Decoupling the variances of heterosis and inbreeding effects is evidenced in yeast’s life-history and proteomic traits

Abstract

Heterosis (hybrid vigor) and inbreeding depression, commonly considered as corollary phenomena, could nevertheless be decoupled under certain assumptions according to theoretical population genetics works. In order to explore this issue on real data, we analyzed the components of genetic variation in a population derived from a half-diallel cross between strains from Saccharomyces cerevisiae and S. uvarum, two related yeast species involved in alcoholic fermentation. A large number of phenotypic traits, either molecular (coming from quantitative proteomics) or related to fermentation and life-history, were measured during alcoholic fermentation. Because the parental strains were included in the design, we were able to distinguish between inbreeding effects, which measures phenotypic differences between inbred and hybrids, and heterosis, which measures phenotypic differences between a specific hybrid and the other hybrids sharing a common parent. The sources of phenotypic variation differed depending on the temperature, indicating the predominance of genotype by environment interactions. Decomposing the total genetic variance into variances of additive (intra-and inter-specific) effects, of inbreeding effects and of heterosis (intra-and inter-specific) effects, we showed that the distribution of variance components defined clear-cut groups of proteins and traits. Moreover, it was possible to cluster fermentation and life-history traits into most proteomic groups. Within groups, we observed positive, negative or null correlations between the variances of heterosis and inbreeding effects. To our knowledge, such a decoupling had never been experimentally demonstrated. This result suggests that, despite a common evolutionary history of individuals within a species, the different types of traits have been subject to different selective pressures. KEYWORDS Hybrid vigor; inbreeding depression; diallel crossing; mixed effect genetic modelHeterosis, or hybrid vigor, refers to the common superiority of hybrids over their parents for quantitative traits. This phenomenon has been observed for virtually any quantitative trait, from mRNA abundances to fitness, and in a large diversity of species, including microorganisms. For decades it has been extensively studied and exploited for plant and animal breeding, since it affects traits of high economical interest such as biomass, fertility, growth rate, disease resistance etc. (Gowen 1952;Schnable and Springer 2013).

Data integration uncovers the metabolic bases of phenotypic variation in yeast

“…In brief, the most important findings were: homeostasis of the interspecific hybrids observed at the trait level (da Silva et al 2015) and the predominance of interspecific heterosis at the proteomic level (Blein-Nicolas et al (2015)). A closer analysis of genetic variance components confirmed that observable phenotypic traits tended to exhibit higher additive genetic variance and lower interaction variance than proteomic traits (Petrizzelli et al, 2019).…”

“…We considered the genetic value of protein abundances and fermentation/life-history traits, rather than their measured/computed value. In a previous study, Petrizzelli et al (2019) decomposed the phenotypic value of a trait at a given temperature, P T , into its genetic, G T , and residual, , contributions:…”