Genes Encoding Mammalian Oviductal Proteins Involved in Fertilization are Subjected to Gene Death and Positive Selection

Abstract

Oviductal proteins play an important role in mammalian fertilization, as proteins from seminal fluid. However, in contrast with the latter, their phylogenetic evolution has been poorly studied. Our objective was to study in 16 mammals the evolution of 16 genes that encode oviductal proteins involved in at least one of the following steps: (1) sperm-oviduct interaction, (2) acrosome reaction, and/or (3) sperm-zona pellucida interaction. Most genes were present in all studied mammals. However, some genes were lost along the evolution of mammals and found as pseudogenes: annexin A5 (ANXA5) and deleted in malignant brain tumor 1 (DMBT1) in tarsier; oviductin (OVGP1) in megabat; and probably progestagen-associated endometrial protein (PAEP) in tarsier, mouse, rat, rabbit, dolphin, and megabat; prostaglandin D2 synthase (PTGDS) in microbat; and plasminogen (PLG) in megabat. Four genes [ANXA1, ANXA4, ANXA5, and heat shock 70 kDa protein 5 (HSPA5)] showed branch-site positive selection, whereas for seven genes [ANXA2, lactotransferrin (LTF), OVGP1, PLG, S100 calcium-binding protein A11 (S100A11), Sperm adhesion molecule 1 (SPAM1), and osteopontin (SPP1)] branch-site model and model-site positive selection were observed. These results strongly suggest that genes encoding oviductal proteins that are known to be important for gamete fertilization are subjected to positive selection during evolution, as numerous genes encoding proteins from mammalian seminal fluid. This suggests that such a rapid evolution may have as a consequence that two isolated populations become separate species more rapidly.

Keywords: Fertilization; Oviduct; Positive selection; Protein evolution; Pseudogene.

Fig. 1

Identification of marks of pseudogenes. A tBlastn analysis allowed the identification of exons presenting STOP codons (*) within tarsier ANXA5, tarsier DMBT1, and megabat OVGP1. For each alignment, the upper number corresponds to the amino acid position and the lower number to the genomic position of nucleotides on the corresponding chromosome

Fig. 2

Proteins present in oviductal fluids and phylogenetic results showing gene loss, gene duplication, and positive selection. The list of oviductal proteins involved in the different processes of sperm storage and gamete fertilization in different mammals was established in the “Material and Methods” section