Divergent genetic and epigenetic post-zygotic isolation mechanisms in Mus and Peromyscus

Abstract

Interspecific hybridization in the rodent genera Peromyscus and Mus results in abnormal placentation. In the Peromyscus interspecies hybrids, abnormal allelic interaction between an X‐linked locus and the imprinted paternally expressed Peg3 locus was shown to cause the placental defects. In addition, loss‐of‐imprinting (LOI) of Peg3 was positively correlated with increased placental size. As in extreme cases this placental dysplasia constitutes a post‐zygotic barrier against interspecies hybridization, this finding was the first direct proof that imprinted genes may be important in speciation and thus in evolution. In the Mus interspecies hybrids, a strong role of an X‐linked locus in placental dysplasia has also been detected. However, here we show by backcross and allele specific expression analyses that neither LOI of Peg3 nor abnormal interactions between Peg3 and an X‐linked locus are involved in generating placental dysplasia in Mus hybrids, although the placental phenotypes observed in the two genera seem to be identical. In contrast to this, another dysgenesis effect common to Peromyscus and Mus hybrids, altered foetal growth, is caused at least in part by the same X‐chromosomal regions in both genera. These findings first underline the strong involvement of the X‐chromosome in the genetics of speciation. Secondly, they indicate that disruption of epigenetic states, such as LOI, at specific loci may be involved in hybrid dysgenesis effects in one group, but not in another. Thus, we conclude that even in closely related groups divergent molecular mechanisms may be involved in the production of phenotypically similar post‐zygotic barriers against hybridization.

Changes in cell cycle and extracellular matrix gene expression during placental development in deer mouse (Peromyscus) hybrids

“…Esx1 is a candidate gene for one of the loci involved in the PO × BW placental hyperplasia (Loschiavo et al 2007). Finally, the M. spretus/B6 crosses bear special note because they have also been termed interspecific hybrids (Zechner et al 2004). However, the B6 strain is a mix of the M. musculus musculus and domesticus subspecies of unknown locales, as well as containing M. spretus sequences (http://www.informatics.jax.org/external/festing/mouse/docs/ C57BL.shtml).…”

Imprinted gene expression in hybrids: perturbed mechanisms and evolutionary implications

“…One candidate is the imprinted Esx1 gene, at which loss of expression leads to placental overgrowth (Salas et al, 2004). The placental dysplasia in M. musculus  M. spretus hybrids is indeed genetically linked to the X chromosome, to a region comprising Esx1 Zechner et al, 2004). Also in Peromyscus, placental overgrowth in hybrids is linked to the X chromosome (Vrana et al, 2000) and is associated with abnormal levels of Esx1 expression (Duselis and Vrana, 2010).…”

Somatic Reactivation of Expression of the Silent Maternal <i>Mest</i> Allele and Acquisition of Normal Reproductive Behaviour in a Colony of <i>Peg1/Mest</i> Mutant Mice

“…Abnormal maintenance of genomic imprinting has been observed in inter-species hybrids between mus musculus and mus spretus, or mus peromyscus [9,11,12, 21,22]. In addition, Croteau et al.…”

“…There are many factors, including learned behaviour as well as gene-environment interactions, that could impact maternal behaviour, and any or all of these factors could potentially have influenced the behavioural outcomes. Given that homozygous Mest mutant mice in our colony were also able to raise their own litters and so exhibited normal nursing behaviour, it seems unlikely that the Mest mutation was solely influencing the maternal behaviour in these mice.Abnormal maintenance of genomic imprinting has been observed in inter-species hybrids between mus musculus and mus spretus, or mus peromyscus [9,11,12, 21,22]. In addition, Croteau et al.…”