The population genetics of speciation: the evolution of hybrid incompatibilities.

Abstract

Speciation often results from the accumulation of "complementary genes," i.e., from genes that, while having no deleterious effect within species, cause inviability or sterility when brought together with genes from another species. Here I model speciation as the accumulation of genic incompatibilities between diverging populations. Several results are obtained. First, and most important, the number of genic incompatibilities between taxa increases much faster than linearly with time. In particular, the probability of speciation increases at least as fast as the square of the time since separation between two taxa. Second, as Muller realized, all hybrid incompatibilities must initially be asymmetric. Third, at loci that have diverged between taxa, evolutionarily derived alleles cause hybrid problems far more often than ancestral alleles. Last, it is "easier" to evolve complex hybrid incompatibilities requiring the simultaneous action of three or more loci than to evolve simple incompatibilities between pairs of genes. These results have several important implications for genetic analyses of speciation.

Chromosomal rearrangements in holocentric organisms lead to reproductive isolation by hybrid dysfunction: The correlation between karyotype rearrangements and germination rates in sedges

“…However, this explanation does not directly explain F 1 hybrid inviability, because imbalanced chromosome pairings under the Baker and Bickham model precede meiotic divisions in the hybrid off spring. We hypothesize that DMIs ( Orr, 1995 ;Orr and Turelli, 2001 ;Coyne and Orr, 2004 ) could be also involved in the postzygotic isolation due to F 1 hybrid inviability that we fi nd in this study, perhaps somehow acting in combination with chromosomal rearrangements.…”

“…Th e Dobzhansky-Muller model explains hybrid dysfunction by epistasis between two or more loci. DMIs arise from alleles that are fi xed independently in diverging populations or lineages, so that genetic incompatibilities between populations emerge without any population passing through a low-fi tness phase ( Orr, 1995 ;Orr and Turelli, 2001 ;Coyne and Orr, 2004 ; for application to chromosome evolution, see Baker and Bickham, 1986 ). While establishment of underdominant chromosome variants may be explained by drift or meiotic drive, DMIs require neither process for establishment ( Fishman and Willis, 2001 ).…”

Complex basis of hybrid female sterility and Haldane’s rule inHeliconiusbutterflies: Z-linkage and epistasis

“…This is because the expected number of two-locus DMIs is predicted to increase approximately as the square of the number of divergent substitutions between species; the “snowball effect” (Orr, 1995; Orr & Turelli, 2001; Matute et al ., 2010). Furthermore, DMIs involving more than two loci should accumulate even more rapidly, because, as the number of interacting loci increases, so too does the number of potentially negative combinations (Orr, 1995). In keeping with these predictions, widespread DMIs across the genomes of a number of species have been inferred from genetic association data (Good et al ., 2008; Schumer et al ., 2014).…”

Evaluating evidence of mitonuclear incompatibilities with the sex chromosomes in an avian hybrid zone

“…As differences accumulate between the genomes of diverging lineages, deleterious epistatic interactions between parental genomes are exposed within a hybrid genomic background and can result in loss of fitness (Bateson‐Dobzhansky‐Muller incompatibilities or BDMIs; Orr 1995, 1996; Coyne and Orr 2004). At face value, BDMIs might appear unlikely to result from mitonuclear interactions.…”