Abstract
Although sexual reproduction is ubiquitous throughout nature, the molecular machinery behind it has been repeatedly disrupted during evolution, leading to the emergence of asexual lineages in all eukaryotic phyla. Despite intensive research, little is known about what causes the switch from sexual reproduction to asexuality. Interspecific hybridization is one of the candidate explanations, but the reasons for the apparent association between hybridization and asexuality remain unclear. In this study, we combined cross‐breeding experiments with population genetic and phylogenomic approaches to reveal the history of speciation and asexuality evolution in European spined loaches (Cobitis). Contemporary species readily hybridize in hybrid zones, but produce infertile males and fertile but clonally reproducing females that cannot mediate introgressions. However, our analysis of exome data indicates that intensive gene flow between species has occurred in the past. Crossings among species with various genetic distances showed that, while distantly related species produced asexual females and sterile males, closely related species produce sexually reproducing hybrids of both sexes. Our results suggest that hybridization leads to sexual hybrids at the initial stages of speciation, but as the species diverge further, the gradual accumulation of reproductive incompatibilities between species could distort their gametogenesis towards asexuality. Interestingly, comparative analysis of published data revealed that hybrid asexuality generally evolves at lower genetic divergences than hybrid sterility or inviability. Given that hybrid asexuality effectively restricts gene flow, it may establish a primary reproductive barrier earlier during diversification than other “classical” forms of postzygotic incompatibilities. Hybrid asexuality may thus indirectly contribute to the speciation process.
Highlights
Sexual reproduction is one of the most ubiquitous properties of eukaryotes
The underlying molecular machinery is highly conserved, it has been repeatedly disrupted in many different ways, leading to independent emergences of asexual lineages occurring in all phyla (Neiman, Sharbel, & Schwander, 2014)
We explore the interconnection between hybrid asexuality and speciation by reconstructing the initiation of asexuality and the diversification history of European spined loaches (Cobitis)
Summary
Sexual reproduction is one of the most ubiquitous properties of eukaryotes. the underlying molecular machinery is highly conserved, it has been repeatedly disrupted in many different ways, leading to independent emergences of asexual lineages occurring in all phyla (Neiman, Sharbel, & Schwander, 2014). Eukaryotic lineages collectively termed as “asexual” are scattered all over the tree of life and employ a wide spectrum of independently arisen cytological mechanisms for gametes production, which can considerably differ even between closely related asexual taxa (Stenberg & Saura, 2009, 2013). The phylogenetic-constraint hypothesis highlights the observation that asexuality prevails only in some taxa (Hotz et al, 1985; Murphy, Fu, Macculloch, Darevsky, & Kupriyanova, 2000), indicating that some phylogenetic lineages have “predispositions” for uniparental reproduction (e.g., inherent production of unreduced gametes in low levels (e.g., Aliyu, Schranz, & Sharbel, 2010), while others are deprived of such possibility (e.g., due to sex-specific imprinting of genes (Kono et al, 2004))
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