Genome-wide data implicate terminal fusion automixis in king cobra facultative parthenogenesis

Abstract

Facultative parthenogenesis (FP) is widespread in the animal kingdom. In vertebrates it was first described in poultry nearly 70 years ago, and since then reports involving other taxa have increased considerably. In the last two decades, numerous reports of FP have emerged in elasmobranch fishes and squamate reptiles (lizards and snakes), including documentation in wild populations of both clades. When considered in concert with recent evidence of reproductive competence, the accumulating data suggest that the significance of FP in vertebrate evolution has been largely underestimated. Several fundamental questions regarding developmental mechanisms, nonetheless, remain unanswered. Specifically, what is the type of automixis that underlies the production of progeny and how does this impact the genomic diversity of the resulting parthenogens? Here, we addressed these questions through the application of next-generation sequencing to investigate a suspected case of parthenogenesis in a king cobra (Ophiophagus hannah). Our results provide the first evidence of FP in this species, and provide novel evidence that rejects gametic duplication and supports terminal fusion as a mechanism underlying parthenogenesis in snakes. Moreover, we precisely estimated heterozygosity in parthenogenetic offspring and found appreciable retained genetic diversity that suggests that FP in vertebrates has underappreciated evolutionary significance.

Facultative Parthenogenesis in California Condors

“…The bird also had scoliosis, which had been noted prior to death, and probably explained an abnormal gait when walking. Other studies of parthenogenetic reproduction in snakes have also noted deformities in parthenogens ( Booth and Schuett 2016 ; Card et al 2021 ). Neither of these birds had reproduced, and none of the post-mortem findings could conclusively be considered to be indicators of lack of fitness.…”

“…Additional markers could clarify whether automixis with terminal fusion or endomitosis after meiosis, involving the duplication of a haploid genome, resulted in partially or completely homozygous offspring, respectively. Card et al (2021) provided evidence for terminal automixis fusion in the king cobra utilizing genome-wide data from reduced representation sequencing. The use of the recently published chromosome-level reference genome of the California condor ( Robinson et al 2021 ) and genome re-sequencing efforts can map genetic variation genome-wide to evaluate the mechanism of parthenogenesis in this species.…”

“…Facultative parthenogenesis in vertebrates has generally been considered limited and phylogenetically restricted, although now repeatedly noted in avian, reptilian ( Boothe and Schuett 2016 ; Card et al 2021 ), and elasmobranch taxa ( Fields, et al, 2015 ). It has been hypothesized that populations at low density may be more likely to have individuals reproduce parthenogenetically ( Fields et al 2015 ).…”

Asexual male production by ZW recombination in Artemia parthenogenetica

“…Under these modes of parthenogenesis, all chromosomes (sex chromosomes, as well as autosomes) become homozygous in a single generation. This occurs for instance in rare cases of parthenogenesis in the king cobra, which lead to male offspring, due to terminal fusion (Card et al 2021). Rare parthenogenesis in heterogametic females leading to the production of males is found in several other species: Komodo dragons where it is associated with complete LOH (Watts et al 2006), turkey (Olsen and Marsden 1954), and silkworm where induced gamete duplication results in all male offspring (Strunnikov 1995).…”

Sexually but not parthenogenetically produced females benefit from mating in a stick insect

“…This seems possible as E. tiaratum females are known to produce some offspring parthenogenetically following the receipt of sperm (Alavi, 2016: chapter 5), and we found that mated females of parthenogenetic origin tended to produce a higher proportion of daughters (perhaps reflecting a higher rate of parthenogenetic reproduction) than did mated females of sexual origin, although the difference in offspring sex ratios was far from statistical significance. Previous studies have reported sexual trait decay in obligately asexual lineages descended from sexual ancestors (Kraaijeveld et al, 2016;Schwander et al, 2013;van der Kooi & Schwander, 2014), and loss of heterozygosity associated with automictic parthenogenesis is known to affect trait development and functionality (Card et al, 2021). Whether female reproductive organs are negatively impacted following a single generation of parthenogenesis remains unclear.…”