David B. Carlon

Larval dispersal distance as an explanation for adult spatial pattern in two Caribbean reef corals

Abstract Larval dispersal distance is a parameter which can account for differences in adult spatial distribution between closely-related marine invertebrates. To examine its importance in relation to Caribbean reef corals, we observed the larval swimming and settlement behavior of two Caribbean coral species; one of which ( Favia fragum [Esper]) has a highly aggregated adult distribution, the other of which ( Agaricia agaricites [Linnaeus]) is less aggregated. Larvae of the highly aggregated species, when followed in situ by divers, settled rapidly (less than 10 min) and showed little discrimination among different types of substrata. Larvae of the less aggregated species swam longer and showed clear discrimination between types of substrata. Our data suggest a correspondence between larval swimming/settlement behavior and adult distribution. Such a relationship between larval behavior and adult distribution could be important in understanding the linkage between life history and adult spatial patterns in sessile marine invertebrates.

The evolution of mating systems in tropical reef corals

The life histories of tropical reef corals (Scleractinia) include two traits that can strongly bias mating systems towards inbreeding: (1) most species express both sexes simultaneously, creating the potential for self-fertilization; and (2) there is philopatric dispersal of planktonic or demersal larvae. Recent studies have confirmed that all hermaphrodite species with broad dispersal potential are either completely, or almost completely, self-incompatible. By contrast, species with limited dispersal potential have high, but variable, rates of self-fertilization. This interspecific variation in coral mating systems is similar to that found in terrestrial plants. Understanding the selective forces that drive mating-system variation in marine environments will undoubtedly broaden our understanding of the evolution of inbreeding and outbreeding in sessile plants and animals.

Incipient speciation across a depth gradient in a scleractinian coral

Abstract.— A few marine cases have demonstrated morphological and genetic divergence in the absence of spatial barriers to gene flow, suggesting that the initial phase of speciation is possible without geographic isolation. In the Bocas del Toro Archipelago of the Atlantic Coast of Panama, we found two morphotypes of the scleractinian coral Favia fragum with opposing depth distributions. One morphotype fit the classical description of F. fragum and was most abundant at 3 m depth. A second morphotype was distinguished by raised corallites and was restricted to ≤ 1 m depth. The two morphotypes overlapped in distribution at 1 m depth. Multivariate analysis of polyp‐level characters (shape and distribution of septa within corallites) divided samples into two groups corresponding to initial qualitative observations of colony shape and corallite relief. To determine whether reduced gene flow maintains morphological variation, we measured the frequencies of alleles at five allozyme loci in both morphotypes at three sites 1–2 km distant. While there were significant differences in allele frequencies between morphotypes within sites, there were also frequency differences among sites at most loci, with the exception of nearly fixed alleles at the PGM locus. Extremely low heterozygosity permitted us to use haplotypes to compare genetic distance between morphotypes and among sites. Comparisons between haplotype data and a null model assuming gene flow between morphotypes showed that the two morphotypes shared significantly fewer haplotypes than expected, and average genetic distance between morphotypes was significantly greater than expected. Partitioning haplotype variation with analysis of molecular variance demonstrated that 35% of the variation was explained by morphotype, whereas 28% of the variation was explained by site. Two PGM heterozygotes and several individuals homozygous for rare PGM alleles are consistent with hybridization, and perhaps introgression by selfing within morphotypes. We consider three hypotheses for this morphological and genetic divergence inF. fragum: (1) intraspecific polymorphism, (2) incipient species, (3) biological species; and discuss the role of reproductive characters in a divergence‐with‐gene flow mechanism of speciation.

Production and supply of larvae as determinants of zonation in a brooding tropical coral

Production and settlement of planktonic larvae of the coral Favia fragum (Esper) were studied. The species is restricted to shallow back- and fore-reef habitats throughout the Caribbean Sea. Adults are in their greatest abundance on the reef-crest and shallow reef slope (<3 m) at Tague Bay, St. Croix, in the US Virgin Islands. Because F. fragum broods larvae that are capable of immediate settlement, this distribution pattern may be due to variation in fecundity among depths. Corals were collected from shallow (1.0 m) and deep depths (10–13 m) and cultured in individual containers exposed to shaded ambient light. Corals from shallow depths had greater fecundity (polyp−1 lunar cycle−1) and were larger than deep corals. To test the hypothesis that fecundity was related to successful fertilization, corals were kept in different densities in an area with sea-grass, where there were no natural adults. Production of larvae 6 months later was not affected by density of adults, possibly due to self-fertilization. Larval choice of habitat was also examined. In the laboratory, twice as many larvae settled on coral rubble fragments collected from depths where adults were common (1.5 and 3 m) than on those from depths where adults were rare (10 m). Larval supply may establish the vertical distribution of adults on St. Croix.

