Coral reefs in the Tropical Eastern Pacific (TEP) are amongst the most peripheral and geographically isolated in the world. This isolation has shaped the biology of TEP organisms and lead to the formation of numerous endemic species. For example, the coral Pocillopora damicornis is a minor reef-builder elsewhere in the Indo-West Pacific, but is the dominant reef-building coral in the TEP, where it forms large, mono-specific stands, covering many hectares of reef. Moreover, TEP P. damicornis reproduces by broadcast spawning, while it broods mostly parthenogenetic larvae throughout the rest of the Indo-West Pacific. Population genetic surveys for P. damicornis from across its Indo-Pacific range indicate that gene flow (i.e. larval dispersal) is generally limited over hundreds of kilometers or less. Little is known about the population genetic structure and the dispersal potential of P. damicornis in the TEP.
Using multilocus microsatellite data, we analyzed the population structure of TEP P. damicornis among and within nine reefs and test for significant genetic structure across three geographically and ecologically distinct regions in Panama.
We detected significant levels of population genetic structure (global RST = 0.162), indicating restricted gene flow (i.e. larvae dispersal), both among the three regions (RRT = 0.081) as well as within regions (RSR = 0.089). Limited gene flow across a distinct environmental cline, like the regional upwelling gradient in Panama, indicates a significant potential for differential adaptation and population differentiation. Individual reefs were characterized by unexpectedly high genet diversity (avg. 94%), relatively high inbreeding coefficients (global FIS = 0.183), and localized spatial genetic structure among individuals (i.e. unique genets) over 10 m intervals. These findings suggest that gene flow is limited in TEP P. damicornis populations, particularly among regions, but even over meter scales within populations.
Citation: Combosch DJ, Vollmer SV (2011) Population Genetics of an Ecosystem-Defining Reef Coral Pocillopora damicornis in the Tropical Eastern Pacific. PLoS ONE 6(8): e21200. https://doi.org/10.1371/journal.pone.0021200
Editor: Debashish Bhattacharya, Rutgers University, United States of America
Received: February 4, 2011; Accepted: May 23, 2011; Published: August 9, 2011
Copyright: © 2011 Combosch and Vollmer. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
Funding: Funding was provided to DJC by the German Academic Exchange Service (DAAD). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
Competing interests: The authors have declared that no competing interests exist.
Populations at the periphery of species' distribution ranges often exist in suboptimal and/or unstable conditions at the organism's physiological or ecological limits . They tend to be small as well as geographically and genetically isolated from central core populations , . Their small population sizes and genetic isolation increase genetic drift and inbreeding and limit genetic diversity and cohesiveness among populations , , . As a result, peripheral populations tend to have reduced genetic diversity and are often heavily reliant on local sources of recruitment rather than long-distance recruitment from core populations [e.g. 7,8,9,10]. Their isolation and low levels of genetic diversity may also hamper their ability to cope with environmental changes (e.g. global climate change) and to recover from disturbances, making them more vulnerable to extinction , . However, small population sizes in genetic isolation can also facilitate local selection and adaptation, give rise to evolutionary innovation  and allow peripheral populations to exploit new ecological niches , .
One of the most isolated and peripheral biogeographic regions of the world's oceans is the Tropical Eastern Pacific (TEP). It is separated from the Indo-West Pacific by 5000 km of open-ocean that Darwin  described as “impassable” for shallow water marine species , . While not completely impassable, the marine fauna of the TEP consists of a limited subset of trans-Pacific species (i.e. species distributed across the Pacific), which are typically interconnected by low levels of gene flow [e.g. 19,20,21,22,23,24,25], as well as numerous endemic species , , . For example, 34 species of reef-building corals are recognized in the TEP (compared to 581 in the Western Pacific), of which 27 are trans-Pacific (80%) and seven (20%) are regional endemics . Major environmental challenges for reef corals in the TEP include significant freshwater discharges and seasonal upwelling, leading to high turbidity, elevated nutrient levels and reduced seawater temperatures. Reef habitats in the TEP are confined mostly to a narrow continental shelf and often fragmented by long stretches of estuaries, mangroves and sandy beaches , .
The isolation of the TEP from the Indo-West Pacific and major differences in environmental factors and species compositions between these regions enabled significant ecological and life-history shifts in many TEP species. For example, the scleractinian coral Pocillopora damicornis is a minor reef-building coral in the Indo-West Pacific, but the primary reef-builder in the TEP , , . Pocillopora damicornis in the TEP forms large, mono-specific carpets measuring tens to hundreds of hectares , that are thought to be maintained predominantly by asexual (i.e. vegetative) fragmentation , . Moreover, while Indo-West Pacific P. damicornis populations brood mostly asexual (parthenogenetic) larvae , , populations in the TEP reproduce by broadcast-spawning its gametes . This reproductive shift could have important genetic consequences since a broadcast spawning coral should not be able to produce parthenogenic larvae ,  and because broadcast spawning corals are often considered to have higher dispersal potentials than brooding corals [e.g. 41,42,43,44,45], particularly over small spatial scales , , , , but see , . Hermaphroditic broadcast-spawning corals might also have a higher potential for selfing and inbreeding resulting from external fertilization , , .
Population genetic surveys among larvae-brooding P. damicornis populations across the Indo-West Pacific indicate that larval dispersal (i.e. gene flow) is generally limited over hundreds of kilometers [e.g. 55,56,57] and in some cases even among neighboring reefs [e.g. 57,58,59]. Some of the highest levels of genetic structure have been described at the margins of P. damicornis Indo-Pacific range , , , . For example, populations in South-East Australia are more genetically distinct over 700 km [FST = 0.32; 56] than more central Great Barrier Reef populations over 1200 km [FST = 0.06; 61]. Most studied populations of P. damicornis in the Indo-West Pacific also showed significant levels of local inbreeding and contained some level of clonality , , , , .
Little is known about the population structure of broadcast-spawning P. damicornis populations in the TEP. Combosch et al.  documented evidence for restricted transpacific dispersal between Central and Eastern Pacific populations of P. damicornis, using ribosomal DNA sequence data (FST = 0.419, p<0.001). Using multilocus genetic data, Pinzon & LaJeunesse  examined the genetic structure among multiple TEP Pocillopora species, including 7 well-recognized Indo-Pacific species (P. damicornis, P. eydouxi, P. meandrina, P. verrucosa, P. capitata, P. elegans, P. woodjonesi). They identified three genetic clusters or types (Type I, II & III) in their multi-species TEP sample of Pocillopora. All three of these types were found in P. damicornis from across the TEP. Type I was found throughout the TEP, including Panama, Type II was found only in Clipperton Atoll and Type III was found in Panama and Galapagos. Yet, no genetic structure was detected within the broadly distributed Type I group over 3500 km of the TEP.
One of the best-studied areas in the TEP is the Pacific coast of Panama, which is dominated by two major gulfs, the Gulf of Chiriqui in the west and the Gulf of Panama in the east. The two gulfs differ in several important ecological factors , , , , , , , most notably in the strength of seasonal upwelling, which is strong in the Gulf of Panama, but virtually absent in the Gulf of Chiriqui , . The Azuero Peninsula, which separates the two gulfs, is a transition zone with moderate upwelling . Corals from the two gulfs differ significantly in their thermal tolerances ,  and ability to recover from major disturbances like El-Niño induced bleaching events .
Using multilocus microsatellite data, we examined the population genetic structure of TEP P. damicornis within and among nine Panamanian populations across the three geographically and ecologically distinct regions (Figure 1). Based on the strong geographic and ecologic differences between the three regions, we predicted significant regional differences in P. damicornis population genetic structure. Within reefs, we analyzed spatial patterns of genetic diversity to estimate the relative contributions of clones versus unique genets to localized spatial genetic structure (SGS). We predict that high rates of vegetative fragmentation should lead to significant SGS due to clonal aggregations. In contrast, high rates of sexual reproduction by broadcast spawning should inhibit SGS due to increased outcrossing and the mixing of genotypes at the sea surface during larval development.
The pie charts show the distribution of the five genetic clusters identified by STRUCTURE 2.3  in the three regional and nine reef populations. The bar plot shows each individual sample as a vertical bar with colors indicating the relative proportions of each genetic cluster. Map created on www.aquarius.ifm-geomar.de. U = Uva Island; C = Canal de Afuera Island; G = Granito de Oro Island; B = Bahia de Damas, Coiba Island; A = Achotines Bay; I = Iguana Island; S = Saboga Island; Co = Contadora Island; T = Taboga Island.
Genetic diversity, heterozygosity and clonality
Multilocus microsatellite data (n≥5 loci) was obtained for 207 Pocillopora damicornis colonies from nine reef populations (Tables 1 and 2). The six amplified loci yielded between four and ten alleles each (mean NA = 7). Three pairs of loci showed indications of significant linkage disequilibria, but none showed consistent significant linkage disequilibria in more than two populations. Consequently, all six loci were considered as unlinked. Significant heterozygote deficits were detected in five loci (Table 1), but only Pv2 showed significant deficits in all populations, which is indicative of null alleles. The program Micro-Checker confirmed the presence of null alleles in Pv2, which was then excluded from further analyses.
Using the five remaining loci, 194 unique genets were identified with a high probability of identity (p<3×10−5; Table 2) among the 207 genotyped samples. All nine populations were comprised predominantly of unique, i.e. sexually derived genets (93.8±5.5%). Clonal genotypes were detected in all but two populations (Canal & Iguana), but only Saboga (Gulf of Panama) contained more than two clones (n = 4, i.e. 18%). No clonal genotypes were shared among populations, in contrast to larvae-brooding Indo-West Pacific populations , . Since clones introduce biases into population genetic analyses, only unique genets were used in subsequent analyses, unless otherwise noted.
Using the genet only dataset, significant heterozygote deficits were detected in six out of the nine populations (Table 2), indicating widespread local inbreeding. Inbreeding was significant in the Gulf of Panama (FIS = 0.255±0.122) and in the Gulf of Chiriqui (FIS = 0.196±0.171), but not in the Azuero Peninsula (FIS = 0.048±0.135) due to an excess of heterozygotes in Achotines. Each population contained on average 4.7 alleles per locus. Slightly more alleles were detected in the Gulf of Chiriqui (avg. NA = 5.1±0.26) than in the Azuero Peninsula (4.5±0.20) and in the Gulf of Panama (4.3±0.31). Interestingly, private alleles were only found in Gulf of Chiriqui populations, which contained the only regional-specific allele (Pd2, 223 bp) as well.
Genetic Structure among reefs and regions
Hierarchical AMOVA revealed significant levels of population genetic structure (p<0.005) among populations, among regions, and among populations within regions (Table 3). Genetic structure among populations was highly significant for both global RST (0.162; p<0.001) and global FST (0.053; p<0.001). For the R-statistics, population structure was equivalent among regions (RRT = 0.081) and among populations within regions (RSR = 0.089). All three regions were significantly different from each other (p<0.001), but the two gulf regions were most distinct (pairwise RST = 0.138), whereas the Azuero Peninsula, which lies between the two gulfs, showed lower pairwise genetic structure (Gulf of Chiriqui RST = 0.070; Gulf of Panama RST = 0.101). For the F-statistics, population structure was predominantly due to differences among populations within regions (FSR = 0.045; Table 3).
