Conditions when hybridization might predispose populations for adaptive radiation

The role of hybridization in evolution is a theme that hasbeen intensively and sometimes controversially debated,particularly amongst zoologists. Long time considered anevolutionary dead end, interspeciﬁc hybridization is nowknown to have left imprints in the genomes of manyplant and animal lineages (Grant et al., 2003; Mallet,2005; Arnold, 2006). While it is clear that hybridizationhas often times been no dead end, questions that remaincontentious are whether and how hybridization affectsrate and direction of evolution, and how it affects specia-tion. Classically, hybridization was thought to put abrake on speciation (Mayr, 1942; Dobzhansky, 1951),but this view is also beginning to change. Hybridspeciation has been quite well documented (Buerkle R Abbott et al., 2013), and hybridizationappears to be particularly common in the most species-rich and rapidly diversifying groups of organisms (Sch-warzer et al., 2012), perhaps just as a consequence ofmany young species in geographical proximity. Eitherway it is clearly not preventing speciation in thesegroups (Salazar et al., 2010; Joyce et al., 2011; Genner TStelkens & Seehausen, 2009). It may bring some geno-types in a hybrid population instantaneously into theattraction zone of an adaptive peak that neither paren-tal population could tap into because of lack of suitablevariation (Mallet, 2007). Additionally, recombination ofthe parental species genomes following hybridizationmay facilitate breaking of genetic correlations. Suchcorrelations that may constrain selection response(Gomulkiewicz & Houle, 2009) may arise in the ﬁrstplace if selective sweeps drive adaptive gene variants toﬁxation that are physically linked or have pleiotropiceffects on several different traits under selection.Besides affecting adaptive potential, hybridizationmay also affect genomic predispositions for the evolutionof reproductive isolation, and this has received far lessattention. I will develop this idea here as a verbal modelwhich might be followed up by theoretical modelling.Ecological divergent selection often leads to onlyincomplete reproductive isolation, and locally adaptedpopulations or partially isolated ecotypes may bemaintained for quite a long time by selection that bal-ances gene ﬂow. However, without progressing furthertowards stronger reproductive isolation, such popu-lations are vulnerable to changes in ecological selectionregimes and genetic differentiation may eventuallycollapse again. Indeed this is likely to happen to mostlocally adapted populations. More robust reproductiveisolation might evolve if genes under extrinsic (ecologi-cal) underdominant selection or independent pairs ofgenes under extrinsic (ecological) disruptive selectionbecame coupled to endogenous incompatibility factors(again single locus underdominant factors or pairs ofinteracting incompatibility loci). However, this opportu-nity may rarely arise during ecological divergence inpanmictic populations because incompatibility-inducingmutations will tend to get purged before they reachappreciable frequencies (Gavrilets, 2004). Herein comesthe importance of hybridization. Classical Bateson–Dobzhansky–Muller incompatibilities (BDMIs) arise dueto incompatibility between derived alleles at two (ormore) loci that diverged unopposed by compatibilityselection between populations in geographical isolation,and they only become expressed upon secondary con-tact with hybridization (Gavrilets, 2004). Underdomi-nant mutations may also ﬁx more readily betweengeographically isolated populations owing to drift thatcan overcome selection in small populations (Wright,1931; Altrock et al., 2011). Hybrid populations will then often suffer some ﬁtnessloss from carrying such incompatibility alleles at highfrequencies (Dobzhansky, 1951), but may at the sametime beneﬁt from elevated variability at ecologically rel-evant loci allowing them to tap into new resources and