Digest: Hybridizing in a big way*

Abstract

Gene regulation plays an important role in an organism's development and morphological evolution. However, the importance of regulatory divergence in speciation remains unclear. Hybrids between mammalian species often differ in size from their parents due to dramatic parent-of-origin growth effects (Vrana 2007; Brekke and Good 2014;Wolf et al. 2014). The parent-of-origin effects on growth usually manifest in the placenta and embryo development stage, when the embryo is highly sensitive to gene dosage/expression (Haig 1996). It is however, unclear whether this observed pattern of abnormal hybrid growth has a common regulatory basis across mammalian species.According to a long-standing hypothesis for abnormal hybrid growth, a loss of imprinting (LOI) results in the disruption to gene expression in hybrid placentas, leading to an imbalance between paternal and maternal growth factors (Vrana 2007). The predictions of LOI are clear; however, empirical support for this model has been mixed. Additionally, most data supporting the LOI in hybrids have come from a limited number of candidate genes, and the generality of this model remains unclear (Wolf et al. 2014).Hybrids of the closely related dwarf hamster species Phodopus sungorus and Phodopus campbelli show extreme parent-oforigin growth effects. The hybrid formed from a P. sungorus female crossed with a P. campbelli male (SxC) show large placental and embryonic overgrowth and also a range of birth defects that can result in late-term pregnancy failure or maternal death. In the reciprocal hybrids (cxs), this does not occur. By comparing genome-wide patterns of placental expressions between both species and hybrids, researchers can determine if abnormal hybrid growth is associated with disrupted expression and also test the central predictions of the LOI model (Vrana 2007;Wolf et al. 2014). In this study, Brekke and colleagues analyzed placental transcriptomes to evaluate expression levels in the hybrids. They found that many genes (approximately ten percent) are misexpressed in the hybrids relative to the parent species, and that the large hybrid (SxC) has more misexpressed genes than the normal hybrid (cxs). This latter observation suggests that abnormal expression is associated with abnormal growth and is not just a general dysregulation from hybrids of these species.The LOI model predicts a connection between LOI and expression level. For this system, the researchers predicted biallelic expression of paternally expressed genes that promote growth in SxC hybrids. Instead, they found that while there was much biallelic expression in the SxC hybrids, candidateimprinted genes were strongly biased toward maternal expression. Additionally, the researchers found that the expression level of biallelic-expressed genes in SxC was severely reduced overall.These results show that the expression levels and predicted functional roles of both maternally and paternally expressed genes were consistent with the phenotypic patterns of hybrid placental overgrowth, but the results co...