Convergent expansions of keystone gene families drive metabolic innovation in a major eukaryotic clade

Abstract

Many remarkable innovations have repeatedly occurred across vast evolutionary distances. When convergent traits emerge on the tree of life, they are sometimes driven by the same underlying gene families, while other times many different gene families are involved. Conversely, a gene family may be repeatedly recruited for a single trait or many different traits. To understand the general rules governing convergence at both genomic and phenotypic levels, we systematically tested associations between 56 binary metabolic traits and gene count in 14,710 gene families from 993 species of Saccharomycotina yeasts. Using a recently developed phylogenetic approach that reduces spurious correlations, we discovered that gene family expansion and contraction was significantly linked to trait gain and loss in 45/56 (80%) of traits. While 601/746 (81%) of significant gene families were associated with only one trait, we also identified several 'keystone' gene families that were significantly associated with up to 13/56 (23%) of all traits. These results indicate that metabolic innovations in yeasts are governed by a narrow set of major genetic elements and mechanisms.