Insights from genomes into the evolutionary importance and prevalence of hybridization in nature

Hybridization [interbreeding between two animals or plants of different groups (of one or more populations of an organism or organisms determined by taxonomists to form a unit] between species, subspecies, or lineages within species — has long been viewed as a powerful tool for understanding evolutionary biology. The study of hybridization has had two primary foci over the past century: one, concerned with understanding species barriers; two, concerned with the role of hybridization in generating novel gene combinations that selection can then act upon. The usefulness of using hybrid zones to understand the process of speciation (i.e. to identify regions of the genome that likely are involved in maintenance of reproductive isolation) is clear, and this has been the focus during hundreds of studies. The crossing-experiments that occur in natural hybrid zones would often be impossible to replicate in the lab, and the importance of studying hybridization in nature is hard to overstate.

The importance of hybridization in the processes of adaptation and speciation has, however, been rigorously debated in the literature, and a consensus that hybridization can, and often does, play a creative role in evolution has recently been forming. Importantly, the role that hybridization plays in the evolutionary history of different taxa is variable (i.e. there may be periods of introgression, hybrid speciation, and/or adaptive introgression), and the emphasis on certain outcomes of hybridization (e.g. hybrid speciation) appear to be skewed in the literature.

Historically, botanists and zoologists have approached this problem with different perspectives. The importance of hybridization in the evolution and diversification of plants is well-documented, and a creative role for hybridization in the evolution of plants has long been accepted. Zoologists, on the other hand, have generally viewed hybridization as a useful tool for studying species barriers and reproductive isolation, but not as a source of genetic novelty that selection can act upon. There has been a significant shift in this view since the mid-1900s, and many now see hybridization as a potentially creative force in evolution and adaptation for both plants and animals.

It is becoming increasingly evident that hybridization, whether intermittent or ongoing, has played a major role in the evolutionary history of many taxa, including hominins (hominids include orangutans, gorillas, chimpanzees, and modern humans). For a long time, however, it has been difficult to fully understand the extent to which hybridization between closely related taxa has influenced their evolutionary histories. This is, in part, because (in the recent past) researchers lacked the tools to dissect genomes at high resolution. Over the past decade, this landscape has rapidly changed, and whole genomes from most non-model taxa can now be sequenced at a relatively low cost. Studies that leverage genome-spanning data in their analyses are uncovering signatures of hybridization in taxa that were never really expected to have a history of hybridization. These studies confirm previous hypotheses about the role of hybridization in diversification. In the era of high-throughput sequencing, scientists are better equipped than ever before to determine the extent to which hybridization has played a role in the evolution of life on Earth.

Authors [see attached review] describe analyses of whole genomes that are providing further insight into this evolutionary problem. Recent studies have documented ancient hybridization in a diverse array of taxa — including mammals, birds, fish, fungi, and insects. Evidence for adaptive introgression (i.e. management and genetic conservation when exposed to a changing environment) is being documented in an increasing number of systems, though demonstrating the adaptive function of introgressed genomic regions remains difficult. And finally, several new homoploid hybrid speciation events have been reported. Authors review herein the current state of the field and specifically evaluate the additional insights gained from having access to whole-genome data. Authors also review challenges that remain, with respect to understanding the evolutionary relevance and frequency of ancient hybridization, adaptive introgression, and hybrid speciation in nature.

DwN

Nature Ecol Evol 2019; 3, 170–177

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