Peter F. Cowman

Coral reefs as drivers of cladogenesis: expanding coral reefs, cryptic extinction events, and the development of biodiversity hotspots

Diversification rates within four conspicuous coral reef fish families (Labridae, Chaetodontidae, Pomacentridae and Apogonidae) were estimated using Bayesian inference. Lineage through time plots revealed a possible late Eocene/early Oligocene cryptic extinction event coinciding with the collapse of the ancestral Tethyan/Arabian hotspot. Rates of diversification analysis revealed elevated cladogenesis in all families in the Oligocene/Miocene. Throughout the Miocene, lineages with a high percentage of coral reef–associated taxa display significantly higher net diversification rates than expected. The development of a complex mosaic of reef habitats in the Indo‐Australian Archipelago (IAA) during the Oligocene/Miocene appears to have been a significant driver of cladogenesis. Patterns of diversification suggest that coral reefs acted as a refuge from high extinction, as reef taxa are able to sustain diversification at high extinction rates. The IAA appears to support both cladogenesis and survival in associated lineages, laying the foundation for the recent IAA marine biodiversity hotspot.

Evolutionary history of the butterflyfishes (f: Chaetodontidae) and the rise of coral feeding fishes

Of the 5000 fish species on coral reefs, corals dominate the diet of just 41 species. Most (61%) belong to a single family, the butterflyfishes (Chaetodontidae). We examine the evolutionary origins of chaetodontid corallivory using a new molecular phylogeny incorporating all 11 genera. A 1759‐bp sequence of nuclear (S7I1 and ETS2) and mitochondrial (cytochrome b) data yielded a fully resolved tree with strong support for all major nodes. A chronogram, constructed using Bayesian inference with multiple parametric priors, and recent ecological data reveal that corallivory has arisen at least five times over a period of 12 Ma, from 15.7 to 3 Ma. A move onto coral reefs in the Miocene foreshadowed rapid cladogenesis within Chaetodon and the origins of corallivory, coinciding with a global reorganization of coral reefs and the expansion of fast‐growing corals. This historical association underpins the sensitivity of specific butterflyfish clades to global coral decline.

Dating the evolutionary origins of wrasse lineages (Labridae) and the rise of trophic novelty on coral reefs.

We estimated ages of divergence between major labrid tribes and the timing of the evolution of trophic novelty. Sequence data for 101 labrid taxa and 14 outgroups consisting of two mitochondrial gene regions (12s, 16s), and two nuclear protein-coding genes (RAG2, TMO4c4), a combined 2567 bp of sequence, were examined using novel maximum likelihood, maximum parsimony and mixed model Bayesian inference methods. These analyses yielded well supported trees consistent with published phylogenies. Bayesian inference using five fossil calibration points estimated the minimum ages of lineages. With origins in the late Cretaceous to early tertiary, the family diversified quickly with both major lineages (hypsigenyine and julidine) present at approximately 62.7 Ma, shortly after the K/T boundary. All lineages leading to major tribes were in place by the beginning of the Miocene (23 Ma) with most diversification in extant lineages occurring within the Miocene. Optimisation of trophic information onto the chronogram revealed multiple origins of novel feeding modes with two distinct periods of innovation. The Palaeocene/Eocene saw the origins of feeding modes that are well represented in other families: gastropod feeders, piscivores and browsing herbivores. A wave of innovation in the Oligocene/Miocene resulted in specialized feeding modes, rarely seen in other groups: coral feeding, foraminifera feeding and fish cleaning. There is little evidence of a general relationship between trophic specialization and species diversity. The current trophic diversity of the Labridae is a result of the accumulation of feeding modes dating back to the K/T boundary at 65 Ma, with all major feeding modes on present day reefs already in place 7.5 million years ago.

