Coevolution Trumps Pleiotropy: Carbon Assimilation Traits Are Independent of Metabolic Network Structure in Budding Yeast

Abstract

Phenotypic traits may be gained and lost together because of pleiotropy, the involvement of common genes and networks, or because of simultaneous selection for multiple traits across environments (multiple-trait coevolution). However, the extent to which network pleiotropy versus environmental coevolution shapes shared responses has not been addressed. To test these alternatives, we took advantage of the fact that the genus Saccharomyces has variation in habitat usage and diversity in the carbon sources that a given strain can metabolize. We examined patterns of gain and loss in carbon utilization traits across 488 strains of Saccharomyces to investigate whether the structure of metabolic pathways or selection pressure from common environments may have caused carbon utilization traits to be gained and lost together. While most carbon sources were gained and lost independently of each other, we found four clusters that exhibit non-random patterns of gain and loss across strains. Contrary to the network pleiotropy hypothesis, we did not find that these patterns are explained by the structure of metabolic pathways or shared enzymes. Consistent with the hypothesis that common environments shape suites of phenotypes, we found that the environment a strain was isolated from partially predicts the carbon sources it can assimilate.

Restricted Pleiotropy Facilitates Mutational Erosion of Major Life-History Traits

“…Based on these findings, the intensity of pleiotropy was judged to be relatively low (Wang et al ). Similar conclusions have been reached in a study in which not thousands of engineered single mutations but hundreds of yeast isolates from different habitats were tested for assimilation of different carbon sources (Opulente et al ). Other researchers, however, advise caution in deriving general conclusions from these specific and still rather few experiments (Paaby and Rockman ).…”

Metabolic variation in natural populations of wild yeast

“…Opulente et al. () showed that metabolic patterns in 448 strains of the genus Saccharomyces were partially predictable from the environments where the strains occurred. Further progress in understanding the maintenance of metabolic variation in microbial populations is likely to depend on elucidating the availability of substrates in natural habitats and relating it to the metabolic specialization of resident strains.…”

“…To distinguish between purifying and diversifying selection as explanations of variation, the crucial prediction is that substrate use by isolates will correspond with substrate availability at sites if variation is adaptive. Opulente et al (2013) showed that metabolic patterns in 448 strains of the genus Saccharomyces were partially predictable from the environments where the strains occurred. Further progress in understanding the maintenance of metabolic variation in microbial populations is likely to depend on elucidating the availability of substrates in natural habitats and relating it to the metabolic specialization of resident strains.…”

Phenotypic diversity of Methylobacterium associated with rice landraces in North-East India

“…This is surprising because prior work shows strong impacts of local environment (including host traits) on microbial communities. For instance, the carbon use profiles of~500 natural yeast isolates were clustered by the substrate from which they were isolated [47]. More specifically, leaf chemistry is strongly correlated with phyllospheric microbial communities of tropical trees [48], and sugar concentration in host plant exudates affects colonization by epiphytic bacteria [49].…”