The role of hybridization in vertebrate speciation

When individuals of two closely related species interbreed, viable hybrids can sometimes be born. Among animals, prominent examples include mules, the hybrids between horses and donkeys, "ligars", the hybrids between lions and tigers, or "pizzlies", the hybrids between polar bears and grizzly bears. Ususally, however, these hybrids are not fertile, meaning that they can not have offspring themselves. Therefore, hybridization is often seen as an evolutionary dead end; the genetic mixture of the hybrids can not be passed on to the next generation. However, this is not always the case. In other species, such as Darwin's finches and sparrows, geneticists have observed that hybrids were able to further reproduce with other hybrids and form a new species; a hybrid species. Even humans carry genetic material which they gained thousands of years ago through hybridization with Neanderthals and other ancient humans. Moreover, it has been shown that this genetic material can be beneficial, and that it contributes for example to the Tibetans' ability to survive at high altitudes. Thus, hybridization clearly was more than just an evolutionary dead end at least in these cases. However, the general role of hybridization is so far very poorly understood: Are Darwin's finches, sparrows, and humans exceptions, and is hybridization an evolutionary dead end for most other species? Or are these reported cases merely the "tip of the iceberg" and hybridization is generally an important force in the evolution of animals? This is the question that is currently being addressed in this science project, using genetic sequence data from various vertebrate groups and state-of-the-art inference methods. This investigation requires multifaceted components, including a reliable family tree of vertebrates, robust methodology to time-calibrate this tree, and tools to estimate rates of hybridization among species. These components have continued to be developed and to mature during the second year of this project. Genetic datasets have been compiled and rare samples of the last remaining vertebrate families without available genetic information have been obtained from museums around the world. Moreover, despite delays resulting from closure of the genetic laboratory due to the coronavirus, DNA has now been extracted successfully from these old samples and is about to be converted into genetic information. This means that a complete family tree of vertebrates is now, for the first time, within reach. Additionally, both the required robust methodology to time-calibrate trees and the tools to estimate rates of hybridization have been developed and tested, and have already been accepted for publication at international scientific journals. The stage is thus set for a successful continuation of this project. In February 2021, the leader of this project has accepted a position as Associate Professor in Vertebrate Zoology at the Natural History Museum, Oslo. His research focus will continue to be on hybridization and speciation in vertebrates, which means that the project can be continued seamlessly in this new position.

The achieved outcomes are in the form of new methodology for phylogenetic divergence-time estimation and for tests of past hybridization with genomic data, genomic resources for rare vertebrate families, a database of vertebrate fossil information, and insights into the processes that regulate introgression in hybridizing species. While the family-level phylogeny of vertebrates has not been completed yet due to the shortened FRIPRO mobility fellowship, the new position and workplace of the project leader (since February 2021) will allow him in an ideal way the continuation and successful completion of the project as planned.

In this interdisciplinary research project, I will address a fundamental question in evolutionary biology: Does hybridization slow down and reverse speciation, or is it in fact a driver for speciation? While the former view has traditionally been assumed and is reflected in most biology textbooks, recent genomic investigations have uncovered traces of past hybridization in many lineages, including some of the most rapidly diversifying groups of species. Consequently, it has been argued that hybridization may in fact facilitate speciation by providing potentially adaptive genetic variation that allows not only intermediate but also transgressive phenotypes. As hybridization occurs more frequently between recently diverged species, a positive effect of hybridization on speciation would be expected to manifest itself in a time-variable speciation rate that declines with species age. This type of age-dependent speciation rate has recently been inferred on a macroevolutionary scale; however, whether this age-dependent speciation is linked to hybridization is so far unknown. The proposed research is therefore designed to test this hypothesis, through a comparison of the degree to which speciation is age dependent and the amount of hybridization observed in vertebrate families. To this end, I will construct the first complete family-level phylogeny of vertebrates, which will allow a thorough analysis of speciation-rate age dependence and its variation among families. In addition, I will use available genomic data sets to test for traces of past hybridization, individually in a large number of vertebrate families. By combining these innovative approaches, this project will allow the first assessment of the general role of hybridization as a putative driver of speciation, and thus promises fundamental insights into the process responsible for all of Earth's biodiversity.