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Clavel, J.

Publications and source records attributed to Clavel, J..

9 recordsLinked to original sources

Explaining the rapid evolution of mammalian meiotic recombination proteins

Meiotic recombination -- the exchange of genetic material between parental chromosomes during gamete production -- is critical for fertility, genome stability, and evolutionary adaptation. In eukaryotes, meiotic recombination is carried out by a deeply conserved molecular machinery. Despite this conservation, the sequences of proteins involved in meiotic recombination evolve at a remarkably high rate in mammalian species. Several biological processes have been proposed to explain this rapid evolution, but none have been quantitatively tested. In this study, we analyzed the variation in evolutionary rates of 100 recombination proteins across approximately 400 placental mammals. Our results show that this rapid evolution is primarily driven by lower levels of purifying selection compared to the rest of the proteome. We show that, although selective pressures exerted on recombination proteins are generally shared across mammals, a few recombination proteins exhibit strong variation in selective pressures. Contrary to previous hypotheses, we demonstrate that chromosome number and genome-wide recombination rates do not account for much of this variation. Instead, these variations are primarily associated with chromosome pairing and synapsis proteins, which tend to experience increased selective pressures throughout mammalian evolution, especially in large and long-lived species. This pattern probably reflects more intense selection for stability of chromosome pairing proteins in the oocytes of long-lived species, in which chromosomes sometimes need to stay paired for decades.

evolutionary biology↗

A probabilistic and phylogenetic principal component analysis for modelling high-dimensional trait evolution

Given the ever-increasing availability of highly detailed phenotypes, modelling trait evolution in a multivariate framework is becoming a challenging task. Current phylogenetic comparative methods often struggle with high-dimensional datasets because they suffer computational limitations and interpretability. Here, we propose a maximum likelihood-based approach called Probabilistic and Phylogenetic Principal Components Analysis (P3CA) to circumvent current limitations. This approach is based on a continuous latent variable model, whereby observed traits are explained by a smaller number of unobserved variables that evolve according to a given evolutionary model. We implement the approach under Pagels lambda model using an Expectation-Maximisation algorithm that makes it computationally efficient and allows missing values. Using simulations, we demonstrate that evolutionary parameters are accurately estimated, regardless of phylogenetic signal, the number of traits or the proportion of missing values. The reconstruction of the reduced space is more accurate than the one obtained using other dimensionality reduction approaches, such as phylogenetic and conventional PCA. Likewise, the estimated values for missing data are more accurate than those obtained using current phylogenetic data imputation approaches. We illustrate the approach on a 3D geometric morphometric dataset describing Crocodyliformes skull shapes and containing around 4% of missing data. Our P3CA method unlocks the possibility to analyse and more easily interpret the large-scale multivariate datasets generated in recent decades within a phylogenetic comparative framework.

evolutionary biology↗

An Empirical Bayes approach for the study of phenotypic evolution from high-dimensional data

Multivariate phylogenetic comparative methods for modelling high-dimensional traits such as 3D shapes or gene expression proBiles have been recently developed. However, these approaches are impractical and almost impossible to use when the number of traits exceeds a few thousands, as they become computationally prohibitive. We overcome these limitations by proposing a new maximum likelihood approach based on the Empirical Bayes framework. This approach takes into account the information of the complete covariances (among species and traits) to infer parameters and compare models of trait evolution for high-dimensional datasets. Through simulations, we demonstrate that the proposed approach can accurately estimate parameters of various trait evolution models, even when the number of traits is ten times larger than the number of lineages; it requires less memory and is at least 10 times faster than currently available approaches. This fast, efBicient framework enabled us to extend the high-dimensional multivariate phylogenetic comparative toolkit by including an Ornstein-Uhlenbeck process with multiple optima to study adaptation to various selective regimes. Applying our approach to the evolution of jaw morphology in relation to dietary adaptation in mammals, we demonstrate morphological convergence in carnivorous and herbivorous lineages. The proposed Empirical Bayes framework, implemented in the R package mvMORPH, enables phylogenetic comparative methods to efBiciently handle high-dimensional datasets and complex models of trait evolution.

evolutionary biology↗

Six million years of vole dental evolution driven by tooth development

Morphological change occurs over macroevolutionary timescales under the action of natural selection and genetic drift combined with developmental processes shaping organogenesis1-3. Although determining their relative weight is made difficult by discrepancies between palaeontological and neontological data4, mammalian tooth morphology may bridge the gap between fossil record and laboratory observations. Fossils indicate that placentals and marsupials diversified after evolving molars bearing more cusps5-7, which emerge through the iterative signalling of enamel knots8,9. However, this theoretical evo-devo model of mammalian tooth evolution has not been explicitly assessed on empirical data. Here, by combining the fossil record with laboratory experiments, we identify a shared developmental basis for the convergent, ratcheted evolution of increasingly complex molars in arvicoline rodents (voles, lemmings, muskrats). Longer, narrower molars lead to more cusps throughout development and deep time, suggesting a developmental driver for tooth evolution. Both the arvicoline fossil record and vole tooth development show slower transitions toward the highest cusp counts. This newly identified pattern suggests that the developmental processes fuelling the evolution of increasingly complex molars may also limit the potential for further complexity increases. Integrating palaeontological and developmental data shows that long-term evolutionary trends can be accurately explained by the simple tinkering of developmental pathways.

