formosa) as example, Stöck and colleagues (2010) proposed the 'rare formation hypothesis', suggesting that asexual hybrid are rare not due to inherent disadvantages of asexuality, but because a very specific genomic combination is needed to allow hybrid viability and clonal reproduction (Stöck et al 2010;Warren et al 2018). Freitas and colleagues (2022) are suggesting a slightly different view, where actual hybridizations are not rare, but most of them do not lead to the establishment of a stable hybrid lineage (Freitas et al 2022). It should be noted that in species that are sperm-dependent (all asexual hybrid fishes and amphibians), the ecology of their establishment and maintenance is particularly complicated to explain in an evolutionary framework, given their need to coexist (but not outcompete) their sexual sperm donors.…”

The evolutionary network of whiptail lizards reveals predictable outcomes of hybridization

“…Further insights could be gained through comparative studies of other unisexual vertebrates. In Darevskia lizards, the specificity of the sexual species involved in the formation of the multiple parthenogenetic lineages and the apparent lack of correlation between gene flow and divergence have been interpreted as support for the phylogenetic constraint hypothesis ( 28 ). The evolutionary divergence separating parents of the unisexuals in these two clades appears to be comparable (table S11).…”