Sex-specific modifications of gametogenesis in natural and lab-bred Fundulus spp. hybrids

Successful hybridization between species can be limited by a variety of reproductive barriers; the emergence of asexual lineages is an example of a strong post zygotic barrier that is relatively rare in animals. In vertebrates, asexual reproduction typically arises through gametogenic alterations such as premeiotic genome endoreplication or meiotic failure, yet the relative frequency and conditions leading to their emergence remain poorly understood. Here, we investigate natural, all female clonal hybrid lineages and laboratory-bred hybrids of both sexes between two North American killifishes, Fundulus diaphanus and F. heteroclitus, to determine the mechanisms underlying and maintaining the emergence of asexual reproduction and male sterility. By combining cytogenetic, molecular, and gametogenetic analyses, we learned that both natural and lab-bred F1 hybrid females can produce diploid and tetraploid oocytes. In diploid oocytes, we observed both bivalents and univalents. In contrast, tetraploid oocytes formed exclusively bivalents with normal crossover formation, consistent with premeiotic genome endoreplication restoring proper meiotic pairing and facilitating clonal reproduction. Hybrid males do not undergo premeiotic genome duplication and exhibit extensive chromosomal mispairing, leading to aberrant meiotic divisions, elevated apoptosis, and decreased fertility or sterility. Together, these findings highlight sex-specific differences in gametogenesis, paralleling patterns observed in other systems, and emphasize the relative ease with which asexual reproduction can arise in hybrid females, in contrast to the sterility commonly observed in hybrid males.