Evaluating hybrid speciation and swamping in wild carnivores with a decision-tree approach

Abstract

Hybridization is an important evolutionary force with a principal role in the origin of new species, known as hybrid speciation. However, ongoing hybridization can create hybrid swamping, in which parental genomes are completely lost. This can become a biodiversity threat if it involves species that have adapted to certain environmental conditions and occur nowhere else. Because conservation scientists commonly have a negative attitude toward hybrids, it is important to improve understanding of the influence of interspecific gene flow on the persistence of species. We reviewed the literature on species hybridization to build a list of all known cases in the order Carnivora. To examine the relative impact, we also noted level of introgression, whether fertile offspring were produced, and whether there was mention of negative or positive evolutionary effects (hybrid speciation and swamping). To evaluate the conservation implications of hybrids, we developed a decision-making tree with which to determine which actions should be taken to manage hybrid species. We found 53 hybrids involving 68 unique taxa, which is roughly 23% of all carnivore species. They mainly involved monophyletic (83%) and sympatric species (75%). For 2 species, the outcome of the assessment was to eliminate or restrict the hybrids: Ethiopian wolf (Canis simensis) and Scottish wildcat (Felis silvestris silvestris). Both species hybridize with their domestic conspecifics. For all other cases, we suggest hybrids be protected in the same manner as native species. We found no evidence of genomic extinction in Carnivora. To the contrary, some species appear to be of hybrid origin, such as the Asiatic black bear (Ursus thibetanus) and African golden wolf (Canis lupaster). Other positive outcomes of hybridization are novel genetic diversity, adaptation to extreme environments, and increased reproductive fitness. These outcomes are particularly valuable for counterbalancing genetic drift and enabling adaptive introgression in a human-dominated world.