Contrasting Clonal Structure Among Pocillopora (Scleractinia) Communities at Two Environmentally Distinct Sites in the Gulf of California

Coral Reefs (2012) 31:765–777 DOI 10.1007/s00338-012-0887-y

REPORT

Contrasting clonal structure among Pocillopora (Scleractinia) communities at two environmentally distinct sites in the Gulf of California

J. H. Pinzo´n • H. Reyes-Bonilla • I. B. Baums • T. C. LaJeunesse

Received: 21 July 2011 / Accepted: 1 February 2012 / Published online: 3 March 2012 Ó Springer-Verlag 2012

Abstract The contributions of sexual versus asexual clone (genet) dominated a large portion (90.9 m long) of the reproduction are thought to play an important role in the protected leeward side of Gaviota Island (Number of genets/ abundance and ecological success of corals, especially in Number of samples = 0.35; observed Genotypic diversity/ marginal habitats. Pocillopora corals are distributed expected Genotypic diversity = 0.087), while an exposed throughout the Indo-Pacific and dominate shallow hard- community at the entrance to La Paz Bay, Punta Galeras, bottom communities in the eastern Pacific where broad exhibited high genotypic diversity (Ng/N = 0.85; Go/ seasonal fluctuations in temperature and water turbidity Ge = 0.714). Gene flow was unrestricted between sites create suboptimal conditions for reef community develop- indicating these communities comprised a single population. ment. Previous work had revealed three genetic clades in the The relative proportion of asexual colonies found between eastern Pacific that show little correspondence with colony community aggregations of Pocillopora in the Gulf of Cal- morphology; the broad distribution of type 1 extends into the ifornia differed significantly and suggests factors at local, not subtropical southern Gulf of California. Here we examine regional, scales affect these patterns. The possibility that genetic and clonal structure of two type 1 communities heterogeneity in clonal structure is common throughout the separated by 10 km with microsatellite data. Samples were eastern Pacific and across the west Indo-Pacific requires collected randomly in six 10 m radius circular plots (20 further study. Finally, since morphological variation in Po- colonies per plot, 3 plots per site). Sites differed in their cillopora has been underappreciated and is in need of taxo- relative clonality because clonemates (ramets) from a single nomic revision, the use of a consistent field-sampling protocol and high-resolution makers will advance ecological research and aid in the conservation of these corals. Communicated by Biology Editor Dr. Ruth Gates Keywords Clonal reproduction Á Eastern Tropical Electronic supplementary material The online version of this article (doi:10.1007/s00338-012-0887-y) contains supplementary Pacific Á Microsatellites Á Pocillopora Á material, which is available to authorized users. Population structure

J. H. Pinzo´n Á I. B. Baums Á T. C. LaJeunesse Department of Biology, The Pennsylvania State University, 221 Mueller Lab, University Park, PA 16802, USA Introduction