Fourteen out of 36 pairwise RST comparisons between populations were significant after sequential Bonferroni adjustments (Table 4). Twelve of the significant pairwise RSTs were between populations from different regions, whereas only two comparisons within regions were significant, both involving the Gulf of Chiriqui population Granito. These strong regional differences can be seen as well in the principal coordinate analyses, where populations cluster into distinct regional groupings (Figure 2). However, no significant isolation-by-distance pattern was observed among populations (p = 0.013).
Distances between populations were analyzed as RST pairwise genetic distances. The two axes explained 90.4% of the total variation. Blue circles = Populations in the Gulf of Chiriqui; Red triangles = Azuero Peninsula; Green squares = Gulf of Panama.
Bayesian clustering implemented in STRUCTURE detected five genetic clusters in the dataset (Figure S1). All five clusters were found in each population, but their distribution differed significantly among populations and particularly among regions (Figure 1). The genetic clusters 1 and 2 were most common in the Gulf of Chiriqui (28% & 25%, respectively), clusters 4 and 5 were most prevalent in the Gulf of Panama (22% & 39%) and cluster 3 was dominant in the Azuero Peninsula (32%). Cluster 1 and 2 were also common in the Azuero Peninsula (23% and 24%), which indicates that its P. damicornis populations are more similar to the Gulf of Chiriqui than to the Gulf of Panama - as indicated by the pairwise RST values.
Fine-scale spatial genetic structure (SGS) on reefs
In addition to the genetic structure among regions and populations, strong fine-scale spatial genetic structure (SGS) was detected among individuals within reefs. SGS was significant over 10 m intervals in both the ramet dataset (i.e. including clones; Framets = 0.102; p<0.001) and the genet dataset (i.e. excluding clones; Fgenets = 0.086, p<0.001). This indicates that corals 10 meters apart are significantly more closely related to each other than to the rest of the population. Kinship among individuals (Fij) was only slightly elevated when clones were included, reflecting the low frequency of clones in the dataset (Figure 3). While SGS is to be expected in coral populations due to clonal aggregations as a consequence of asexual (vegetative) fragmentation, significant SGS in the genet dataset indicates that the observed structure is due to non-random spatial relatedness among distinct, i.e. sexually produced, genets. Across all nine populations, the average genetic patch size (i.e. the distance at which individuals on average are as related as across the entire population) was 50 m and the Sp statistic was 0.055 [i.e. rather high compared to plant literature data; 78].
Black lines represent the genet dataset, excluding clones and grey lines show the results for the ramet dataset, including clones. Dashed lines are the permuted 95% confidence intervals. Error bars are 95% bootstrap errors of the genet datasets. Figure 3a) Spatial correlogram of the average pairwise kinship Fij  as a function of distance over all populations. Figure 3b–d) Spatial correlograms over the populations in each of the three regions, b) the Gulf of Chiriqui, c) the Azuero Peninsula and d) the Gulf of Panama.
Significant levels of SGS out to 10 m were detected in all three regions (p<0.05; Figure 3b–d). Average F10m-kinship in the Azuero Peninsula and Gulf of Panama was similarly high (F10m ∼0.109), almost equivalent to a first-cousin relatedness (FIJ = 0.125) whereas F10m-kinship in the Gulf of Chiriqui was two times lower (0.059; p<0.05). The genetic patch size was almost twice as large in the Gulf of Panama (70 m) than in the Gulf of Chiriqui and Azuero Peninsula (40 m). These differences in the strength and extent of SGS are reflected in the Sp statistic, which indicates that SGS is strongest in the western Gulf of Panama (0.062), intermediate in the central Azuero Peninsula (0.059) and lowest in the eastern Gulf of Chiriqui (0.049).
The Tropical Eastern Pacific (TEP) is one of the most geographically isolated biogeographic regions in the world's oceans . Its isolation has profound consequences for the diversity and ecology of TEP ecosystems, most notably coral reefs . TEP coral reefs are remarkable since they are built predominantly by Pocillopora damicornis , , . TEP P. damicornis also distinguish by its broadcast gamete-spawning reproductive strategy. Multilocus microsatellite data from nine Panamanian populations demonstrate that TEP P. damicornis populations from Panama are characterized by strong population genetic structure (RST = 0.162), within and particularly among its three major regions, the Gulf of Chiriqui, the Azuero Peninsula and the Gulf of Panama. Moreover, the large and mono-specific stands of P. damicornis that characterize TEP reefs are not dominated by a few, highly clonal genotypes as previously thought , , but instead are comprised of numerous distinct genets, indicating frequent sexual reproduction. Significant fine-scale spatial genetic structure (SGS) among individual genets and highly significant levels of heterozygote deficits further indicate widespread inbreeding and limited gene dispersal over meter scales, which is unusual for free-spawners. These tiered layers of significant population genetic structure indicate that gene flow (i.e. larval dispersal) is restricted among and within reefs, particularly between the environmentally distinct regions, which indicates a significant potential for regional adaptations to the different ecological conditions in each region.
As hypothesized, we detected strong genetic differences among the three geographically and ecologically distinct regions in Panamanian P. damicornis populations (RRT = 0.081). Panama's two major gulfs – the Gulf of Chiriqui and the Gulf of Panama - which are geographically most distant, were most genetically distinct (RST = 0.138). These genetic differences correspond with pronounced ecological differences between these two regions, e.g. in species compositions and environmental factors [e.g. 38,67,73]. The most significant environmental difference is the pattern of seasonal upwelling, which is strong in the Gulf of Panama dropping temperatures down to 15°C, but is virtually absent in the Gulf of Chiriqui , . The Azuero Peninsula, which bisects the two regions, is a transition zone with intermediate upwelling conditions . It also has intermediate levels of genetic structure compared to the other regions (RST = 0.070 & 0.101).
Upwellings deliver cool, nutrient-rich waters to the near-shore environment. In tropical habitats like the TEP, they have significant impacts on nutrient and temperature-sensitive reef fauna , . In the TEP, variations in the severity of upwelling restrict the regional and local distributions of coral reefs ,  and of major reef taxa, including corals  and key corallivores like the sea star Acanthaster planci . Lower temperatures associated with seasonal upwellings reduce reef development , coral growth rates  and coral reproduction , while elevated nutrients increase competition with algae , , bioerosion  and water turbidity . Corals from regions with different upwelling regimes often display different thermal tolerances, indicating local adaptations. For example, P. damicornis from the non-upwelling Gulf of Chiriqui are less sensitive to higher temperatures than those from the upwelling Gulf of Panama , . Similar differences in thermal adaptation among P. damicornis populations have also been reported from the Great Barrier Reef . Yet, upwellings can also buffer against critically high sea surface temperatures and reduce coral bleaching and mortality. For example, during the 1997/98 El-Niño, seasonal upwelling in the Gulf of Panama reduced rising seawater temperatures (mean 27°C), preventing significant coral bleaching and mortality. In contrast, at the same time in the non-upwelling Gulf of Chiriqui, mean seawater temperature rose to 30°C causing severe coral bleaching and mortality . While reefs in upwelling environments may thus be better able to weather predicted increases in sea surface temperatures and El Niño frequencies resulting from global climate change [e.g. 81], coral populations in non-upwelling habitats seem to be better adapted to elevated temperatures , . The genetic structure of Panamanian P. damicornis indicates that even among broadcast-spawning coral populations, adaptations to different thermal regimes can occur over distances of ∼100 km.
Limited inter-regional gene flow in Panamanian P. damicornis may also explain prolonged differences in post-disturbance reef recovery between the Gulf of Chiriqui and the Gulf of Panama. For example, the 1982/83 El Niño caused mass coral mortalities and reduced average coral cover on most Panamanian reefs by 80%, but even though mortality rates were similar in both gulfs, reefs in the Gulf of Panama had recovered by 1992, whereas reefs in the Gulf of Chiriqui recovered only 3–6% of their populations by 1997 . The significant population genetic structure between regions indicates that larval dispersal from recovered Gulf of Panama populations to the still depauperate Gulf of Chiriqui populations was very limited and this may have prolonged the recovery of reefs in the Gulf of Chiriqui. Moreover, due to the limited gene flow (i.e. larval dispersal) between individual reefs, damaged populations depended strongly on surviving colonies for repopulation. Acanthaster predation on surviving colonies in the Gulf of Chiriqui potentially hampered initial recovery significantly, while corallivorous sea stars are absent in the Gulf of Panama. Another important factor for the differences in P. damicornis recovery between Gulfs may be geographic differences in Symbiodinium identity (or type). Baker et al  showed that in the Gulf of Panama, Pocillopora corals with clade C bleached severely in 1997 while colonies with clade D were unaffected by bleaching, which lead to a relative increase in colonies with clade D from 43% in 1995 to 63% in 2001. Higher levels of clonality in the Gulf of Panama (e.g. Saboga) further indicate that asexual fragmentation might have played a more prominent role in the recovery of Gulf of Panama populations compared to their Gulf of Chiriqui counterparts.
Using multiple genetic markers, Pinzon & LaJeunesse  recently suggested that TEP Pocillopora are comprised of three distinct genetic types (Type I–III), independent of species identity and morphology. This is controversial because they included at least seven well-recognized Indo-Pacific species that must then either be reclassified or synonymized by their genetic types. Their dataset included a limited number of P. damicornis samples from the Gulf of Panama (n = 26), which were comprised of two of the three genetic types (Type I & II). Using a similar set of microsatellites, our STRUCTURE analyses do not support two distinct genetic types, but instead identified five genetic clusters (Figure 1 & Figure S1). In addition, Pinzon & LaJeunesse  failed to detect significant genetic structures within their Pocillopora type I over 3500 km from Mexico to Panama and the Galapagos. Given that we observe strong genetic structure in P. damicornis within Panama, it seems likely that the absence of geographic structure in Pinzon & LaJeunesse's  analyses are an artifact of pooling multiple species (i.e. gene pools) for population genetic analyses.
Comparisons with brooding Indo-West Pacific P. damicornis populations
Similar levels of population genetic structure over scales of hundreds of kilometers have also been observed in other brooding and broadcast-spawning coral species in the Indo-Pacific and the Caribbean , . In P. damicornis, allozyme studies from across the Indo-West Pacific indicate that populations exhibit a range of significant population genetic structures with FST values ranging from 0.06 to as high as 0.39 (Table 5). Some of the highest levels of population structure have been detected in isolated or peripheral populations. For example, FST values among high-latitude P. damicornis populations in south-east Australia averaged 0.37 over 700 km  compared to 0.06 among Great Barrier Reef populations over 1200 km . Similarly, FST values among the southernmost P. damicornis populations around Lord Howe Island  were twice as high as among similarly spaced populations on the Great Barrier Reef (FST = 0.102 vs. FST = 0.044).
