The neutral rate of whole-genome duplication varies among yeast species and their hybrids

Abstract

Hybridization and polyploidization are powerful mechanisms of speciation. Hybrid speciation often coincides with whole-genome duplication (WGD) in eukaryotes. This suggests that WGD may allow hybrids to thrive by increasing fitness, restoring fertility and/or increasing access to adaptive mutations. Alternatively, it has been suggested that hybridization itself may trigger WGD. Testing these models requires quantifying the rate of WGD in hybrids without the confounding effect of natural selection. Here we show, by measuring the spontaneous rate of WGD of more than 1300 yeast crosses evolved under relaxed selection, that some genotypes or combinations of genotypes are more prone to WGD, including some hybrids between closely related species. We also find that higher WGD rate correlates with higher genomic instability and that WGD increases fertility and genetic variability. These results provide evidence that hybridization itself can promote WGD, which in turn facilitates the evolution of hybrids.

Hybridization drives mitochondrial DNA degeneration and metabolic shift in a species with biparental mitochondrial inheritance

“…cerevisiae and S. paradoxus, crosses between diverged isolates often have low fertility (Greig et al 2003;Charron et al 2014b;Leducq et al 2016;Eberlein et al 2019), including most of our MA crosses (Charron et al 2019;Marsit et al 2021). Our results show that loss of respiration adds another reproductive barrier, since meiosis (sporulation) is dependent on functioning respiratory metabolism (Jambhekar and Amon 2008).…”

Loss of heterozygosity spectrum varies with ploidy levels in natural yeast populations

“…The size of these events were 10.3 kb and 4.3 kb in diploid and polyploid lines, respectively. Similarly, artificial S. cerevisiae / S. paradoxus hybrid tetraploids that spontaneously evolved from ancestral hybrid diploids in an MA experiment displayed shorter events compared to their diploid counterparts (Marsit et al, 2021). Utilizing a microarray-based approach, Yim et al, (2014) described two distinct classes of conversion events with median sizes of 6 kb (more frequent) and 54 kb (less frequent), arising from different DNA lesions and repair mechanisms.…”

“…Artificially generated diploid and polyploid hybrids have shown to increase or decrease their overall ploidy level during propagation (Charron et al, 2019;Marsit et al, 2021). Moreover, experimentally generated tetraploid S. cerevisiae strains frequently revert to a diploid state through loss of chromosomes during mitotic progression (Gerstein et al, 2008;Selmecki et al, 2015).…”

Insights on life cycle and cell identity regulatory circuits for unlocking genetic improvement in Zygosaccharomyces and Kluyveromyces yeasts

“…This genome instability is also observed in artificial hybrids created in the lab (Sipiczki 2018 ; Marsit et al . 2021 ). This does not necessarily mean hybrids cannot contribute to continued evolution, indeed the whole post-WGD clade is derived from a hybrid between two species that was initially sterile.…”

“…With continuous rounds of fermentation, genome instability was observed as previously described (Sipiczki 2018 ; Marsit et al . 2021 ). These regenerated tetraploid spores are now homozygous across the two parental genomes, except for mating type, and being homothallic are not easily used in a continuous breeding strategy.…”