Present Address: Among animals capable of both sexual and asexual repro- & J. H. Pinzoń( ) duction, the relative contribution of each reproductive mode Department of Biology, The University of Texas Arlington, 501 South Nedderman, Arlington, TX 76019, USA influences demography, genetic diversity, and evolution e-mail: [email protected] among and between populations (Jackson 1986; Halkett et al. 2005; Eckert et al. 2008). Both modes of reproduction offer H. Reyes-Bonilla advantages under different environmental conditions (Crow Departamento de Biologıá Marina, Universidad Autonoma de Baja California Sur, Apartado postal 19-B, 23080 La Paz, BCS, 1992). Because highly clonal species tend to dominate local Mexico stable habitats through intraspecific competition, asexual 123 766 Coral Reefs (2012) 31:765–777 reproduction is usually important to local persistence settlement is relatively low (Birkeland 1977; Highsmith (Tatarenkov et al. 2005). In contrast, sexual recombination 1982; Richmond 1985; 1987b; Glynn et al. 1991). Because increases diversity and contributes to long-range dispersal type 1 in the ETP lack asexual brooded larvae, clonal and the colonization of new habitats and is therefore favored reproduction is restricted to branch fragmentation, which in variable and/or unpredictable environments (Williams can generate numerous clone mates from small numbers of 1975). sexually produced individuals (Richmond 1987a). Scleractinian corals are a notable example of clonal ani- Earlier assumptions presumed that sexual reproduction mals that can exhibit both sexual and asexual life history was limited among Eastern Tropical Pacific populations strategies (Harrison and Wallace 1990; Harrison 2011). As (Richmond 1987a). Recent phylogenetic and population average sea surface temperatures increase and coral popu- genetic analysis of Pocillopora morphospecies in the ETP lations colonize habitats at higher latitudes (Marsh 1993; concluded that much of the community comprises one Precht and Aronson 2004; Vargas-Angel et al. 2003; Ya- genetically cohesive population, Pocillopora type 1 (Pinzoń mano et al. 2011), the relative contribution of clonal versus and LaJeunesse 2011, but see Combosch and Vollmer sexual propagation might therefore be expected to change. 2011). These data suggest that sexually produced larvae There is some indication that clonal replication is important contribute significantly to the size of a population and that for maintaining populations of corals in peripheral high- demes of Pocillopora type 1 are relatively homogenized by latitude habitats. In Florida, the northernmost limit of the frequent and widespread dispersal. However, samples for distribution of Acropora palmata, stands of this species are these population genetic studies were obtained in a manner highly clonal compared to other more central populations in that avoided potential clone mates and likely missed small- the Caribbean (Baums et al. 2006). Studies on the relative scale spatial patterns (\10 m) in clonal structure. influence of sexual and asexual reproduction have often To further address speculation about what reproductive focused on the branching species of the common coral genus mode dominates eastern Pacific populations of Pocillo- Pocillopora (Stoddart 1983, 1984a, b, c; Ayre et al. 1997; pora, the relative prevalence and spatial distribution of Adjeroud and Tsuchiya 1999; Ridgway et al. 2001; Miller asexually reproduced colonies in the Gulf of California and Ayre 2004; Whitaker 2006; Yeoh and Dai 2010). Clo- were investigated. Colonies were sampled randomly from nality measured among and between populations of these replicate circular plots (10 m in radius) (cf. Baums et al. corals varies widely throughout the Indo-Pacific and such 2006) at two sites with different habitat characteristics. differences may be attributed to particular environmental One site was situated on the protected leeward side of a conditions and/or disturbance frequency (Ayre et al. 1997; small island and the other was located 10 km away at the Baird et al. 2009). In addition, data on the genetic diversity northern end of an exposed peninsula near the entrance to and level of clonality among populations from environ- La Paz Bay. Seven microsatellite loci were used to assess mentally marginal and/or isolated locations are limited (but how asexual reproduction contributes to the genetic struc- see Miller and Ayre 2004). ture of Pocillopora type 1 near to its upper latitudinal range Environments of the Eastern Tropical Pacific (ETP, also by examining genotypic diversity, clonemate proximity, referred as Tropical Eastern Pacific) are considered sub- and genetic connectivity. optimal for most scleractinians, yet communities of abundant individuals comprising a small number of coral genera (Psammacora, Pavona, Porites, and Pocillopora; Reyes- Materials and methods Bonilla 1992) can dominate shallow hard bottom habitats ranging from 1–7 m in depth. Many of these communities Collection sites and sampling are often dominated by colonies of Pocillopora spp. (Glynn 1976; Cortes 1997). Recent phylogenetic and population Collections from Pocillopora colonies were made at two genetic analysis of Pocillopora morphospecies in the sites, Punta Galeras (PGAL) and Gaviota Island (ISLG) off ETP concluded that much of the community comprises La Paz, Baja California Sur, Mexico (Fig. 1). These reefs one genetically cohesive population, Pocillopora type 1, differ from each other in their habitable area and exposure despite major morphological differences among colonies to currents and wave action. PGAL at the head of a pen- (Pinzoń and LaJeunesse 2011). Histological studies in the insula north of La Paz is situated on a gradually sloping region have found the same reproductive patterns across platform with rock boulders mixed with pockets of sand. different morphologically defined species, indicating that PGAL is exposed to significant wave action and deep Gulf tropical and subtropical populations of Pocillopora spp. waters carried by currents across the San Lorenzo channel broadcast spawn and appear to release eggs and sperm (Jimeńez-Illescaz 1996). ISLG is situated well within La during late summer months (Richmond 1987a; Glynn et al. Paz Bay and is protected from wave action and experiences 1991; Cha´vez-Romo and Reyes-Bonilla 2007), yet sexual limited current strengths. Here, the coral communities are 123 Coral Reefs (2012) 31:765–777 767

Fig. 1 Study sites of Pocillopora type 1 at Punta N Galeras (PGAL) and Gaviota Island (ISLG) in La Paz Bay, Isla Espíritu Gulf of California

