The Cretaceous breakup of Gondwana strongly modified the global distribution of shallow tropical seas reshaping the geographic configuration of marine basins. However, the links between tropical reef availability, plate tectonic processes and marine biodiversity distribution patterns are still unknown. Here, we show that a spatial diversification model constrained by absolute plate motions for the past 140 million years predicts the emergence and movement of diversity hotspots on tropical reefs. The spatial dynamics of tropical reefs explains marine fauna diversification in the Tethyan Ocean during the Cretaceous and early Cenozoic, and identifies an eastward movement of ancestral marine lineages towards the Indo-Australian Archipelago in the Miocene. A mechanistic model based only on habitat-driven diversification and dispersal yields realistic predictions of current biodiversity patterns for both corals and fishes. As in terrestrial systems, we demonstrate that plate tectonics played a major role in driving tropical marine shallow reef biodiversity dynamics.

Aim The importance of quantifying the contribution of historical processes in shaping current biodiversity patterns is now recognized, but quantitative approaches that explicitly link speciation, extinction and dispersal processes to palaeo‐environmental changes are currently lacking. Here, we propose a spatial diversification model of lineages through time (SPLIT) based on the reconstruction of palaeo‐environments. We illustrate our approach using mangroves as a case study and evaluate whether habitat changes caused by plate tectonics explain the current biodiversity patterns of this group. Innovations The SPLIT model allows one to simulate the evolutionary dynamics of species ranges by spatially linking speciation, extinction and dispersal processes to habitat changes over geological time periods. The SPLIT model provides a mechanistic expectation of speciation and extinction assuming that species are ecologically identical and not interacting. The likelihood of speciation and extinction is equivalent across species and depends on two dispersal parameters interacting with habitat dynamics (d a maximum dispersal distance and ds a distance threshold beyond which gene flow is absent). Beyond classical correlative approaches, this model tracks biodiversity dynamics under palaeo‐environmental changes and provides multiple expectations (i.e., α‐, β‐diversity, phylogenies) that can be compared to empirical patterns. Main conclusions The SPLIT model allows a better understanding of the origin of biodiversity by explicitly accounting for habitat changes over geological times. The simulations applied to the mangrove case study reproduced the observed longitudinal gradient in species richness, the empirical pattern of β‐diversity and also provided inference on diversification rates. Future developments may include niche evolution and species interactions to evaluate the importance of non‐neutral mechanisms. The method is fully implemented in the InsideDNA platform for bioinformatics analyses, and all modelling results can be accessed via interactive web links.

The role of speciation processes in shaping current biodiversity patterns represents a major scientific question for ecologists and biogeographers. Hence, numerous methods have been developed to determine the geography of speciation based on co-occurrence between sister-species. Most of these methods rely on the correlation between divergence time and several metrics based on the geographic ranges of sistertaxa (i.e. overlap, asymmetry). The relationship between divergence time and these metrics has scarcely been examined in a spatial context beyond regression curves. Mapping this relationship across spatial grids, however, may unravel how speciation processes have shaped current biodiversity patterns through space and time. This can be particularly relevant for coral reef fishes of the Indo-Pacific since the origin of the exceptional concentration of biodiversity in the Indo-Australian Archipelago (IAA) has been actively debated, with several alternative hypotheses involving species diversification and dispersal. We reconstructed the phylogenetic relationships between three species-rich families of coral reef fish (Chaetodontidae, Labridae, Pomacentridae) and calculated co-occurrence metrics between closely related lineages of those families. We demonstrated that repeated biogeographic processes can be identified in present-day species distribution by projecting co-occurrence metrics between related lineages in a geographical context. Our study also evidence that sister-species do not co-occur randomly across the Indo-Pacific, but tend to overlap their range within the IAA. We identified the imprint of two important biogeographic processes that caused this pattern in 48% of the sister-taxa considered: speciation events within the IAA and repeated divergence between the Indian and Pacific Ocean, with subsequent secondary contact in the IAA.

We develop a spatially explicit model of diversification based on palaeohabitat to explore the predictions of four major hypotheses potentially explaining the latitudinal diversity gradient (LDG), namely, the ‘time-area’, ‘tropical niche conservatism’, ‘ecological limits’ and ‘evolutionary speed’ hypotheses. We compare simulation outputs to observed diversity gradients in the global reef fish fauna. Our simulations show that these hypotheses are non-mutually exclusive and that their relative influence depends on the time scale considered. Simulations suggest that reef habitat dynamics produced the LDG during deep geological time, while ecological constraints shaped the modern LDG, with a strong influence of the reduction in the latitudinal extent of tropical reefs during the Neogene. Overall, this study illustrates how mechanistic models in ecology and evolution can provide a temporal and spatial understanding of the role of speciation, extinction and dispersal in generating biodiversity patterns.

