Costs of parthenogenesis on growth and longevity in ex situ zebra sharks Stegostoma tigrinum

Abstract

The zebra shark Stegostoma tigrinum, a popular aquarium fish, is an endangered species that is known to readily reproduce both sexually and through facultative parthenogenesis while in human care. Artificial insemination trials that took place between 2011 and 2013 resulted in the hatching of 2 sexually produced (herein heterozygotes) and 10 parthenogenetic sharks that allowed for a retrospective comparison of growth, feeding and longevity between offspring produced from 2 distinct reproductive modes. Parthenogenetic offspring were generally smaller at hatch than their heterozygous counterparts and, after the first several months post-hatch, failed to increase in mass and length at the same rate as heterozygotes. Parthenogenetic offspring exhibited non-normal swimming behaviors such as spiraling, spy hopping and head standing, which may have been correlated with a gradual decline in the ability of some sharks to properly suction feed. Median lifespan for the parthenotes was 1.05 yr (range: 0.27-6.64 yr); one of the heterozygotes lived to 2.37 yr of age, and the other was alive at the time of this writing in August 2022 and had reached reproductive maturity. By contrast, the 2 longest surviving parthenotes perished just prior to reaching sexual maturity (~5.5 and ~6.5 yr). Parthenogenesis has been documented among ex situ S. tigrinum maintained in aquariums across the globe, and this study demonstrates substantial negative costs to fitness in parthenogenetic offspring compared with their heterozygous siblings. The reduced fitness of parthenotes has implications for managing populations in human care as well as for in situ conservation efforts.

Discovery of facultative parthenogenesis in a new world crocodile

“…SNPs, total number of SNP loci in the dataset that were genotyped in both mother and offspring; initial per-base error, conservative estimate of per-base genotyping error rate; maternal homozygous, number of SNP loci in the dataset for which the mother was homozygous; expected discordant, number of offspring genotypes at maternal homozygous loci expected to differ from maternal genotype based on initial per-base error rate; observed discordant, number of offspring genotypes at maternal homozygous loci that were observed to differ from the maternal genotype; updated per-base error, per-base genotyping error rate assumed for heterozygosity scan analysis based on observed discordance between maternal and offspring genotypes at maternal homozygous loci; maternal heterozygous, number of SNP loci for which the mother was heterozygous; expected offspring heterozygous, number of offspring genotypes at maternal heterozygous loci that were expected to be heterozygous based on updated per-base genotyping error rate alone, assuming a null hypothesis of gametic duplication; observed offspring heterozygous, number of observed heterozygous offspring genotypes at maternal heterozygous loci.) dataset While it is disappointing that the crocodile parthenogen produced here failed to hatch, it is not uncommon to see non-viable fetuses and developmental abnormalities within litters or clutches of parthenogens [1,21,33], and long-term failure to thrive even for individuals born outwardly healthy [34]. For example, following a 9-year study of FP in turkeys, it was found that on average 3.3% of parthenogenetic eggs hatch [33].…”

“…Furthermore, parthenogens have attained adulthood in a variety of species studied, including turkeys, Meleagris gallopavo [10], California condors, Gymnogyps californianus [20], boa constrictors, Boa imperator [16] and the whitespotted bambooshark Chiloscyllium plagiosum [18]. Studies following the fitness of parthenogens are lacking; however, substantial negative costs associated with the trait have been demonstrated in sharks [34]. While fitness costs are evident, it has been shown that turkey parthenogens and both boa constrictors, B. imperator and royal pythons, Python regius, that survive to adulthood are reproductively competent ( [33], W. Booth 2015/2016, personal observation).…”

“…While it is disappointing that the crocodile parthenogen produced here failed to hatch, it is not uncommon to see non-viable fetuses and developmental abnormalities within litters or clutches of parthenogens [1,21,33], and long-term failure to thrive even for individuals born outwardly healthy [34]. For example, following a 9-year study of FP in turkeys, it was found that on average 3.3% of parthenogenetic eggs hatch [33].…”

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

“…In addition to mixoploidy, genome-wide homozygosity constitutes another obstacle to normal development as each recessive deleterious allele is exposed in the hemizygous state. Indeed, arrested development and abnormal phenotypes are observed in FP whiptails, as well as in FP animals across many other species (16, 27, 59, 60). It is important to note though that some whiptails of FP origin developed normally, much like their sexually produced counterparts.…”

Parthenogenesis, sexual conflict, and selection on fertilization rates in switching environments

“…We therefore introduce an additional fixed cost, 1 ≥ C z ≥ 0, applied to fertilized zygotes independent of their mass. Similarly, there can be costs associated to parthenogenetic development such as reduced fitness due to lack of genetic diversity [53] and the possibility of failure of parthenogenetic development [40]. The final probability of survival for a zygote formed from the fertilization of two gametes of sizes m 1 and m 2 is then given by (1 − C z ) exp [ − β /( m 1 + m 2 ) ], while the probability of survival for an unfertilized cell of size m is (1 − C p ) exp [ − β / m ].…”