San Lorenzo Channel

250 km

PGAL

ISLG Bay of La Paz

5 km situated on a narrow platform that slopes steeply into deep LaJeunesse et al. (2003). A small piece of skeleton bearing water approximately 20 m from the island. animal tissue was combined with glass beads (Ceroglass, At each site, three randomly selected circular plots (10 m Columbia, USA) and 600 ll of a cell lysis solution (0.2 M radius) whose centers were separated by at least 30 m were Tris, 2 mM EDTA, 0.7% SDS, pH 7.6), and shaken at high surveyed following the methods described by Baums et al. speed using a BioSpec beadbeater. The extract was then (2006) and GPS coordinates of the centers of each plot were incubated with 3 ll proteinase K (20 mg/ml) at 65°C for recorded (Garmin, Etrex Venture HC). Briefly, coordinates 1 h. After incubation, proteins were precipitated from (compass bearing and distance from the center) were ran- solution using ammonium acetate (9 M) and the sample domly generated in Excel for each plot (Microsoft). To avoid stored at -20°C overnight. The frozen extract was centri- re-sampling of the same colony, increments were set to 1 fuged (10,000 g), the supernatant removed and placed into a degree and 50 cm, respectively. Each sample coordinate new tube, and the DNA precipitated from solution with was located using a compass and measuring tape attached to 100% isopropanol, and centrifuged (10,000 g for 5 min.). the center of the plot via SCUBA. Colonies directly under- The DNA pellet was washed with 70% EtOH, air dried, and neath a coordinate were sampled; if no colony existed, the resuspended in 75 ll of distilled water and stored at -20°C. next random coordinate was used until a total of 20 colonies To verify the identity of the colony type (sensu Pinzoń were visited. From each colony, a small fragment (1–3 cm) and LaJeunesse 2011), the mitochondrial open reading was removed, placed into a numbered zip-lock bag, fixed in frame (ORF) was amplified with the FATP6.1 and the sodium chloride–20% DMSO buffer (Seutin et al. 1991), RORF primers (Flot et al. 2008). Amplified products were and stored at -20°C. sequenced with the forward primer using Big Dye 3.1 terminator mix (Applied Biosystems) following the man- DNA extraction, sequencing, and microsatellite ufacturer’s protocol on an ABI Hitachi 3730XL genetic genotyping analyzer. DNA sequence chromatograms were reviewed and edited using Geneious Pro 5.0 (Drummond et al. 2009). Genomic DNA extractions were performed using a non- Multilocus genotypes were obtained using a set of seven toxic Promega wizard (Madison, WI) protocol modified by microsatellite loci (Pd3-002, Pd3-005, Pd2-006, Pd2-007,

123 768 Coral Reefs (2012) 31:765–777

Pd3-008, Pd3-009, and Poc40—Starger et al. 2007; Pinzoń equal number of ramets. A third parameter for the char- and LaJeunesse 2011). Loci amplifications and allele acterization of a clonal population, the Pareto distribution scoring were done after Pinzoń and LaJeunesse (2011). (Arnaud-Haond et al. 2007), was not estimated here Singleplex reactions using primers labeled with different because this statistic is not defined when only one genet is dyes (HEX and FAM) were combined in pairs and ran with present as was the case at ISLG. an internal size standard (LIZ—500; Applied Biosystems), Spatial arrangement of genets was assessed based on on an ABI Hitachi 3730XL genetic analyzer. Alleles were aggregation (Ac) and edge effect (Ee) indices (Arnaud- identified and scored with GeneMarker 1.6 (Softgenetics, Haond et al. 2007). The aggregation index (Ac) describes State College PA). the degree to which ramets of the same MLL are spatially

aggregated. It is estimated as Ac = (Psg-Psp)/Psg; where Analysis of clonal structure Psg is the average probability of clonal identity of all sample pairs and Psp is the average probability of clonal Clonal structure was assessed with the software GenClone identity among pairwise nearest neighbors. It ranges from V2.0 (Arnaud-Haond and Belkhir 2007), unless otherwise zero (random distribution) to one (clonal aggregation). Its specified. This package includes all statistical procedures significance is tested by randomly assigning samples to the suggested for the study of clonality in natural populations sampling coordinates and comparing those distributions to (Baums et al. 2006; Arnaud-Haond et al. 2007). The first the observed data. The sampling design can bias estimates step was to assign samples to genets, followed by esti- of genotypic diversity through edge effects. If edge effects mating the genotypic diversity and the spatial arrangements are present, rare MLLs are found more frequently toward of the genets. the edges of the sampled area (i.e., the polar plots). The

