Positive selection in gamete interaction proteins inCarnivora

Abstract

The jaguar (Panthera onca) is the most relevant predator in South America and an endangered species in Argentina. Therefore genomic, evolutionary and functional studies of this species are strategic to gain biological insights and support conservation efforts. With the advent of sequencing advances the study of relevant character species evolution has to be revisited. Recent comparative genomic analysis revealed a long history of hybridization among extant big cats, which indicates an absence of inter-specific isolation barriers. We aimed to uncover the molecular basis of this interspecies crossing and the evolution of the functional capacities of pantherine gamete interaction Zona Pellucida proteins (ZP) and JUNO. Hi-C long-range sequencing and chromosome-resolved jaguar genome assembly was used to resolve ZP genes loci and reconstruct the evolutionary history of these proteins. Exploring sequence variability in more that 30 Carnivora species, Feliforme and Caniforme sister groups show significant differences in average sequence identity for all studied proteins except ZP4, always showing Caniformes as a more diverse group than Feliformes. Molecular evolution of ZP isoforms involved in sperm-recognition, ZP3 and ZP2, showed similar phylogenetic histories, displaying signatures of positive selection among Carnivores and Caniformes, but not among Pantherines or Feliformes. On the other hand, structural cross-linking ZP subunits, ZP1 and ZP4, displayed a different evolutionary history. The fusion protein IZUMO1R was found to be highly conserved in all studied phylogenetic groups. These results strengthen the idea that ZPs are proteins more related to specific-specificity isolation than IZUMO1R, which is specialized in fusion events. Altogether, our findings indicate that sperm-oocyte interaction and fusion proteins lack the degree of diversification necessary to establish a prezygotic reproductive isolation barrier between pantherines, which would explain observed reticulated patterns of evolution in this clade.

Oviductin sets the species-specificity of the mammalian zona pellucida

“…ZP proteins and sperm-oocyte fusion protein are usually found to evolve under selection pressure. It is proposed that this rapid evolution plays an important role in the reproductive isolation of diverging taxa ( 4, 5 ). The mechanism of fusion between the sperm and oolemma membranes is not fully understood, although various candidate molecules have been identified ( 6–8 ).…”