Carlos Prada

Long prereproductive selection and divergence by depth in a Caribbean candelabrum coral

Long-lived corals, the foundation of modern reefs, often follow ecological gradients, so that populations or sister species segregate by habitat. Adaptive divergence maintains sympatric congeners after secondary contact or may even generate species by natural selection in the face of gene flow. Such ecological divergence, initially between alternative phenotypes within populations, may be aided by immigrant inviability, especially when a long period separates larval dispersal and the onset of reproduction, during which selection can sort lineages to match different habitats. Here, we evaluate the strength of one ecological factor (depth) to isolate populations by comparing the genes and morphologies of pairs of depth-segregated populations of the candelabrum coral Eunicea flexuosa across the Caribbean. Eunicea is endemic to the Caribbean and all sister species co-occur. Eunicea flexuosa is widespread both geographically and across reef habitats. Our genetic analysis revealed two depth-segregated lineages. Field survivorship data, combined with estimates of selection coefficients based on transplant experiments, suggest that selection is strong enough to segregate these two lineages. Genetic exchange between the Shallow and Deep lineages occurred either immediately after divergence or the two have diverged with gene flow. Migration occurs asymmetrically from the Shallow to Deep lineage. Limited recruitment to reproductive age, even under weak annual selection advantage, is sufficient to generate habitat segregation because of the cumulative prolonged prereproductive selection. Ecological factors associated with depth can act as filters generating strong barriers to gene flow, altering morphologies, and contributing to the potential for speciation in the sea.

Cryptic diversity hides host and habitat specialization in a gorgonian-algal symbiosis

Shallow water anthozoans, the major builders of modern coral reefs, enhance their metabolic and calcification rates with algal symbionts. Controversy exists over whether these anthozoan–algae associations are flexible over the lifetimes of individual hosts, promoting acclimative plasticity, or are closely linked, such that hosts and symbionts co‐evolve across generations. Given the diversity of algal symbionts and the morphological plasticity of many host species, cryptic variation within either partner could potentially confound studies of anthozoan‐algal associations. Here, we used ribosomal, organelle and nuclear sequences, along with microsatellite variation, to study the relationship between lineages of a common Caribbean gorgonian and its algal symbionts. The gorgonian Eunicea flexuosa is a broadcast spawner, composed of two recently diverged, genetically distinct lineages largely segregated by depth. We sampled colonies of the two lineages across depth gradients at three Caribbean locations. We find that each host lineage is associated with a unique Symbiodinium B1/184 phylotype. This relationship between host and symbiont is maintained when host colonies are reciprocally transplanted, although cases of within phylotype switching were also observed. Even when the phylotypes of both partners are present at intermediate depths, the specificity between host and symbiont lineages remained absolute. Unrecognized cryptic diversity may mask host‐symbiont specificity and change the inference of evolutionary processes in mutualistic associations. Symbiotic specificity thus likely contributes to the ecological divergence of the two partners, generating species diversity within coral reefs.

Octocoral bleaching during unusual thermal stress

We describe a bleaching event in octocoral communities at four reefs in southwest Puerto Rico during October 2005 following a period of elevated sea surface temperatures. Percentages of colonies bleached varied among taxa, ranging from 0% for Pseudopterogorgia, Eunicea and Gorgonia to over 90% for Muricea. Other taxa exhibiting bleaching included Pseudoplexaura (22.3%), Muriceopsis (36.6%), Briareum (46.1%), Plexaurella (69.6%) and Pterogorgia (84.5%).

Strong Natural Selection on Juveniles Maintains a Narrow Adult Hybrid Zone in a Broadcast Spawner

Natural selection can maintain and help form species across different habitats, even when dispersal is high. Selection against inferior migrants (immigrant inviability) acts when locally adapted populations suffer high mortality on dispersal to unsuitable habitats. Habitat-specific populations undergoing divergent selection via immigrant inviability should thus show (1) a change in the ratio of adapted to nonadapted individuals among age/size classes and (2) a cline (defined by the environmental gradient) as selection counterbalances migration. Here we examine the frequencies of two depth-segregated lineages in juveniles and adults of a Caribbean octocoral, Eunicea flexuosa. Distributions of the two lineages in both shallow and deep environments were more distinct when inferred from adults than juveniles. Despite broad larval dispersal, we also found an extremely narrow hybrid zone (<100 m), with coincident clines for molecular and morphological characters of the host coral and its algal symbiont. Effective dispersal estimates derived from the hybrid zone are remarkably small (<20 m) for a broadcast spawner. The large selection coefficient against mismatched genotypes derived from cohort data is consistent with that from field transplant experiments. Narrow hybrid zones and limited effective dispersal may be a common outcome of long periods of postsettlement, prereproductive selection across steep ecological gradients. Strong diversifying selection provides a mechanism to explain the prevalence of depth-segregated sibling species in the sea.

