A Test of the Snowball Theory for the Rate of Evolution of Hybrid Incompatibilities

Abstract

Hybrids between species are often sterile or inviable because the long-diverged genomes of their parents cause developmental problems when they come together in a single individual. According to the Dobzhansky-Muller (DM) model, the number of genes involved in these "intrinsic postzygotic incompatibilities" should increase faster than linearly with the divergence time between species. This straightforward prediction of the DM model has remained contentious owing to a lack of explicit tests. Examining two pairs of Drosophila species, we show that the number of genes involved in postzygotic isolation increases at least as fast as the square of the number of substitutions (an index of divergence time) between species. This observation verifies a key prediction of the DM model.

Coadapted genomes and selection on hybrids: Fisher's geometric model explains a variety of empirical patterns

“…2016b), and this is true of the strongest empirical demonstrations of the effect (Matute et al. 2010; Moyle and Nakazato 2010; Wang et al. 2015).…”

Macroevolutionary speciation rates are decoupled from the evolution of intrinsic reproductive isolation in Drosophila and birds

“…In this case, the level of RI between two species (Y ij ) as a function of genetic distance between them (X ij ) is given by Y ij = β 0 + (β 1 + ψ i + ψ j )X ij + «, where β 0 and β 1 are the intercept and slope terms, and « is an error term (Materials and Methods). We also considered a quadratic model, which allows for increasing rates of RI accumulation through time consistent with "snowball" models for the evolution of genetic incompatibilities (10,27,28). Finally, we considered an asymptotic model, where the rate of RI accumulation between taxa decreases through time as it asymptotically approaches an upper bound at Y = 1.0.…”

“…At the population level, a microevolutionary research program on the biology of speciation has focused on the factors that lead to various forms of reproductive isolation (RI) between populations (5, 6). Explaining how and why RI evolves is generally considered to be the central and defining challenge in the study of speciation (2, 7-9), and recent studies have made great progress toward explaining the genetic and ecological basis for various forms of RI (7,8,10).…”

“…At the population level, a microevolutionary research program on the biology of speciation has focused on the factors that lead to various forms of reproductive isolation (RI) between populations (5, 6). Explaining how and why RI evolves is generally considered to be the central and defining challenge in the study of speciation (2, 7-9), and recent studies have made great progress toward explaining the genetic and ecological basis for various forms of RI (7,8,10).Most microevolutionary research on speciation implicitly assumes that RI is the defining and rate-limiting step in the speciation process (7,8,11), but the evolution of RI need not bear any predictive relationship to rates of species diversification as realized over macroevolutionary timescales (12). This has long been recognized by the paleontological community, where "successful" speciation is believed to entail not only the evolution of reproductive isolation but also the persistence of incipient species (13-15).…”

Heterosis and outbreeding depression in crosses between natural populations of Arabidopsis thaliana

“…Introducing these alleles into a different genetic background by crossing can cause negative epistatic interactions. The frequency of epistatic incompatibilities is predicted to increase with increasing genetic distance between the parents (Lynch, 1991;Orr and Turelli, 2001;Matute et al, 2010). Alternatively, decreased fitness in crosses between widely diverged populations could be due to chromosomal rearrangements (Lande, 1985;Charlesworth, 1992;Kirkpatrick and Barton, 2006), or to underdominance and/or negative epistatic interactions between closely linked loci (Schierup and Christiansen, 1996).…”