Hybrid asexuality as a primary reproductive barrier: on the interconnection between asexuality and speciation

Abstract

Speciation usually proceeds in a continuum from intensively hybridizing populations until the formation of irreversibly isolated species. Restriction of interspecific gene flow may often be achieved by gradual accumulation of intrinsic postzygotic incompatibilities with hybrid infertility typically evolving more rapidly than inviability. A reconstructed history of speciation in European loaches (Cobitis) reveals that accumulation of postzygotic reproductive incompatibilities may take an alternative, in the literature largely neglected, pathway through initiation of hybrids' asexuality rather than through a decrease in hybrids' fitness. Combined evidence shows that contemporary Cobitis species readily hybridize in hybrid zones, but their gene pools are isolated as hybridization produces infertile males and fertile but clonally reproducing females that cannot mediate introgressions. Nevertheless, coalescent analyses indicated intensive historical gene flow during earlier stages of Cobitis diversification, suggesting that non-clonal hybrids must have existed in the past. The revealed patterns imply that during the initial stages of speciation, hybridization between little diverged species produced recombinant hybrids mediating gene flow, but growing divergence among species caused disrupted meiosis in hybrids resulting in their clonality, which acts as a barrier to gene flow. Comparative analysis of published data on other fish hybrids corroborated the generality of our findings; the species pairs producing asexual hybrids were more genetically diverged than those pairs producing fertile sexual hybrids but less diverged than species pairs producing infertile hybrids. Hybrid asexuality therefore appears to evolve at lower divergence than other types of postzygotic barriers and might thus represent a primary reproductive barrier in many taxa.

Challenges and costs of asexuality: Variation in premeiotic genome duplication in gynogenetic hybrids from Cobitis taenia complex

“…Previous studies showed that their hybridization produces hybrids both in laboratory and natural conditions (Choleva et al, 2012;Janko et al, 2018). Male hybrids between C. elongatoides and C. taenia are sterile due to the aberrant pairing of their chromosomes (Figure 1) (Dedukh et al, 2020;Juchno and Boroń, 2006).…”

“…15.452483 doi: bioRxiv preprint At least in hybrid asexuals, it appears that the switch from sexual to clonal reproduction involves the modification of conservative gametogenic pathways, which is already occurring in the F1 generation (Lenormand et al, 2016;Neaves and Baumann, 2011;Saura, 2013, 2009). Interestingly, in cases where hybridization leads to aberrant chromosomal pairing and hybrid sterility, the adoption of clonal gametogenesis may partially overcome such conflicts and restore fertility (Figure 1) (Dedukh et al, 2020;Janko et al, 2018;Neaves and Baumann, 2011;Stenberg and Saura, 2013). One example of this is premeiotic endoreplication, which is a widespread gametogenic alteration found among a vast variety of unrelated asexual organisms such as plants, invertebrates and vertebrates (Figure 1) (Stenberg and Saura, 2009; Storme and Geelen, 2013; Suomalainen, 1987).…”

“…As a result, endoreplication rescues the hybrid`s fertility and ensures clonal propagation of the maternal genome (Figure 1) (Dedukh et al, 2020; Kuroda et al, 2019). Hybrid asexuality and sterility thus share some common cytological ground; both tend to emerge in hybrids between substantially diverged species rather than between closely related ones (Bateson, 1909;Ernst, 1918;Janko et al, 2018;Moritz, 1989;Russell, 2003).…”

The transcriptomic signature of obligate parthenogenesis

“…Substantial empirical evidence supporting Dobzhansky-Muller incompatibilities has emerged over the years (Rawson and Burton 2002; Barbash et al 2003; Presgraves 2003; Mack and Nachman 2016). However, obligate parthenogens with hybrid origin have not been explicitly considered under this theoretical framework (but see Janko et al 2018).…”

“…Compared to other modes of origin, hybridization is attributed for the largest number of obligate parthenogens by far, with nearly all vertebrate parthenogens having hybrid ancestry (Avise 2015). It is still controversial whether hybridization directly leads to parthenogenesis in the F 1 generation (Kearney et al 2009), as only a few attempts succeeded in generating parthenogenetic F 1 s by crossing identified parental lineages found in nature (e.g., Schultz 1973; White et al 1977; Hotz et al 1985; Janko et al 2018). Also, some obligate parthenogens (e.g., Daphnia ) are backcrosses derived from complex introgression events (Xu et al 2013; Xu et al 2015).…”