Quaternary coral reef refugia preserved fish diversity

Ancient reefs provided fishy refuges Climate fluctuations have occurred repeatedly in Earths history, and so there is much to be learned from examining the responses of past systems. Pellessier et al. reconstructed paleoenvironments over the past 3 million years from sediment cores collected across coral reef systems to explore the impacts of past conditions on reef fish diversity. Coral reefs survived in the Indo-Australian regions during times of otherwise extensive habitat loss. These robust reefs can explain much of the diversity found in present-day reef fish species. Science, this issue p. 1016 Ancient reefs protected fish from past climate changes, contributing to highly diverse fish in Indo-Australian reefs today. The most prominent pattern in global marine biogeography is the biodiversity peak in the Indo-Australian Archipelago. Yet the processes that underpin this pattern are still actively debated. By reconstructing global marine paleoenvironments over the past 3 million years on the basis of sediment cores, we assessed the extent to which Quaternary climate fluctuations can explain global variation in current reef fish richness. Comparing global historical coral reef habitat availability with the present-day distribution of 6316 reef fish species, we find that distance from stable coral reef habitats during historical periods of habitat loss explains 62% of the variation in fish richness, outweighing present-day environmental factors. Our results highlight the importance of habitat persistence during periods of climate change for preserving marine biodiversity.

Quantifying Phylogenetic Beta Diversity: Distinguishing between ‘True’ Turnover of Lineages and Phylogenetic Diversity Gradients

The evolutionary dissimilarity between communities (phylogenetic beta diversity PBD) has been increasingly explored by ecologists and biogeographers to assess the relative roles of ecological and evolutionary processes in structuring natural communities. Among PBD measures, the PhyloSor and UniFrac indices have been widely used to assess the level of turnover of lineages over geographical and environmental gradients. However, these indices can be considered as ‘broad-sense’ measures of phylogenetic turnover as they incorporate different aspects of differences in evolutionary history between communities that may be attributable to phylogenetic diversity gradients. In the present study, we extend an additive partitioning framework proposed for compositional beta diversity to PBD. Specifically, we decomposed the PhyloSor and UniFrac indices into two separate components accounting for ‘true’ phylogenetic turnover and phylogenetic diversity gradients, respectively. We illustrated the relevance of this framework using simple theoretical and archetypal examples, as well as an empirical study based on coral reef fish communities. Overall, our results suggest that using PhyloSor and UniFrac may greatly over-estimate the level of spatial turnover of lineages if the two compared communities show contrasting levels of phylogenetic diversity. We therefore recommend that future studies use the ‘true’ phylogenetic turnover component of these indices when the studied communities encompass a large phylogenetic diversity gradient.

Vicariance across major marine biogeographic barriers: temporal concordance and the relative intensity of hard versus soft barriers

The marine tropics contain five major biogeographic regions (East Pacific, Atlantic, Indian Ocean, Indo-Australian Archipelago (IAA) and Central Pacific). These regions are separated by both hard and soft barriers. Reconstructing ancestral vicariance, we evaluate the extent of temporal concordance in vicariance events across three major barriers (Terminal Tethyan Event (TTE), Isthmus of Panama (IOP), East Pacific Barrier, EPB) and two incomplete barriers (either side of the IAA) for the Labridae, Pomacentridae and Chaetodontidae. We found a marked lack of temporal congruence within and among the three fish families in vicariance events associated with the EPB, TTE and IOP. Vicariance across hard barriers separating the Atlantic and Indo-Pacific (TTE, IOP) is temporally diffuse, with many vicariance events preceding barrier formation. In marked contrast, soft barriers either side of the IAA hotspot support tightly concordant vicariance events (2.5 Myr on Indian Ocean side; 6 Myr on Central Pacific side). Temporal concordance in vicariance points to large-scale temporally restricted gene flow during the Late Miocene and Pliocene. Despite different and often complex histories, both hard and soft barriers have comparably strong effects on the evolution of coral reef taxa.