Direct comparisons of population genetic data are possible with two P. damicornis microsatellite datasets from peripheral populations in East-African  and core populations in the Indonesian Archipelago  since they used the same or similar subsets of the microsatellite loci used here. Both studies found highly significant population genetic structure. Levels of genetic differentiation among the peripheral East-African populations were lower (FST = 0.02 over 860 km) than among TEP populations (FST = 0.05 over 400 km). Indonesian populations show the same degree of genetic differentiation as TEP populations (FST = 0.05) over a 10-fold wider geographic distance (3000 km vs. 400 km). We observed a much lower allelic diversity in the TEP (NA/locus = 7) compared to P. damicornis in Indonesia and East-Africa (NA/locus = 14.0 & 13.4, respectively). Lower allelic diversities are expected for peripheral populations and the lower diversity in TEP populations, compared to the similarly peripheral East-African populations, is likely due to the extreme isolation of the TEP and very limited transpacific gene flow [FST = 0.419; 21]. As expected, inbreeding was found to be highly significant in both peripheral populations, in the TEP and in Eastern Africa . Comparisons among P. damicornis allozyme studies confirm all three population genetic trends in peripheral populations: 1) higher genetic structure [e.g. 62 vs. 56], 2) decreased allelic diversity  and 3) higher inbreeding . These patterns have also been observed in peripheral populations of other coral species , , , .
Our results indicate lower genetic diversity and higher levels of population structure among broadcast-spawning populations (TEP) than among larvae brooding populations (Indo-West Pacific), which may reflect intrinsic differences between the two reproductive strategies. In Indo-West Pacific populations, parthenogenetic larvae brooding preserves genotypes, which reduces the rate of genetic drift and allelic loss, while allelic diversity in TEP populations is likely reduced due to reproductive sweepstakes, promoted by its broadcast-spawning reproductive strategy , , . Contrary to our results, inter-specific comparisons mostly indicate that brooding corals have reduced dispersal potentials compared to broadcast-spawners , , , . This indicates that population structure in reef corals is not predominantly driven by reproductive strategies. Other factors are likely as important, for example effective population sizes and species-specific larval behaviors [e.g. 51,90].
Fine-scale Population Genetic Structure
The observed fine-scale spatial genetic structure (SGS) and the high inbreeding coefficients (average FIS = 0.18) indicate that gene dispersal is limited in Panamanian P. damicornis, not only between reefs, but within reefs as well. Fine-scale SGS arises from a variety of historic, demographic, and evolutionary processes , , . Over small spatial scales, SGS is most often the result of limited gene dispersal and can be influenced by a broad array of life-history and reproductive traits including clonality, selfing, inbreeding, fertilization, fecundity, larval life history, and recruitment , , . Clonality can be an important determinant of SGS because clonal aggregations increase the average kinship over short distance intervals [e.g. 46]. We observed fine-scale SGS out to 10 m in both, the genet-only and the genet-plus-clone dataset, but since clones were rare (6.2% of samples), clonality had only a small effect on the observed SGS (Figure 3). Instead, the fine-scale SGS observed in TEP P. damicornis was predominantly driven by significant non-random relatedness among individual genets out to 10 meters, which is unusual for free-spawning benthic marine populations.
The two most likely explanations for the observed SGS among genets in TEP P. damicornis are cohort recruitment (i.e. SGS among larval recruits, independent of parents) or proximity recruitment (i.e. SGS among parents and recruits). In brooding coral species, proximity recruitment is facilitated by the internal (i.e. stationary) larval development and the frequent settlement of larvae within meters of the maternal colony , , . Although broadcast-spawning was never directly observed, several independent studies provide convincing evidence that TEP P. damicornis do not release brooded larvae , ,  but instead free-spawn gametes . In broadcast-spawning corals, like TEP P. damicornis, larval development occurs externally and larval settlement after gamete release takes at least 1–3 days . Although corals generally spawn during times of minimal water movement , , it is unlikely that drifting coral larvae would stay so close together (cohort recruitment) or remain within meters of the maternal colony (inhibiting proximity recruitment) over several days during their dispersive phase to create such a fine-scale spatial genetic structure (10 m).
One potential scenario that could significantly reduce passive dispersal would be if gametes and/or larvae sink down and escape the flow of the water column. Although coral gametes typically float on the sea surface during fertilization and development , gametes of two Pocillopora [P. eydouxi & P. verrucosa, 103] and several other coral species (e.g. Fungia scutaria, F. fungites, Goniastrea favulus) are known to be negatively buoyant , , , . Negatively buoyant gametes sink down after spawning and fertilize close to the substrate. Fertilization at the substrate also favors mating among nearby colonies, which limits gene dispersal, and should facilitate SGS. Even if fertilization occurs at the sea surface but the zygotes sink down promptly, larval dispersal would still be reduced considerably. A minority of propagules could then remain in the water column to account for long-distance dispersal. Whether TEP P. damicornis gametes or larvae are positively or negatively buoyant is currently unknown, since gamete spawning has not yet been observed directly.
A second indication for limited gene dispersal within populations is the significant inbreeding coefficients. Inbreeding is a consequence of non-random mating among a limited number of individuals, which limits gene dispersal and promotes SGS . The broadcast-spawning reproductive strategy of TEP P. damicornis might facilitate inbreeding in several ways. Firstly, the external fertilization of broadcast-spawners lacks the potential parental control of internal fertilization in brooders , . Secondly, the high fecundity of broadcast-spawners leads to reproductive sweepstakes, which can promote inbreeding , , . However, heterozygote deficits were as pronounced in larvae-brooding East-African populations (FIS = 0.26), and significant inbreeding is common in P. damicornis populations throughout the Indo-Pacific, regardless of reproductive strategy, local environment, population history, and analyzed genetic marker (Table 5). Inbreeding, and potentially SGS, may thus be inherent features of P. damicornis.
While SGS is common in plants [reviews by 78,107,108], it has only been documented in four other coral species. Underwood et al.  described a similar pattern of SGS in the brooding coral Seriatopora hystrix, including a significantly elevated kinship among genets in the smallest distance interval (F1 = 20 m) and a roughly comparable genetic patch size (80 m). Among broadcast-spawning corals, Stoddart  and Miller and Ayre  found no significant genet SGS in Acropora digitifera and Goniastrea favulus, respectively. However, Miller and Ayre  found significant genet SGS in the broadcast-spawning Platygyra daedalea, including significantly positive kinship in the smallest distance interval (F1 = 5 m) and a Genetic Patch Size of only 17 m. This is the only other documented broadcast-spawning coral with genet SGS. To account for this pattern, Miller and Ayre  suspected “an unknown element of larval behavior or development” - e.g. that larvae might be negatively buoyant.
Small-scale SGS over tens of meters has been documented for at least eight other sessile marine invertebrates, including two sponges , , a temperate soft coral , a black coral , a red coral , a bryozoan  and two tunicates , . For six out of these eight taxa, SGS seems to be driven by limited dispersal of brooded, philopatric larvae. Both broadcast spawners with significant SGS, the Anthipatharian coral Antipathes fiordensis  and the solitary tunicate Styela plicata  have negatively buoyant larvae (A. fiordensis) or eggs (S. plicata).
Because of its large mono-specific stands and little to no detectable larvae recruitment , TEP P. damicornis reefs were long thought to be highly clonal, persisting locally through vegetative asexual fragmentation , . Our data indicate that only 6% of corals sampled every 10 m apart were clones, i.e. big clones (>10 m) were uncommon. In contrast, 94% of samples consist of unique, sexually-derived genets. This indicates that sexual recruitment is sufficient to maintain high levels of genet diversity in TEP P. damicornis. Simulation models by Neigel & Avise  indicate that in populations of the Caribbean coral Acropora cervicornis, which depends heavily on vegetative fragmentation, 5% sexual recruitment (i.e. 95% asexual) is enough to generate high genotypic diversities (∼60%), independent of initial genet diversity.
Compared to other P. damicornis studies, levels of clonality in the TEP (6%) seem low. However, direct comparisons among studies are biased by different sampling strategies and genetic markers. Lower levels of clonality tend to be detected with microsatellites compared to allozyme markers (avg. 22% vs. 43%; Table 5) and with large sampling intervals compared to exhaustive samplings [e.g. 80,81 and the present study vs. 37]. Comparisons among studies using the same marker and similar sampling indicate higher levels of clonality in peripheral populations (TEP, East Africa & Lord Howe Island) compared to more central populations (Indonesia & Great Barrier Reef)(Table 5). Higher clonality in peripheral populations has been observed in other corals ,  and terrestrial plants , . Clonal reproduction is considered to enable persistence in the commonly adverse environmental conditions towards range margins, at the expense of sexual reproduction benefits . One example of reduced sexual benefits due to asexual reproduction is limited gene flow among and within populations as described here for the peripheral TEP P. damicornis populations.
Regional structure and localized SGS detected in Panamanian Pocillopora damicornis has important consequences for the conservation management of TEP coral reefs. Recent devastating mass mortalities, for example due to El Niño, demonstrate the fragility of TEP coral reefs , , , , . However, regional populations reacted very differently to these large scale disturbances  and are further differently affected by regional disturbances including Acanthaster predation , , toxic algal blooms  and seasonal upwellings . In combination with the significant genetic differences among regions, these variations highlight the importance of environmentally, ecologically and genetically defined regional management and conservation units in Panama and possibly throughout the TEP. Limited gene flow and significant genetic differences between reefs further indicate that local population dynamics on individual reefs are vital for reef resilience and adaptation in Panama. For example, although the limited gene flow potentially hampers population recovery, it also allows for local and regional adaptation, which should be preserved and accounted for in conservation management.
Materials and Methods
Collection of coral samples for this project was approved by the Autoridad Nacional del Ambiente and was conducted under permit number ANAM SEA7108.
Pocillopora damicornis was sampled from nine reefs out of three regions (Gulf of Chiriqui, Azuero Peninsula, Gulf of Panama) across a well-documented upwelling gradient [e.g. 73] along 1400 km of coastline in Panama (Figure 1). Four reefs (Uva Island, Granito de Oro, Canal de Afuera Island and Bahia de Damas on Coiba Island) were sampled in the Gulf of Chiriqui in the west, where upwelling is absent and sea surface temperatures rarely drop below 25°C . Coastal coral reefs are poorly developed in the Gulf of Chiriqui due to extensive freshwater runoff, but substantial reef development has occurred around its numerous islands, including the largest (136 ha), thickest (13 m) and oldest (5600a) TEP reefs , . Two reefs (Achotines Bay and Iguana Island) were sampled in the centrally located Azuero Peninsula where occasional moderate upwelling occurs . Coastal reefs are more common in the Azuero Peninsula than in the gulfs, most likely due to reduced freshwater runoff. Three reefs (Saboga and Contadora Islands in the Perlas Archipelago and Taboga Island) were sampled in the eastern Gulf of Panama where strong seasonal upwelling leads to declines in sea surface temperature to ∼15°C . Coastal reefs are uncommon in the Gulf of Panama and reef development occurs primarily around near-shore islands and in the Perlas Archipelago.
Sampling and Genetic analyses
On each reef, 18 to 36 nubbins (2 cm) of P. damicornis were sampled every ten meters along reef sites composed of dense stands of P. damicornis to analyze its small-scale spatial genetic structure. Samples were preserved in Guanidinium-Isothiocyanate (GITC) DNA buffer for genetic analysis . DNA was extracted using standard Phenol-Chloroform extraction and ethanol precipitation.
