A phylogenomics approach to resolving fungal evolution, and phylogenetic method development

Bien que les champignons soient régulièrement utilisés comme modèle d'étude des systèmes eucaryotes, leurs relations phylogénétiques soulèvent encore des questions controversées. Parmi celles-ci, la classification des zygomycètes reste inconsistante. Ils sont potentiellement paraphylétiques, i.e. regroupent de lignées fongiques non directement affiliées. La position phylogénétique du genre Schizosaccharomyces est aussi controversée: appartient-il aux Taphrinomycotina (précédemment connus comme archiascomycetes) comme prédit par l'analyse de gènes nucléaires, ou est-il plutôt relié aux Saccharomycotina (levures bourgeonnantes) tel que le suggère la phylogénie mitochondriale? Une autre question concerne la position phylogénétique des nucléariides, un groupe d'eucaryotes amiboïdes que l'on suppose étroitement relié aux champignons. Des analyses multi-gènes réalisées antérieurement n'ont pu conclure, étant donné le choix d'un nombre réduit de taxons et l'utilisation de six gènes nucléaires seulement. Nous avons abordé ces questions par le biais d'inférences phylogénétiques et tests statistiques appliqués à des assemblages de données phylogénomiques nucléaires et mitochondriales. D'après nos résultats, les zygomycètes sont paraphylétiques (Chapitre 2) bien que le signal phylogénétique issu du jeu de données mitochondriales disponibles est insuffisant pour résoudre l'ordre de cet embranchement avec une confiance statistique significative. Dans le Chapitre 3, nous montrons à l'aide d'un jeu de données nucléaires important (plus de cent protéines) et avec supports statistiques concluants, que le genre Schizosaccharomyces appartient aux Taphrinomycotina. De plus, nous démontrons que le regroupement conflictuel des Schizosaccharomyces avec les Saccharomycotina, venant des données mitochondriales, est le résultat d'un type d'erreur phylogénétique connu: l'attraction des longues branches (ALB), un artéfact menant au regroupement d'espèces dont le taux d'évolution rapide n'est pas représentatif de leur véritable position dans l'arbre phylogénétique. Dans le Chapitre 4, en utilisant encore un important jeu de données nucléaires, nous démontrons avec support statistique significatif que les nucleariides constituent le groupe lié de plus près aux champignons. Nous confirmons aussi la paraphylie des zygomycètes traditionnels tel que suggéré précédemment, avec support statistique significatif, bien que ne pouvant placer tous les membres du groupe avec confiance. Nos résultats remettent en cause des aspects d'une récente reclassification taxonomique des zygomycètes et de leurs voisins, les chytridiomycètes. Contrer ou minimiser les artéfacts phylogénétiques telle l'attraction des longues branches (ALB) constitue une question récurrente majeure. Dans ce sens, nous avons développé une nouvelle méthode (Chapitre 5) qui identifie et élimine dans une séquence les sites présentant une grande variation du taux d'évolution (sites fortement hétérotaches - sites HH); ces sites sont connus comme contribuant significativement au phénomène d'ALB. Notre méthode est basée sur un test de rapport de vraisemblance (likelihood ratio test, LRT). Deux jeux de données publiés précédemment sont utilisés pour démontrer que le retrait graduel des sites HH chez les espèces à évolution accélérée (sensibles à l'ALB) augmente significativement le support pour la topologie « vraie » attendue, et ce, de façon plus efficace comparée à d'autres méthodes publiées de retrait de sites de séquences. Néanmoins, et de façon générale, la manipulation de données préalable à l'analyse est loin d’être idéale. Les développements futurs devront viser l'intégration de l'identification et la pondération des sites HH au processus d'inférence phylogénétique lui-même.

The effects of topological inaccuracy in evolutionary trees on the phylogenetic comparative method of independent contrasts

Computer simulations were used to test the effect of increasing phylogenetic topological inaccuracy on the results obtained from correlation tests of independent contrasts. Predictably, increasing the number of disruptions in the tree increases the likelihood of significant error in the r values produced and in the statistical conclusions drawn from the analysis. However, the position of the disruption in the tree is important: Disruptions closer to the tips of the tree have a greater effect than do disruptions that are close to the root of the tree. Independent contrasts derived from inaccurate topologies are more likely to lead to erroneous conclusions when there is a true significant relationship between the variables being tested (i.e., they tend to be conservative). The results also suggest that random phylogenies perform no better than nonphylogenetic analyses and, under certain conditions, may perform even worse than analyses using raw species data. Therefore, the use of random phylogenies is not beneficial in the absence of knowledge of the true phylogeny.

