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.

ZP4 Is Present in Murine Zona Pellucida and Is Not Responsible for the Specific Gamete Interaction

“…Moreover, comparative sequencing studies among taxonomic groups have led to the discovery that reproductive proteins evolve more rapidly than other genes expressed in other tissues (Swanson et al, 2001 ; Torgerson et al, 2002 ). This positive selection has been described in seminal plasma proteins (Kingan et al, 2003 ; Dorus et al, 2004 ), oviductal proteins (Moros-Nicolás et al, 2018b ), and also in other proteins related with fertilization, such as ZP3, CatSper1 or CD9 (Swanson et al, 2001 , 2003 ) These proteins would have been under a selective pressure that may be related to male-female interaction, in this case, sperm-egg interaction. Our analysis identified two sites in Zp4 that are under positive selection (141R and 547L ) .…”

A Comparative View on the Oviductal Environment during the Periconception Period

“…It is consistent with the reported information about OVGP1 gene existing before the divergence of mammals and being from this species [ 132 ]. In megabat it is also considered a pseudogene [ 133 ].…”

Rapid divergence of a gamete recognition gene promoted macroevolution of Eutheria

“…To assess relationships of positive selection to phylogenetic support more broadly, we retrieved all reliable sequences of all genes previously shown to have evolved by positive selection [24,91,95,100,[107][108][109][110][111][112][113][114][115][116][117][118][119][120][121][122] and conducted Bayesian and selection analyses on individually constructed gene trees. Excluding 12 genes with too little taxonomic representation (either fewer than nine Orders total or no basal Orders), the analysis yielded Bayesian (>95% posterior support) and M7 and M8 model selection data (magnitude = dN/dS = ω, and frequency= f) for 40 positively selected genes with widely ranging functions, including 23 genes that function in reproduction, seven in sensory perception, five in immunity, three in metabolism, and one each in the nervous system and the cell cycle.…”