Genetic incompatibilities do not snowball in a demographic model of speciation

Abstract

Two populations evolving in isolation can accumulate genetic differences over time that cause incompatibilities in their hybrid offspring. These “Dobzhansky-Muller incompatibilities” (DMIs) are predicted to accumulate at a rate faster than linear as the number of incompatible gene interactions “snowballs”. Here we show that this snowball prediction is an artifact of two unrealistic modeling assumptions that stem from ignoring demography. We introduce a new alternative “demographic speciation model” in which the rate of DMI accumulation between populations is affected by the efficiency of purifying selection to remove incompatibilities that arise within populations. This model yields new testable predictions for understanding the tempo and mode of speciation based on population demographic parameters. A large-scale empirical analysis of bird and mammal datasets supports a unique prediction of our model: a negative relationship between effective population sizes and speciation rates. Our results challenge views of the snowball theory, and of ecological speciation models rooted in positive selection, showing instead that purifying selection may play a major role in mediating speciation rates.

The genomic consequences of hybridization

“…Data consistent with this phenomenon has been documented in several systems ( Matute et al, 2010 ; Moyle and Nakazato, 2010 ; Wang et al, 2015 ). However, if the mutations that cause DMIs are enriched in the same genes or genomic regions, the rate of this accumulation should slow ( Kalirad and Azevedo, 2017 ; Maya-Lastra and Eaton, 2021 ). Similar predictions emerge from theoretical studies of gene regulatory network evolution, where the likelihood of a gene’s involvement in DMIs is directly related to the density of the gene network ( Yang and Scarpino, 2020 ; Satokangas, 2020 ).…”

Genetic drift promotes and recombination hinders speciation on holey fitness landscapes

“…They found a significantly negative correlation in one genus, in agreement with our prediction, but no significant correlations in the other two genera. A larger phylogenetic study found significant negative correlations between speciation rates and a different proxy for N e —geographic range size—in both birds and mammals 52 . These results, while encouraging, have the limitation that they have used overall speciation rate, which may not be driven primarily by postzygotic RI.…”

“…for N e -geographic range size-in both birds and mammals 52 . These results, while encouraging, have the limitation that they have used overall speciation rate, which may not be driven primarily by postzygotic RI.…”

Mating system and speciation I: Accumulation of genetic incompatibilities in allopatry

“…The phase during which BDMi mutations emerge, spread through the population and eventually get fixed is often dismissed ( e.g ., [ 42 ]). This necessary phase has recently been argued to have important implications in speciation genetics [ 63 , 64 ]. Considering that BDMi alleles may segregate in natural populations at polymorphic frequencies allows for instance to better explain (i) why hybrid incompatibility may be variable between different pairs of individuals originating from the same two populations (reviewed in [ 63 ]), and (ii) why genetic incompatibilities are widespread within species, as found in Drosophila melanogaster [ 65 ], Caenorhabditis elegans [ 66 ], Arabidopsis thaliana [ 67 ], or the genus Draba [ 18 , 19 ].…”