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.

Figure 1

(a) Proposed mechanisms of automixis in snakes. (1) Primordial germ cell. (2) Meiotic products following DNA replication and recombination during the first round of cell division. (3) Meiotic products following the second round of cell division. (4) Potential sex chromosomal arrangements following terminal fusion and gametic duplication (here depicted for one Z chromosome). Note that parthenogens with a WW sex chromosome arrangement are not, at present, known to be viable. (Modified from). (b) Adult king cobra (Ophiophagus hannah). Photo courtesy of Freek Vonk.

Figure 2

(a) Bootstrap densities of two measures of individual heterozygosity for each member of the cobra family (female = mother, OS 1 = offspring 1, OS 2 = offspring 2) based on 100 bootstrap replicates of 20,562 independent RAD loci: (top) Proportion of heterozygous sites (Observed Heterozygosity), and (bottom) the standardized level of homozygosity (Homozygosity by Loci). (b) Bootstrap densities of two measures of pairwise relatedness between the mother and each parthenogenetic offspring based on 100 bootstrap replicates sampled variants: (top) shared alleles index (B_xy) and (bottom) genotype sharing index (M_xy). Sexual reproduction would produce measures at 0.5.

Figure 3

Scaled density of Jaccard index measures of the overlap in heterozygous sites in the two offspring, showing that the degree of overlap in the empirical dataset (in gold) is nonrandom and significantly greater than expected based on measures from 100 randomly permutated datasets (in blue).