Department of Biology, Johannes Gutenberg University, Mainz, Germany.
Institute of Quantitative and Computational Biosciences, Johannes Gutenberg University, Mainz, Germany.
Elife. 2024 Jun 7;13:e97035. doi: 10.7554/eLife.97035.
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 either a high degree of homozygosity at microsatellite loci or low levels of heterozygosity detected in next-generation sequencing data. This has led to the proposal that second polar body fusion following the meiotic divisions restores diploidy and thereby mimics fertilization. Here, we show that FP occurring in the gonochoristic species and 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 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, offspring arising from both fertilized eggs and parthenogenetic development were 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, for animals that develop normally, FP could potentially exert strong purifying selection as all lethal recessive alleles are purged in a single generation.
兼性孤雌生殖（FP）在脊椎动物中历来被认为很少见，但近年来，在越来越多的鱼类、爬行动物和鸟类物种中都有报道。尽管人们对这一现象越来越感兴趣，但潜在的机制和进化意义仍不清楚。在许多 FP 案例中，一个常见的发现是微卫星位点高度纯合或下一代测序数据中检测到的杂合度低。这导致了这样的假设，即减数分裂后的第二极体融合恢复了二倍体性，从而模拟了受精。在这里，我们表明，在雌雄同体的物种中发生的 FP 导致了全基因组的纯合性，这一观察结果与极体融合作为恢复的潜在机制不一致。相反，提供了一个高质量的参考基因组和来自多个 FP 和对照动物的全基因组测序分析表明，一种减数分裂后机制导致来自单倍体、未受精的卵母细胞的纯合动物。与普遍认为的雌性需要与雄性隔离才能进行 FP 的观点相反，与同种和异种雄性一起饲养的雌性产生了未受精的卵子，这些卵子自发发育。此外，还观察到来自受精卵子和孤雌生殖发育的后代都来自一个单一的卵。引人注目的是，我们的数据支持了一种兼性孤雌生殖的机制，这种机制可以在一代中消除所有的异质性。完全的纯合性暴露了遗传负荷，并解释了许多物种中与 FP 相关的先天性畸形和胚胎死亡率高的原因。相反，对于正常发育的动物来说，FP 可能会产生强烈的净化选择，因为所有致命的隐性等位基因都可以在一代中被清除。
