A Combinatorial View on Speciation and Adaptive Radiation

Recent studies show that cases of rapid speciation and rapid species radiations often involve old genetic variants that arose long before the speciation events. Old genetic variation, previously tested by selection and occurring at higher allele frequency than new mutations, is a good substrate for speciation. Admixture variation from divergent lineages may be particularly important, potentially causing intrinsic and extrinsic incompatibilities, transgressive traits, or novel trait combinations in hybrid populations. We review the evidence for rapid speciation involving a ‘combinatorial mechanism’ – the reassembly of old genetic variants into novel combinations. This genetic mechanism might not only facilitate rapid speciation but also adaptive radiation and sympatric speciation, and it might contribute to variation in speciation rates among lineages. Speciation is often thought of as a slow process due to the waiting times for mutations that cause incompatibilities, and permit ecological differentiation or assortative mating. Cases of rapid speciation and particularly cases of rapid adaptive radiation into multiple sympatric species have remained somewhat mysterious. We review recent findings from speciation genomics that reveal an emerging commonality among such cases: reassembly of old genetic variation into new combinations facilitating rapid speciation and adaptive radiation. The polymorphisms in old variants frequently originated from hybridization at some point in the past. We discuss why old variants are particularly good fuel for rapid speciation, and hypothesize that variation in access to such old variants might contribute to the large variation in speciation rates observed in nature. Speciation is often thought of as a slow process due to the waiting times for mutations that cause incompatibilities, and permit ecological differentiation or assortative mating. Cases of rapid speciation and particularly cases of rapid adaptive radiation into multiple sympatric species have remained somewhat mysterious. We review recent findings from speciation genomics that reveal an emerging commonality among such cases: reassembly of old genetic variation into new combinations facilitating rapid speciation and adaptive radiation. The polymorphisms in old variants frequently originated from hybridization at some point in the past. We discuss why old variants are particularly good fuel for rapid speciation, and hypothesize that variation in access to such old variants might contribute to the large variation in speciation rates observed in nature. several ecologically differentiated species evolve from a single hybrid population, wherein admixture variation not only facilitates adaptation to a variety of new niches but importantly also reproductive isolation among the emerging species. a selective process by which two or more alleles are maintained in the gene pool of a population at frequencies larger than expected under neutrality. Mechanisms include negative frequency-dependent selection, spatial or temporal heterogeneity in the direction of selection, or global heterozygote advantage. alleles at different loci that are incompatible with each other when present in the same genome. speciation following a founder effect, in which reproductive isolation arises because strong drift-induced allele-frequency changes alter selection pressures on epistatically interacting genes. two species through hybridization generate a third stable lineage, isolated from both parental species, either with a mosaic of parental chromosome blocks (i.e., homoploid hybrid speciation) or combining both parental chromosome sets (i.e., allopolyploid hybrid speciation). Deeply divergent haplotypes are immediately available throughout the genome, thereby facilitating response of the hybrid population to divergent selection between parental species and the hybrid population, as well as associated ecological differentiation within the hybrid lineage. The hybrid species might become reproductively isolated from both parental species through sorting of incompatibilities additional to mating trait divergence and divergent adaptation. introgression from a distant relative of a ‘magic trait’, namely a trait conferring both ecological divergence and reproductive isolation, triggers speciation in the introgressed lineage. haplotypes that strongly influence the phenotype, its ecological function, its mating function, and/or fitness. a special form of hybrid speciation involving karyotype evolution (e.g., chromosome arm translocations) between the hybrid species and its parental lineages. extreme trait values in hybrids that lie outside the range of the values of both parental species combined. a mechanism by which the standing genetic variation of a population or species is replenished by recurrent gene flow from a population or species adapted to an alternative habitat, and thereby facilitates repeated adaptation to the alternative habitat in additional locations, including possible parallel speciation.