A Phylogenetic Analysis of Macroevolutionary Patterns in Fermentative Yeasts RocIo Paleo-Lopez 1, Julian F
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A phylogenetic analysis of macroevolutionary patterns in fermentative yeasts Rocıo Paleo-Lopez 1, Julian F. Quintero-Galvis1, Jaiber J. Solano-Iguaran1, Angela M. Sanchez-Salazar1, Juan D. Gaitan-Espitia1,2 & Roberto F. Nespolo1,3 1Instituto de Ciencias Ambientales y Evolutivas, Universidad Austral de Chile, Valdivia 5090000, Chile 2CSIRO Oceans & Atmosphere, GPO Box 1538, Hobart, 7001 Tasmania, Australia 3Center of Applied Ecology and Sustainability (CAPES), Facultad de Ciencias Biologicas, Universidad Catolica de Chile, Santiago 6513677, Chile Keywords Abstract Adaptive radiation, comparative method, fermentation, phylogenetic signal, When novel sources of ecological opportunity are available, physiological inno- Saccharomicotina. vations can trigger adaptive radiations. This could be the case of yeasts (Saccha- romycotina), in which an evolutionary novelty is represented by the capacity to Correspondence exploit simple sugars from fruits (fermentation). During adaptive radiations, Roberto F. Nespolo, Center of Applied diversification and morphological evolution are predicted to slow-down after Ecology and Sustainability (CAPES), Facultad early bursts of diversification. Here, we performed the first comparative phylo- de Ciencias Biologicas, Universidad Catolica genetic analysis in yeasts, testing the “early burst” prediction on species diversi- de Chile, Santiago 6513677, Chile. Tel: 0632221344; fication and also on traits of putative ecological relevance (cell-size and E-mail: [email protected] fermentation versatility). We found that speciation rates are constant during the time-range we considered (ca., 150 millions of years). Phylogenetic signal of Funding Information both traits was significant (but lower for cell-size), suggesting that lineages This study was funded by Fondecyt grant resemble each other in trait-values. Disparity analysis suggested accelerated evo- 1130750 to Roberto Nespolo. lution (diversification in trait values above Brownian Motion expectations) in cell-size. We also found a significant phylogenetic regression between cell-size Received: 1 December 2015; Revised: 2 2 = March 2016; Accepted: 3 March 2016 and fermentation versatility (R 0.10), which suggests correlated evolution between both traits. Overall, our results do not support the early burst predic- Ecology and Evolution 2016; 6(12): 3851– tion both in species and traits, but suggest a number of interesting evolutionary 3861 patterns, that warrant further exploration. For instance, we show that the Whole Genomic Duplication that affected a whole clade of yeasts, does not doi: 10.1002/ece3.2097 seems to have a statistically detectable phenotypic effect at our level of analysis. In this regard, further studies of fermentation under common-garden condi- tions combined with comparative analyses are warranted. Introduction phenomenon fall in one of the situations described before, is unclear. Evolutionary innovations can trigger diversification Phylogenies can give information about speciation pat- (adaptive radiations: sudden increases in speciation rates terns (the topology) and time of divergence among spe- (Yoder et al. 2010), ecological success of a single lineage cies (branch lengths), that can be assessed with simple or a combination of both (the ecological success is speciation models, such as the rate of species production followed by later speciation and diversification). As a con- in time (Nee 2006). When this information is put sequence of the later phenomenon, it is usually possible together with trait values, several patterns and processes to identify entire clades bearing an innovation (Pincheira- that are not evident from qualitative assessments can Donoso et al. 2015). Among microorganisms, a probable emerge. For instance, the distribution of character states case of adaptive evolution is yeasts and fermentation, can be compared across basal and derived nodes, which where a physiological innovation related to the capacity permits the inference of losses and acquisitions (Revell to extract energy from single sugars, seems to have trig- 2012). On the other hand, simply asking whether lineages gered a major adaptive change (see reviews in Dashko resemble each others more or less than what is expected et al. 2014; Hagman and Piskur 2015). Whether this by a Brownian Motion model (BM) of evolution, reveals ª 2016 The Authors. Ecology and Evolution published by John Wiley & Sons Ltd. 3851 This is an open access article under the terms of the Creative Commons Attribution License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited. Macroevolutionary Patterns in Yeasts R. Paleo-Lopez et al. whether homogenizing or