All samples that shared identical alleles at all loci (i.e., edge effect index is given by Ee = (Du-Da)/Da; where Du had identical multilocus genotypes, MLGs) were consid- is the average geographic distance between unique MLLs ered to be the product of asexual reproduction (identical and center of the polar plots and Da is the average geo- by descent). Together all samples with the same MLG graphic distance between all samples and the center of the (ramets) comprised one genet. The high variability of the polar plots. The null hypothesis of random distribution of microsatellite markers used here resulted in a very low MLGs irrespective of their number of ramets is tested with -6 probability (Pid = 4.2 9 10 ) that samples with the same a permutation procedure (Arnaud-Haond et al. 2007) in this MLG were identical by chance rather than the result of case set to 1,000 permutations. Finally, a test of spatial asexual reproduction and thus this method of assigning autocorrelation was implemented in GenAlex v.6.3 samples to genets was justified. Then, because genotyping (Peakall and Smouse 2006) to determine whether or not the errors and somatic mutations can cause slight allelic dif- genotypes are distributed randomly within the circular ferences among ramets of the same genet, all pairwise plots (Smouse and Peakall 1999). allelic differences among genets were calculated (Arnaud- Haond et al. 2007). Following the identification of samples Analysis of genetic connectivity with single allele differences and correcting scoring errors, samples were assigned to distinct multilocus lineages Tests for population differentiation incorporating only the (MLLs). unique multilocus lineages (MLLs, n = 66) were per- Two indices were estimated to assess clonal population formed between circular plots and sites using Analysis of structure. (1) The clonal richness index (R) was calculated Molecular Variance (AMOVA) calculated in GenAlex as R = Ng-1/N-1, where Ng is the number of MLLs, and V6.3 (Peakall and Smouse 2006). Rst and Fst values were N is the total number of samples. This index varies from acquired to determine the degree of similarity/differentia- zero, when all samples belong to a single genet, to one tion between populations. This procedure was repeated when each sample represents a unique MLG (Arnaud- with corrected allele frequencies after null alleles were Haond et al. 2005, 2007). (2) Genotypic evenness was detected in three loci (Pd3-002, Pd2-006, and Pd3-009) calculated to describe the equitability in the distribution of using Microchecker (van Oosterhout et al. 2004). Exact the MLLs in the sample set (Arnaud-Haond et al. 2007). tests for Hardy–Weinberg Equilibrium (HWE) and het- Evenness was estimated with the Simpson’s evenness erozygote deficiencies were performed in Genepop on the complement index (V = (D-Dmin)/(Dmax-Dmin)). With D, web (Raymond and Rousset 1995; Rousset 2008); P values the observed diversity, Dmax the value assumed if all genets were adjusted using a Bonferroni procedure. Inbreeding have the same number of ramets, and Dmin the diversity rates per plot, reef, and in total were assessed with the value when all but one genet has one individual (Hurlbert RMES software (David et al. 2007). 1971). V values range from zero when a single genet Additionally, a Bayesian analysis to determine the most dominates the population to one when each genet has an likely number of genetically homogenous clusters (K) 123 Coral Reefs (2012) 31:765–777 769 in the dataset was conducted using Structure V2.3.X ramets of the same genet. Out of the 119 samples analyzed (Pritchard et al. 2000) assuming admixture, correlated (a sample from ISLG2 was lost), a total of 72 unique MLGs allele frequencies, and specifying a location prior. Con- were detected, with 6 of these showing evidence of somatic ditions were set to 1,000,000 chain length after a mutations (defined by a single allele difference between burn-in of 100,000 assuming admixture. Simulations were MLGs), resulting in a total of 66 MLLs that were retained run between K = 1 and K = 10 with 5 replicates for each for all further population genetic analysis. K value. The optimal K was detected with Structure Clear differences in the ratio of genets to samples were Harvester (Earl 2009) and graphs were drawn using the observed among locations (Table 1; Fig. 2). An average of Distruct V1.1 software (Rosenberg 2004) after all repli- 6.5 and 16.0 MLLs were found in each plot at ISLG and cates for each K were analyzed in Clumpp V1.1.2 PGAL, respectively. A MLL was found more than once in (Jakobsson and Rosenberg 2007). nine instances from plots at PGAL and the number of MLLs per plot ranged from two to four. At this site, genets were not shared among plots (Fig. 2a). In contrast, only one, albeit Results large, genet with 43 ramets was found at ISLG. This genet was abundant in all three plots, comprising the most common Clonal identity and relative abundance MLL in each (Fig. 2a). Genotype richness (R) therefore differed between locations, with significantly higher values Sequences of the mitochondrial DNA ORF identified all found in PGAL (0.772 ± 0.060; mean ± SD) compared to 119 colonies as Pocillopora type 1 (sensu Pinzoń and ISLG (0.286 ± 0.027; mean ± SD) values (t test P = LaJeunesse 2011). To analyze clonal structure of these 0.001). Dominance of a single genet in ISLG resulted in a samples, seven microsatellite loci were employed. The low average evenness (V) 0.562 ± 0.026 (mean ± SD) number of loci was higher than the minimum suggested by compared to PGAL (0.965 ± 0.0194; mean ± SD) Genclone for the assessment of clonal structure in these (Table 1). The high genotype richness and evenness at populations. The seven loci used had a high probability PGAL indicated that this was a ‘‘mostly sexual’’ population -6 (Pid = 4.2 9 10 ) of distinguishing unique genets from while ISLG was a mostly ‘‘asexual population.’’