The West Pacific diversity hotspot as a source or sink for new species? Population genetic insights from the Indo‐Pacific parrotfish Scarus rubroviolaceus

We used a population genetic approach to quantify major population subdivisions and patterns of migration within a broadly distributed Indo‐Pacific parrotfish. We genotyped 15 microsatellite loci in Scarus rubroviolaceus collected from 20 localities between Africa and the Americas. A STRUCTURE model indicates the presence of four major populations: Eastern Pacific, Hawaii, Central‐West Pacific and a less well‐differentiated Indian Ocean. We used the isolation and migration model to estimate splitting times, population sizes and migration patterns between sister population pairs. To eliminate loci under selection, we used BayeScan to select loci for three isolation and migration models: Eastern Pacific and Central‐West Pacific, Hawaii and the Central‐West Pacific, and Indian Ocean and the Central‐West Pacific. To test the assumption of a stepwise mutation model (SMM), we used likelihood to test the SMM against a two‐phase model that allowed mutational complexity. A posteriori, minor departures from SMM were estimated to affect ≤2% of the alleles in the data. The data were informative about the contemporary and ancestral population sizes, migration rates and the splitting time in the eastern Pacific/Central‐West Pacific comparison. The model revealed a splitting time ∼17 000 bp, a larger contemporary Ne in the Central‐West Pacific than in the eastern Pacific and a strong bias of east to west migration. These characteristics support the Center of Accumulation model of peripatric diversification in low‐diversity peripheral sites and perhaps migration from those sites to the western Pacific diversity hotspot.

Life-History Variation Among Three Temperate Hermit Crabs: The Importance of Size in Reproductive Strategies

The supply and quality of empty gastropod shells may play important roles in the ecology and evolution of hermit crabs. We compare the life histories of three subtidal hermit crabs in Nantucket Harbor, Massachusetts: Pagurus annulipes, P. longicarpus, and P. pollicaris. Specifically, we examine seasonal patterns of reproduction in females, male and female size structure, reproductive effort, and temporal patterns of larval abundance. We also compare shell size among the three species. Life-history features vary with size among the three species. The smallest species (P. annulipes) reproduce soon after metamorphosis and have a high reproductive effort. The two larger species (P. longicarpus and P. pollicaris) delayed reproduction to an intermediate size, and have lower reproductive efforts than P. annulipes. There is no effect of body size on reproduction in P. annulipes, but there is a strong positive effect in P. longicarpus and P. pollicaris. Seasonal patterns of early stage larvae correlated with seasonal patterns of ovigery in all three species, with highest larval densities sampled in P. annulipes and P. longicarpus. Size differences among species were related to patterns of shell usage. Male and female P. annulipes were always found in large shells relative to body size. In comparison, male and female P. longicarpus and P. pollicaris were found in small shells compared to body size. We suggest that early maturity and high reproductive effort have evolved in response to a high risk of mortality associated with small shells. Delayed maturity and low reproductive effort are favored in species that reach a size refuge from shell-crushing predators. Effects of shell limitation are more likely to be common in large species and may also be an important selective in shaping hermit crab life histories.

High cryptic diversity across the global range of the migratory planktonic copepods Pleuromamma piseki and P. gracilis.

