Processus d'émergence des patrons de diversité supra-spécifiques lors des radiations évolutives

Evolutionary radiations are phenomena of rapid diversification, and one of the major sources of biodiversity on Earth. Here, I explore the hypothesis that ecological and genetic mechanisms underpinning evolutionary radiations structure macroecological and macroevolutionary patterns of diversity. To this end, I analyse the predictions of several models in which radiations emerge from spatio-temporal dynamics at the scale of the individual. These analyses first show that spatial structure is a major driver of diversity and endemism on oceanic archipelagos due to interactions between dispersal and allopatric speciation. Second, by integrating landscape dynamics and the processes of competitive interactions, I reveal how these factors combine to shape phylogenetic trees, and in particular to beget trees that are unbalanced and exhibit a deceleration in branching tempo, which is often observed on molecular phylogenies. I then explore the mechanisms responsible for this deceleration. I show that it reflects a negative diversity-dependence of the speciation rate, itself linked to a reduction in the persistence and ecological differentiation of new populations. The extinction rate is, on the other hand, uninfluenced by species diversity, extinctions being here mainly caused by a combinaison of competitive exclusion and hybridization of incipient species. Finally, I show that during mass extinctions the ranked topology of phylogenetic trees and the distribution of extinctions among the tips have a strong impact on the loss of phylogenetic diversity, and hence on the potential for future evolution.Les radiations évolutives sont des phénomènes de diversification rapide, et une source majeure de la diversité biologique sur Terre. J'explore ici l'hypothèse selon laquelle les mécanismes écologiques et génétiques à la base des radiations évolutives structurent les patrons macroécologiques et macroévolutifs de diversité. Pour ce faire, j'analyse les prédictions de plusieurs modèles de radiation émergeant des dynamiques spatio-temporelles à l'échelle individuelle. Ces analyses montrent d'abord que la structuration spatiale est un facteur majeur de diversité et d'endémisme au sein des archipels océaniques, en raison d'interactions entre dispersion et spéciation allopatrique. L'intégration de la dynamique des paysages et des processus d'interactions compétitives révèle ensuite comment ces facteurs se combinent pour structurer la forme des arbres phylogénétiques, et notamment générer des arbres déséquilibrés et une décélération du tempo de branchement, souvent observés dans les phylogénies moléculaires. J'explore alors les mécanismes responsables de cette décélération. Je montre qu'elle reflète une diversité-dépendance négative du taux de spéciation, liée à une réduction de la persistance et différentiation écologique des nouvelles populations. Le taux d'extinction n'est lui pas influencé par la diversité, les extinctions étant ici surtout causées par une combinaison d'exclusion compétitive et d'hybridation d'espèces incipientes. Enfin, je mets en évidence l'importance, lors d'une crise d'extinction, de la topologie rangée des arbres phylogénétiques et de la distribution des extinctions sur les pertes de diversité phylogénétique, et donc sur le potentiel d'évolution future

Processes of emergence of large scale diversity patterns during evolutionary radiations