Table 1 Estimates of the indices of clonal structure for samples taken from circular plots from two populations of Pocillopora type 1, Gulf of California, Mexico Isla Gaviota Punta Galeras ISLG1 ISLG2 ISLG3 PGAL1 PGAL2 PGAL3 Sample size (N) 20 19 20 20 20 20

Genotypic Diversity and richness Unique genotypes (Ng) 6 6 7 15 17 15

R = (Ng21/N21) 0.26 0.28 0.32 0.74 0.84 0.74

G = Ng/N 0.30 0.32 0.35 0.75 0.85 0.75

Gd = Go/Ge 0.09 0.10 0.10 0.67 0.71 0.53 Shannon (H) 0.97 1.00 1.15 2.65 2.76 2.55 Simpson (D) 0.45 0.47 0.52 0.97 0.98 0.95 Hill’s 1.81 1.88 2.09 38.00 47.50 21.11

NC = N/Ng 3.33 3.17 2.86 1.33 1.18 1.33 Genotypic Evenness Simpson (V) 0.00 0.00 0.00 0.86 0.47 0.51 Shannon (HV) 0.54 0.56 0.59 0.98 0.98 0.94

GE = Go/Ng 0.29 0.30 0.28 0.95 0.98 0.95 Pareto n.e. n.e. n.e. n.e. -1.76 -1.10

Spatial Edge Effect (Ee) 0.19 -0.05 0.05 0.106* 0.06 -0.03

Aggregation (Ac) -0.09 0.12 0.06 0.06 0.132* 0.06

Genetic diversity Observed (Ho) 0.41 0.26 0.36 0.39 0.50 0.43

Expected (He) 0.55 0.42 0.52 0.43 0.49 0.40 Indices in bold are explained in the text. Additional explanations on these indices can be found in Arnaoud-Haond (2007) P 2 Go = (1/ gi ); Ge = N; NC mean clonal size; n.e. not estimated * Signiﬁcant after Bonferroni corrections

123 770 Coral Reefs (2012) 31:765–777

Fig. 2 a Randomized polar plot a Giant clone Clonal genotypes sampling schemes and genotypic identities of colonies Unique genotypes from ISLG and PGAL. b Pairwise genetic distance ISLG1 PGAL 1 calculations among colony multilocus genotypes sampled at ISLG and PGAL, respectively. The dominance of a single common genet at ISLG is evidenced by the presence of a prominent peak representing short genetic distances between ramets of the same genet (Plots are 10 m in radius) 2 2

3 3

b clonally represented genotypes 2.0

1.5

1.0 Frequency

0.5

0 50 100 151 200 250 300 50 100 151 200 250 300 Genetic distance (pairwise)

Spatial autocorrelation analyses did not reveal deviation (Table 1). Ramets in ISLG were separated by an average of from random distributions of MLLs within a plot. Fur- 6.7 ± 3.3 m (mean ± SD) within each plot; however, as thermore, there were no signiﬁcant levels (P \ 0.05) of stated above, this genet was distributed in all three plots clonal aggregation at either location, with the exception of with one ramet pair separated by 90.9 m (Table 2). PGAL2 where ramets were aggregated (Ac = 0.132; p = 0.006). At PGAL, the average overall pairwise dis- No genetic differentiation between sites tance between clonemates was 9.2 ± 4.6 m (mean ± SD) with a maximum and minimum of 12.5 m and 3.0 m, The allelic compositions of Pocillopora type 1 at ISLG were respectively (Table 2). Signiﬁcant edge effects, after indistinguishable from PGAL. Pairwise comparisons among

Bonferroni corrections, were observed only in PGAL1 plots and between sites (Rst =-0.009, P = 0.530 and (Ee = 0.10; P = 0.002), yet this plot did not show signif- Fst = 0.007, P = 0.080) revealed no signiﬁcant difference icant levels of clonal aggregation (Ac = 0.062; P = 0.334) in the population genetic structure. These values can be

