A mitochondrial genetic divergence proxy predicts the reproductive compatibility of mammalian hybrids

Abstract

Numerous pairs of evolutionarily divergent mammalian species have been shown to produce hybrid offspring. In some cases, F₁ hybrids are able to produce F₂s through matings with F₁s. In other instances, the hybrids are only able to produce offspring themselves through backcrosses with a parent species owing to unisexual sterility (Haldane's Rule). Here, we explicitly tested whether genetic distance, computed from mitochondrial and nuclear genes, can be used as a proxy to predict the relative fertility of the hybrid offspring resulting from matings between species of terrestrial mammals. We assessed the proxy's predictive power using a well-characterized felid hybrid system, and applied it to modern and ancient hominins. Our results revealed a small overlap in mitochondrial genetic distance values that distinguish species pairs whose calculated distances fall within two categories: those whose hybrid offspring follow Haldane's Rule, and those whose hybrid F₁ offspring can produce F₂s. The strong correlation between genetic distance and hybrid fertility demonstrated here suggests that this proxy can be employed to predict whether the hybrid offspring of two mammalian species will follow Haldane's Rule.

Keywords: evolution; gene flow; genetic distance; hybrid.

Figure 1.

A depiction of the correlation between CYTB divergence between mammalian species pairs and the relative fertility of their hybrid offspring. In column (a), the green circles represent species capable of producing fully fertile F₁ offspring which can reproduce independently of their parent species (category 1). Brown circles represent species pairs that follow Haldane's Rule and require backcrossing of a female F₁ with a parent species, or both sexes are sterile (category 2). The single grey dot represents the distance between mountain hares and European rabbits that, despite numerous attempts, failed to produce any offspring. The green and brown shaded regions represent the range of divergence values of the two categories. Column (b) depicts the divergence between three wild felid species and domestic cats, as well as the minimum number of generations of backcrosses with domestic cats before full fertility of the hybrid is restored. The white circles in column (c) depict the divergence between three ancient hominins and anatomically modern humans (AMH), as well as the distances between AMH and chimpanzees and bonobos (in category 2). The asterisks represent those pairs that include modern samples of AMH. The lack of an asterisk signifies that only sequences derived from archaeological AMH were used to compute the divergence values. Details regarding the specific species pairs are listed in the electronic supplementary material, figure S1 and table S1. (Online version in colour.)