Les radiations évolutives sont des phénomènes de diversification rapide, et une source majeure de la diversité biologique sur Terre. J'explore ici l'hypothèse selon laquelle les mécanismes écologiques et génétiques à la base des radiations évolutives structurent les patrons macroécologiques et macroévolutifs de diversité. Pour ce faire, j'analyse les prédictions de plusieurs modèles de radiation émergeant des dynamiques spatio-temporelles à l'échelle individuelle. Ces analyses montrent d'abord que la structuration spatiale est un facteur majeur de diversité et d'endémisme au sein des archipels océaniques, en raison d'interactions entre dispersion et spéciation allopatrique. L'intégration de la dynamique des paysages et des processus d'interactions compétitives révèle ensuite comment ces facteurs se combinent pour structurer la forme des arbres phylogénétiques, et notamment générer des arbres déséquilibrés et une décélération du tempo de branchement, souvent observés dans les phylogénies moléculaires. J'explore alors les mécanismes responsables de cette décélération. Je montre qu'elle reflète une diversité-dépendance négative du taux de spéciation, liée à une réduction de la persistance et différentiation écologique des nouvelles populations. Le taux d'extinction n'est lui pas influencé par la diversité, les extinctions étant ici surtout causées par une combinaison d'exclusion compétitive et d'hybridation d'espèces incipientes. Enfin, je mets en évidence l'importance, lors d'une crise d'extinction, de la topologie rangée des arbres phylogénétiques et de la distribution des extinctions sur les pertes de diversité phylogénétique, et donc sur le potentiel d'évolution future.Evolutionary radiations are phenomena of rapid diversification, and one of the major sources of biodiversity on Earth. Here, I explore the hypothesis that ecological and genetic mechanisms underpinning evolutionary radiations structure macroecological and macroevolutionary patterns of diversity. To this end, I analyse the predictions of several models in which radiations emerge from spatio-temporal dynamics at the scale of the individual. These analyses first show that spatial structure is a major driver of diversity and endemism on oceanic archipelagos due to interactions between dispersal and allopatric speciation. Second, by integrating landscape dynamics and the processes of competitive interactions, I reveal how these factors combine to shape phylogenetic trees, and in particular to beget trees that are unbalanced and exhibit a deceleration in branching tempo, which is often observed on molecular phylogenies. I then explore the mechanisms responsible for this deceleration. I show that it reflects a negative diversity-dependence of the speciation rate, itself linked to a reduction in the persistence and ecological differentiation of new populations. The extinction rate is, on the other hand, uninfluenced by species diversity, extinctions being here mainly caused by a combinaison of competitive exclusion and hybridization of incipient species. Finally, I show that during mass extinctions the ranked topology of phylogenetic trees and the distribution of extinctions among the tips have a strong impact on the loss of phylogenetic diversity, and hence on the potential for future evolution

Simulation_ntagged

R code for the simulation of the mode

InferenceFunctions

R code for the inference of the model parameter

Appendix

This document contains all the supplementary informations

Data from: How ecology and landscape dynamics shape phylogenetic trees

Whether biotic or abiotic factors are the dominant drivers of clade diversification is a long-standing question in evolutionary biology. The ubiquitous patterns of phylogenetic imbalance and branching slowdown have been taken as supporting the role of ecological niche filling and spatial heterogeneity in ecological features, and thus of biotic processes, in diversification. However, a proper theoretical assessment of the relative roles of biotic and abiotic factors in macroevolution requires models that integrate both types of factors, and such models have been lacking. In this study, we use an individual-based model to investigate the temporal patterns of diversification driven by ecological speciation in a stochastically fluctuating geographic landscape. The model generates phylogenies whose shape evolves as the clade ages. Stabilization of tree shape often occurs after ecological saturation, revealing species turnover caused by competition and demographic stochasticity. In the initial phase of diversification (allopatric radiation into an empty landscape), trees tend to be unbalanced and branching slows down. As diversification proceeds further due to landscape dynamics, balance and branching tempo may increase and become positive. Three main conclusions follow. First, the phylogenies of ecologically saturated clades do not always exhibit branching slowdown. Branching slowdown requires that competition be wide or heterogeneous across the landscape, or that the characteristics of landscape dynamics vary geographically. Conversely, branching acceleration is predicted under narrow competition or frequent local catastrophes. Second, ecological heterogeneity does not necessarily cause phylogenies to be unbalanced—short time in geographical isolation or frequent local catastrophes may lead to balanced trees despite spatial heterogeneity. Conversely, unbalanced trees can emerge without spatial heterogeneity, notably if competition is wide. Third, short isolation time causes a radically different and quite robust pattern of phylogenies that are balanced and yet exhibit branching slowdown. In conclusion, biotic factors have a strong and diverse influence on the shape of phylogenies of ecologically saturating clades and create the evolutionary template in which branching slowdown and tree imbalance may occur. However, the contingency of landscape dynamics and resource distribution can cause wide variation in branching tempo and tree balance. Finally, considerable variation in tree shape among simulation replicates calls for caution when interpreting variation in the shape of real phylogenies

