Interspecific Tests of Allelism Reveal the Evolutionary Timing and Pattern of Accumulation of Reproductive Isolation Mutations

Abstract

Despite extensive theory, little is known about the empirical accumulation and evolutionary timing of mutations that contribute to speciation. Here we combined QTL (Quantitative Trait Loci) analyses of reproductive isolation, with information on species evolutionary relationships, to reconstruct the order and timing of mutations contributing to reproductive isolation between three plant (Solanum) species. To evaluate whether reproductive isolation QTL that appear to coincide in more than one species pair are homologous, we used cross-specific tests of allelism and found evidence for both homologous and lineage-specific (non-homologous) alleles at these co-localized loci. These data, along with isolation QTL unique to single species pairs, indicate that >85% of isolation-causing mutations arose later in the history of divergence between species. Phylogenetically explicit analyses of these data support non-linear models of accumulation of hybrid incompatibility, although the specific best-fit model differs between seed (pairwise interactions) and pollen (multi-locus interactions) sterility traits. Our findings corroborate theory that predicts an acceleration (‘snowballing’) in the accumulation of isolation loci as lineages progressively diverge, and suggest different underlying genetic bases for pollen versus seed sterility. Pollen sterility in particular appears to be due to complex genetic interactions, and we show this is consistent with a snowball model where later arising mutations are more likely to be involved in pairwise or multi-locus interactions that specifically involve ancestral alleles, compared to earlier arising mutations.

The Pace of Hybrid Incompatibility Evolution in House Mice

“…Our findings add the house mouse to the list of species groups that show evidence for a faster-than-linear accumulation of hybrid incompatibilities (Matute et al 2010;Moyle and Nakazato 2010;Sherman et al 2014). In contrast to previous studies of the snowball effect, our results explicitly incorporate phylogenetic information.…”

“…Matute et al (2010) and Moyle and Nakazato (2010) each found evidence for the snowball effect. Although the results from Solanum provided mixed support, with incompatibilities associated with pollen sterility accumulating linearly with divergence time (Moyle and Nakazato 2010), the pattern of incompatibility sharing among Solanum species as determined by tests of allelism subsequently revealed that this trait fits the snowball prediction as well (Sherman et al 2014).…”

The origins of reproductive isolation in plants

“…Research on the genetics of reproductive isolation between tomato species has begun to fill this gap in plants. Regions associated with RI have been identified and mapped onto the phylogeny of several of these species (Sherman et al ., ), thus allowing the study of the timing and accumulation of quantitative trait loci responsible for hybrid seed sterility and hybrid pollen sterility between Solanum species (Moyle & Nakazato, ). Although the dataset is small, loci underlying traits for hybrid seed set and hybrid pollen fertility appear to evolve faster than linear with time, as predicted by theory.…”

Determining epistatic selection in admixed populations

“…; Matute & Gavin‐Smyth ; Sherman et al . ). Such experiments are much like traditional quantitative trait loci (QTL) studies, with two complications.…”