Microsatellite abundance across the Anthozoa and Hydrozoa in the phylum Cnidaria

Background: Microsatellite loci have high mutation rates and thus are indicative of mutational processes within the genome. By concentrating on the symbiotic and aposymbiotic cnidarians, we investigated if microsatellite abundances follow a phylogenetic or ecological pattern. Individuals from eight species were shotgun sequenced using 454 GS-FLX Titanium technology. Sequences from the three available cnidarian genomes (Nematostella vectensis, Hydra magnipapillata and Acropora digitifera) were added to the analysis for a total of eleven species representing two classes, three subclasses and eight orders within the phylum Cnidaria. Results: Trinucleotide and tetranucleotide repeats were the most abundant motifs, followed by hexa- and dinucleotides. Pentanucleotides were the least abundant motif in the data set. Hierarchical clustering and log likelihood ratio tests revealed a weak relationship between phylogeny and microsatellite content. Further, comparisons between cnidaria harboring intracellular dinoflagellates and those that do not, show microsatellite coverage is higher in the latter group. Conclusions: Our results support previous studies that found tri- and tetranucleotides to be the most abundant motifs in invertebrates. Differences in microsatellite coverage and composition between symbiotic and non-symbiotic cnidaria suggest the presence/absence of dinoflagellates might place restrictions on the host genome

Mendelian microsatellite loci for the Caribbean coral Acropora palmata

The genus Acropora constitutes the most species-rich clade of hermatypic corals, and its members are important reef builders throughout their broad tropical range. In the Caribbean, acroporid populations have declined over the last 2 decades due to disease, hurricanes, predation, and bleaching episodes, and some are now subjects of conservation efforts. Genetic estimates of population connectivity and clonal structure should be part of these efforts, but such studies have been hampered by low levels of mitochondrial DNA variation in corals, and an apparent dearth of variable single-copy nuclear markers. Developing microsatellite markers in Acropora has proven especially difficult. We used Southern blotting to reveal that, indeed, some microsatellite motifs (AAC, AAG) are rare in the genome of the Caribbean species Acropora palmata. However, repeats with the motif AAT are both abundant and variable. We developed 8 polymorphic microsatellite markers for A. palmata, and performed crosses to confirm co-dominant inheritance patterns. Five of the 8 markers tested show simple Mendelian inheritance (mean observed heterozygosity = 0.84, mean number of alleles per locus = 8.6). Along with outcrossed sexual larvae, individual egg donors also produced some triploid and selfed larvae that developed normally and survived for 80 h, when the experiment was terminated. The markers reveal variation among 3 Florida populations of A. palmata and among clones within 1 of these populations. Seven of the markers amplify DNA from A. cervicornis and 8 from the hybrid A. prolifera. These markers should prove to be valuable tools for developing conservation strategies for Caribbean acroporid species. © Inter-Research 2005

Geographic variation in clonal structure in a reef-building Caribbean coral, Acropora palmata

Species that build the physical structure of ecosystems often reproduce clonally, both in terrestrial (e.g., grasses, trees) and marine (e.g., corals, seagrasses) environments. The degree of clonality may vary over a species\u27 range in accordance with the relative success of sexual and asexual recruitment. High genotypic (clonal) diversity of structural species may promote the species diversity and resilience of ecosystems in the face of environmental extremes. Conversely, low genotypic diversity may indicate an asexual strategy to maintain resources and genetic variation during population decline. Here, we use microsatellite markers to assess geographic variation in clonality in the coral Acropora palmata sampled from 26 reefs in eight regions spanning its tropical western Atlantic range (n=751). Caribbean-wide, the ratio (±SD) of genets (Ng) to sampled ramets (N) was 0.51 ± 0.28. Within reefs (30-70 m) and among reefs (10-100 km) within regions, clonal structure varied from being predominantly asexual (Ng/N approaching 0) to purely sexual (N g/N = 1). However, two genetically isolated regions (western and eastern Caribbean) differed in clonal structure: genotypically depauperate populations (Ng/N=0.43 ± 0.31) with lower densities (0.13 ± 0.08 colonies/m2) characterized the western region, while denser (0.30 ± 0.21 colonies/m2), genotypically rich stands (Ng/N = 0.64 ± 0.17) typified the eastern Caribbean. Genotypic richness (standardized to sample size; Ng/N) and genotypic diversity (Go/Ge) were negatively related to colony density within each province (r2 = 0.49-0.66, P \u3c 0.001), indicating that dense stands have higher rates of asexual recruitment than less dense populations. Asexual recruitment was not correlated with largescale disturbance history or abundance of large colonies (potential fragment sources) but was negatively correlated with shelf area (r2 = 0.57, P \u3c 0.01). We argue that sexual recruitment is more prevalent in the eastern range of A. palmata than the west, and that these geographic differences in the contribution of reproductive modes to population structure may be related to habitat characteristics. The two populations of the threatened A. palmata differ fundamentally in reproductive character and may respond differently to environmental change. © 2006 by the Ecological Society of America