diversifying processes were without a statistical test, to determine in what degree important (Blomberg et al. 2003). Trait diversification, lineages resemble each other in trait values. Third, histori- analyzed in the time elapsed from the most basal node in cal (genomic rearrangements, in this case) events cannot the phylogeny to the actual species (i.e., the “tips”), and be unambiguously associated to a given phenotypic value compared with BM expectations indicate whether a trait (although many authors claim the contrary, reviewed by showed peaks of diversification, concomitant with species Dashko et al. 2014). A similar visualization in a continu- diversification (Harmon et al. 2003). In this context, cor- ous trait such as cell size (a “phenogram”) is presented in related evolution between traits can be analyzed using the Figure 2. Here, it can be seen that the species with largest phylogeny as a part of the process (i.e., phylogenetic cell-size is Eremothecium coryli, the sole fermentative spe- regression models; Pollux et al. 2014). cies of this genus (it ferments three sugars, the remaind- Yeasts (Ascomycota:Saccharomycotina) are a mono- ing four do not ferment any sugar, see Fig. 1A, species in phyletic lineage of unicellular fungi that counts over black text). This qualitative pattern suggest that compara- thousand species (James et al. 2006; Kurtzman et al. tively larger cells can ferment more sugars, but large intr- 2011). Wild yeasts live as saprobes, often in the interface aclade variation in both characters preclude any firm between plants and animals, but an important number conclusion (for instance, the lowest in cell-size ranking is are domesticated for industrial processes such as baking, Tetrapisispora nanseiensis, which ferment two sugars, see brewing and synthesis of recombinant proteins. Although Fig. 1A). Therefore, some metrics are needed to treat this best known by their capacity to produce and metabolize variation at the phylogenetic level. ethanol, the diversity of substrates metabolized by yeasts Phylogenetic signal (PS), which is at the core of mod- is enormous. Yeasts can metabolize sugars (BM e.g., ern phylogenetic analysis, is a measure of how much spe- sucrose, galactose, trehalose, maltose), heavy metals (e.g., cies resemble each other in trait values (Blomberg et al. Cu, Zn, Cd), aromatic compounds (e.g., catechol, vanil- 2003; Munkemuller et al. 2012; Paradis 2012). In other lin) and nitrates (Kurtzman et al. 2011). This makes them words, it gives an idea, on average, of how a given trait of commercial, ecological and medical relevance, and at followed the topology of a phylogeny in its diversification, the same time have generated a rich nomenclature of assuming that this diversification followed a BM model of standardized responses to biochemical and physiological evolution (Pennell et al. 2014). One of the most used tests, including fermentation (Kurtzman et al. 2011). metrics for PS is the K-statistic (Blomberg et al. 2003), Here, we were focused on the maximum number of sug- see examples in (Munkemuller et al. 2012; Fisher et al. ars a species can ferment, a trait that we defined opera- 2013; Gingras et al. 2013; Wang and Clarke 2014) which tionally as “fermentation versatility”. We are aware that is computed from the phylogenetic variance-covariance this trait definition is blind to the specific fermented matrix (vcv; see Material and Methods), when K = 1 the sugar, which could limit our conclusions. However, this trait variation is equal to BM expectations (Blomberg is a good proxy of the metabolic machinery that permits et al. 2003). If a phylogeny was built based on morpho- (or constraint) the maximum fermentative capacity. logical data, then the PS of a morphological trait in this The distribution of fermentation versatility (trait values phylogeny will be 1.0. from Kurtzman et al. 2011; see Material and Methods) on According to a number of authors, the appearance of a yeast’s phylogeny is depicted in Figure 1A, together fruits coincided with the appareance of fermentative with some important genomic rearrangements that yeasts yeasts (especially Saccharomyces), which has supported experienced during the last 150 millions of years the hypothesis of novel ecological niches provided by (reviewed in Dujon 2010; Hagman et al. 2013; Dashko fruits and simple sugars (Hagman et al. 2013; Dashko et al. 2014). These events are important because it is et al. 2014; Williams et al. 2015). These authors suggested hypothesized that they were relevant in determining their that fermentative capacity represents an ecological inno- fermentative capacity (particularly the Whole Genomic vation that triggered an adaptive radiation. One predic- Duplication [WGD]), by increasing the relative dosage of tion of adaptive radiation theory is to observe