Hybrid asexuality as a primary postzygotic barrier between nascent species: On the interconnection between asexuality, hybridization and speciation

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. K E Y W O R D Sbalance hypothesis, coalescence, evolution of asexuality, hybridization, phylogeography,

Histological evidence that diploid hybrids of Cobitis taenia and C. elongatoides (Teleostei, Cobitidae) develop into fertile females and sterile males

“…Hybrids of substantially diverged species, e.g. C. elongatoides and C. taenia, cannot mediate gene flow, so these species hybridize and produce sterile males and fertile females (Janko et al, 2017) which was indicated by Choleva et al (2012) and confirmed based on the structure of gonads in the present study.…”

“…According to this hypothesis, hybrid asexuality is a primary postzygotic barrier between nascent species (Janko et al, 2017). Hybridization and hybrid fitness depend on the genetic distance between hybridizing species (Seehausen et al, 2014) which has also been proven in Cobitis species (Janko et al, 2017). Recently diverged C. taenia and C. pontica were hybridized, producing mostly fertile and recombining progeny of both sexes.…”

“…Recently, Janko et al (2017), using Cobitis complex as model and widely discussed published data, formulated a new hypothesis of hybrid asexuality as an inherent stage of the speciation process that arises before other Dobzhansky-Müller incompatibilities take over the isolation of reproduction. According to this hypothesis, hybrid asexuality is a primary postzygotic barrier between nascent species (Janko et al, 2017).…”

“…The presented investigations join the research stream of recent excellent findings about hybridization, hybrid fitness and asexuality Seehausen et al, 2014;Janko et al, 2017), contributing to the question of the potential role that hybrids play in the evolution of species.…”

Parthenogenesis and developmental constraints

“…When the chromosomes of two hybridizing species differ sufficiently, this can disrupt meiosis due to the imperfect pairing of chromosomes, alterations in spindle dynamics, or asynchrony of signaling from both chromosome sets (e.g., Carman, 1997;De Storme & Mason, 2014;Janko et al, 2018;White, 1978). It is thought that a rare balance between similarity and dissimilarity is necessary (the balance hypothesis, Janko et al, 2018;Moritz et al, 1989;Vrijenhoek, 1989). Hence it is vital that there should not be too much dissimilarity.…”