Code_tree_shape_final

Code of the individual-based model of diversification resulting from ecological speciation in a dynamical landscape. We provide the simulation code as a ready-to-use R function. This makes the simulations very easy to run: the user only needs to edit the parameter values, then to run the function. Explanations and additional information are given in the file “readme.txt”

Data from: How ecology and landscape dynamics shape phylogenetic trees

Whether biotic or abiotic factors are the dominant drivers of clade diversification is a long-standing question in evolutionary biology. The ubiquitous patterns of phylogenetic imbalance and branching slowdown have been taken as supporting the role of ecological niche filling and spatial heterogeneity in ecological features, and thus of biotic processes, in diversification. However, a proper theoretical assessment of the relative roles of biotic and abiotic factors in macroevolution requires models that integrate both types of factors, and such models have been lacking. In this study, we use an individual-based model to investigate the temporal patterns of diversification driven by ecological speciation in a stochastically fluctuating geographic landscape. The model generates phylogenies whose shape evolves as the clade ages. Stabilization of tree shape often occurs after ecological saturation, revealing species turnover caused by competition and demographic stochasticity. In the initial phase of diversification (allopatric radiation into an empty landscape), trees tend to be unbalanced and branching slows down. As diversification proceeds further due to landscape dynamics, balance and branching tempo may increase and become positive. Three main conclusions follow. First, the phylogenies of ecologically saturated clades do not always exhibit branching slowdown. Branching slowdown requires that competition be wide or heterogeneous across the landscape, or that the characteristics of landscape dynamics vary geographically. Conversely, branching acceleration is predicted under narrow competition or frequent local catastrophes. Second, ecological heterogeneity does not necessarily cause phylogenies to be unbalanced—short time in geographical isolation or frequent local catastrophes may lead to balanced trees despite spatial heterogeneity. Conversely, unbalanced trees can emerge without spatial heterogeneity, notably if competition is wide. Third, short isolation time causes a radically different and quite robust pattern of phylogenies that are balanced and yet exhibit branching slowdown. In conclusion, biotic factors have a strong and diverse influence on the shape of phylogenies of ecologically saturating clades and create the evolutionary template in which branching slowdown and tree imbalance may occur. However, the contingency of landscape dynamics and resource distribution can cause wide variation in branching tempo and tree balance. Finally, considerable variation in tree shape among simulation replicates calls for caution when interpreting variation in the shape of real phylogenies

Clade diversification dynamics and the biotic and abiotic controls of speciation and extinction rates

The history and patterns of species diversity are shaped by a variety of ecological and evolutionary factors. Here, the authors develop a computational model to predict clade diversification dynamics and rates of speciation and extinction under the influences of resource competition, genetic differentiation, and random landscape fluctuation

The effects of archipelago spatial structure on island diversity and endemism: predictions from a spatially-structured neutral model

International audienceIslands are particularly suited to testing hypotheses about the ecological and evolutionary mechanisms underpinning community assembly. Yet the complex spatial arrangements of real island systems have received little attention from both empirical studies and theoretical models. Here, we investigate the extent to which the spatial structure of archipelagos affects species diversity and endemism. We start by proposing a new spatially structured neutral model that explicitly considers archipelago structure, and then investigate its predictions under a diversity of scenarios. Our results suggest that considering the spatial structure of archipelagos is crucial to understanding their diversity and endemism, with structured island systems acting both as museums and cradles of biodiversity. These dynamics of diversification may change the traditionally expected pattern of decrease in species richness with distance from the mainland, even potentially leading to increasing patterns for taxa with high speciation rates in archipelagos off species-poor continental areas. Our results also predict that, within spatially structured archipelagos, metapopulation dynamics and evolutionary processes can generate higher diversity on islands more centrally placed than at the periphery. We derive from our results a set of theoretical predictions, potentially testable with empirical data