Contributions to Zoology, 84 (3) – 2015Camille Meslin; Michel Laurin; Isabelle Callebaut; Xavier Druart; Philippe Monget: Evolution of species-specific major seminal fluid proteins in placental mammals by gene death and positive selection

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Diversification of proteins in seminal fluid

The present work suggests that the high diversity of proteins present in seminal fluid of mammals is associated with a species-specific evolutionary pattern of the corresponding genes by fairly frequent pseudogenisation, high expression diversity, and positive selection. Pseudogenisation has been previously demonstrated for TGM4 and semenogelin genes in some ape species (Jensen-Seaman and Li, 2003). We also have previously shown that TGM4 has also been lost in cattle, horse, dog, and likely several other mammalian species (Tian, Pascal, Fouchécourt, et al., 2009) and that the ortholog of porcine Sal1 and Major allergen Equine C1 Precursor has also been lost in human as well as in the Neanderthal genome (Meslin et al., 2011). It is difficult to determine if the pseudogenisation rate of 0.00048 events/lineage/gene/Ma is especially high because such rates have seldom been reported in the literature. We reported before, from a different set of 69 genes and a different taxonomic sample, rates ranging from 0 (in teleosts) to 0.016 (in eutherians) (Meslin et al., 2012). The latter value, to be meaningfully compared with our rates, has to be converted into a rate per gene, which gives about 0.00023 events/lineage/gene/Ma for eutherians. Given that our sample is also composed of eutherians, the 20 genes studied here appear to have undergone more pseudogenisation than most of the 69 genes studied previously (Meslin et al., 2012).

A few examples illustrate how this diversity appeared. The gene encoding KLK2, a kallikrein expressed in the prostate in humans, was previously shown to be lost in several primates (Gorilla gorilla Savage 1847, Papio anubis Lesson 1827, (Marques et al., 2012)), and under positive selection in others, as were two other genes encoding the proteases ACPP and TGM4 (Clark and Swanson, 2005). In the present study, we found that KLK2 has been lost in cattle, horse, and mouse (i.e. we found traces of pseudogenes), probably independently because close relatives of these taxa retain this gene. The situation of the TGM4 gene is different. It is present in birds, squamates, platypus, several primates and at least three rodents, but is absent in all sampled laurasiatherians. Thus, it may have been lost before the appearance of Laurasiatheria. Interestingly KLK1, a paralog of KLK2, a major protein found in equine seminal fluid (named KLK1E2), is under positive selection in cattle, horse, mouse as well as in human. KLK1 seems to be mainly expressed in the kidney, the pancreas and the salivary glands in the mouse (, so some investigations are needed to confirm its presence in the seminal fluid of other species (except horse). Nevertheless, this suggests that at least in horse, KLK1 may replace KLK2 for an important biological function in the seminal fluid.