Habitat dynamics interacting with species dispersal abilities could generate gradients in species diversity and prevalence of species traits when the latter are associated with species dispersal potential. Using a process-based model of diversification constrained by a dispersal parameter, we simulated the interplay between reef habitat dynamics during the past 140 million years and dispersal, shaping lineage diversification history and assemblage composition globally. The emerging patterns from the simulations were compared to current prevalence of species traits related to dispersal for 6315 tropical reef fish species. We found a significant spatial congruence between the prevalence of simulated low dispersal values and areas with a large proportion of species characterized by small adult body size, narrow home range mobility behaviour, pelagic larval duration shorter than 21 days and diurnal activity. Species characterized by such traits were found predominantly in the Indo-Australian Archipelago and the Caribbean Sea. Furthermore, the frequency distribution of the dispersal parameter was found to match empirical distributions for body size, PLD and home range mobility behaviour. Also, the dispersal parameter in the simulations was associated to diversification rates and resulted in trait frequency matching empirical distributions. Overall, our findings suggest that past habitat dynamics, in conjunction with dispersal processes, influenced diversification in tropical reef fishes, which may explain the present-day geography of species traits.

1. Evolutionary forces affect the distribution of phenotypes both within and among species. Yet, at the macro-evolutionary scale, the evolution of intraspecific variance is rarely considered. Here, we present an r and a BEAST 2 implementation that extends the JIVE (Joint inter-and Intraspecific Variance Evolution) model aimed at the analysis of continuous trait evolution at both inter-and intraspecific level. 2. Using a hierarchical Bayesian approach, we implemented a range of models for continuous trait evolution that operate independently on species means and variances along a phylogeny. The package uses Markov chain Monte Carlo for the inference of parameters and the evaluation of model fit. JIVE is available in the bite (Bayesian Integrative models of Trait Evolution) r package, as well as in BEAST 2. The two implementations offer the same continuous trait evolutionary models, but differ in their use and types of analyses. The r implementation allows for faster analyses by taking the phylogeny as data, while providing graphical and statistical functions as part of tools for model comparison, result parsing and summary, and plotting. In the BEAST 2 implementation, the species tree is a parameter, and both its topology and divergence times are jointly estimated with trait model parameters. 3. The bite package and the BEAST 2 implementation introduce new frameworks within comparative phylogenetics that explicitly model intraspecific variance. These tools allow users to tackle long-standing questions in evolutionary biology, such as the identification of key evolutionary processes determining niche conservatism, niche partitioning, and life-history strategies.

Generating genomic data for 19 tropical reef fish species of the Western Indian Ocean, we investigate how species ecology influences genetic diversity patterns from local to regional scales. We distinguish between the α , β and γ components of genetic diversity, which we subsequently link to six ecological traits. We find that the α and γ components of genetic diversity are strongly correlated so that species with a high total regional genetic diversity display systematically high local diversity. The α and γ diversity components are negatively associated with species abundance recorded using underwater visual surveys and positively associated with body size. Pelagic larval duration is found to be negatively related to genetic β diversity supporting its role as a dispersal trait in marine fishes. Deviation from the neutral theory of molecular evolution motivates further effort to understand the processes shaping genetic diversity and ultimately the diversification of the exceptional diversity of tropical reef fishes.

Past environmental changes are expected to have profoundly impacted diversity dynamics through time. While some previous studies showed an association between past climate changes or tectonic events and important shifts in lineage diversification, it is only recently that past environmental changes have been explicitly integrated in diversification models to test their influence on diversification rates. Here, we used a global reconstruction of tropical reef habitat dynamics during the Cenozoic and phylogenetic diversification models to test the influence of (i) major geological events, (ii) reef habitat fragmentation and (iii) reef area on the diversification of 9 major clades of tropical reef fish (Acanthuridae, Balistoidea, Carangoidea, Chaetodontidae, Haemulinae, Holocentridae, Labridae, Pomacentridae and Sparidae). The diversification models revealed a weak association between paleo-habitat changes and diversification dynamics. Specifically, the fragmentation of tropical reef habitats over the Cenozoic was found to be a driver of tropical reef fish diversification for 2 clades. However, overall, our approach did not allow the identification of striking associations between diversification dynamics and paleo-habitat fragmentation in contrast with theoretical model’s predictions.