Danwei Huang

More evidence for pervasive paraphyly in scleractinian corals: systematic study of Southeast Asian Faviidae (Cnidaria; Scleractinia) based on molecular and morphological data.

Coral taxonomy and systematics continue to be plagued by a host of problems. Due to high phenotypic variability within species, morphological approaches have often failed to recognize natural taxa, and molecular techniques have yet to be applied to many groups. Here, we summarize the levels of paraphyly found for scleractinian corals and test, based on new data, whether paraphyly is also a significant problem in Faviidae, the second-most speciose hermatypic scleractinian family. Using both DNA sequence and morphological data we find that, regardless of analysis technique (maximum parsimony, maximum likelihood and Bayesian likelihood), many conventional taxonomic groups are not monophyletic. Based on two mitochondrial markers (COI and a noncoding region) that we amplified for 81 samples representing 41 faviid species and 13 genera, five genera that are represented by more than one species are paraphyletic, as is the family Faviidae. The morphological characters currently used to identify these corals similarly fail to recover many genera. Furthermore, trees based on both data types are incongruent, and total evidence analysis does little to salvage conventional taxonomic groupings. Morphological convergence, phenotypic variability in response to the environment, and recent speciation are likely causes for these conflicts, which suggest that the present classification of corals is in need of a major overhaul. We propose more detailed studies of problematic faviid taxa using standardized morphological, mitochondrial, and nuclear genetic markers to facilitate combining of data.

The Coral Trait Database, a curated database of trait information for coral species from the global oceans

Trait-based approaches advance ecological and evolutionary research because traits provide a strong link to an organism’s function and fitness. Trait-based research might lead to a deeper understanding of the functions of, and services provided by, ecosystems, thereby improving management, which is vital in the current era of rapid environmental change. Coral reef scientists have long collected trait data for corals; however, these are difficult to access and often under-utilized in addressing large-scale questions. We present the Coral Trait Database initiative that aims to bring together physiological, morphological, ecological, phylogenetic and biogeographic trait information into a single repository. The database houses species- and individual-level data from published field and experimental studies alongside contextual data that provide important framing for analyses. In this data descriptor, we release data for 56 traits for 1547 species, and present a collaborative platform on which other trait data are being actively federated. Our overall goal is for the Coral Trait Database to become an open-source, community-led data clearinghouse that accelerates coral reef research.

Towards a phylogenetic classification of reef corals: the Indo-Pacific genera Merulina, Goniastrea and Scapophyllia (Scleractinia, Merulinidae)

Recent advances in scleractinian systematics and taxonomy have been achieved through the integration of molecular and morphological data, as well as rigorous analysis using phylogenetic methods. In this study, we continue in our pursuit of a phylogenetic classification by examining the evolutionary relationships between the closely related reef coral genera Merulina, Goniastrea, Paraclavarina and Scapophyllia (Merulinidae). In particular, we address the extreme polyphyly of Favites and Goniastrea that was discovered a decade ago. We sampled 145 specimens belonging to 16 species from a wide geographic range in the Indo‐Pacific, focusing especially on type localities, including the Red Sea, western Indian Ocean and central Pacific. Tree reconstructions based on both nuclear and mitochondrial markers reveal a novel lineage composed of three species previously placed in Favites and Goniastrea. Morphological analyses indicate that this clade, Paragoniastrea Huang, Benzoni & Budd, gen. n., has a unique combination of corallite and subcorallite features observable with scanning electron microscopy and thin sections. Molecular and morphological evidence furthermore indicates that the monotypic genus Paraclavarina is nested within Merulina, and the former is therefore synonymised.