Although holoplankton are ocean drifters and exhibit high dispersal potential, a number of studies on single species are finding highly divergent genetic clades. These cryptic species complexes are important to discover and describe, as identification of common marine species is fundamental to understanding ecosystem dynamics. Here we investigate the global diversity within Pleuromamma piseki and P. gracilis, two dominant members of the migratory zooplankton assemblage in subtropical and tropical waters worldwide. Using DNA sequence data from the mitochondrial gene cytochrome c oxidase subunit II (mtCOII) from 522 specimens collected across the Pacific, Atlantic and Indian Oceans, we discover twelve well-resolved genetically distinct clades in this species complex (Bayesian posterior probabilities >0.7; 6.3–17% genetic divergence between clades). The morphologically described species P. piseki and P. gracilis did not form monophyletic groups, rather they were distributed throughout the phylogeny and sometimes co-occurred within well-resolved clades: this result suggests that morphological characters currently used for taxonomic identification of P. gracilis and P. piseki may be inaccurate as indicators of species’ boundaries. Cryptic clades within the species complex ranged from being common to rare, and from cosmopolitan to highly restricted in distribution across the global ocean. These novel lineages appear to be ecologically divergent, with distinct biogeographic distributions across varied pelagic habitats. We hypothesize that these mtDNA lineages are distinct species and suggest that resolving their systematic status is important, given the ecological significance of the genus Pleuromamma in subtropical-tropical waters worldwide.

Can AFLP genome scans detect small islands of differentiation? The case of shell sculpture variation in the periwinkle Echinolittorina hawaiiensis

Genome scans have identified candidate regions of the genome undergoing selection in a wide variety of organisms, yet have rarely been applied to broadly dispersing marine organisms experiencing divergent selection pressures, where high recombination rates can reduce the extent of linkage disequilibrium (LD) and the ability to detect genomic regions under selection. The broadly dispersing periwinkle Echinolittorina hawaiiensis exhibits a heritable shell sculpture polymorphism that is correlated with environmental variation. To elucidate the genetic basis of phenotypic variation, a genome scan using over 1000 AFLP loci was conducted on smooth and sculptured snails from divergent habitats at four replicate sites. Approximately 5% of loci were identified as outliers with Dfdist, whereas no outliers were identified by BayeScan. Closer examination of the Dfdist outliers supported the conclusion that these loci were false positives. These results highlight the importance of controlling for Type I error using multiple outlier detection approaches, multitest corrections and replicate population comparisons. Assuming shell phenotypes have a genetic basis, our failure to detect outliers suggests that the life history of the target species needs to be considered when designing a genome scan.

Molecules and fossils reveal punctuated diversification in Caribbean "faviid" corals.

BackgroundEven with well-known sampling biases, the fossil record is key to understanding macro-evolutionary patterns. During the Miocene to Pleistocene in the Caribbean Sea, the fossil record of scleractinian corals shows a remarkable period of rapid diversification followed by massive extinction. Here we combine a time-calibrated molecular phylogeny based on three nuclear introns with an updated fossil stratigraphy to examine patterns of radiation and extinction in Caribbean corals within the traditional family Faviidae.ResultsConcatenated phylogenetic analysis showed most species of Caribbean faviids were monophyletic, with the exception of two Manicina species. The time-calibrated tree revealed the stem group originated around the closure of the Tethys Sea (17.0 Ma), while the genus Manicina diversified during the Late Miocene (8.20 Ma), when increased sedimentation and productivity may have favored free-living, heterotrophic species. Reef and shallow water specialists, represented by Diploria and Favia, originate at the beginning of the Pliocene (5 – 6 Ma) as the Isthmus of Panama shoaled and regional productivity declined.ConclusionsLater origination of the stem group than predicted from the fossil record corroborates the hypothesis of morphological convergence in Diploria and Favia genera. Our data support the rapid evolution of morphological and life-history traits among faviid corals that can be linked to Mio-Pliocene environmental changes.

Fifteen new microsatellite markers for the reef coral Favia fragum and a new Symbiodinium microsatellite.

Sixteen new microsatellite loci were isolated from the Tropical Atlantic coral Favia fragum. One locus amplified with pure zooxanthellae DNA template, revealing a symbiont (Symbiodinium) origin. We genotyped 48 short and 45 tall ecomorphs of F. fragum from the Bocas del Toro region of Panama. For 15 host loci, allelic diversity ranged from three to 23 with an average of 5.75 alleles per locus. Analysis of genotypic data revealed significant heterozygote deficits at all loci and linkage disequilibrium between loci, as did a previous study of the two ecomorphs with allozymes. We found evidence for null alleles at four of the host loci in the form of locus‐specific polymerase chain reaction failure; however, extreme inbreeding via self‐fertilization is likely to explain the large departures from Hardy–Weinberg equilibrium.