Maternal–foetal genomic conflict and speciation: no evidence for hybrid placental dysplasia in crosses between two house mouse subspecies

Abstract

Interspecific hybridization between closely related mammalian species, including various species of the genus Mus, is commonly associated with abnormal growth of the placenta and hybrid foetuses, a phenomenon known as hybrid placental dysplasia (HPD). The role of HPD in speciation is anticipated but still poorly understood. Here, we studied placental and foetal growth in F 1 crosses between four inbred mouse strains derived from two house mouse subspecies, Mus musculus musculus and Mus musculus domesticus. These subspecies are in the early stage of speciation and still hybridize in nature. In accordance with the maternal-foetal genomic conflict hypothesis, we found different parental influences on placental and foetal development, with placental weight most affected by the father's body weight and foetal weight by the mother's body weight. After removing the effects of parents' body weight, we did not find any significant differences in foetal or placental weights between intra-subspecific and inter-subspecific F 1 crosses. Nevertheless, we found that the variability in placental weight in inter-subspecific crosses is linked to the X chromosome, similarly as for HPD in interspecific mouse crosses. Our results suggest that maternal-foetal genomic conflict occurs in the house mouse system, but has not yet diverged sufficiently to cause abnormalities in placental and foetal growth in inter-subspecific crosses. HPD is thus unlikely to contribute to speciation in the house mouse system. However, we cannot rule out that it might have contributed to other speciation events in the genus Mus, where differences in the levels of polyandry exist between the species.

Speciation and reduced hybrid female fertility in house mice

“…Our results are consistent with another recent study that showed no differences in fetal or placental growth between intrasubspecific and intersubspecific crosses using different strains of M. m. musculus and M. m. domesticus (Kropackova et al. ). These findings are noteworthy because this same species ( M. musculus ) is involved in parent‐of‐origin growth effects in hybrids when crossed to Mus spretus , a slightly more distantly related species with which M. musculus is broadly sympatric and sometimes hybridizes (Zechner et al.…”

“…Although we found no evidence for overgrowth or undergrowth phenotypes in F1s, consistent with Kropackova et al. (), a role for imprinting in some of the phenotypes cannot be completely ruled out. The fact that asymmetry is seen in some crosses suggests that either cyto‐nuclear interactions or imprinting may be involved.…”

“…() suggested that there might also be a slight reduction in embryonic viability in F1 females, although another recent study failed to find a reduction in fetal or placental growth in crosses between different inbred strains of M. m. musculus and M. m. domesticus (Kropackova et al. ). Using inbred strains with a standard karyotype ( M. m. domesticus WLA and M. m. musculus PWK ) Britton‐Davidian et al.…”

Hybrid asexuality as a primary postzygotic barrier between nascent species: On the interconnection between asexuality, hybridization and speciation

“…A pervasive observation in speciation literature is that hybridization capability decreases as one moves from closely to distantly related pairs of taxa (Kropáčková, Piálek, Gergelits, Forejt, & Reifová, ; Russell, ; Rykena, ; Sánchez‐Guillén, Córdoba‐Aguilar, Cordero‐Rivera, & Wellenreuther, ), which is believed to result from gradual accumulation of genetic incompatibilities that cause intrinsic postzygotic isolation, that is, hybrid infertility and inviability (rev. in Seehausen et al., ).…”

Hybrid asexuality as a primary reproductive barrier: on the interconnection between asexuality and speciation

“…in [1]). The study of intrinsic postzygotic isolation has a strong tradition in evolutionary biology [2,3] and comparative studies showed that hybridization capability decreases as one moves from closely to distantly related pairs of taxa [4][5][6][7]. Although the rate at which intrinsic postzygotic RIMs accumulate is probably nonlinear [8][9][10] and varies among taxa [11], hybrid infertility generally evolves at lower genetic distances than hybrid inviability [5,12] and according to Haldane's rule, both hybrid sterility and inviability evolve faster in the heterogametic sex [13].…”