Conditions when hybridization might predispose populations for adaptive radiation

The role of hybridization in evolution is a theme that has been intensively and sometimes controversially debated, particularly amongst zoologists. Long time considered an evolutionary dead end, interspecific hybridization is now known to have left imprints in the genomes of many plant and animal lineages (Grant et al., 2003; Mallet, 2005; Arnold, 2006). While it is clear that hybridization has often times been no dead end, questions that remain contentious are whether and how hybridization affects rate and direction of evolution, and how it affects speciation. Classically, hybridization was thought to put a brake on speciation (Mayr, 1942; Dobzhansky, 1951), but this view is also beginning to change. Hybrid speciation has been quite well documented (Buerkle Abbott et al., 2013), and hybridization appears to be particularly common in the most species-rich and rapidly diversifying groups of organisms (Schwarzer et al., 2012), perhaps just as a consequence of many young species in geographical proximity. Either way it is clearly not preventing speciation in these groups (Salazar et al., 2010; Joyce et al., 2011; Genner Stelkens Altrock et al., 2013). Hybrid populations will then often suffer some fitness loss from carrying such incompatibility alleles at high frequencies (Dobzhansky, 1951), but may at the same time benefit from elevated variability at ecologically relevant loci allowing them to tap into new resources and undergo niche expansion. Additionally they will often have elevated variability at loci that affect mating assortment, such as at mate or habitat preference genes or genes that affect breeding seasonality. All such genes are potential reproductive barrier loci. I suggest that in the presence of disruptive ecological selection affecting some of the loci directly, perhaps as a result of reaching carrying capacity after niche expansion, individual incompatibility loci or independent pairs of interacting loci might then become coupled together by selection. Analogous to conditions modelled by Barton Arnold et al., 2012) is consistent with this idea but is of course no direct evidence. The coupling mechanism would perhaps also contribute to explaining the highly variable progression towards ecological speciation that is often observed within and between taxa under similar ecological conditions and remains currently often unexplained (Nosil, 2012). The model makes predictions that can be tested empirically: (i) when crossed in the laboratory, ecologically divergent sister species in adaptive radiations should often reveal more or stronger endogenous incompatibilities than expected under drift, given their (recent) divergence time. Their discovery may not be trivial though, may often require two hybrid generations to be bred and either direct phenotypic detection followed by a screen for allelic variants genome-wide or at candidate genes, or testing for segregation distortion across a large number of genomic loci in juveniles reaching adulthood. (ii) When the incompatibility loci can be identified, divergently fixed alleles at incompatibility loci should coalesce deeper in time than alleles at average genomic loci. (iii) The same endogenous incompatibilities may contribute to coupled reproductive barriers in several species pairs, but be coupled to different extrinsic barrier loci in different species pairs or be coupled to similar extrinsic barrier loci with the direction of allele coupling different in different species pairs and different from the ancestral species that gave rise to the hybrid swarm (contrary to expectations from reinforcement). Abbott et al. (2013) ask the question whether ecology should still be thought of as the initial catalytic agent of speciation when reproductive isolation depends on endogenous incompatibilities. For the coupling mechanism that I outlined above for speciation from a hybrid population, the answer would have to be Yes. This is because selection for coupling under this model requires disruptive ecological selection on at least one of the incompatibility loci or pairs of loci, that is, speciation is initiated by disruptive selection between ecological niches, but requires coupling between extrinsic and endogenous barriers to go to completion. Which one of these scenarios happens will depend on the interplay between ecological opportunity (divergent selection between niches), geographical context and historical contingency (initial level of reproductive isolation and segregation of incompatibilities and their genetic architectures) and may become predictable to some extent when these factors are jointly taken into account. Speciation is a complex phenomenon and the effects of hybridization on it may be more highly dimensional than previously thought. Katie Wagner read and commented two earlier versions of this article, and I discussed my idea with Mark Kirkpatrick and Sander van Doorn during a fish lunch on Lake Lucerne.