The evolutionary ecology of corals

Corals display a wide range of complex life histories. The evolutionary consequences of factors such as clonality, indeterminate growth, asexual reproduction coupled with various (sexual) breeding systems, different levels of gene flow, and strongly overlapping generations have only just begun to be explored. We identify a series of problems and areas for new research that may be resolved b y the application of novel theoretical approaches (including nonequilibrium population genetic models and demographic models incorporating modular processes such as colony fission and polyp mortality), greater in situ experimentation, long-term monitoring of population dynamics and the use of new genetic techniques.     

The future of evolutionary diversity in reef corals

One-third of the world''s 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.     

Reproductive ecology of Caribbean reef corals

The last decade has seen a resurgence of interest in the processes of sexual reproduction by scleractinian reef corals. Earlier investigations had focused fortuitously on brooding (planulating) species, which resulted in the general misconception that brooding was the main form of larval development of reef corals. More recent work on Indo-Pacific species has shown broadcast spawning and short annual reproductive periods to predominate. This report presents the reproductive patterns of eleven Caribbean coral species and attempts to explain the adaptive features and selective pressures that have led to the evolution of the four reproductive patterns described to date: (a) hermaphroditic broadcasters; (b) gonochoric broadcasters; (c) hermaphroditic broadcasters; (b) gonochoric brooders. Both (a) and (b) correlate with large colony size and short annual spawning periods; and (c) and (d) correlate with small colony size, multiple planulating cycles per year, and occupation of unstable habitats. Selection for outcrossing between long-lived individuals is proposed as the reason for gonochorism and for synchronous spawning of hermaphroditic broadcasters, and also for the large amount of sperm produced by hermaphroditic brooders. Selection for high rates of local recruitment is proposed as the force behind the evolution of brooding by species inhabiting unstable habitats and suffering high rates of adult mortality.     

Lipid composition of positively buoyant eggs of reef building corals

Lipid composition of the eggs of three reef building corals, Acropora millepora, A. tenuis and Montipora digitata, were determined. Sixty to 70% of the egg dry weight was lipid, which consisted of wax esters (69.5–81.8%), triacylglycerols (1.1–8.4%) and polar lipids c/mainly phospholipids (11.9–13.2%). Montipora digitata also contained some polar lipids typical of the thylakoid membrane in chloroplasts, probably due to the presence of symbiotic zooxanthellae in the eggs. The wax esters appeared to be the major contributor to positive buoyancy of the eggs, and specific gravity of wax esters in A. millepora was estimated to be 0.92. Among the fatty acids of the wax esters, 34.9–51.3% was hexadecanoic acid (16:0) while the major fatty acids in polar lipids were octadecenoic acid (18:1), hexadecanoic acid (16:0), eicosapentaenoic acid (20:5) and eicosatetraenoic acid (20:4). The wax ester appears to be the main component of the 4.5 6.0 m diameter lipid droplets which fill most of the central mass of the coral eggs.     

Symbiodinium genotypic and environmental controls on lipids in reef building corals

Background

Lipids in reef building corals can be divided into two classes; non-polar storage lipids, e.g. wax esters and triglycerides, and polar structural lipids, e.g. phospholipids and cholesterol. Differences among algal endosymbiont types are known to have important influences on processes including growth and the photobiology of scleractinian corals yet very little is known about the role of symbiont types on lipid energy reserves.

Methodology/Principal Findings

The ratio of storage lipid and structural lipid fractions of Scott Reef corals were determined by thin layer chromatography. The lipid fraction ratio varied with depth and depended on symbiont type harboured by two corals (Seriatopora hystrix and Pachyseris speciosa). S. hystrix colonies associated with Symbiodinium C1 or C1/C# at deep depths (>23 m) had lower lipid fraction ratios (i.e. approximately equal parts of storage and structural lipids) than those with Symbiodinium D1 in shallow depths (<23 m), which had higher lipid fraction ratios (i.e. approximately double amounts of storage relative to structural lipid). Further, there was a non-linear relationship between the lipid fraction ratio and depth for S. hystrix with a modal peak at ∼23 m coinciding with the same depth as the shift from clade D to C types. In contrast, the proportional relationship between the lipid fraction ratio and depth for P. speciosa, which exhibited high specificity for Symbiodinium C3 like across the depth gradient, was indicative of greater amounts of storage lipids contained in the deep colonies.

Conclusions/Significance

This study has demonstrated that Symbiodinium exert significant controls over the quality of coral energy reserves over a large-scale depth gradient. We conclude that the competitive advantages and metabolic costs that arise from flexible associations with divergent symbiont types are offset by energetic trade-offs for the coral host.     

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.     