123 Coral Reefs (2012) 31:765–777 771

Table 2 Number and average distance (m) between ramets for each asexually versus sexually produced recruits (Dorken and multi locus lineages (MLL) found in Punta Galeras (PGAL) and Isla Eckert 2001; Honnay and Bossuyt 2005). Therefore, Gaviota (ISLG) asexual propagation in low density coral communities may Clone Plot Ramets Distance (SD) allow a population to persist until enough genetically distinct individuals are present in high abundance to overcome PGAL Allee effects (Knowlton 2001; Baums et al. 2006). Alter- A 1 2 7.7 natively, environmental conditions at the margins might B 1 2 5.2 exert strong selection pressure on recruits favoring C 1 2 3.0 fragments from locally adapted genets over recombinant D 1 2 12.5 settlers (Ayre 1984). E 1 2 11.7 F 2 2 8.0 Genetic and genotypic diversity between aggregations G 2 3 6.4 (4.4) of Pocillopora H 3 4 11.5 (5.6) I 3 3 9.9 (4.3) The relative proportion of asexual colonies found between ISLG community aggregations of Pocillopora in the Gulf of J 1 15 6.2 (3.0) California differed significantly and suggests factors at 2 14 6.5 (3.5) local, not regional, scales affect these patterns. In contrast 3 14 7.5 (3.5) to expectations, numerous unique, genetically diverse, ALL 43 6.7 (3.3) and sexually recombinant MLLs (genotypes) were found Clones from PGAL are organized to match the symbols in Fig. 1 among Pocillopora communities in the Gulf of California (Fig. 2a, b). With the notable exception of one prevalent genet at ISLG, rarely was a genet found to contain large overestimated by the presence of possible null alleles, which numbers of ramets. However, while clonal propagation appeared significant for three loci (Pd3-002, Pd2-006, and was important at ISLG, all other colonies at this site were Pd3-009) that were not in HWE (P \ 0.05). Significant products of sexual reproduction (Table 2; Fig. 2a). In other frequencies of homozygous individuals did not appear to regions of the Eastern Pacific, populations of the morpho- result from inbreeding (P [ 0.05) or amplification mistakes species Pocillopora damicornis in Panama comprised (i.e., homozygous samples were re-amplified under different unique individuals, the independent products of sexual conditions resulting in the same genotype). Population recombination, whereas clonemates were rarely identified divergence calculations, after alleles frequencies corrections (*8% of samples; Combosch and Vollmer 2011). While for the loci with putative null alleles, again did not reveal investigations carried out in the less environmentally any difference between sites (Rst = 0.023; P = 0.100 and variable, Eastern Tropical Pacific intended to evaluate Fst = 0.014; P = 0.050). Bayesian simulations showed connectivity (not clonal structure) among P. damicornis congruent results with those from the AMOVA and the populations, it suggests that asexual reproduction contrib-