Life histories of the Insectivora : the role of phylogeny, metabolism and sex differences

Life-history data for 63 species from the mammalian order Insectivora have been collated from the literature. These data were analysed for covariation and for correlations with body mass, brain mass and mass-specific resting metabolic rate. An independent contrasts method has been used to remove the effect of phylogeny. Due to uncertainties surrounding their evolutionary relationships, 22 different phylogenies of insectivores have been used as a basis for comparative analysis. The results show that several key correlations between life-history variables are only significant when certain phylogenies are used, highlighting the problems of such analyses when the phylogeny used is inaccurate. After removing the effect of phylogeny, relatively few significant correlations remain. Insectivores that have a high body mass have relatively lower metabolic rates, longer lifespans and longer gestation lengths. There is some support for a fast±slow continuum in insectivore life-history evolution: there are some significant positive correlations between measures of growth rates (e.g. gestation length and age at weaning) and lifespan, and some negative correlations between growth rates and measures of reproductive output. It is suggested that the seasonality of life of many insectivores may have played an influential role in the evolution of the group, in particular in delaying the onset of sexual maturity. There is little indication that brain size influences life-history evolution in this order, but metabolism may play an important role. The energetic requirements of maintaining high metabolic rates in small mammals such as insectivores may be constraining life histories to a greater extent than occurs in larger mammals. This effect may have obscured the relationship between metabolic rate and life histories in wider inter-order analyses. Finally, there is considerable evidence that sex differences play a large role in shaping insectivore evolution, and it is suggested that this factor must be considered more often in future studies of mammalian life histories in general.

Error, Bias, and Long-Branch Attraction in Data for Two Chloroplast Photosystem Genes in Seed Plants

Sequences of two chloroplast photosystem genes, psaA and psbB, together comprising about 3,500 bp, were obtained for all five major groups of extant seed plants and several outgroups among other vascular plants. Strongly supported, but significantly conflicting, phylogenetic signals were obtained in parsimony analyses from partitions of the data into first and second codon positions versus third positions. In the former, both genes agreed on a monophyletic gymnosperms, with Gnetales closely related to certain conifers. In the latter, Gnetales are inferred to be the sister group of all other seed plants, with gymnosperms paraphyletic. None of the data supported the modern ‘‘anthophyte hypothesis,’’ which places Gnetales as the sister group of flowering plants. A series of simulation studies were undertaken to examine the error rate for parsimony inference. Three kinds of errors were examined: random error, systematic bias (both properties of finite data sets), and statistical inconsistency owing to long-branch attraction (an asymptotic property). Parsimony reconstructions were extremely biased for third-position data for psbB. Regardless of the true underlying tree, a tree in which Gnetales are sister to all other seed plants was likely to be reconstructed for these data. None of the combinations of genes or partitions permits the anthophyte tree to be reconstructed with high probability. Simulations of progressively larger data sets indicate the existence of long-branch attraction (statistical inconsistency) for third-position psbB data if either the anthophyte tree or the gymnosperm tree is correct. This is also true for the anthophyte tree using either psaA third positions or psbB first and second positions. A factor contributing to bias and inconsistency is extremely short branches at the base of the seed plant radiation, coupled with extremely high rates in Gnetales and nonseed plant outgroups. M. J. Sanderson,* M. F. Wojciechowski,*† J.-M. Hu,* T. Sher Khan,* and S. G. Brady

Phylogenetic mixture models can reduce node-density artifacts

We investigate the performance of phylogenetic mixture models in reducing a well-known and pervasive artifact of phylogenetic inference known as the node-density effect, comparing them to partitioned analyses of the same data. The node-density effect refers to the tendency for the amount of evolutionary change in longer branches of phylogenies to be underestimated compared to that in regions of the tree where there are more nodes and thus branches are typically shorter. Mixture models allow more than one model of sequence evolution to describe the sites in an alignment without prior knowledge of the evolutionary processes that characterize the data or how they correspond to different sites. If multiple evolutionary patterns are common in sequence evolution, mixture models may be capable of reducing node-density effects by characterizing the evolutionary processes more accurately. In gene-sequence alignments simulated to have heterogeneous patterns of evolution, we find that mixture models can reduce node-density effects to negligible levels or remove them altogether, performing as well as partitioned analyses based on the known simulated patterns. The mixture models achieve this without knowledge of the patterns that generated the data and even in some cases without specifying the full or true model of sequence evolution known to underlie the data. The latter result is especially important in real applications, as the true model of evolution is seldom known. We find the same patterns of results for two real data sets with evidence of complex patterns of sequence evolution: mixture models substantially reduced node-density effects and returned better likelihoods compared to partitioning models specifically fitted to these data. We suggest that the presence of more than one pattern of evolution in the data is a common source of error in phylogenetic inference and that mixture models can often detect these patterns even without prior knowledge of their presence in the data. Routine use of mixture models alongside other approaches to phylogenetic inference may often reveal hidden or unexpected patterns of sequence evolution and can improve phylogenetic inference.

Escherichia coli phylogenetic group determination and its application in the identification of the major animal source of fecal contamination

Fundação de Amparo à Pesquisa do Estado de São Paulo (FAPESP)