Universal target-enrichment baits for anthozoan (Cnidaria) phylogenomics: new approaches to long-standing problems

Anthozoans (e.g., corals, anemones) are an ecologically important and diverse group of marine metazoans that occur from shallow to deep waters worldwide. However, our understanding of the evolutionary relationships among the ~7,500 species within this class is hindered by the lack of phylogenetically informative markers that can be reliably sequenced across a diversity of taxa. We designed and tested 16,306 RNA baits to capture 720 ultraconserved element loci and 1,071 exon loci. Library preparation and target enrichment were performed on 33 taxa from all orders within the class Anthozoa. Following Illumina sequencing and Trinity assembly, we recovered 1,774 of 1,791 targeted loci. The mean number of loci recovered from each species was 638 ± 222, with more loci recovered from octocorals (783 ± 138 loci) than hexacorals (475 ± 187 loci). Parsimony informative sites ranged from 26 to 49% for alignments at differing hierarchical taxonomic levels (e.g., Anthozoa, Octocorallia, Hexacorallia). The per cent of variable sites within each of three genera (Acropora, Alcyonium, and Sinularia) for which multiple species were sequenced ranged from 4.7% to 30%. Maximum‐likelihood analyses recovered highly resolved trees with topologies matching those supported by other studies, including the monophyly of the order Scleractinia. Our results demonstrate the utility of this target‐enrichment approach to resolve phylogenetic relationships from relatively old to recent divergences. Redesigning the baits with improved affinities to capture loci within each subclass will provide a valuable toolset to address systematic questions, further our understanding of the timing of diversifications and help resolve long‐standing controversial relationships in the class Anthozoa.

Intraspecific and interspecific variation in thermotolerance and photoacclimation in Symbiodinium dinoflagellates

Light and temperature are major drivers in the ecology and biogeography of symbiotic dinoflagellates living in corals and other cnidarians. We examined variations in physiology among 11 strains comprising five species of clade A Symbiodinium. We grew cultures at 26°C (control) and 32°C (high temperature) over a duration of 18 days while measuring growth and photochemical efficiency (Fv/Fm). Responses to thermal stress ranged from susceptible to tolerant across species and strains. Most strains exhibited a decrease in cell densities and Fv/Fm when grown at 32°C. Tolerance to high temperature (T32) was calculated for all strains, ranging from 0 (unable to survive at high temperature) to 1 (able survive at high temperature). There was substantial variation in thermotolerance across species and among strains. One strain had a T32 close to 1, indicating that growth was not reduced at 32°C for only this one strain. To evaluate the combined effect of temperature and light on physiological stress, we selected three strains with different levels of thermotolerance (tolerant, intermediate and susceptible) and grew them under five different light intensities (65, 80, 100, 240 and 443 µmol quanta m−2 s−1) at 26 and 32°C. High irradiance exacerbated the effect of high temperature, particularly in strains from thermally sensitive species. This work further supports the recognition that broad physiological differences exist not only among species within Symbiodinium clades, but also among strains within species demonstrating that thermotolerance varies widely between species and among strains within species.

Isolation and characterization of 12 microsatellite loci to study connectivity in the yellow jawfish Opistognathus aurifrons

Marine Protected Areas (MPAs) are conservation strategies to preserve the degradation of marine ecosystems by allowing species to naturally recover. Central to MPA design is the assumption of connectivity in marine populations over hundreds of kilometers, but only in a few handful of species the scale of connectivity has been estimated. To facilitate the study of connectivity of reef fishes, we newly developed 12 microsatellite loci for the yellow jawfish Opistognathus aurifrons. We tested all microsatellite loci in eight Caribbean populations with various degrees of divergence. We found between 9 and 26 alleles per locus with polymorphism that ranged from 0.652 to 0.976. All loci were in Hardy–Weinberg equilibrium, except loci 1588 and 7983. The described markers provide the most sensitive tools yet available to study connectivity at the finest spatial scale and evaluate if current networks of Caribbean MPAs maximize the potential for the recovery of reef fish populations.

Ecological Speciation in Corals

The ocean is generally a homogenous environment with few geographic barriers that allow populations to connect over hundreds of kilometers, increasing gene flow and slowing down diversification and the formation of species. However, biodiversity in the ocean is vast across thousands of kilometers and even within single individuals (e.g., coral colonies). Species diversity peaks at coral reef ecosystems, which house at least one quarter of the marine biodiversity. Why are these systems so diverse? How do species differentiate despite rampant genetic connectivity? One possibility to explain biodiversity hotspots in the ocean, along with physical barriers, is through ecological factors. Populations can diverge if they specialize ecologically, reducing interbreeding, which can lead to reproductive isolation. We reviewed cases of speciation in coral reefs with emphasis on those driven by ecological factors. We find few studies in coral research using genomic approaches to understand the genetics of reproductive isolation. We propose the cases of the coral Orbicella spp. and the octocoral Eunicea spp. as ideal examples to study ecological speciation in corals.

Effective Dispersal of Caribbean Reef Fish is Smaller than Current Spacing Among Marine Protected Areas

The oceans are deteriorating at a fast pace. Conservation measures, such as Marine Protected Areas, are being implemented to relieve areas from local stressors and allow populations to restore to natural levels. Successful networks of MPAs operate if the space among MPAs is smaller than the dispersal capacity of the species under protection. We studied connectivity patterns across populations in a series of MPAs in the common yellowhead Jawfish, Opistognathus aurifrons. Using the power of genome-wide variation, we estimated that the maximum effective dispersal is 8.3 km. We found that MPAs exchange migrants likely via intermediate unprotected habitats through stepping stone dispersal. At scales >50 km such connectivity is decreased, particularly across the Mona Passage. The MPA network studied would be unable to maintain connectivity of these small benthic fishes if habitat in between them is extirpated. Our study highlights the power of SNPs to derive effective dispersal distance and the ability of SNPs to make inferences from single individuals. Given that overall reef fish diversity is driven by species with life histories similar to that of the yellowhead jawfish, managers face a challenge to develop strategies that allow connectivity and avoid isolation of populations and their possible extinction.