The future of evolutionary diversity in reef corals

One-third of the worlds reef-building corals are facing heightened extinction risk from climate change and other anthropogenic impacts. Previous studies have shown that such threats are not distributed randomly across the coral tree of life, and future extinctions have the potential to disproportionately reduce the phylogenetic diversity of this group on a global scale. However, the impact of such losses on a regional scale remains poorly known. In this study, we use phylogenetic metrics in conjunction with geographical distributions of living reef coral species to model how extinctions are likely to affect evolutionary diversity across different ecoregions. Based on two measures—phylogenetic diversity and phylogenetic species variability—we highlight regions with the largest losses of evolutionary diversity and hence of potential conservation interest. Notably, the projected loss of evolutionary diversity is relatively low in the most species-rich areas such as the Coral Triangle, while many regions with fewer species stand to lose much larger shares of their diversity. We also suggest that for complex ecosystems like coral reefs it is important to consider changes in phylogenetic species variability; areas with disproportionate declines in this measure should be of concern even if phylogenetic diversity is not as impacted. These findings underscore the importance of integrating evolutionary history into conservation planning for safeguarding the future diversity of coral reefs.

Anthropogenic extinction threats and future loss of evolutionary history in reef corals

Extinction always results in loss of phylogenetic diversity (PD), but phylogenetically selective extinctions have long been thought to disproportionately reduce PD. Recent simulations show that tree shapes also play an important role in determining the magnitude of PD loss, potentially offsetting the effects of clustered extinctions. While patterns of PD loss under different extinction scenarios are becoming well characterized in model phylogenies, analyses of real clades that often have unbalanced tree shapes remain scarce, particularly for marine organisms. Here, we use a fossil-calibrated phylogeny of all living scleractinian reef corals in conjunction with IUCN data on extinction vulnerabilities to quantify how loss of species in different threat categories will affect the PD of this group. Our analyses reveal that predicted PD loss in corals varies substantially among different threats, with extinctions due to bleaching and disease having the largest negative effects on PD. In general, more phylogenetically clustered extinctions lead to larger losses of PD in corals, but there are notable exceptions; extinction of rare corals from distantly-related old and unique lineages can also result in substantial PD loss. Thus our results show that loss of PD in reef corals is dependent on both tree shape and the nature of extinction threats.

The new systematics of Scleractinia: Integrating molecular and morphological evidence.

The taxonomy of scleractinian corals has traditionally been established based on morphology at the “macro” scale since the time of Carl Linnaeus. Taxa described using macromorphology are useful for classifying the myriad of growth forms, yet new molecular and small-scale morphological data have challenged the natural historicity of many familiar groups, motivating multiple revisions at every taxonomic level. In this synthesis of scleractinian phylogenetics and systematics, we present the most current state of affairs in the field covering both zooxanthellate and azooxanthellate taxa, focusing on the progress of our phylogenetic understanding of this ecologically-significant clade, which today is supported by rich sets of molecular and morphological data. It is worth noting that when DNA sequence data was first used to investigate coral evolution in the 1990s, there was no concerted effort to use phylogenetic information to delineate problematic taxa. In the last decade, however, the incompatibility of coral taxonomy with their evolutionary history has become much clearer, as molecular analyses for corals have been improved upon technically and expanded to all major scleractinian clades, shallow and deep. We describe these methodological developments and summarise new taxonomic revisions based on robust inferences of the coral tree of life. Despite these efforts, there are still unresolved sections of the scleractinian phylogeny, resulting in uncertain taxonomy for several taxa. We highlight these and propose a way forward for the taxonomy of corals.

Inference of phylogenetic relationships within Fabriciidae (Sabellida, Annelida) using molecular and morphological data

Cladistic relationships among fabriciids have to date been explored in the context of adult morphology, but resolution has been declining as more species are described. In this study, we incorporated data on the reproductive system, including features related to the male sperm and sperm storage by females, to supplement existing data on adult morphology (for a total of 50 characters). Three nuclear DNA markers (18S rDNA approximately 1800 bp, the D1 region of 28S rDNA approximately 320 bp, and histone H3 approximately 330 bp) were sequenced from 21 species of fabriciids. We assessed the phylogeny of Fabriciidae based on an integrative analysis of these morphological and molecular characters. Our results show that, in addition to three previously recovered apomorphies for Fabriciidae (absence of ventral lips, modification of abdominal uncini to an elongate manubrium, and presence of branchial hearts), six more apomorphies associated with the reproductive system can be used to support this clade—spermiogenesis only in the thorax, spermiogenesis in large clusters with a central cytophore, single dorsal sperm duct, sperm nuclear projection, thickening of the sperm nuclear membrane and the sperm extra‐axonemal sheath. The results require the erection of two new genera and two new species, which are described.

