Diverse signatures of convergent evolution in cacti-associated yeasts

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Abstract

Many distantly related organisms have convergently evolved traits and lifestyles that enable them to live in similar ecological environments. However, the extent of phenotypic convergence evolving through the same or distinct genetic trajectories remains an open question. Here, we leverage a comprehensive dataset of genomic and phenotypic data from 1,049 yeast species in the subphylum Saccharomycotina (Kingdom Fungi, Phylum Ascomycota) to explore signatures of convergent evolution in cactophilic yeasts, ecological specialists associated with cacti. We inferred that the ecological association of yeasts with cacti arose independently ∼17 times. Using machine-learning, we further found that cactophily can be predicted with 76% accuracy from functional genomic and phenotypic data. The most informative feature for predicting cactophily was thermotolerance, which is likely associated with duplication and altered evolutionary rates of genes impacting the cell envelope in several cactophilic lineages. We also identified horizontal gene transfer and duplication events of plant cell wall-degrading enzymes in distantly related cactophilic clades, suggesting that putatively adaptive traits evolved through disparate molecular mechanisms. Remarkably, multiple cactophilic lineages and their close relatives are emerging human opportunistic pathogens, suggesting that the cactophilic lifestyle—and perhaps more generally lifestyles favoring thermotolerance—may preadapt yeasts to cause human disease. This work underscores the potential of a multifaceted approach involving high throughput genomic and phenotypic data to shed light onto ecological adaptation and highlights how convergent evolution to wild environments could facilitate the transition to human pathogenicity.

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  1. copy number variation 11–13, gene losses 14–16, or gene gains (e.g., horizontal gene transfer or HGT) 17,18.

    Gene loss and gene gains are just the mechanisms by which (gene) copy number variation arises "Maybe reword this passage as: "but can also arise through distinct molecular paths and by distinct evolutionary mechanisms, such as copy number variation that arises via either gene losses or gene gains (e.g., horizontal gene transfer or HGT)."

  2. 1–3.

    I think it would be worth citing this recent excellent paper that synthesizes the many different perspectives on convergence vs parallel evolution, etc. The framework they outline for distinguishing these different processes would be useful to borrow from throughout, particularly as you begin to delve into the hierarchical nature of convergence (described nicely in Rosenblum et al., 2014).

  3. Convergent evolution, the repeated evolution of similar traits among distantly related taxa

    I'd suggest just clarifying up front that convergence specifically refers to the case where similar traits independently evolve from distinct ancestral states, as is commonly the case in distantly related species. This differs from parallel evolution, in which similar traits evolve, but from the same ancestral state - this can still occur among distantly related species, but more commonly manifests at the population level, or among more closely related species.

    This could be as simple as: "Convergent evolution, the repeated evolution of similar traits from distinct ancestral states, is ubiquitous in nature, commonly occurs among distantly related taxa, and has been..."