Threatened reef corals of the world

A substantial proportion of the world's living species, including one-third of the reef-building corals, are threatened with extinction and in pressing need of conservation action. In order to reduce biodiversity loss, it is important to consider species' contribution to evolutionary diversity along with their risk of extinction for the purpose of setting conservation priorities. Here I reconstruct the most comprehensive tree of life for the order Scleractinia (1,293 species) that includes all 837 living reef species, and employ a composite measure of phylogenetic distinctiveness and extinction risk to identify the most endangered lineages that would not be given top priority on the basis of risk alone. The preservation of these lineages, not just the threatened species, is vital for safeguarding evolutionary diversity. Tests for phylogeny-associated patterns show that corals facing elevated extinction risk are not clustered on the tree, but species that are susceptible, resistant or resilient to impacts such as bleaching and disease tend to be close relatives. Intensification of these threats or extirpation of the endangered lineages could therefore result in disproportionate pruning of the coral tree of life.     

The role of resource imbalances in the evolutionary ecology of tropical arboreal ants

In numbers and biomass, ants (Hymenoptera, Formicidae) often dominate arthropod faunas of tropical rainforest canopies. Extraordinary ant abundance is due principally to one or a few species able to tap the high productivity of canopy foliage by feeding on plant and homopteran exudates. Prior studies of nitrogen isotopic ratios show that exudate-feeders derive much of their nitrogen (N) by processing large quantities of N-poor, but carbohydrate (CHO)-rich, exudates. CHOs in excess of those that can be coupled with protein for growth and reproduction (postulated as the colony's first priorities) may be directed at little cost and some profit to functions that increase access to limiting protein. High dietary CHO:protein ratios for exudate-feeders appear to subsidize 'high tempo' foraging activity, defence of absolute (level III) territories, and production of N-free alarm/defence exocrine products that enhance ecological dominance in contests with other ants. Among organisms (e.g. plants and Lepidoptera) symbiotic with ants, CHO:protein ratios of ant rewards may control both the identities of ant associates and the quality of ant-rendered services. Dietary ratios of CHO:protein play an important and previously unrecognized role in the ecology and evolution of ants generally. Modifications of worker digestive systems in certain ant subfamilies and genera represent key innovations for handling and processing large volumes of liquid food. The supreme tropical dominants are species released from nest site limitation and able to place their nests in the vicinity of abundant exudate resources. Polydomy appears to be typical of these species and should produce energetic savings by taking colony fragments to the resource.     

The evolutionary ecology of metacommunities

Research on the interactions between evolutionary and ecological dynamics has largely focused on local spatial scales and on relatively simple ecological communities. However, recent work demonstrates that dispersal can drastically alter the interplay between ecological and evolutionary dynamics, often in unexpected ways. We argue that a dispersal-centered synthesis of metacommunity ecology and evolution is necessary to make further progress in this important area of research. We demonstrate that such an approach generates several novel outcomes and substantially enhances understanding of both ecological and evolutionary phenomena in three core research areas at the interface of ecology and evolution.     

Towards an understanding of the evolutionary role of fire in animals

Wildfires underpin the dynamics and diversity of many ecosystems worldwide, and plants show a plethora of adaptive traits for persisting recurrent fires. Many fire-prone ecosystems also harbor a rich fauna; however, knowledge about adaptive traits to fire in animals remains poorly explored. We review existing literature and suggest that fire is an important evolutionary driver for animal diversity because (1) many animals are present in fire-prone landscapes and may have structural and phenotypic characters that contribute to adaptation to these open landscapes; and (2) in some cases, animals from fire-prone ecosystems may show specific fire adaptations. While there is limited evidence on morphological fire adaptations in animals, there is evidence suggesting that different behaviors might provide a rich source of putative fire adaptations; this is because, in contrast to plants, most animals are mobile, unitary organisms, have reduced survival when directly burnt by fire and can move away from the fire. We call for research on fire adaptations (morphological, behavioral, and physiological) in animals, and emphasize that in the animal kingdom many fire adaptations are likely to be behavioral. While it may be difficult to discern these adaptations from other animal behaviors, making this distinction is fundamental if we want to understand the role of fire in shaping biodiversity. Developing this understanding is critical to how we view and manage our ecosystems in the face of current global and fire regime changes.     

