The diversity of millions of species depends on the multiplication of species and speciation, in which reproductive isolation evolves, such as hybrid sterility: a puzzle that still remains unknown. Crosses between closely related species results in sterile hybrid males, the perturbances of spermatogenesis in the F1 hybrid males usually affect the later stages of development, arresting at the sperm individualization stage, which could be due to the rapid interspecies divergence of reproductive genes experiencing strong selective constraints between species. We annotated and analyzed the molecular evolution of 6 key spermatogenesis genes playing an important role in the sperm developmental pathway in 15 strains of Drosophila bipectinata species subcomplex, where the interspecies crosses are known to produce sterile hybrid males. We analyzed nucleotide divergence and characterized the patterns of sequence polymorphism in the protein-coding regions to validate or reject the nature of adaptive divergence using its phylogenetic histories. Except for spermatocyte arrest (sa) and twine, all 4 genes - always early(aly), bag of marbles(bam), don juan (dj) and matotopetli (topi) showed signatures of positive selection with more nonsynonymous to synonymous fixed differences between species. However, departure from neutrality in polymorphism analysis was only significant for topi, twine and aly. Consistent with our analysis proving rapid divergence of don juan(dj) and topi, hybrids involving the three species Drosophila bipectinata, Drosophila parabipectinata and Drosophila malerkotliana, have found immotile sperm and unindividualized spermatids. Bag of marbles(bam) and aly showed rapid divergence coherent to the aspermic testes abnormality found in the hybrid males from crosses involving the Drosophila pseudoananassae with the other three species. We propose that faster evolution of spermatogenesis genes due to a yet unknown underlying mechanism acting upon the germ cell line developmental pathway of these four species might be operating as a perpetual dynamo for interspecies divergence and hybrid male sterility. Our study is the first attempt to understand the molecular genetic basis of post-zygotic reproductive isolation in bipectinata species complex and lays a foundation for future detailed exploration to better understand the mechanisms involved.
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