Engineering evolution to study speciation in yeasts

Abstract

The Saccharomyces 'sensu stricto' yeasts are a group of species that will mate with one another, but interspecific pairings produce sterile hybrids. A retrospective analysis of their genomes revealed that translocations between the chromosomes of these species do not correlate with the group's sequence-based phylogeny (that is, translocations do not drive the process of speciation). However, that analysis was unable to infer what contribution such rearrangements make to reproductive isolation between these organisms. Here, we report experiments that take an interventionist, rather than a retrospective approach to studying speciation, by reconfiguring the Saccharomyces cerevisiae genome so that it is collinear with that of Saccharomyces mikatae. We demonstrate that this imposed genomic collinearity allows the generation of interspecific hybrids that produce a large proportion of spores that are viable, but extensively aneuploid. We obtained similar results in crosses between wild-type S. cerevisiae and the naturally collinear species Saccharomyces paradoxus, but not with non-collinear crosses. This controlled comparison of the effect of chromosomal translocation on species barriers suggests a mechanism for the generation of redundancy in the S. cerevisiae genome.

Reproductive isolation in Saccharomyces

“…All the other yeast species have fewer (or no) rearrangements and produce hybrids that are more sterile than S. paradoxus and S. cariocanus. This was confirmed by Delneri et al (2003), who engineered one or two reciprocal translocations into the genome of S. cerevisiae to make it collinear with one or other of two S. mikatae strains. Crosses between the engineered S. cerevisiae strains and wild-type S. cerevisiae strains showed the predicted reductions in fertility to 50 or 25% (0.5 2 ¼ 0.25) of normal.…”

DNA sequence and analysis of human chromosome 18

“…As a consequence, human 18p corresponds to the proximal region of chimpanzee 18q. As large-scale chromosomal rearrangements can facilitate speciation 19,20 , it is possible that this inversion had had a role in hominid evolution.…”

Intrachromosomal rearrangements in avian genome evolution: evidence for regions prone to breakpoints

“…It has been long established that chromosome rearrangements between species can cause or reinforce reproductive isolation (Noor et al, 2001;Rieseberg, 2001;Delneri et al, 2003). Hybrids arising from parents with subtly different karyotypes can be compromised in their ability to reproduce and this can function as an evolutionary barrier that ultimately leads to speciation.…”