Germline novelty through recurrent copy-number, protein, and regulatory evolution of the synaptonemal complex

Abstract

ABSTRACTThe synaptonemal complex (SC) is a protein-rich structure necessary to tether homologous chromosomes for meiotic recombination and faithful segregation. Despite being found in most major eukaryotic taxa implying a deep evolutionary origin, components of the complex can exhibit unusually high rates of sequence evolution, particularly inDrosophilawhere orthologs of several components could not be identified outside of the genus. To understand the cause of this paradoxical lack of conservation, we examine the evolutionary history of the SC in Drosophila, taking a comparative phylogenomic approach with high species density to circumvent obscured homology due to rapid sequence evolution. We find that in addition to elevated rates of coding evolution due to recurrent and widespread positive selection, components of the SC, in particular the central elementconaand transverse filamentc(3)Ghave diversified through tandem and retro-duplications, repeatedly generating paralogs with novel germline functions. Strikingly, independentc(3)Gduplicates under positive selection in separate lineages both evolved to have high testes expression and similar structural changes to the proteins, suggesting molecular convergence of novel function. In other instances of germline novelty, twoconaderived paralogs were independently incorporated into testes- expressed lncRNA. Surprisingly, the expression of SC genes in the germline is exceedingly prone to change suggesting recurrent regulatory evolution which, in many species, resulted in high testes expression even thoughDrosophilamales are achiasmic. Overall, our comprehensive study recapitulates the adaptive sequence evolution of several components of the SC, and further uncovers that the lack of conservation not only extends to other modalities including copy number, genomic locale, and germline regulation, it may also underlie repeated germline novelties especially in the testes. Given the unexpected and frequently elevated testes expression in a large number of species and the ancestor, we speculate that the function of SC genes in the male germline, while still poorly understood, may be a prime target of constant evolutionary pressures driving repeated adaptations and innovations.