Ten microsatellite loci were amplified using primers developed by Magalon et al.  (Pv2 & Pv6) and Starger et al.  (Pd2, Pd4, Pd5, Pd6, Pd7, Pd8, Pd9 & Pd10). Six of these loci (Pd2, Pd4, Pd5, Pd6, Pv2 & Pv6) amplified consistently using modified PCR protocols. PCR amplifications were carried out separately for each locus, following a nested PCR protocol for labeling, including forward primers with M13 tails and M13 primers with IR-labels . Each PCR mix contained 2 pmol forward and 8 pmol of each reverse and m13 primer in a 10 µl reaction with 1 µl 10× PCR buffer, 0.2 mM dNTPs, 0.25U AmpliTaq DNA polymerase (Applied Biosystems) and 0.5 µl template DNA. PCR profiles varied slightly by locus: For Pd2, Pd4, Pd5 and Pd6, the PCR profile consisted of 30 cycles at 94°C for 45 s, 55°C for 35 s and 72°C for 35 s followed by 8 cycles with a lower annealing temperature (53°C) for the M13 labeling. For Pv2 and Pv6, the profile was modified to 30 cycles at 94°C for 45 s, 56°C for 45 s and 72°C for 30 s followed by 8 labeling cycles with 53°C annealing temperature. Both protocols included an initial 3 min denaturing step at 94°C and a final extension step at 72°C for 7 min. The PCR products with incorporated infrared dyes were then sized and scored on a LICOR 4300 Genetic Analyzer.
Population genetic statistics, including allele frequencies, clonality, probability of identity, F-statistics and Analyses of Molecular Variance (AMOVA) were calculated using GenAlEx 6.1 . The program Micro-Checker 2.3  was used to test for stutter bands, large allele dropout and null alleles. Linkage disequilibrium among loci was assessed using a Markov chain method  in GENEPOP 4.0.10 , followed by sequential Bonferroni correction to account for multiple comparisons . Clones were identified in GenAlEx and because they introduce biases into population genetic analyses, only unique genets were used unless otherwise noted.
Population genetic structure was calculated as FST , which assumes an infinite allele model , and RST , which is based on a stepwise mutation model of allele evolution . Hierarchical AMOVA were used to estimate genetic structure among regions, among populations and among populations within regions . Statistical significance of RST and FST is based on 999 permutations. RST recovered more genetic structure, especially among regions, whereas FST had a lower resolution and higher intra-regional variation (FRT = 15% of FST compared to RRT = 50% of RST). As a result, we preferentially focus on RST (e.g. Tables 3 & 4). Principal Coordinate Analyses , implemented in GenAlEx, were used to detect and visualize the major patterns of pairwise RST population comparisons. Isolation by distance among populations was tested using a Mantel test, implemented in GenAlEx 6.1, to test for an association between pairwise population genetic differences and geographic distances.
The Bayesian clustering method implemented in STRUCTURE 2.3  was used to infer the likely number of genetic clusters (K) in the dataset. STRUCTURE estimates the posterior probability P (X | K) that the data fit the hypothesis of K clusters using a Markov chain Monte Carlo approach to optimize genotypic equilibrium (linkage equilibrium and HWE) within each cluster. Five independent runs for each K from 2 to 19 were conducted using the admixture model and independent allele frequencies with a burn-in period of 105 steps and 106 Markov chain Monte Carlo replications for data collection (Figure S1). STRUCTURE runs were aligned using Clumpp1.1  and the bar plot was generated with Distruct1.1 . To verify the optimal value for K, we compared the P (X | K) results with ΔK, the second order rate of change in the likelihood of K , which corresponds to the strength of genetic subdivision among clusters in the data (Figure S1b).
Fine-scale Spatial Genetic Structure (SGS) within populations was analyzed using the program SPAGeDi 1.2 . To distinguish between spatial genetic structure (SGS) due to clonal aggregations and SGS among unique genets, we analyzed and compared two different dataset: one dataset consisted of all 207 samples including clones (i.e. the ramet dataset) and one dataset contained only the 194 unique genotypes excluding clones (i.e. the genet dataset). SGS was estimated for each of the three regions separately and for all populations combined using the pairwise kinship coefficient Fij , . Other kinship coefficients including Ritland  and Moran's I  produced similar results (not shown). 95% confidence intervals and standard errors were estimated by 10,000 permutations of the genetic and the spatial datasets. Kinship values outside the 95% confidence intervals were interpreted as significant SGS at the spatial distance. Three parameters were used to describe and compare SGS among regions and studies: F(1), genetic patch size and Sp. F(1) is the average kinship among individuals within the smallest distance interval (10 m). Its statistical significance (p) was obtained by comparing the slope b(F) of F(r) on ln(r) to 9999 random permutations of individuals among locations within populations using a Mantel test. The genetic patch size is the distance that corresponds to the first x-intercept of the kinship correlogram [cf. 148]. Within the genetic patch, individuals are more closely related than the population average, i.e. the association between genotypes is positive, while individuals outside of the patch are genetically independent, i.e. their correlation is negative. The Sp statistic (Vekemans and Hardy  is based on F(1) and the decrease of SGS with distance (b(F)).
Results of the Bayesian clustering approach implemented in STRUCTURE 2.3  that were used to infer the number of genetic clusters (K) in the microsatellite dataset. The graph shows the mean log likelihood L(K) for K = 1–19 (±SD) and ΔK, the second order rate of change of L(K) for K = 2–18 . The most likely number of cluster is K = 5, since it has the highest likelihood value (L(K) = −2059) and a local maximum for ΔK.
Field and logistics support was provided by Rich Aronson, Ian McIntyre and Carmen Schloeder. Thank you to Sarah Lemer, Liz Hemond, Sean Kent, Silvia Libro, Flavia Nunes and two anonymous reviewers for their comments on the manuscript.
Conceived and designed the experiments: DJC SVV. Performed the experiments: DJC. Analyzed the data: DJC. Contributed reagents/materials/analysis tools: SVV. Wrote the paper: DJC SVV.
- 1. Soule M (1973) The epistasis cycle: a theory of marginal populations. Annual Review of Ecology and Systematics 4: 165–187.M. Soule1973The epistasis cycle: a theory of marginal populations.Annual Review of Ecology and Systematics4165187
- 2. Brown J, Stevens G, Kaufman D (1996) The geographic range: size, shape, boundaries, and internal structure. Annual Review of Ecology and Systematics 27: 597–623.J. BrownG. StevensD. Kaufman1996The geographic range: size, shape, boundaries, and internal structure.Annual Review of Ecology and Systematics27597623
- 3. Vucetich J, Waite T (2003) Spatial patterns of demography and genetic processes across the species' range: null hypotheses for landscape conservation genetics. Conservation Genetics 4: 639–645.J. VucetichT. Waite2003Spatial patterns of demography and genetic processes across the species' range: null hypotheses for landscape conservation genetics.Conservation Genetics4639645
- 4. Slatkin M (1987) Gene flow and the geographic structure of natural populations. Science 236: 787.M. Slatkin1987Gene flow and the geographic structure of natural populations.Science236787
- 5. Garcia-Ramos G, Kirkpatrick M (1997) Genetic models of adaptation and gene flow in peripheral populations. Evolution 51: 21–28.G. Garcia-RamosM. Kirkpatrick1997Genetic models of adaptation and gene flow in peripheral populations.Evolution512128
- 6. Wright S (1931) Evolution in Mendelian populations. Genetics 16: 97–159.S. Wright1931Evolution in Mendelian populations.Genetics1697159
- 7. Beatty G, McEvoy P, Sweeney O, Provan J (2008) Range-edge effects promote clonal growth in peripheral populations of the one-sided wintergreen Orthilia secunda. Diversity and Distributions 14: 546–555.G. BeattyP. McEvoyO. SweeneyJ. Provan2008Range-edge effects promote clonal growth in peripheral populations of the one-sided wintergreen Orthilia secunda.Diversity and Distributions14546555
- 8. Arnaud-Haond S, Teixeira S, Massa S, Billot C, Saenger P, et al. (2006) Genetic structure at range edge: low diversity and high inbreeding in Southeast Asian mangrove (Avicennia marina) populations. Molecular Ecology 15: 3515–3525.S. Arnaud-HaondS. TeixeiraS. MassaC. BillotP. Saenger2006Genetic structure at range edge: low diversity and high inbreeding in Southeast Asian mangrove (Avicennia marina) populations.Molecular Ecology1535153525
- 9. Bergl R, Vigilant L (2007) Genetic analysis reveals population structure and recent migration within the highly fragmented range of the Cross River gorilla (Gorilla gorilla diehli). Molecular Ecology 16: 501–516.R. BerglL. Vigilant2007Genetic analysis reveals population structure and recent migration within the highly fragmented range of the Cross River gorilla (Gorilla gorilla diehli).Molecular Ecology16501516
- 10. Noreen A, Harrison P, Van Oppen M (2009) Genetic diversity and connectivity in a brooding reef coral at the limit of its distribution. Proceedings of the Royal Society B: Biological Sciences 276: 3927.A. NoreenP. HarrisonM. Van Oppen2009Genetic diversity and connectivity in a brooding reef coral at the limit of its distribution.Proceedings of the Royal Society B: Biological Sciences2763927
- 11. Hoffmann A, Blows M (1994) Species borders: ecological and evolutionary perspectives. Trends in Ecology & Evolution 9: 223–227.A. HoffmannM. Blows1994Species borders: ecological and evolutionary perspectives.Trends in Ecology & Evolution9223227
- 12. Lawton J (1993) Range, population abundance and conservation. Trends in Ecology & Evolution 8: 409–413.J. Lawton1993Range, population abundance and conservation.Trends in Ecology & Evolution8409413
- 13. Budd AF, Pandolfi JM (2010) Evolutionary novelty is concentrated at the edge of coral species distributions. Science 328: 1558–1561.AF BuddJM Pandolfi2010Evolutionary novelty is concentrated at the edge of coral species distributions.Science32815581561