Regionally isolated populations of an imperiled Caribbean coral, Acropora palmata

The movements of larvae between marine populations are difficult to follow directly and have been the subject of much controversy, especially in the Caribbean. The debate centres on the degree to which populations are demographically open, such that depleted populations can be replenished by recruitment from distant healthy populations, or demographically closed and thus in need of local management. Given the depressed state of many tropical reef populations, the understanding of these movements now bears critically on the number, placement, and size of marine reserves. Most genetic analyses assume that dispersal patterns have been stable for thousands of generations, thus they commonly reflect past colonization histories more than ongoing dispersal. Recently developed multilocus genotyping approaches, however, have the demonstrated ability to detect both migration and population isolation over far shorter timescales. Previously, we developed five microsatellite markers and demonstrated them to be both Mendelian and coral-specific. Using these markers and Bayesian analyses, we show here that populations of the imperiled reef-building coral, Acropora palmata, have experienced little or no recent genetic exchange between the western and the eastern Caribbean. Puerto Rico is identified as an area of mixing between the two subregions. As a consequence of this regional isolation, populations in the western and eastern Caribbean should have the potential to adapt to local conditions and will require population-specific management strategies. © 2005 Blackwell Publishing Ltd

Unrecognized coral species diversity masks differences in functional ecology

Porites corals are foundation species on Pacific reefs but a confused taxonomy hinders understanding of their ecosystem function and responses to climate change. Here, we show that what has been considered a single species in the eastern tropical Pacific, Porites lobata, includes a morphologically similar yet ecologically distinct species, Porites evermanni. While P. lobata reproduces mainly sexually, P. evermanni dominates in areas where triggerfish prey on bioeroding mussels living within the coral skeleton, thereby generating asexual coral fragments. These fragments proliferate in marginal habitat not colonized by P. lobata. The two Porites species also show a differential bleaching response despite hosting the same dominant symbiont subclade. Thus, hidden diversity within these reef-builders has until now obscured differences in trophic interactions, reproductive dynamics and bleaching susceptibility, indicative of differential responses when confronted with future climate change. © 2013 The Author(s) Published by the Royal Society

Fallen Pillars: The Past, Present, and Future Population Dynamics of a Rare, Specialist Coral–Algal Symbiosis

With ongoing changes in climate, rare and ecologically specialized species are at increased risk of extinction. In sessile foundation fauna that reproduce asexually via fragmentation of existing colonies, the number of colonies does not reflect the number of genets and thus can obscure genotypic diversity. Colonies that are the product of fragmentation are not visually distinguishable from colonies that stem from sexual recruits. For this reason, molecular markers are necessary to assess genotypic variation and population structure in clonal organisms such as reef-building corals and their endosymbiotic dinoflagellates. For the rare Caribbean pillar coral, Dendrogyra cylindrus, and its endosymbiotic dinoflagellate, Breviolum dendrogyrum, we use de novo microsatellite markers to infer past demographic changes, describe modern population structure, and quantify the frequency of asexual reproduction. Our analyses show that D. cylindrus comprises three distinct populations across the Greater Caribbean whereas the symbiont could be differentiated into four populations, indicating barriers to gene flow differ between host and symbiont. In Florida, host and symbiont populations reproduced mainly asexually, yielding lower genotypic diversity than predicted from census size. When multiple coral ramets were present, they often associated with the same clonal strain of B. dendrogyrum, pointing to the high fidelity of this relationship. Models of past demographic events revealed no evidence for historical changes in population sizes, consistent with the paleontological record of D. cylindrus indicating it has been rare for hundreds of thousands of years. The most recent global thermal stress event likely triggered a severe disease outbreak among D. cylindrus in Florida, resulting in a severe population decline. Projections indicate a high likelihood that this species will become extinct in the Northern Greater Caribbean within a few decades. The ecosystem consequences of losing rare coral species and their symbionts with increasingly frequent extreme warming events are not known but require urgent study

Rapid Recovery of a Coral Reef at Darwin Island, Galapagos Islands

Surveys at Darwin Island in 2006 and 2007 have demonstrated that this northernmost Galapagos Islands coral reef has recovered significantly since the 1982–3 El Niño event. When first surveyed in 1975, this structural reef exhibited actively accreting frameworks of pocilloporid and poritid corals. The coral suffered severe mortality in 1983, resulting in the near total loss of pocilloporids and extensive partial mortality of poritid corals. Large sections of the reef had not recovered by 1992 and dead frameworks were subject to bio-erosion, although small numbers of sexual recruits of pocilloporid corals and numerous recruits plus regenerating patches of Porites lobata were present in some areas. An increase in live coral cover and recruitment was apparent through 2000 and 2002. Recent sampling at three sites along the reef has demonstrated mean (± 1 SD) live coral cover of 21.9 ± 1.7 % with P. lobata as the predominant species. Pocillopora spp. were present, but not so abundant as in earlier surveys. In spite of moderate erosion by echinoid and fish grazers, much of the original coral framework remained intact, providing a substrate for coral regeneration and recruitment. Recovery can be attributed to the original reef structure remaining intact, asexual regrowth of surviving tissues and sexual recruitment of poritid corals from surviving source populations