The evolutionary ecology of myco-heterotrophy

Nonphotosynthetic mycorrhizal plants have long attracted the curiosity of botanists and mycologists, and they have been a target for unabated controversy and speculation. In fact, these puzzling plants dominated the very beginnings of the field of mycorrhizal biology. However, only recently has the mycorrhizal biology of this diverse group of plants begun to be systematically unravelled, largely following a landmark Tansley review a decade ago and crucial developments in the field of molecular ecology. Here I explore our knowledge of these evolutionarily and ecologically diverse plant-fungal symbioses, highlighting areas where there has been significant progress. The focus is on what is arguably the best understood example, the monotropoid mycorrhizal symbiosis, and the overarching goal is to lay out the questions that remain to be answered about the biology of myco-heterotrophy and epiparasitism.     

Oriented translocation of energy in grafted reef corals

Colonies of the Red Sea reef coral Stylophora pistillata were grafted with alien branches (alografts), which had been labelled by NaH¹⁴CO₃ in the light. The “cold” host-colonies translocated the ¹⁴C-containing photosynthetic metabolites in an oriented pathway from the grafted branches into their own tissues. The highest accumulations of ¹⁴C products were detected in specific branch-tips of the host, away from the contact zones. The “recipient” colonies utilize these energy-rich materials for their metabolic requirements. The ¹⁴CO₂ produced through respiration is consequently detected in the skeletal-carbonate of the tips as Ca¹⁴CO₃. The purple morph of S. pistillata is found to be superior to the yellow morph.     

Snorkeler damage to reef corals in the Maldive Islands

Rapid and intensive survey methods were used to measure coral breakage by snorkelers on a Maldivian resort reef. On the most impacted section of reef, breakage over a one month period was estimated at 17% of susceptible coral cover and 7% of total coral cover.     

Genomic insights into hybridization of reef corals

Coral Reefs - Hybridization plays a fundamental role in speciation and diversification of plants and animals. Hybridization among highly diverse assemblages of reef corals is well known and widely...     

Effects of water motion on reef corals

The Hawaiian reef coral Pocillopora meandrina Dana is restricted to turbulent environments. P. damicornis (L.) is most abundant on semi-protected reefs, while Montipora verrucosa (Lamarck) is characteristic of very calm environments. These species were grown in the laboratory under various conditions of water motion. Water motion influenced the growth, mortality, and reproductive rate, of each species differently. The differences may be attributed to morphological adaptations of the corals to their normal hydrodynamic environment. Water motion appears to influence corals by controlling the rate of exchange of material across the interface between the sea water and the coral tissue.     

Species delimitation of common reef corals in the genus Pocillopora using nucleotide sequence phylogenies, population genetics and symbiosis ecology

Stony corals in the genus Pocillopora are among the most common and widely distributed of Indo-Pacific corals and, as such, are often the subject of physiological and ecological research. In the far Tropical Eastern Pacific (TEP), they are major constituents of shallow coral communities, exhibiting considerable variability in colony shape and branch morphology and marked differences in response to thermal stress. Numerous intermediates occur between morphospecies that may relate to extensive hybridization. The diversity of the Pocillopora genus in the TEP was analysed genetically using nuclear ribosomal (ITS2) and mitochondrial (ORF) sequences, and population genetic markers (seven microsatellite loci). The resident dinoflagellate endosymbiont (Symbiodinium sp.) in each sample was also characterized using sequences of the internal transcribed spacer 2 (ITS2) rDNA and the noncoding region of the chloroplast psbA minicircle. From these analyses, three symbiotically distinct, reproductively isolated, nonhybridizing, evolutionarily divergent animal lineages were identified. Designated types 1, 2 and 3, these groupings were incongruent with traditional morphospecies classification. Type 1 was abundant and widespread throughout the TEP; type 2 was restricted to the Clipperton Atoll; and type 3 was found only in Panama and the Galapagos Islands. Each type harboured a different Symbiodinium'species lineage' in Clade C, and only type 1 associated with the 'stress-tolerant'Symbiodinium glynni (D1). The accurate delineation of species and implementation of a proper taxonomy may profoundly improve our assessment of Pocillopora's reproductive biology, biogeographic distributions, and resilience to climate warming, information that must be considered when planning for the conservation of reef corals.     

The evolutionary ecology of mast seeding

The past seven years have seen a revolution in understanding the causes of mast seeding In perennial plants. Before 1987, the two main theories were resource matching (i.e. plants vary their reproductive output to match variable resources) and predator satiation (i.e. losses to predators are reduced by varying the seed crop). Today, resource matching is restricted to a proximate role, and predator satiation is only one of many theories for the ultimate advantage of masting. Wind pollination, prediction of favourable years for seedling establishment, animal pollination, animal dispersal of fruits, high accessory costs of reproduction and large seed size have all been advanced as possible causes of masting. Of these, wind pollination, predator satiation and environmental prediction are important in a number of species, but the other theories have less support. In future, Important advances seem likely from quantifying synchrony within a population, and examining species with very constant reproduction between years.