- 14. Templeton A (1980) The theory of speciation via the founder principle. Genetics 94: 1011.A. Templeton1980The theory of speciation via the founder principle.Genetics941011
- 15. Carson H, Templeton A (1984) Genetic revolutions in relation to speciation phenomena: the founding of new populations. Annual Review of Ecology and Systematics 15: 97–132.H. CarsonA. Templeton1984Genetic revolutions in relation to speciation phenomena: the founding of new populations.Annual Review of Ecology and Systematics1597132
- 16. Darwin C (1859) On the origins of species by means of natural selection or the preservation of favoured races in the struggle for life. London: John Murray. C. Darwin1859On the origins of species by means of natural selection or the preservation of favoured races in the struggle for life.LondonJohn Murray
- 17. Ekman S (1935) Tiergeographie des Meeres: Akademische Verlagsgesellschaft mbh. S. Ekman1935Tiergeographie des Meeres: Akademische Verlagsgesellschaft mbh
- 18. Mayr E (1954) Geographic speciation in tropical echinoids. Evolution. pp. 1–18.E. Mayr1954Geographic speciation in tropical echinoids.Evolution118
- 19. Lessios H, Robertson D (2006) Crossing the impassable: genetic connections in 20 reef fishes across the eastern Pacific barrier. Proceedings of the Royal Society B: Biological Sciences 273: 2201–2209.H. LessiosD. Robertson2006Crossing the impassable: genetic connections in 20 reef fishes across the eastern Pacific barrier.Proceedings of the Royal Society B: Biological Sciences27322012209
- 20. Lessios HA, Kessing BD, Robertson DR, Paulay G (1999) Phylogeography of the pantropical sea urchin Eucidaris in relation to land barriers and ocean currents. Evolution 53: 806–817.HA LessiosBD KessingDR RobertsonG. Paulay1999Phylogeography of the pantropical sea urchin Eucidaris in relation to land barriers and ocean currents.Evolution53806817
- 21. Combosch D, Guzman H, Schuhmacher H, Vollmer S (2008) Interspecific hybridization and restricted trans-Pacific gene flow in the Tropical Eastern Pacific Pocillopora. Molecular Ecology 17: 1304–1312.D. ComboschH. GuzmanH. SchuhmacherS. Vollmer2008Interspecific hybridization and restricted trans-Pacific gene flow in the Tropical Eastern Pacific Pocillopora.Molecular Ecology1713041312
- 22. Colborn J, Crabtree R, Shaklee J, Pfeiler E, Bowen B (2001) The evolutionary enigma of bonefishes (Albula spp.): cryptic species and ancient separations in a globally distributed shorefish. Evolution 55: 807–820.J. ColbornR. CrabtreeJ. ShakleeE. PfeilerB. Bowen2001The evolutionary enigma of bonefishes (Albula spp.): cryptic species and ancient separations in a globally distributed shorefish.Evolution55807820
- 23. Lessios HA, Kessing BD, Pearse JS (2001) Population structure and speciation in tropical seas: Global phylogeography of the sea urchin Diadema. Evolution 55: 955–975.HA LessiosBD KessingJS Pearse2001Population structure and speciation in tropical seas: Global phylogeography of the sea urchin Diadema.Evolution55955975
- 24. McCartney M, Keller G, Lessios H (2000) Dispersal barriers in tropical oceans and speciation in Atlantic and eastern Pacific sea urchins of the genus Echinometra. Molecular Ecology 9: 1391–1400.M. McCartneyG. KellerH. Lessios2000Dispersal barriers in tropical oceans and speciation in Atlantic and eastern Pacific sea urchins of the genus Echinometra.Molecular Ecology913911400
- 25. Duda T, Lessios H (2009) Connectivity of populations within and between major biogeographic regions of the tropical Pacific in Conus ebraeus, a widespread marine gastropod. Coral Reefs 28: 651–659.T. DudaH. Lessios2009Connectivity of populations within and between major biogeographic regions of the tropical Pacific in Conus ebraeus, a widespread marine gastropod.Coral Reefs28651659
- 26. Hughes TP, Bellwood DR, Connolly SR (2002) Biodiversity hotspots, centres of endemicity, and the conservation of coral reefs. Ecology Letters 5: 775–784.TP HughesDR BellwoodSR Connolly2002Biodiversity hotspots, centres of endemicity, and the conservation of coral reefs.Ecology Letters5775784
- 27. Glynn P, Ault J (2000) A biogeographic analysis and review of the far eastern Pacific coral reef region. Coral Reefs 19: 1–23.P. GlynnJ. Ault2000A biogeographic analysis and review of the far eastern Pacific coral reef region.Coral Reefs19123
- 28. Veron JEN (2000) Corals of the World. Townsville, Australia: AIMS. JEN Veron2000Corals of the World.Townsville, AustraliaAIMS
- 29. Briggs JC (1974) Marine Zoogeography. New York: McGraw-Hill. JC Briggs1974Marine Zoogeography.New YorkMcGraw-Hill
- 30. Glynn P, Macintyre I (1977) Growth rate and age of coral reefs on the Pacific coast of Panama. pp. 251–259.P. GlynnI. Macintyre1977Growth rate and age of coral reefs on the Pacific coast of Panama.251259Proceedings of the 3rd International Coral Reef Symposium. Proceedings of the 3rd International Coral Reef Symposium.
- 31. Glynn P, Wellington G (1983) Corals and Coral Reefs of the Galpagos Islands (with an annotated list of the scleractinian corals of the Galpagos by JW Wells). Berkeley California, USA: University of California. P. GlynnG. Wellington1983Corals and Coral Reefs of the Galpagos Islands (with an annotated list of the scleractinian corals of the Galpagos by JW Wells).Berkeley California, USAUniversity of California
- 32. Guzman H, Cortes J (1993) Arrecifes coralinos del Pacifico Oriental Tropical: revision y perspectivas - Coral reefs of the Tropical Eastern Pacific: review and perspectives. Revista de Biologia Tropical 41: 535–557.H. GuzmanJ. Cortes1993Arrecifes coralinos del Pacifico Oriental Tropical: revision y perspectivas - Coral reefs of the Tropical Eastern Pacific: review and perspectives.Revista de Biologia Tropical41535557
- 33. Glynn P, Veron J, Wellington G (1996) Clipperton Atoll (eastern Pacific): oceanography, geomorphology, reef-building coral ecology and biogeography. Coral Reefs 15: 71–99.P. GlynnJ. VeronG. Wellington1996Clipperton Atoll (eastern Pacific): oceanography, geomorphology, reef-building coral ecology and biogeography.Coral Reefs157199
- 34. Highsmith RC (1982) Reproduction by fragmentation in corals. Marine Ecology Progress Series 7: 207–226.RC Highsmith1982Reproduction by fragmentation in corals.Marine Ecology Progress Series7207226
- 35. Richmond R (1987) Energetic relationships and biogeographical differences among fecundity, growth and reproduction in the reef coral Pocillopora damicornis. Bulletin of Marine Science 41: 594–604.R. Richmond1987Energetic relationships and biogeographical differences among fecundity, growth and reproduction in the reef coral Pocillopora damicornis.Bulletin of Marine Science41594604
- 36. Stoddart JA (1983) Asexual production of planulae in the coral Pocillopora damicornis. Marine Biology 76: 279–284.JA Stoddart1983Asexual production of planulae in the coral Pocillopora damicornis.Marine Biology76279284
- 37. Yeoh S, Dai C (2010) The production of sexual and asexual larvae within single broods of the scleractinian coral, Pocillopora damicornis. Marine Biology 157: 351–359.S. YeohC. Dai2010The production of sexual and asexual larvae within single broods of the scleractinian coral, Pocillopora damicornis.Marine Biology157351359
- 38. Glynn P, Gassman N, Eakin C, Cortes J, Smith D, et al. (1991) Reef coral reproduction in the eastern Pacific: Costa Rica, Panama, and Galapagos Islands (Ecuador). I. Pocilloporidae. Marine Biology 109: 355–368.P. GlynnN. GassmanC. EakinJ. CortesD. Smith1991Reef coral reproduction in the eastern Pacific: Costa Rica, Panama, and Galapagos Islands (Ecuador). I. Pocilloporidae.Marine Biology109355368
- 39. Richmond R, Hunter C (1990) Reproduction and recruitment of corals: Comparisons among the Caribbean, the Tropical Pacific, and the Red Sea. Marine Ecology Progress Series 60: 185–203.R. RichmondC. Hunter1990Reproduction and recruitment of corals: Comparisons among the Caribbean, the Tropical Pacific, and the Red Sea.Marine Ecology Progress Series60185203
- 40. Harrison P, Wallace C (1990) Reproduction, dispersal, and recruitment of scleractinian corals. In: Dubinsky Z, editor. Ecosystems of the world: Coral reefs: Elseiver. pp. 133–207.P. HarrisonC. Wallace1990Reproduction, dispersal, and recruitment of scleractinian corals.Z. DubinskyEcosystems of the world: Coral reefs: Elseiver133207
- 41. Hellberg ME (1995) Stepping-Stone Gene Flow in the Solitary Coral Balanophyllia Elegans - Equilibrium and Nonequilibrium at Different Spatial Scales. Marine Biology 123: 573–581.ME Hellberg1995Stepping-Stone Gene Flow in the Solitary Coral Balanophyllia Elegans - Equilibrium and Nonequilibrium at Different Spatial Scales.Marine Biology123573581
- 42. Nishikawa A, Katoh M, Sakai K (2003) Larval settlement rates and gene flow of broadcast-spawning (Acropora tenuis) and planula-brooding (Stylophora pistillata) corals. Marine Ecology Progress Series 256: 87–97.A. NishikawaM. KatohK. Sakai2003Larval settlement rates and gene flow of broadcast-spawning (Acropora tenuis) and planula-brooding (Stylophora pistillata) corals.Marine Ecology Progress Series2568797
- 43. Ayre DJ, Hughes TP (2000) Genotypic diversity and gene flow in brooding and spawning corals along the Great Barrier Reef, Australia. Evolution 54: 1590–1605.DJ AyreTP Hughes2000Genotypic diversity and gene flow in brooding and spawning corals along the Great Barrier Reef, Australia.Evolution5415901605
- 44. Nishikawa A (2008) Degree and Pattern of Gene Flow in Several Scleractinian Corals in the Ryukyu Archipelago, Southern Japan. Pacific Science 62: 413–421.A. Nishikawa2008Degree and Pattern of Gene Flow in Several Scleractinian Corals in the Ryukyu Archipelago, Southern Japan.Pacific Science62413421
- 45. Hellberg M (1996) Dependence of gene flow on geographic distance in two solitary corals with different larval dispersal capabilities. Evolution 50: 1167–1175.M. Hellberg1996Dependence of gene flow on geographic distance in two solitary corals with different larval dispersal capabilities.Evolution5011671175
- 46. Stoddart J (1988) Historecognition and fine-scale spatial genetic structure in sessile benthic invertebrates. In: Grosberg R, Hedgecock D, Nelson K, editors. Invertebrate Historecognition. New York: Plenum Publishing Corporation. pp. 111–125.J. Stoddart1988Historecognition and fine-scale spatial genetic structure in sessile benthic invertebrates.R. GrosbergD. HedgecockK. NelsonInvertebrate HistorecognitionNew YorkPlenum Publishing Corporation111125