Rst and Fst values, with an optimal number of genetically utes little to genetic structure in this region (at least over different clusters (i.e., populations) set to one (K = 1; spatial scales larger than 10 m, see sampling protocol of Electronic Supplemental Material, ESM Fig. S1). Combosch and Vollmer 2011). Pocillopora type 1 populations throughout the ETP appear genetically diverse and interconnected (Pinzoń and Discussion LaJeunesse 2011; although see Combosch and Vollmer 2011) in contrast to earlier suppositions that Pocillopora Populations located at the margins of a species distribution populations in the region were exclusively asexual (Rich- often exhibit low genetic variation due to isolation, mond 1987b). The lack of population subdivision between inbreeding, and/or genetic drift (Brown 1984; Kapralov ISLG and PGAL indicate that populations in the Gulf 2004). Genotypic diversity usually decreases toward the receive recruits from locations 10 km or more apart and are margins of species’ ranges in terrestrial (Widen et al. 1994; not necessarily dependent on self-seeding. Type 1 Pocil- Dorken and Eckert 2001; Eckert 2002) and marine plants lopora are broadcast spawners (Richmond 1987b; Glynn (Tatarenkov et al. 2005), and sedentary animals (e.g., et al. 1991; Cha´vez-Romo and Reyes-Bonilla 2007), and anemones, Ayre 1984; corals, Baums et al. 2006). This while Pocillopora spawning has yet to be formally docu- increase in clonality toward the margins has been explained mented in the ETP, it likely occurs during mid summer to by Allee effects: lower population densities offer fewer early fall based histological evidence (Cha´vez-Romo and mating opportunities resulting in a relative increase of Reyes-Bonilla 2007). These genetic data clearly indicate 123 772 Coral Reefs (2012) 31:765–777 that sexually produced larvae recruit frequently. Reyes- Because these data were generated from just two loca- Bonilla (1993) studied the mode of recruitment in a pop- tions, further sampling from comparable ‘‘exposed’’ and ulation at Cabo Pulmo, located in the most southern part of ‘‘protected’’ sites will validate the generality of our find- the Gulf. By examining the skeletons of whole colonies, he ings and conclusions. Indeed, other factors (i.e., historical found that 41% of individuals had originated as settled contingency, physiological and ecological adaptations, and larvae, whereas 59% grew from a fragmented branch local extinction), or their combined effects (Ayre 1984; indicating that asexual propagation was important at this Gaston 2009), may offer alternate explanations for the location. These data suggest that local factors in the Gulf of presence of a large clone at ISLG. Therefore, while these California contribute to the success of clonal lineages. findings are preliminary, they offer a template for additional sampling among different habitats found at a loca- Local factors influence clonal structure tion, different found locations within a region, and across regions (Baums et al. 2006). Local environmental conditions and small-scale disturbances influence variation in clonality at small spatial Contribution of asexual reproduction to population scales (Widen et al. 1994; Baums et al. 2006). The marked maintenance across the Indo-Pacific contrast in clonal structure observed between ISLG and PGAL suggests that differences in habitat affect the rela- Populations of Pocillopora spp from east coast of Africa tive success of clonal propagation (Fig. 1). The clonal (Ridgway et al. 2001), Western Australia (Stoddart 1984b, population of Pocillopora at ISLG is situated on a narrow 1984c; Whitaker 2006), Indonesian Archipelago (Starger (20 m wide) shelf along the protected leeward side of a et al. 2010); the Great Barrier Reef (GBR) (Benzie et al. small island (Gaviota Island) and is rarely exposed to 1995; Ayre et al. 1997; Sherman et al. 2006), Lord Howe disturbances from storm surges. Under normal conditions, Island (Miller and Ayre 2004), Japan (Adjeroud and water currents move slowly back and forth along the shore Tsuchiya 1999), Taiwan (Yeoh and Dai 2010) Hawaii and are influenced by tidal direction (Zaytsev et al. 2010). (Stoddart 1984a), and eastern (Combosch and Vollmer However, hurricanes periodically enter La Paz Bay from 2011) and south Pacific (Magalon et al. 2005) show vary- the southwest (usually one hurricane, or major storm, every ing patterns of genetic diversity, genotypic diversity, and/ 2 years; National Hurricane Center), and on these occa- or connectivity (Table 3). While sampling protocols in sions ISLG is exposed to intense wave energy that damages these studies were not designed to explicitly assess clonal and fragments colonies (pers obs). Afterward, stable con- structure (Baums et al. 2006), populations at certain loca- ditions return for periods of time (many months to years) tions were highly clonal (Stoddart 1984a; Yeoh and Dai that allow for fragmented colonies to reattach and grow. 2010). In contrast, populations of the morphospecies These conditions may explain the spread, persistence, and P. verrucosa from the east coast of Africa and P. dami- dominance of a large clone across all three ISLG plots cornis along the GBR were genetically diverse, highly extending more than 90.9 m (Fig. 2a). By contrast, all connected, and exhibited little clonality within each sam- other MLLs found at this location were unique and well pling site (Stoddart 1984b, 1984c; Ridgway et al. 2001). differentiated from this dominant genet. The reduced Some studies identified sites with significant differences in genotypic diversity at ISLG may therefore be the result of clonal structure within a region similar to that observed for (1) competitive exclusion by a locally adapted clone and/or PGAL and ISLG. For example, while many populations in (2) limited access to larval recruits. Western Australia appeared mostly clonal (similar to In comparison with the low energy environment of ISLG), other populations were genetically diverse (similar ISLG, the site at PGAL is exposed to fast moving surface to PGAL; Stoddart 1984b, 1984c; Whitaker 2006). currents entering and leaving La Paz Bay from the Gulf and Finally, the majority of these studies were based on al- experiences greater wave energy especially in winter when lozyme variation, markers that typically lack the resolving wind and storm generated swells regularly contact the power of microsatellites (Delmotte et al. 2002), are not shallow sloping shelf (Fig. 1). The population of Pocillo- scored with the same precision, and exhibit allelic fre- pora at this site is large and positioned across the San quencies that are potentially affected by local selection Lorenzo channel from an even larger population situated pressures (Benzie et al. 1995; Sherman et al. 2006). Indeed off the southern end of Espiritu Santo Island (Hernańdez these markers showed genetic differentiation between the et al. 2009a, 2009b, 2010). Plots sampled at PGAL Gulf of California and more southern locations from exhibited few clonemates and most colonies were dissim- mainland Mexico (Cha´vez-Romo et al. 2009), whereas ilar in allelic composition indicating high levels of sexual higher resolution microsatellite markers do not (Pinzoń recruitment (Fig. 2b), perhaps influenced by its proximity and LaJeunesse 2011). Despite the possibility that com- to other large populations. paring studies based on protein variation with recent 123 oa ef 21)31:765–777 (2012) Reefs Coral Table 3 Summary of genetic indices from studies investigating the genotypic variation and clonality among populations of Pocillopora spp examined at various spatial scales (* These studies did not address sexuality directly; km kilometers, Ng number of unique genotypes)