Fossils, phylogenies, and the challenge of preserving evolutionary history in the face of anthropogenic extinctions

Significance Anthropogenic impacts are endangering many species, potentially leading to a disproportionate loss of evolutionary history (EH) in the future. However, surprisingly little is known about the loss of EH during extinctions in the geological past, and thus we do not know whether anthropogenic extinctions are pruning the tree of life in a manner that is unique in Earths history. Comparisons of EH loss during past and ongoing extinctions is difficult because of conceptual differences in how ages are estimated from paleontological data versus molecular phylogenies. We used simulations and empirical analyses to show that the differences between the two data types do not preclude such comparisons, which are essential for improving evolutionarily informed models of conservation prioritization. Anthropogenic impacts are endangering many long-lived species and lineages, possibly leading to a disproportionate loss of existing evolutionary history (EH) in the future. However, surprisingly little is known about the loss of EH during major extinctions in the geological past, and thus we do not know whether human impacts are pruning the tree of life in a manner that is unique in the history of life. A major impediment to comparing the loss of EH during past and current extinctions is the conceptual difference in how ages are estimated from paleontological data versus molecular phylogenies. In the former case the age of a taxon is its entire stratigraphic range, regardless of how many daughter taxa it may have produced; for the latter it is the time to the most recent common ancestor shared with another extant taxon. To explore this issue, we use simulations to understand how the loss of EH is manifested in the two data types. We also present empirical analyses of the marine bivalve clade Pectinidae (scallops) during a major Plio–Pleistocene extinction in California that involved a preferential loss of younger species. Overall, our results show that the conceptual difference in how ages are estimated from the stratigraphic record versus molecular phylogenies does not preclude comparisons of age selectivities of past and present extinctions. Such comparisons not only provide fundamental insights into the nature of the extinction process but should also help improve evolutionarily informed models of conservation prioritization.

Conservation of reef corals in the South China Sea based on species and evolutionary diversity

The South China Sea in the Central Indo-Pacific is a large semi-enclosed marine region that supports an extraordinary diversity of coral reef organisms (including stony corals), which varies spatially across the region. While one-third of the world’s reef corals are known to face heightened extinction risk from global climate and local impacts, prospects for the coral fauna in the South China Sea region amidst these threats remain poorly understood. In this study, we analyse coral species richness, rarity, and phylogenetic diversity among 16 reef areas in the region to estimate changes in species and evolutionary diversity during projected anthropogenic extinctions. Our results show that richness, rarity, and phylogenetic diversity differ considerably among reef areas in the region, and that their outcomes following projected extinctions cannot be predicted by species diversity alone. Although relative rarity and threat levels are high in species-rich areas such as West Malaysia and the Philippines, areas with fewer species such as northern Vietnam and Paracel Islands stand to lose disproportionately large amounts of phylogenetic diversity. Our study quantifies various biodiversity components of each reef area to inform conservation planners and better direct sparse resources to areas where they are needed most. It also provides a critical biological foundation for targeting reefs that should be included in a regional network of marine protected areas in the South China Sea.

The origin and evolution of coral species richness in a marine biodiversity hotspot

The Coral Triangle (CT) region of the Indo‐Pacific realm harbors an extraordinary number of species, with richness decreasing away from this biodiversity hotspot. Despite multiple competing hypotheses, the dynamics underlying this regional diversity pattern remain poorly understood. Here, we use a time‐calibrated evolutionary tree of living reef coral species, their current geographic ranges, and model‐based estimates of regional rates of speciation, extinction, and geographic range shifts to show that origination rates within the CT are lower than in surrounding regions, a result inconsistent with the long‐standing center of origin hypothesis. Furthermore, endemism of coral species in the CT is low, and the CT endemics are older than relatives found outside this region. Overall, our model results suggest that the high diversity of reef corals in the CT is largely due to range expansions into this region of species that evolved elsewhere. These findings strongly support the notion that geographic range shifts play a critical role in generating species diversity gradients. They also show that preserving the processes that gave rise to the striking diversity of corals in the CT requires protecting not just reefs within the hotspot, but also those in the surrounding areas.