Getting a grip at the edge: recolonization and introgression in eastern Pacific Porites corals

© 2016 John Wiley & Sons Ltd Aim: To infer species identity, population isolation, and geographical variation in inter-specific hybridization among corals of the genus Porites from the central and eastern tropical Pacific, with a focus on the timing of separation between populations of P. evermanni and P. lobata divided by the Eastern Pacific Barrier. Location: Hawaii, American Samoa, Panama and the Galapagos Islands of Ecuador. Methods: Maximum likelihood gene trees were obtained for mitochondrial DNA (COI), the internal transcribed spacer (ITS), and 5 single-copy nuclear (scn) gene regions. Allelic networks were used to group multi-locus scn data into species clusters despite some allele sharing. Coalescent analyses (IMa2) of the 5 scn markers were used to estimate the time of population divergence and test for introgression between P. evermanni and P. lobata. Results: Allelic networks based on scn gene sequences agreed with mtCOI and ITS designations. Divergence times between Hawaiian and eastern Pacific populations are consistent with an early Pleistocene recolonization of the eastern Pacific by P. evermanni followed by a more recent arrival of P. lobata. The two species were fully isolated in Hawaii/American Samoa populations, but introgression from P. evermanni into P. lobata was evident in the eastern Pacific. Main conclusions: These results are consistent with a scenario where a bout of introgression with P. evermanni, an early-arriving colonizer of the eastern Pacific suited to marginal environmental conditions, facilitated the later colonization of the more sensitive P. lobata

Marginal Coral Populations: the Densest Known Aggregation of Pocillopora in the Galápagos Archipelago is of Asexual Origin

Coral populations at distributional margins frequently experience suboptimal and variable conditions. Recurrent El Niño-Southern Oscillation (ENSO) warming events have caused extensive mortality of reef-building corals in the Eastern Pacific, and particularly impacted branching pocilloporid corals in the Galápagos Islands. Pocillopora spp. were previously more common and formed incipient reefs at several locations in the archipelago but now occur as scattered colonies. Here, we report an unusually concentrated aggregation of colonies and evaluate their current genetic diversity. In particular we focus on a large population of 1614 live Pocillopora colonies found in a volcanic lagoon along the southern shore of Isabela Island. Forty seven colonies were sampled, primarily using a spatially explicit sampling design, and all colonies belonged to Pocillopora mitochondrial open reading frame lineage type 3a. Typing of additional Pocillopora samples (n = 40) from three other islands indicated that this stand is the only known representative of type 3a in the Galápagos Islands. The Isabela Pocillopora type 3a colonies harbored Symbiodinium ITS-2 clade C1d. Multilocus genotyping (n = 6 microsatellites) capable of resolving individual clones indicated that this stand is monogenotypic and thus the high density of colonies is a result of asexual reproduction, likely via fragmentation. Colony size distribution, while an imperfect measure, suggested the stand regrew from remnant colonies that survived the 1997/98 ENSO event but may postdate the 1982/83 ENSO. The community of Pocillopora colonies at Isabela is of particular ecological value due to its high density and support of associated organisms such as fish and benthic invertebrates. The Galapagos Pocillopora corals will continue to provide insights into the genetic structure and population dynamics of marginal coral populations

The impact of estimator choice: Disagreement in clustering solutions across K estimators for Bayesian analysis of population genetic structure across a wide range of empirical data sets

The software program STRUCTURE is one of the most cited tools for determining population structure. To infer the optimal number of clusters from STRUCTURE out- put, the ΔK method is often applied. However, a recent study relying on simulated microsatellite data suggested that this method has a downward bias in its estimation of K and is sensitive to uneven sampling. If this finding holds for empirical data sets, conclusions about the scale of gene flow may have to be revised for a large number of studies. To determine the impact of method choice, we applied recently described es- timators of K to re-estimate genetic structure in 41 empirical microsatellite data sets; 15 from a broad range of taxa and 26 from one phylogenetic group, coral. We com- pared alternative estimates of K (Puechmaille statistics) with traditional (ΔK and pos- terior probability) estimates and found widespread disagreement of estimators across data sets. Thus, one estimator alone is insufficient for determining the optimal num- ber of clusters; this was regardless of study organism or evenness of sampling scheme. Subsequent analysis of molecular variance (AMOVA) did not necessarily clarify which clustering solution was best. To better infer population structure, we suggest a com- bination of visual inspection of STRUCTURE plots and calculation of the alternative estimators at various thresholds in addition to ΔK. Disagreement between traditional and recent estimators may have important biological implications, such as previously unrecognized population structure, as was the case for many studies reanalysed here