evolutionary biology↗

The drivers of dark diversity in the Scandinavian tundra are metric-dependent

AimDark diversity refers to the set of species that are not observed in an area but could potentially occur based on suitable local environmental conditions. In this paper, we applied both niche-based and co-occurrence-based methods to estimate the dark diversity of vascular plant species in the subarctic tundra. We then aimed to unravel the drivers explaining (1) why some locations were missing relatively more suitable species than others, and (2) why certain plant species were more often absent from suitable locations than others. LocationThe Scandinavian tundra around Abisko, northern Sweden. MethodsWe calculated the dark diversity in 107 plots spread out across four mountain trails using four different methods. Two niche-based (Beals index and hypergeometric method) and two co-occurrences-based (climatic niche model and climatic niche model followed by species-specific threshold) methods. This was then followed by multiple generalized linear mixed models and general linear models to determine which habitat characteristics and species traits contributed most to the dark diversity. ResultsThe study showed a notable divergence in the predicted drivers of dark diversity depending on the method used. Nevertheless, we can conclude that plot-level dark diversity was generally 18% higher in areas at low elevations and 30% and 10% higher in areas with a low species richness or low levels of habitat disturbance, respectively. ConclusionOur findings call for caution when interpreting statistical findings of dark diversity estimates. Even so, all analyses point towards an important role for natural processes such as competitive dominance as main driver of the spatial patterns found in dark diversity in the northern Scandes.

ecology↗

The mammalian forelimb diversity as a morphological gradient of increasing evolutionary versatility

Vertebrate limb morphology often reflects the environment, due to variation in locomotor requirements and other ecological traits. However, proximal and distal limb segments may evolve differently to each other, reflecting an anatomical gradient of functional specialization that has been suggested to be impacted by the timing of bone condensation during ontogeny. Here we explore whether the temporal sequence of bone condensation predicts variation in the capacity of evolution to generate morphological diversity between proximal and distal forelimb segments across more than 600 species of mammals. Our findings are consistent with the hypothesis that late developing distal limb elements should display greater morphological variation than more proximal limb elements, which condense earlier during morphogenesis. Distal limb elements, belonging to the autopod, not only exhibit higher diversity of form, but are also more integrated and, on average, show greater evolutionary versatility than intermediate and upper limb segments. Our findings indicate that the macroevolutionary patterns of proximal and distal limb segments are not the same, suggesting that strong functional selection, combined with the higher potential of development to generate variation in more distal limb structures, facilitate the evolution of high autopodial disparity in mammals.

evolutionary biology↗

No latitudinal gradients in tempo or mode of morphological evolution in birds

The latitudinal diversity gradient is one of the most striking patterns in nature yet its implications for morphological evolution are poorly understood. In particular, it has been proposed that an increased intensity of species interactions in tropical biota may either promote or constrain trait evolution, but which of these outcomes predominates remains uncertain. Here, we develop tools for fitting phylogenetic models of phenotypic evolution in which the impact of species interactions--namely, competition--can vary across lineages. Deploying these models on a global avian trait dataset to explore differences in trait divergence between tropical and temperate lineages, we find that the effect of latitude on the mode and tempo of morphological evolution is weak and clade- or trait-dependent. Our results indicate that competition does not disproportionately impact morphological evolution in tropical bird families and question the validity of previously reported patterns of slower trait evolution in the tropics.

evolutionary biology↗

Multiple evolutionary origins and losses of tooth complexity in squamates

Teeth act as tools for acquiring and processing food and so hold a prominent role in vertebrate evolution1,2. In mammals, dental-dietary adaptations rely on tooth shape and complexity variations controlled by cusp number and pattern - the main features of the tooth surface3,4. Complexity increase through cusp addition has dominated the diversification of many mammal groups3,5-9. However, studies of Mammalia alone dont allow identification of patterns of tooth complexity conserved throughout vertebrate evolution. Here, we use morphometric and phylogenetic comparative methods across fossil and extant squamates ("lizards" and snakes) to show they also repeatedly evolved increasingly complex teeth, but with more flexibility than mammals. Since the Late Jurassic, six major squamate groups independently evolved multiple-cusped teeth from a single-cusped common ancestor. Unlike mammals10,11, reversals to lower cusp numbers were frequent in squamates, with varied multiple-cusped morphologies in several groups resulting in heterogenous evolutionary rates. Squamate tooth complexity evolved in correlation with dietary change - increased plant consumption typically followed tooth complexity increases, and the major increases in speciation rate in squamate evolutionary history are associated with such changes. The evolution of complex teeth played a critical role in vertebrate evolution outside Mammalia, with squamates exemplifying a more labile system of dental- dietary evolution.

evolutionary biology↗

Reliable Phylogenetic Regressions for Multivariate Comparative Data: Illustration with the MANOVA and Application to the Effect of Diet on Mandible Morphology in Phyllostomid Bats

Understanding what shapes species phenotypes over macroevolutionary time scales from comparative data requires the use of reliable phylogenetic regression techniques and associated tests (e.g. phylogenetic Generalized Least Squares, pGLS and phylogenetic analyses of variance and covariance, pANOVA, pANCOVA). While these tools are well established for univariate data, their multivariate counterparts are lagging behind. This is particularly true for high dimensional phenotypic data, such as morphometric data. Here we implement well-needed likelihood-based multivariate pGLS, pMANOVA and pMANCOVA, and use a recently-developed penalized likelihood framework to extend their application to the difficult case when the number of traits p approaches or exceeds the number of species n. We then focus on the pMANOVA and use intensive simulations to assess the performance of the approach as p increases, under various levels of phylogenetic signal and correlations between the traits, phylogenetic structure in the predictors, and under various types of phenotypic differences across species groups. We show that our approach outperforms available alternatives under all circumstances, with a greater power to detect phenotypic differences across species group when they exist, and a low risk to improperly detect inexistent differences. Finally, we provide an empirical illustration of our pMANOVA on a geometric-morphometric dataset describing mandible morphology in phyllostomid bats along with data on their diet preferences. Our approach, implemented in the R package mvMORPH, provides efficient multivariate phylogenetic regression tools for understanding what shapes phenotypic differences across species.

evolutionary biology↗