- 47. McFadden CS, Aydin KY (1996) Spatial autocorrelation analysis of small-scale genetic structure in a clonal soft coral with limited larval dispersal. Marine Biology 126: 215–224.CS McFaddenKY Aydin1996Spatial autocorrelation analysis of small-scale genetic structure in a clonal soft coral with limited larval dispersal.Marine Biology126215224
- 48. Miller K (1998) Short-distance dispersal of black coral larvae: inference from spatial analysis of colony genotypes. Marine Ecology Progress Series 163: 225–233.K. Miller1998Short-distance dispersal of black coral larvae: inference from spatial analysis of colony genotypes.Marine Ecology Progress Series163225233
- 49. Costantini F, Fauvelot C, Abbiati M (2007) Fine-scale genetic structuring in Corallium rubrum: evidence of inbreeding and limited effective larval dispersal. Marine Ecology Progress Series 340: 109–119.F. CostantiniC. FauvelotM. Abbiati2007Fine-scale genetic structuring in Corallium rubrum: evidence of inbreeding and limited effective larval dispersal.Marine Ecology Progress Series340109119
- 50. Underwood JN, Smith LD, Van Oppen MJH, Gilmour JP (2007) Multiple scales of genetic connectivity in a brooding coral on isolated reefs following catastrophic bleaching. Molecular Ecology 16: 771–784.JN UnderwoodLD SmithMJH Van OppenJP Gilmour2007Multiple scales of genetic connectivity in a brooding coral on isolated reefs following catastrophic bleaching.Molecular Ecology16771784
- 51. Miller K, Ayre D (2008) Population structure is not a simple function of reproductive mode and larval type: insights from tropical corals. Journal of Animal Ecology 77: 713–724.K. MillerD. Ayre2008Population structure is not a simple function of reproductive mode and larval type: insights from tropical corals.Journal of Animal Ecology77713724
- 52. Willis BL, Babcock RC, Harrison PL, Wallace CC (1997) Experimental hybridization and breeding incompatibilities within the mating systems of mass spawning reef corals. Coral Reefs 16: S53–S65.BL WillisRC BabcockPL HarrisonCC Wallace1997Experimental hybridization and breeding incompatibilities within the mating systems of mass spawning reef corals.Coral Reefs16S53S65
- 53. Heyward A, Babcock R (1986) Self-and cross-fertilization in scleractinian corals. Marine Biology 90: 191–195.A. HeywardR. Babcock1986Self-and cross-fertilization in scleractinian corals.Marine Biology90191195
- 54. Hedgecock D (1994) Does variance in reproductive success limit effective population sizes of marine organisms. In: Beaumont A, editor. Genetics and evolution of aquatic organisms: Chapman & Hall. pp. 122–134.D. Hedgecock1994Does variance in reproductive success limit effective population sizes of marine organisms.A. BeaumontGenetics and evolution of aquatic organisms: Chapman & Hall122134
- 55. Ayre D, Hughes T (2004) Climate change, genotypic diversity and gene flow in reef-building corals. Ecology Letters 7: 273–278.D. AyreT. Hughes2004Climate change, genotypic diversity and gene flow in reef-building corals.Ecology Letters7273278
- 56. Miller K, Ayre D (2008) Protection of genetic diversity and maintenance of connectivity among reef corals within marine protected areas. Conservation Biology 22: 1245–1254.K. MillerD. Ayre2008Protection of genetic diversity and maintenance of connectivity among reef corals within marine protected areas.Conservation Biology2212451254
- 57. Miller K, Ayre D (2004) The role of sexual and asexual reproduction in structuring high latitude populations of the reef coral Pocillopora damicornis. Heredity 92: 557–568.K. MillerD. Ayre2004The role of sexual and asexual reproduction in structuring high latitude populations of the reef coral Pocillopora damicornis.Heredity92557568
- 58. Ayre D, Miller K (2004) Where do clonal coral larvae go? Adult genotypic diversity conflicts with reproductive effort in the brooding coral Pocillopora damicornis. Marine Ecology Progress Series 277: 95–105.D. AyreK. Miller2004Where do clonal coral larvae go? Adult genotypic diversity conflicts with reproductive effort in the brooding coral Pocillopora damicornis.Marine Ecology Progress Series27795105
- 59. Benzie J, Haskell A, Lehman H (1995) Variation in the genetic composition of coral (Pocillopora damicornis and Acropora palifera) populations from different reef habitats. Marine Biology 121: 731–739.J. BenzieA. HaskellH. Lehman1995Variation in the genetic composition of coral (Pocillopora damicornis and Acropora palifera) populations from different reef habitats.Marine Biology121731739
- 60. Stoddart J (1984) Genetic differentiation amongst populations of the coral Pocillopora damicornis off Southwest Australia. Coral Reefs 3: 149–156.J. Stoddart1984Genetic differentiation amongst populations of the coral Pocillopora damicornis off Southwest Australia.Coral Reefs3149156
- 61. Ayre D, Hughes T, Standish R (1997) Genetic differentiation, reproductive mode, and gene flow in the brooding coral Pocillopora damicornis along the Great Barrier Reef, Australia. Marine Ecology Progress Series 159: 175–187.D. AyreT. HughesR. Standish1997Genetic differentiation, reproductive mode, and gene flow in the brooding coral Pocillopora damicornis along the Great Barrier Reef, Australia.Marine Ecology Progress Series159175187
- 62. Sherman C, Ayre D, Miller K (2006) Asexual reproduction does not produce clonal populations of the brooding coral Pocillopora damicornis on the Great Barrier Reef, Australia. Coral Reefs 25: 7–18.C. ShermanD. AyreK. Miller2006Asexual reproduction does not produce clonal populations of the brooding coral Pocillopora damicornis on the Great Barrier Reef, Australia.Coral Reefs25718
- 63. Adjeroud M, Tsuchiya M (1999) Genetic variation and clonal structure in the scleractinian coral Pocillopora damicornis in the Ryukyu Archipelago, southern Japan. Marine Biology 134: 753–760.M. AdjeroudM. Tsuchiya1999Genetic variation and clonal structure in the scleractinian coral Pocillopora damicornis in the Ryukyu Archipelago, southern Japan.Marine Biology134753760
- 64. Souter P, Henriksson O, Olsson N, Grahn M (2009) Patterns of genetic structuring in the coral Pocillopora damicornis on reefs in East Africa. BMC Ecology 9: 19.P. SouterO. HenrikssonN. OlssonM. Grahn2009Patterns of genetic structuring in the coral Pocillopora damicornis on reefs in East Africa.BMC Ecology919
- 65. Whitaker K (2006) Genetic evidence for mixed modes of reproduction in the coral Pocillopora damicornis and its effect on population structure. Marine Ecology Progress Series 306: 115–124.K. Whitaker2006Genetic evidence for mixed modes of reproduction in the coral Pocillopora damicornis and its effect on population structure.Marine Ecology Progress Series306115124
- 66. Pinzón JH, LaJeunesse T (2011) Species delimitation of common reef corals in the genus Pocillopora using nucleotide sequence phylogenies, population genetics and symbiosis ecology. Molecular Ecology 20: 311–325.JH PinzónT. LaJeunesse2011Species delimitation of common reef corals in the genus Pocillopora using nucleotide sequence phylogenies, population genetics and symbiosis ecology.Molecular Ecology20311325
- 67. Glynn P (1976) Some physical and biological determinants of coral community structure in the eastern Pacific. Ecological Monographs 46: 431–456.P. Glynn1976Some physical and biological determinants of coral community structure in the eastern Pacific.Ecological Monographs46431456
- 68. Glynn P (1977) Coral growth in upwelling and nonupwelling areas off the Pacific coast of Panama. Journal of Marine Research 35: 567–585.P. Glynn1977Coral growth in upwelling and nonupwelling areas off the Pacific coast of Panama.Journal of Marine Research35567585
- 69. Glynn P, Leyte Morales G (1997) Coral reefs of Huatulco, West Mexico: reef development in upwelling Gulf of Tehuantepec. Revista de Biologia Tropical 45: 1033–1048.P. GlynnG. Leyte Morales1997Coral reefs of Huatulco, West Mexico: reef development in upwelling Gulf of Tehuantepec.Revista de Biologia Tropical4510331048
- 70. Glynn P, Stewart R (1973) Distribution of coral reefs in the Pearl Islands (Gulf of Panama) in relation to thermal conditions. Limnology and Oceanography 18: 367–379.P. GlynnR. Stewart1973Distribution of coral reefs in the Pearl Islands (Gulf of Panama) in relation to thermal conditions.Limnology and Oceanography18367379
- 71. Glynn P, Stewart R, McCosker J (1972) Pacific coral reefs of Panama: structure, distribution and predators. International Journal of Earth Sciences 61: 483–519.P. GlynnR. StewartJ. McCosker1972Pacific coral reefs of Panama: structure, distribution and predators.International Journal of Earth Sciences61483519
- 72. Highsmith R (1980) Geographic patterns of coral bioerosion: a productivity hypothesis. Journal of Experimental Marine Biology and Ecology 46: 177–196.R. Highsmith1980Geographic patterns of coral bioerosion: a productivity hypothesis.Journal of Experimental Marine Biology and Ecology46177196
- 73. Glynn P, Mate J (1997) Field guide to the Pacific coral reefs of Panama. pp. 145–166.P. GlynnJ. Mate1997Field guide to the Pacific coral reefs of Panama145166
- 74. D'Croz L, Mate J (2004) Experimental responses to elevated water temperature in genotypes of the reef coral Pocillopora damicornis from upwelling and non-upwelling environments in Panama. Coral Reefs 23: 473–483.L. D'CrozJ. Mate2004Experimental responses to elevated water temperature in genotypes of the reef coral Pocillopora damicornis from upwelling and non-upwelling environments in Panama.Coral Reefs23473483
- 75. Glynn P, D'Croz L (1990) Experimental evidence for high temperature stress as the cause of El Nino-coincident coral mortality. Coral Reefs 8: 181–191.P. GlynnL. D'Croz1990Experimental evidence for high temperature stress as the cause of El Nino-coincident coral mortality.Coral Reefs8181191
- 76. Glynn P (2001) History of significant coral bleaching events and insights regarding amelioration. In: Salm R, Coles S, editors. Coral Bleaching and Marine Protected Areas. pp. 36–39.P. Glynn2001History of significant coral bleaching events and insights regarding amelioration.R. SalmS. ColesCoral Bleaching and Marine Protected Areas36392001 29-31 May 2001;Bishop Museum, Honolulu, Hawaii. Nature Conservancy, Asia Pacific Coastal Marine Program. 2001 29-31 May 2001;Bishop Museum, Honolulu, Hawaii. Nature Conservancy, Asia Pacific Coastal Marine Program.
