Post-meiotic mechanism of facultative parthenogenesis in gonochoristic whiptail lizard species

Abstract

Facultative parthenogenesis (FP) has historically been regarded as rare in vertebrates, but in recent years incidences have been reported in a growing list of fish, reptile, and bird species. Despite the increasing interest in the phenomenon, the underlying mechanism and evolutionary implications have remained unclear. A common finding across many incidences of FP is a high degree of homozygosity at microsatellite loci. This has led to the proposal that first or second polar body fusion following the meiotic divisions restores diploidy and thereby mimics fertilization. Here we show that FP occurring in the gonochoristic Aspidoscelis species A. marmoratus and A. arizonae results in genome-wide homozygosity, an observation inconsistent with polar body fusion as the underlying mechanism of restoration. Instead, a high-quality reference genome for A. marmoratus and analysis of whole-genome sequencing from multiple FP and control animals reveals that a post-meiotic mechanism gives rise to homozygous animals from haploid, unfertilized oocytes. Contrary to the widely held belief that females need to be isolated from males to undergo FP, females housed with conspecific and heterospecific males produced unfertilized eggs that underwent spontaneous development. In addition, a mixture of offspring arising from fertilized eggs and parthenogenetic development was observed to arise from a single clutch. Strikingly, our data support a mechanism for facultative parthenogenesis that removes all heterozygosity in a single generation. Complete homozygosity exposes the genetic load and explains the high rate of congenital malformations and embryonic mortality associated with FP in many species. Conversely, FP constitutes strong purifying selection as non-functional alleles of all essential genes are purged in a single generation.

Evolution of alternative reproductive systems inBacillusstick insects

“…lynceorum and with the fact that they achieve parthenogenesis via endoduplication (as discussed above), thus leading to the complete maintenance of heterozygosity (Marescalchi et al, 1991). The fact that the facultative parthenogenetic species (B. rossius) is non-hybrid and loses heterozygosity while obligate asexuals are hybrid and retain high levels of heterozygosity parallels what is found in whiptail lizards (Lutes et al, 2010;Barley et al, 2022;Ho et al, 2023). More generally, the higher retention of heterozygosity in hybrid vs non-hybrid asexuals appears to be a general pattern across taxa, regardless of the proximal mechanisms of parthenogenesis (Jaron et al, 2022).…”

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. The same mechanism was uncovered in the studied representatives of eight or nine independent hybrid origins of obligate parthenogenesis: in the teiid diploids A. tesselata (Lutes et al, 2010) (1) and A. neomexicana (Newton et al, 2016) (2), in the triploid A. uniparens (Cuellar, 1971) and tetraploid A. priscillae originating from the laboratory cross of A. uniparens with a male of sexual diploid A. inornatus (Cole et al, 2017) (3), in the triploid geckos Heteronotia binoei (Dedukh et al, 2022) (4) and Hemiphyllodactylus typus (Dedukh et al, 2022) (5), in the diploid and triploid geckos Lepidodactylus lugubris (Dedukh et al, 2022) (6), and -as shown in this study, in the diploid lacertids D. unisexualis (7), D. dahli (8), and D. armeniaca (9 -depending on the mode of its origin, as it might inherited parthenogenesis from its already parthenogenetic ancestor; Tarkhnishvili et al, 2020).…”

“…Therefore, in most cases it would be more correct to speak of accidental or spontaneous parthenogenesis, but for simplicity, we use the term facultative parthenogenesis here. In all vertebrates studied, facultative parthenogenesis has been associated with partial or even complete loss of heterozygosity in the offspring (Booth et al, 2012(Booth et al, , 2014Booth and Schuett, 2016;Kratochvíl et al, 2020;Ho et al, 2023). Direct cytological evidence for the process of oogenesis in facultatively parthenogenetic vertebrates is lacking.…”

“…Direct cytological evidence for the process of oogenesis in facultatively parthenogenetic vertebrates is lacking. Based on the observations of the genetic variability in the offspring, it is assumed that the ploidy level of the egg is restored after meiosis by a "fusion" of the nuclei of an egg and a polar body (more likely by the suppression of the second meiotic division) (Booth et al, 2012(Booth et al, , 2014Booth and Schuett, 2016;Kratochvíl et al, 2020), or by doubling of the haploid egg genome leading to the total loss of heterozygosity (Ho et al, 2023).…”

Tendency towards clonality: deviations of meiosis in parthenogenetic Caucasian rock lizards

“…An important question is, after the discovery of premeiotic genome endoduplication in D. armeniaca, can we reject the possibility of a postmeiotic automictic mechanism through central fusion -the fusion of the oocyte and the rst polar body (Spangenberg et al, 2020;Ho et al, 2023)? The mechanism of premeiotic endoduplication ensures long-term preservation of heterozygosity of the unisexual form.…”