The role of homoploid hybridization in evolution: A century of studies synthesizing genetics and ecology

Abstract

While homoploid hybridization was viewed as maladaptive by zoologists, the possibility that it might play a creative role in evolution was explored and debated by botanists during the evolutionary synthesis. Owing to his synthetic work on the ecological and genetic factors influencing the occurrence and effects of hybridization, G. Ledyard Stebbins' contributions to this debate were particularly influential. We revisit Stebbins' views on the frequency of hybridization, the evolution of hybrid sterility, and the evolutionary importance of transgressive segregation, introgression, and homoploid hybrid speciation in the context of contemporary evidence. Floristic surveys indicate that ∼10% of plant species hybridize, suggesting that natural hybridization is not as ubiquitous as Stebbins argued. There is stronger support for his contention that chromosomal sterility is of greater importance in plants than in animals and that selection drives the evolution of hybrid sterility. Stebbins' assertions concerning the frequent occurrence of transgressive segregation and introgressive hybridization have been confirmed by contemporary work, but few studies directly link these phenomena to adaptive evolution or speciation. Stebbins proposed a mechanism by which chromosomal rearrangements partially isolate hybrid lineages and parental species, which spurred the development of the recombinational model of homoploid speciation. While this model has been confirmed empirically, the establishment of reproductively independent hybrid lineages is typically associated with the development of both intrinsic and extrinsic reproductive barriers. We conclude by reflecting on outcomes of hybridization not considered by Stebbins and on possible future research that may extend our understanding of the evolutionary role of hybridization beyond Stebbins' legacy.

Hybridization in Plants: Old Ideas, New Techniques

“…Verifying a case of homoploid hybrid speciation requires both demonstrating the hybrid origin of the lineage and showing that the hybridization is directly accountable for establishing reproductive isolation (Schumer et al, 2014). While homoploid hybrid speciation often is invoked upon the demonstration of hybrid origin and a distinct ecological niche, there are very few examples that draw a compelling mechanistic link between hybridization and the establishment of a new, isolated species (Schumer et al, 2014;Yakimowski and Rieseberg, 2014). Furthermore, there is evidence that genetic divergence affects the relative likelihood of homoploid (more likely between less-diverged species) or polyploid (more likely between more-diverged species) hybrid speciation (Chapman and Burke, 2007).…”

Is homoploid hybrid speciation that rare? An empiricist’s view

“…Beyond this basic definition, complete agreement is lacking on key aspects of the process, such as the relative proportions of each parental genome present in a hybrid species, the mechanisms leading to reproductive isolation (RI), the degree of RI or the role played by hybridization in the process (Rieseberg, 1997;Abbott et al, 2010). While our understanding of HHS has been improved by detailed evolutionary case studies documented by recent reviews (Abbott et al, 2013;Yakimowski and Rieseberg, 2014;Payseur and Rieseberg, 2016) and empirical studies focused on mechanisms leading to HHS (Renaut et al, 2014;Selz et al, 2014;Lukhtanov et al, 2015), there is controversy concerning the criteria to identify and demonstrate HHS, and even the range of situations that HHS might encompass.…”

“…However, the HHS concept is widely used, and we think that pointing out potential weaknesses in criteria that are too stringent is useful to avoid misconceptions and contribute to a solid and, at the same time, open conceptual framework (Wiens, 2004) for such a complex topic. Yakimowski and Rieseberg (2014) list 19 putative cases of HHS among seed plants, two of them in genera in which more than one species is of hybrid origin.…”

Hybrid swarms: catalysts for multiple evolutionary events inSenecioin the British Isles

“…Depending on fertility constraints, different genomic combinations occurring within hybrid swarms can break down character coherence and give rise to new recombinants and introgressants (Anderson and Stebbins 1954;Rieseberg and Wendel 1993;Rieseberg et al 2003;Yakimowski and Rieseberg 2014). Indeed, trait expression within many hybrid derivatives can be transgressive (i.e.…”