- 77. Starger C, Barber P, Ambariyanto , Baker A (2010) The recovery of coral genetic diversity in the Sunda Strait following the 1883 eruption of Krakatau. Coral Reefs. pp. 1–19.C. StargerP. BarberAmbariyantoA. Baker2010The recovery of coral genetic diversity in the Sunda Strait following the 1883 eruption of Krakatau.Coral Reefs119
- 78. Vekemans X, Hardy O (2004) New insights from fine-scale spatial genetic structure analyses in plant populations. Molecular Ecology 13: 921–935.X. VekemansO. Hardy2004New insights from fine-scale spatial genetic structure analyses in plant populations.Molecular Ecology13921935
- 79. Birkeland C (1977) The importance of rate of biomass accumulation in early successional stages of benthic communities to the survival of coral recruits: Proceedings of the Third International Coral Reef Symposium. 1: 16–21.C. Birkeland1977The importance of rate of biomass accumulation in early successional stages of benthic communities to the survival of coral recruits: Proceedings of the Third International Coral Reef Symposium.11621
- 80. Ulstrup K, Berkelmans R, Ralph P, Van Oppen M (2006) Variation in bleaching sensitivity of two coral species across a latitudinal gradient on the Great Barrier Reef: the role of zooxanthellae. Marine Ecology Progress Series 314: 135–148.K. UlstrupR. BerkelmansP. RalphM. Van Oppen2006Variation in bleaching sensitivity of two coral species across a latitudinal gradient on the Great Barrier Reef: the role of zooxanthellae.Marine Ecology Progress Series314135148
- 81. Trenberth K, Hoar T (1997) El Nino and climate change. Geophysical Research Letters 24: 3057–3060.K. TrenberthT. Hoar1997El Nino and climate change.Geophysical Research Letters2430573060
- 82. Glynn P, Mate J, Baker A, Calderon M (2001) Coral bleaching and mortality in Panama and Ecuador during the 1997/98 El Nino Southern Oscillation Event: spatial/temporal patterns and comparisons with the 1982/83 event. Bulletin of Marine Science 69: 79–109.P. GlynnJ. MateA. BakerM. Calderon2001Coral bleaching and mortality in Panama and Ecuador during the 1997/98 El Nino Southern Oscillation Event: spatial/temporal patterns and comparisons with the 1982/83 event.Bulletin of Marine Science6979109
- 83. Vollmer SV, Palumbi SR (2007) Restricted gene flow in the Caribbean staghorn coral Acropora cervicomis: Implications for the recovery of endangered reefs. Journal of Heredity 98: 40–50.SV VollmerSR Palumbi2007Restricted gene flow in the Caribbean staghorn coral Acropora cervicomis: Implications for the recovery of endangered reefs.Journal of Heredity984050
- 84. van Oppen M, Gates R (2006) Conservation genetics and the resilience of reef-building corals. Molecular Ecology 15: 3863–3883.M. van OppenR. Gates2006Conservation genetics and the resilience of reef-building corals.Molecular Ecology1538633883
- 85. Stoddart J (1988) Coral populations fringing islands - larval connections. Australian Journal of Marine and Freshwater Research 39: 109–115.J. Stoddart1988Coral populations fringing islands - larval connections.Australian Journal of Marine and Freshwater Research39109115
- 86. Nunes F, Norris R, Knowlton N (2009) Implications of isolation and low genetic diversity in peripheral populations of an amphi-Atlantic coral. Molecular Ecology 18: 4283–4297.F. NunesR. NorrisN. Knowlton2009Implications of isolation and low genetic diversity in peripheral populations of an amphi-Atlantic coral.Molecular Ecology1842834297
- 87. Christie M, Johnson D, Stallings C, Hixon M (2010) Self-recruitment and sweepstakes reproduction amid extensive gene flow in a coral-reef fish. Molecular Ecology 19: 1042–1057.M. ChristieD. JohnsonC. StallingsM. Hixon2010Self-recruitment and sweepstakes reproduction amid extensive gene flow in a coral-reef fish.Molecular Ecology1910421057
- 88. Ruzzante D, Taggart C, Cook D (1996) Spatial and temporal variation in the genetic composition of a larval cod (Gadus morhua) aggregation: cohort contribution and genetic stability. Canadian Journal of Fisheries and Aquatic Sciences 53: 2695–2705.D. RuzzanteC. TaggartD. Cook1996Spatial and temporal variation in the genetic composition of a larval cod (Gadus morhua) aggregation: cohort contribution and genetic stability.Canadian Journal of Fisheries and Aquatic Sciences5326952705
- 89. Carlon DB (1999) The evolution of mating systems in tropical reef corals. Trends in Ecology & Evolution 14: 491–495.DB Carlon1999The evolution of mating systems in tropical reef corals.Trends in Ecology & Evolution14491495
- 90. Palumbi S (1995) Using genetics as an indirect estimator of larval dispersal. In: McEdward L, editor. Ecology of marine invertebrate larvae. Boca Raton, FL: CRC Press. pp. 369–387.S. Palumbi1995Using genetics as an indirect estimator of larval dispersal.L. McEdwardEcology of marine invertebrate larvaeBoca Raton, FLCRC Press369387
- 91. Epperson B (2003) Geographical genetics. Princeton University Press. B. Epperson2003Geographical geneticsPrinceton University Press
- 92. Loveless M, Hamrick J (1984) Ecological determinants of genetic structure in plant populations. Annual Review of Ecology and Systematics 15: 65–95.M. LovelessJ. Hamrick1984Ecological determinants of genetic structure in plant populations.Annual Review of Ecology and Systematics156595
- 93. Born C, Hardy O, Chevallier H, Ossari S, Atteke C, et al. (2008) Small-scale spatial genetic structure in the Central African rainforest tree species Aucoumea klaineana: a stepwise approach to infer the impact of limited gene dispersal, population history and habitat fragmentation. Molecular Ecology 17: 2041–2050.C. BornO. HardyH. ChevallierS. OssariC. Atteke2008Small-scale spatial genetic structure in the Central African rainforest tree species Aucoumea klaineana: a stepwise approach to infer the impact of limited gene dispersal, population history and habitat fragmentation.Molecular Ecology1720412050
- 94. Gerrodette T (1981) Dispersal of the solitary coral Balanophyllia elegans by demersal planular larvae. Ecology 62: 611–619.T. Gerrodette1981Dispersal of the solitary coral Balanophyllia elegans by demersal planular larvae.Ecology62611619
- 95. Best B, Resing J (1987) Active settlement of coral planulae: the effect of flow and swimming behavior on local recruitment. American Zoologist 127: 103A.B. BestJ. Resing1987Active settlement of coral planulae: the effect of flow and swimming behavior on local recruitment.American Zoologist127103A
- 96. Carlon D, Olson R (1993) Larval dispersal distance as an explanation for adult spatial pattern in two Caribbean reef corals. Journal of Experimental Marine Biology and Ecology 173: 247–263.D. CarlonR. Olson1993Larval dispersal distance as an explanation for adult spatial pattern in two Caribbean reef corals.Journal of Experimental Marine Biology and Ecology173247263
- 97. Richmond R (1985) Variations in the population biology of Pocillopora damicornis across the Pacific. Proceedings of the 5th International Coral Reef Congress 6: 101–106.R. Richmond1985Variations in the population biology of Pocillopora damicornis across the Pacific.Proceedings of the 5th International Coral Reef Congress6101106
- 98. Carpizo-Ituarte E, Vizcaino-Ochoa V, Chi-Barrag·n G, Tapia-Vazquez O, Cupul-Magana A, et al. (2010) Evidence of sexual reproduction in the hermatypic corals Pocillopora damicornis, Porites panamensis, and Pavona gigantea in Banderas Bay, Mexican Pacific. Ciencias Marinas 37: 97–112.E. Carpizo-ItuarteV. Vizcaino-OchoaG. Chi-Barrag·nO. Tapia-VazquezA. Cupul-Magana2010Evidence of sexual reproduction in the hermatypic corals Pocillopora damicornis, Porites panamensis, and Pavona gigantea in Banderas Bay, Mexican Pacific.Ciencias Marinas3797112
- 99. Miller K, Mundy C (2003) Rapid settlement in broadcast spawning corals: implications for larval dispersal. Coral Reefs 22: 99–106.K. MillerC. Mundy2003Rapid settlement in broadcast spawning corals: implications for larval dispersal.Coral Reefs2299106
- 100. Babcock R, Bull G, Harrison P, Heyward A, Oliver J, et al. (1986) Synchronous Spawnings of 105 Scleractinian Coral Species on the Great-Barrier-Reef. Marine Biology 90: 379–394.R. BabcockG. BullP. HarrisonA. HeywardJ. Oliver1986Synchronous Spawnings of 105 Scleractinian Coral Species on the Great-Barrier-Reef.Marine Biology90379394
- 101. van Woesik R (2009) Calm before the spawn: global coral spawning patterns are explained by regional wind fields. Proceedings of the Royal Society B: Biological Sciences 277: 715–722.R. van Woesik2009Calm before the spawn: global coral spawning patterns are explained by regional wind fields.Proceedings of the Royal Society B: Biological Sciences277715722
- 102. Willis B, Oliver J (1990) Direct tracking of coral larvae - implications for dispersal studies of plaktonic larvae in topographically complex environments. Ophelia 32: 145–162.B. WillisJ. Oliver1990Direct tracking of coral larvae - implications for dispersal studies of plaktonic larvae in topographically complex environments.Ophelia32145162
- 103. Kinzie R (1993) Spawning in the reef corals Pocillopora verrucosa and Pocillopora eydouxi at Sesoko Island, Okinawa. Galaxea 11: 93–105.R. Kinzie1993Spawning in the reef corals Pocillopora verrucosa and Pocillopora eydouxi at Sesoko Island, Okinawa.Galaxea1193105
- 104. Krupp D (1983) Sexual reproduction and early development of the solitary coral Fungia scutaria (Anthozoa: Scleractinia). Coral Reefs 2: 159–164.D. Krupp1983Sexual reproduction and early development of the solitary coral Fungia scutaria (Anthozoa: Scleractinia).Coral Reefs2159164
- 105. Gilmour J (2002) Substantial asexual recruitment of mushroom corals contributes little to population genetics of adults in conditions of chronic sedimentation. Marine Ecology Progress Series 235: 81–91.J. Gilmour2002Substantial asexual recruitment of mushroom corals contributes little to population genetics of adults in conditions of chronic sedimentation.Marine Ecology Progress Series2358191
- 106. Zhao R, Xia H, Bao-Rong L (2009) Fine-scale genetic structure enhances biparental inbreeding by promoting mating events between more related individuals in wild soybean (Glycine soja; Fabaceae) populations. American Journal of Botany 96: 1138–1147.R. ZhaoH. XiaL. Bao-Rong2009Fine-scale genetic structure enhances biparental inbreeding by promoting mating events between more related individuals in wild soybean (Glycine soja; Fabaceae) populations.American Journal of Botany9611381147
- 107. Heywood J (1991) Spatial analysis of genetic variation in plant populations. Annual Review of Ecology and Systematics 22: 335–355.J. Heywood1991Spatial analysis of genetic variation in plant populations.Annual Review of Ecology and Systematics22335355
- 108. Hardy O, Vekemans X (1999) Isolation by distance in a continuous population: reconciliation between spatial autocorrelation analysis and population genetics models. Heredity 83: 145–154.O. HardyX. Vekemans1999Isolation by distance in a continuous population: reconciliation between spatial autocorrelation analysis and population genetics models.Heredity83145154
- 109. Calderon I, Ortega N, Duran S, Becerro M, Pascual M, et al. (2007) Finding the relevant scale: clonality and genetic structure in a marine invertebrate (Crambe crambe, Porifera). Molecular Ecology 16: 1799–1810.I. CalderonN. OrtegaS. DuranM. BecerroM. Pascual2007Finding the relevant scale: clonality and genetic structure in a marine invertebrate (Crambe crambe, Porifera).Molecular Ecology1617991810
