Repeated horizontal gene transfer ofGALactose metabolism genes violates Dollo’s law of irreversible loss

Abstract

Dollo’s law posits that evolutionary losses are irreversible, thereby narrowing the potential paths of evolutionary change. While phenotypic reversals to ancestral states have been observed, little is known about their underlying genetic causes. The genomes of budding yeasts have been shaped by extensive reductive evolution, such as reduced genome sizes and the losses of metabolic capabilities. However, the extent and mechanisms of trait reacquisition after gene loss in yeasts have not been thoroughly studied. Here, through phylogenomic analyses, we reconstructed the evolutionary history of the yeast galactose utilization pathway and observed widespread and repeated losses of the ability to utilize galactose, which occurred concurrently with the losses of GALactose (GAL) utilization genes. Unexpectedly, we detected three galactose-utilizing lineages that were deeply embedded within clades that underwent ancient losses of galactose utilization. We show that at least two, and possibly three, lineages reacquired the GAL pathway via yeast-to-yeast horizontal gene transfer. Our results show how trait reacquisition can occur tens of millions of years after an initial loss via horizontal gene transfer from distant relatives. These findings demonstrate that the losses of complex traits and even whole pathways are not always evolutionary dead-ends, highlighting how reversals to ancestral states can occur.

Giant GAL gene clusters for the melibiose‐galactose pathway in Torulaspora

“…Therefore, many strains of both T. delbrueckii and T. pretoriensis contain GAL10 but no other GAL genes. This situation has also been seen in other yeasts (Haase et al, 2020), but its physiological significance is unknown.…”

“…For example, in the T. pretoriensis clusters, the intact gene upstream of GAL1 can be GAL10, GAL2 , GAL4 or MEL1 (Figure 2). Haase et al (2020) recently identified a similar fusion of two GAL clusters (one ancestral and one horizontally transferred) in N. fulvescens .…”

“…It seems likely that regulatory changes, involving duplication of PGM1 , loss of GAL80 , and movement of GAL4 into the cluster were central to expansion of the cluster. Previous work has shown that Gal4 became the major regulator of the GAL pathway relatively recently, displacing Rtg1/Rtg3 in an ancestor of the family Saccharomycetaceae (Choudhury & Whiteway, 2018; Haase et al, 2020). In the Torulaspora/Zygotorulaspora clade, the further step of moving the GAL4 gene into the cluster has occurred.…”

“…A similar cluster of GAL 1‐10‐7 , interspersed with two genes of unknown function, occurs in Candida albicans and other species in the CUG‐Ser1 clade (Slot & Rokas, 2010). In more divergent yeasts, the GAL genes are generally not clustered, except for four genera ( Schizosaccharomyces , Nadsonia , Brettanomyces and Wickerhamomyces ) that gained clusters by horizontal transfer from donors in the CUG‐Ser1 clade and two genera ( Cryptocococcus and Lipomyces ) in which GAL clusters appear to have formed independently (Haase et al, 2020; Slot & Rokas, 2010).…”

Macroevolutionary diversity of traits and genomes in the model yeast genus Saccharomyces

“…Phenotypic traits are gained and lost frequently in animals, plants, and fungi 30, 96–98 . Alternatively, traits can be retained in a species by balancing selection when different lineages or populations maintain genes or even multi-locus gene networks encoding traits due to local adaptation or fluctuating conditions.…”