Premeiotic endoreplication is essential for obligate parthenogenesis in geckos

Abstract

ABSTRACT Obligate parthenogenesis evolved in reptiles convergently several times, mainly through interspecific hybridization. The obligate parthenogenetic complexes typically include both diploid and triploid lineages. Offspring of parthenogenetic hybrids are genetic copies of their mother; however, the cellular mechanism enabling the production of unreduced cells is largely unknown. Here, we show that oocytes go through meiosis in three widespread, or even strongly invasive, obligate parthenogenetic complexes of geckos, namely in diploid and triploid Lepidodactylus lugubris, and triploid Hemiphyllodactylus typus and Heteronotia binoei. In all four lineages, the majority of oocytes enter the pachytene at the original ploidy level, but their chromosomes cannot pair properly and instead form univalents, bivalents and multivalents. Unreduced eggs with clonally inherited genomes are formed from germ cells that had undergone premeiotic endoreplication, in which appropriate segregation is ensured by the formation of bivalents made from copies of identical chromosomes. We conclude that the induction of premeiotic endoreplication in reptiles was independently co-opted at least four times as an essential component of parthenogenetic reproduction and that this mechanism enables the emergence of fertile polyploid lineages within parthenogenetic complexes.