Evolution and molecular bases of reproductive isolation

Abstract

The most challenging problem in speciation research is disentangling the relative strength and order in which different reproductive barriers evolve. Here, we review recent developments in the study of reproductive isolation in yeasts. With over a thousand genome-sequenced isolates readily available for testing the viability, sterility, and fitness of both intraspecies and interspecies hybrid crosses, Saccharomyces yeasts are an ideal model to study such fundamental questions. Our survey demonstrates that, while chromosomal-level mutations are widespread at the intraspecific level, anti-recombination-driven chromosome missegregation is the primary reproductive barrier between species. Finally, despite their strength, all of these postzygotic barriers can be resolved through the asexual life history of hybrids.

Figure 1

Mechanisms of reproductive isolation in yeast. The main reproductive barriers in yeast can be broadly broken down into three categories: those that affect whole chromosomes, those that are caused by genetic incompatibility at a few loci, and prezygotic isolation. Anti‐recombination inhibits correct segregation of chromosomes during meiosis, resulting in spores that carry either two copies or zero copies (inviable) of the chromosome. Both polyploidy and aneuploidy can result in difficulties segregating chromosomes evenly during meiosis. Chromosomal rearrangements, such as the reciprocal translocations represented here, lead to unbalanced gametes missing genes in translocated regions. Genetic incompatibilities can act either between nuclear genes and mitochondrial genes or between sets of nuclear genes. Finally, prezygotic isolation in the form of ecological isolation can occur when different genotypes are able to thrive under different environmental conditions.

Figure 2

Genetic distance results in an exponential decay in hybrid gamete viability. Genome-wide sequence divergence results in a correlated exponential decline (blue line; R²=0.9307; df=66) in viability of hybrids with collinear genomes (blue symbols). This negative impact is noticeable even at divergence levels < 2%, highlighting the role of anti‐recombination in the early phases of the yeast speciation process. On the other hand, large-scale chromosomal differences constitute a powerful part of RI across many incipient species crosses but not between established species (gray symbols — excluded from the correlation analysis). Data for this figure are extracted from [–15,35,76] and are available in Supplementary Data 1.