- 110. Blanquer A, Uriz M, Caujape-Castells J (2009) Small-scale spatial genetic structure in Scopalina lophyropoda, an encrusting sponge with philopatric larval dispersal and frequent fission and fusion events. Marine Ecology Progress Series 380: 95–102.A. BlanquerM. UrizJ. Caujape-Castells2009Small-scale spatial genetic structure in Scopalina lophyropoda, an encrusting sponge with philopatric larval dispersal and frequent fission and fusion events.Marine Ecology Progress Series38095102
- 111. Pemberton A, Hansson L, Craig S, Hughes R, Bishop J (2007) Microscale genetic differentiation in a sessile invertebrate with cloned larvae: investigating the role of polyembryony. Marine Biology 153: 71–82.A. PembertonL. HanssonS. CraigR. HughesJ. Bishop2007Microscale genetic differentiation in a sessile invertebrate with cloned larvae: investigating the role of polyembryony.Marine Biology1537182
- 112. Yund PO, O'Neil PG (2000) Microgeographic genetic differentiation in a colonial ascidian (Botryllus schlosseri) population. Marine Biology 137: 583–588.PO YundPG O'Neil2000Microgeographic genetic differentiation in a colonial ascidian (Botryllus schlosseri) population.Marine Biology137583588
- 113. David G, Marshall D, Riginos C (2010) Latitudinal variability in spatial genetic structure in the invasive ascidian, Styela plicata. Marine Biology 157: 1955–1965.G. DavidD. MarshallC. Riginos2010Latitudinal variability in spatial genetic structure in the invasive ascidian, Styela plicata.Marine Biology15719551965
- 114. Neigel J, Avise J (1983) Clonal diversity and population structure in a reef-building coral, Acropora cervicornis: self-recognition analysis and demographic interpretation. Evolution. pp. 437–453.J. NeigelJ. Avise1983Clonal diversity and population structure in a reef-building coral, Acropora cervicornis: self-recognition analysis and demographic interpretation.Evolution437453
- 115. Baums IB, Miller MW, Hellberg ME (2006) Geographic variation in clonal structure in a reef-building Caribbean coral, Acropora palmata. Ecological Monographs 76: 503–519.IB BaumsMW MillerME Hellberg2006Geographic variation in clonal structure in a reef-building Caribbean coral, Acropora palmata.Ecological Monographs76503519
- 116. Eckert C, Barrett S (1993) Clonal reproduction and patterns of genotypic diversity in Decodon verticillatus. American Journal of Botany 80: 1175–1182.C. EckertS. Barrett1993Clonal reproduction and patterns of genotypic diversity in Decodon verticillatus.American Journal of Botany8011751182
- 117. Herlihy C, Eckert C (2002) Genetic cost of reproductive assurance in a self-fertilizing plant. Nature 416: 320–323.C. HerlihyC. Eckert2002Genetic cost of reproductive assurance in a self-fertilizing plant.Nature416320323
- 118. Glynn P, Colgan M (1992) Sporadic disturbances in fluctuating coral reef environments: El Nino and coral reef development in the eastern Pacific. Integrative and Comparative Biology 32: 707–718.P. GlynnM. Colgan1992Sporadic disturbances in fluctuating coral reef environments: El Nino and coral reef development in the eastern Pacific.Integrative and Comparative Biology32707718
- 119. Glynn P (1985) El Nino-associated disturbance to coral reefs and post-disturbance mortality by Acanthaster planci. Marine Ecology Progress Series 26: 4.P. Glynn1985El Nino-associated disturbance to coral reefs and post-disturbance mortality by Acanthaster planci.Marine Ecology Progress Series264
- 120. Glynn P (1990) Coral mortality and disturbances to coral reefs in the tropical eastern Pacific. Elsevier oceanography series 52: 55–126.P. Glynn1990Coral mortality and disturbances to coral reefs in the tropical eastern Pacific.Elsevier oceanography series5255126
- 121. Eakin C, Glynn P (1996) Low tidal exposures and reef mortalities in the eastern Pacific. Coral Reefs 15: 120.C. EakinP. Glynn1996Low tidal exposures and reef mortalities in the eastern Pacific.Coral Reefs15120
- 122. LaJeunesse T, Reyes-Bonilla H, Warner M (2007) Spring 'bleaching' among Pocillopora in the Sea of Cortez, Eastern Pacific. Coral Reefs 26: 265–270.T. LaJeunesseH. Reyes-BonillaM. Warner2007Spring 'bleaching' among Pocillopora in the Sea of Cortez, Eastern Pacific.Coral Reefs26265270
- 123. Glynn P (1973) Acanthaster: effect on coral reef growth in Panama. Science 180: 504.P. Glynn1973Acanthaster: effect on coral reef growth in Panama.Science180504
- 124. Glynn P (1988) Predation on coral reefs: some key process, concepts and research directions. Proceedings of the 6th International Coral Reef Symposium 1: 51–62.P. Glynn1988Predation on coral reefs: some key process, concepts and research directions.Proceedings of the 6th International Coral Reef Symposium15162
- 125. Guzman H, Cortes J, Glynn P, Richmond R (1990) Coral mortality associated with dinoflagellate blooms in the eastern Pacific (Costa Rica and Panama). Marine Ecology Progress Series 60: 299–303.H. GuzmanJ. CortesP. GlynnR. Richmond1990Coral mortality associated with dinoflagellate blooms in the eastern Pacific (Costa Rica and Panama).Marine Ecology Progress Series60299303
- 126. Fukami H, Budd A, Levitan D, Jara J, Kersanach R, et al. (2004) Geographic differences in species boundaries among members of the Montastraea annularis complex based on molecular and morphological markers. Evolution 58: 324–337.H. FukamiA. BuddD. LevitanJ. JaraR. Kersanach2004Geographic differences in species boundaries among members of the Montastraea annularis complex based on molecular and morphological markers.Evolution58324337
- 127. Magalon H, Samadi S, Richard M, Adjeroud M, Veuille M (2004) Development of coral and zooxanthella-specific microsatellites in three species of Pocillopora (Cnidaria, Scleractinia) from French Polynesia. Molecular Ecology Notes 4: 206–208.H. MagalonS. SamadiM. RichardM. AdjeroudM. Veuille2004Development of coral and zooxanthella-specific microsatellites in three species of Pocillopora (Cnidaria, Scleractinia) from French Polynesia.Molecular Ecology Notes4206208
- 128. Starger CJ, Yeoh SSR, Dai CF, Baker AC, Desalle ROB (2007) Ten polymorphic STR loci in the cosmopolitan reef coral, Pocillopora damicornis. Molecular Ecology Notes. CJ StargerSSR YeohCF DaiAC BakerROB Desalle2007Ten polymorphic STR loci in the cosmopolitan reef coral, Pocillopora damicornis.Molecular Ecology Notes
- 129. Schuelke M (2000) An economic method for the fluorescent labeling of PCR fragments. Nature Biotechnology 18: 233–234.M. Schuelke2000An economic method for the fluorescent labeling of PCR fragments.Nature Biotechnology18233234
- 130. Peakall R, Smouse PE (2006) GENALEX 6: genetic analysis in Excel. Population genetic software for teaching and research. Molecular Ecology Notes 6: 288–295.R. PeakallPE Smouse2006GENALEX 6: genetic analysis in Excel. Population genetic software for teaching and research.Molecular Ecology Notes6288295
- 131. van Oosterhout C, Hutchinson W, Willis D, Shipley P (2004) MICRO-CHECKER: software for identifying and correcting genotyping errors in microsatellite data. Molecular Ecology Notes 4: 535–538.C. van OosterhoutW. HutchinsonD. WillisP. Shipley2004MICRO-CHECKER: software for identifying and correcting genotyping errors in microsatellite data.Molecular Ecology Notes4535538
- 132. Guo SW, Thompson EA (1992) A Monte-Carlo Method for Combined Segregation and Linkage Analysis. American Journal of Human Genetics 51: 1111–1126.SW GuoEA Thompson1992A Monte-Carlo Method for Combined Segregation and Linkage Analysis.American Journal of Human Genetics5111111126
- 133. Raymond M, Rousset F (1995) Genepop (Version-1.2) - Population-Genetics Software for Exact Tests and Ecumenicism. Journal of Heredity 86: 248–249.M. RaymondF. Rousset1995Genepop (Version-1.2) - Population-Genetics Software for Exact Tests and Ecumenicism.Journal of Heredity86248249
- 134. Rice W (1989) Analyzing tables of statistical tests. Evolution 43: 223–225.W. Rice1989Analyzing tables of statistical tests.Evolution43223225
- 135. Wright S (1951) The genetical structure of populations. Annuals Eugenetics 15: 323–354.S. Wright1951The genetical structure of populations.Annuals Eugenetics15323354
- 136. Kimura M, Crow J (1964) The number of alleles that can be maintained in a finite population. Genetics 49: 725.M. KimuraJ. Crow1964The number of alleles that can be maintained in a finite population.Genetics49725
- 137. Slatkin M (1995) A measure of population subdivision based on microsatellite allele frequencies. Genetics 139: 457.M. Slatkin1995A measure of population subdivision based on microsatellite allele frequencies.Genetics139457
- 138. Kimura M, Ohta T (1978) Stepwise mutation model and distribution of allelic frequencies in a finite population. Proceedings of the National Academy of Sciences 75: 2868.M. KimuraT. Ohta1978Stepwise mutation model and distribution of allelic frequencies in a finite population.Proceedings of the National Academy of Sciences752868
- 139. Excoffier L, Smouse PE, Quattro JM (1992) Analysis of Molecular Variance Inferred from Metric Distances among DNA Haplotypes - Application to Human Mitochondrial-DNA Restriction Data. Genetics 131: 479–491.L. ExcoffierPE SmouseJM Quattro1992Analysis of Molecular Variance Inferred from Metric Distances among DNA Haplotypes - Application to Human Mitochondrial-DNA Restriction Data.Genetics131479491
- 140. Orloci L (1978) Multivariante analysis in vegetation research. The Hange-Boston 135: L. Orloci1978Multivariante analysis in vegetation research.The Hange-Boston135
- 141. Pritchard JK, Stephens M, Donnelly P (2000) Inference of population structure using multilocus genotype data. Genetics 155: 945–959.JK PritchardM. StephensP. Donnelly2000Inference of population structure using multilocus genotype data.Genetics155945959
- 142. Jakobsson M, Rosenberg NA (2007) CLUMPP1: CLUster Matching and Permutation Program Version 1.1 Bioinformatics 23: 1801–1806.M. JakobssonNA Rosenberg2007CLUMPP1: CLUster Matching and Permutation Program Version 1.1 Bioinformatics2318011806
- 143. Rosenberg NA (2004) DISTRUCT: a program for the graphical display of population structure. Molecular Ecology Notes 4: 137–138.NA Rosenberg2004DISTRUCT: a program for the graphical display of population structure.Molecular Ecology Notes4137138
- 144. Evanno G, Regnaut S, Goudet J (2005) Detecting the number of clusters of individuals using the software STRUCTURE: a simulation study. Molecular Ecology 14: 2611–2620.G. EvannoS. RegnautJ. Goudet2005Detecting the number of clusters of individuals using the software STRUCTURE: a simulation study.Molecular Ecology1426112620
- 145. Hardy OJ, Vekemans X (2002) SPAGeDi: a versatile computer program to analyse spatial genetic structure at the individual or population levels. Molecular Ecology Notes 2: 618–620.OJ HardyX. Vekemans2002SPAGeDi: a versatile computer program to analyse spatial genetic structure at the individual or population levels.Molecular Ecology Notes2618620
- 146. Loiselle B, Sork V, Nason J, Graham C (1995) Spatial genetic structure of a tropical understory shrub, Psychotria officinalis (Rubiaceae). American Journal of Botany 82: 1420–1425.B. LoiselleV. SorkJ. NasonC. Graham1995Spatial genetic structure of a tropical understory shrub, Psychotria officinalis (Rubiaceae).American Journal of Botany8214201425
- 147. Ritland K (1996) Estimators for pairwise relatedness and individual inbreeding coefficients. Genetical Research 67: 175–185.K. Ritland1996Estimators for pairwise relatedness and individual inbreeding coefficients.Genetical Research67175185
- 148. Sokal R, Wartenberg D (1983) A test of spatial autocorrelation analysis using an isolation-by-distance model. Genetics 105: 219.R. SokalD. Wartenberg1983A test of spatial autocorrelation analysis using an isolation-by-distance model.Genetics105219