Human-Mediated Loss of Phylogenetic and Functional Diversity in Coral Reef Fishes

Beyond the loss of species richness, human activities may also deplete the breadth of evolutionary history (phylogenetic diversity) and the diversity of roles (functional diversity) carried out by species within communities, two overlooked components of biodiversity. Both are, however, essential to sustain ecosystem functioning and the associated provision of ecosystem services, particularly under fluctuating environmental conditions. We quantified the effect of human activities on the taxonomic, phylogenetic, and functional diversity of fish communities in coral reefs, while teasing apart the influence of biogeography and habitat along a gradient of human pressure across the Pacific Ocean. We detected nonlinear relationships with significant breaking points in the impact of human population density on phylogenetic and functional diversity of parrotfishes, at 25 and 15 inhabitants/km(2), respectively, while parrotfish species richness decreased linearly along the same population gradient. Over the whole range, species richness decreased by 11.7%, while phylogenetic and functional diversity dropped by 35.8% and 46.6%, respectively. Our results call for caution when using species richness as a benchmark for measuring the status of ecosystems since it appears to be less responsive to variation in human population densities than its phylogenetic and functional counterparts, potentially imperiling the functioning of coral reef ecosystems.

Parasitic plants have increased rates of molecular evolution across all three genomes

BackgroundTheoretical models and experimental evidence suggest that rates of molecular evolution could be raised in parasitic organisms compared to non-parasitic taxa. Parasitic plants provide an ideal test for these predictions, as there are at least a dozen independent origins of the parasitic lifestyle in angiosperms. Studies of a number of parasitic plant lineages have suggested faster rates of molecular evolution, but the results of some studies have been mixed. Comparative analysis of all parasitic plant lineages, including sequences from all three genomes, is needed to examine the generality of the relationship between rates of molecular evolution and parasitism in plants.ResultsWe analysed DNA sequence data from the mitochondrial, nuclear and chloroplast genomes for 12 independent evolutionary origins of parasitism in angiosperms. We demonstrated that parasitic lineages have a faster rate of molecular evolution than their non-parasitic relatives in sequences for all three genomes, for both synonymous and nonsynonymous substitutions.ConclusionsOur results prove that raised rates of molecular evolution are a general feature of parasitic plants, not confined to a few taxa or specific genes. We discuss possible causes for this relationship, including increased positive selection associated with host-parasite arms races, relaxed selection, reduced population size or repeated bottlenecks, increased mutation rates, and indirect causal links with generation time and body size. We find no evidence that faster rates are due to smaller effective populations sizes or changes in selection pressure. Instead, our results suggest that parasitic plants have a higher mutation rate than their close non-parasitic relatives. This may be due to a direct connection, where some aspect of the parasitic lifestyle drives the evolution of raised mutation rates. Alternatively, this pattern may be driven by an indirect connection between rates and parasitism: for example, parasitic plants tend to be smaller than their non-parasitic relatives, which may result in more cell generations per year, thus a higher rate of mutations arising from DNA copy errors per unit time. Demonstration that adoption of a parasitic lifestyle influences the rate of genomic evolution is relevant to attempts to infer molecular phylogenies of parasitic plants and to estimate their evolutionary divergence times using sequence data.

Exploring the Relationships between Mutation Rates, Life History, Genome Size, Environment, and Species Richness in Flowering Plants

A new view is emerging of the interplay between mutation at the genomic level, substitution at the population level, and diversification at the lineage level. Many studies have suggested that rate of molecular evolution is linked to rate of diversification, but few have evaluated competing hypotheses. By analyzing sequences from 130 families of angiosperms, we show that variation in the synonymous substitution rate is correlated among genes from the mitochondrial, chloroplast, and nuclear genomes and linked to differences in traits among families (average height and genome size). Within each genome, synonymous rates are correlated to nonsynonymous substitution rates, suggesting that increasing the mutation rate results in a faster rate of genome evolution. Substitution rates are correlated with species richness in protein-coding sequences from the chloroplast and nuclear genomes. These data suggest that species traits contribute to lineage-specific differences in the mutation rate that drive both synonymous and nonsynonymous rates of change across all three genomes, which in turn contribute to greater rates of divergence between populations, generating higher rates of diversification. These observations link mutation in individuals to population-level processes and to patterns of lineage divergence.

Plate tectonics drive tropical reef biodiversity dynamics

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.