bioRxiv Science⌕ Search

bioRxiv · 10.1101/2023.02.21.529360

Two waves of evolution in the rodent pregnancy-specific glycoprotein (PSG) gene family lead to structurally diverse PSGs

Abstract

The evolution of pregnancy-specific glycoproteins (PSGs) within the CEA gene family of primates correlates with the evolution of hemochorial placentation about 45 Myr ago. Thus, we hypothesized that hemochorial placentation with intimate contact between fetal cells and maternal immune cells favors the evolution and expansion of PSGs. With only a few exceptions, all rodents have hemochorial placentas thus the question arises whether PSGs evolved in most rodent genera. Analyzing genomic data of 94 rodent species we could identify PSGs only in three families of the suborder Myomorpha (characteristic species in brackets) namely in the Muridae (mouse), Cricetidae (hamster) and Nesomyidae (giant pouched rat) families. No PSGs were detected in the suborders Anomaluromorpha (springhare), Castorimorpha (beaver), Hystricognatha (guinea pig) and Sciuromorpha (squirrel). Thus, PSGs evolved only recently in Myomorpha shortly upon their most recent common ancestor (MRCA) has coopted the retroviral genes syncytin-A and syncytin-B which enabled the evolution of the three-layered trophoblast. This may suggest that the evolution of Psgs in rodents may have been favored by the challenge of the newly invented architecture of the maternal-fetal interface. In addition, a second hallmark of rodent PSG evolution seems to be the translocation of genes from the CEA gene family locus into a unique genomic region. Rodents without PSGs do not have any CEA-related genes in this locus. In contrast, rodent species in which PSGs evolved have lost ITAM-encoding CEACAM genes indicating that such a gene was translocated and thereby destroyed to form the new rodent PSG locus. This locus contains at least one Psg and Ceacam9 indicating that one of them was the founder gene of rodent Psgs. These genes are composed of various numbers of IgV-like domains (N domains) and one carboxy-terminal IgC-like domain of the A2-type. In a second wave of gene amplification in the PSG locus a gene encoding a protein composed of two N domain gave rise to four genes in mice (Ceacam11-14). In light of the divergent structure of PSGs in various mammalian species, we hypothesized that the Ceacam11-14 encode also functional PSGs and indeed we found that they are preferentially expressed by spongiotrophoblast cells, like Psg genes.

Source connections

Explore related subjects

Keep this discovery

Explore connections, maps & timelines

BibTeXRIS

Kammerer, R., Zimmermann, W.. 2023-02-21. Two waves of evolution in the rodent pregnancy-specific glycoprotein (PSG) gene family lead to structurally diverse PSGs. https://doi.org/10.1101/2023.02.21.529360

Cite the original work for its findings. Save a collection to share your selection of sources.

KEEP EXPLORING

Related preprints

Measuring the strength of selection and pollen limitation on flower colour along an urban rural cline in Hesperis matronalis

Closely located urban and rural environments can differ in temperature, water availability, species diversity, and more. As a result, organisms in urban environments may experience different selection than those in rural environments. We investigated whether differences in selection might explain a previously identified urban-rural cline in the flower colour of Hesperis matronalis (dame's rocket). To explore whether plants in urban and rural environments are impacted by possible differences in pollinator availability or behavior, we performed a pollen supplementation experiment. We did not detect an effect of pollen supplementation on seed production in either setting (urban or rural), indicating that there is limited opportunity for any differences in pollinator availability or visitation to explain the cline in flower colour. We also measured the strength of selection acting on flower colour to investigate if it differed between urban and rural populations. In all but one population, we failed to detect significant linear or non-linear selection on flower colour, suggesting that selection on flower colour does not differ between urban and rural populations. Our results suggest that the urban-rural flower colour cline is likely not caused by differences in selection or pollen-limitation and may be due to stochastic forces.

evolutionary biology↗

An elongated lifespan is associated with higher oxidative protection of flight tissue in Heliconiini butterflies

Evolutionary theories of ageing often invoke trade-offs in resource allocation between somatic maintenance and other important physiological functions. One proposed mechanistic mediator of these trade-offs is oxidative stress, which arises from an imbalance between an organism's production of reactive oxygen species and its ability to detoxify them. Accordingly, many long-lived species across the animal kingdom show evidence for resistance to oxidative stress. However, it can be difficult to associate lifespan differences with oxidative phenotypes when comparing species across wide taxonomic distances, which may also show large differences in physiology. Butterflies in the long-lived Heliconius genus show a 3-fold lifespan extension and slowed ageing in comparison with their close relatives in the Heliconiini tribe, to whom they are phylogenetically, ecologically, and physiologically similar. However, proximate explanations for this extended longevity are currently lacking. Here, we leverage the neat comparative framework between Heliconius hecale and Dryas iulia, a shorter-lived Heliconiini outgroup, to test whether the observed lifespan differences between the two species are associated with differences in oxidative physiology. Our findings suggest superior oxidative protection of thoracic tissue in the longer-lived H. hecale compared to D. iulia, as evidenced by increased superoxide dismutase activity, increased total antioxidant capacity, and a corresponding reduction in lipid peroxidation in this tissue. Considering the metabolic demands of insect flight, we suggest that this oxidative phenotype may contribute to the extended longevity of Heliconius by enhancing protection of thoracic tissues against oxidative damage, representing a plausible proximate pro-longevity mechanism in this genus.

evolutionary biology↗

Both genetic and social inheritance influence female aggressive and submissive behavior in a wild primate

Agonistic interactions are important determinants of resource access in wild animals, but their genetic basis remains poorly understood. Here we use a quantitative genetics approach to estimate the heritability of aggressive and submissive behavior of wild female baboons, considering relative rates of both individual and dyadic aggression and submission. To control for the social inheritance that creates kin-based dominance hierarchies, we implemented a multi-matrix model that included a social status similarity matrix alongside the additive genetic matrix. Despite a substantial contribution of social inheritance, especially for submissive behavior, we found heritable components for both aggressive and submissive behavior (h2=0.21 and h2=0.09-0.11, respectively). In dyadic models, aggressive behavior was primarily influenced by the aggressor's genotype (a direct genetic effect), while submissive behavior was primarily affected by the social partner's genotype (an indirect genetic effect). Finally, we found evidence for a negative genetic (but not phenotypic) correlation between aggressive and submissive behavior within dyads, and a negative genetic correlation between submissive behavior and eliciting submissive behavior. Together, our results highlight how direct genetic, indirect genetic, and social inheritance effects combine to influence primate social behavior.

evolutionary biology↗