Paper Pocillopora Region Location Habitat Geographic Genetic Range of Ng/N (mean) Range of Go/Ge (mean) Population Observed morphospecies Range (km) Marker (# connectivity Range heterozygosity loci) of Fst (mean) (Ho)

Stoddart damicornis Indian Ocean— Rottness Island, Not specified 500 Allozymes 0.15–0.75 (0.18) 0.09–0.61 (0.40) 0.08–0.30 (0.21) (1984a, c) Western Lancelin, Jurian (10) Australia Bay, and Houtman Abrolhos Islands Stoddart damicornis Central Kaneobe Bay Reef flat 10 Allozymes 43 Unique MLG/320 samples N/A (1984b) Pacific— (10) Hawaii Benzie et al. damicornis Pacific—Great One Tree Island Lagoon, microatolls, and 1 Allozymes 0.81–0.96 0.72–1.03 0.00–0.16 0.43–0.50 (1995) Barrier Reef Crest (6) Adjeroud and damicornis Pacific— Ryukyu Shallow (\2 m) reef flat 650 Allozymes 0.47–0.75 0.30 –0.64 0.03–0.09 (0.06) 0.24–0.37 Tsuchiya Southern Archipelago (7) (1999) Japan Ayre et al. damicornis Pacific—Great Lizard Island, Reef Crest 1,200 Allozymes 0.54–0.96 0.63–1.01 (0.08) (1997) Barrier Reef Davies Reefs, (7) and Heron Isl. Ridgway et al. verrucosa Indian Ocean— KwaZulu Natal Reef Slope (12–15 m) 100–150 Allozymes 0.55–0.81 0.52–0.79 0.02–0.04 0.11–0.15 (2001) South Africa (5) Ayre and damicornis Pacific— One Tree Island Reef Crest 2 Allozymes 0.64–0.87 0.87–1.03 (0.04) Miller Eastern (7) (2004)* Australia Miller and damicornis Pacific— Lord Howe Island Protected and Exposed sites 2 Allozymes 0.55–0.86 (0.58) 0.55–0.91 (0.61) (0.10) Ayre (2004) Eastern (8) Australia Magalon et al. meandrina South Pacific Tonga, Society Outer reef slope *2,000 Microsats 0.85–1.00 (0.94) 0.00–0.16 0.56–0.86 (2005)* Islands, Bora (4) Bora, Moorea, Tahiti Sherman et al. damicornis Pacific—Great One Tree Island Reef flat, lagoon, patch 0.2–1 Allozymes 0.68–0.92; 0.54–0.65 0.69–1.00; 0.35–0.53 0.06 ± 0.01 0.22–0.40 (2006)* Barrier Reef reefs, microatolls, and the (8) (sites with recent (sites with recent reef slope mortality) mortality) Whitaker damicornis Indian Ocean— Ningaloo Reef and Back reef and Lagoon 800 Allozymes 0.41–1.00 0.07–0.77 0.02–0.59 (0.36) (2006) Western Houtman (\5m) (6) Australia Abrolhos Islands Souter (2010)* damicornis Indian Ocean– 10 reefs Not specified *800 Microsats 0.35–0.46 Tanzania and (6) Kenya Starger et al. damicornis Indonesia Numerous Not specified *2,800 Microsats 0.80—1.00 (0.98) 0.00–0.21 (0.05) 0.07–0.91 (2010)* Archipelago locations (9) Yeoh and Dai damicornis Pacific— Nanwan Bay Non specified, but close to a 0.5 Microsats 0.32–0.44 Not given 0.22–0.38 (2010) Southern power plant (7) Taiwan 123 773 774 Coral Reefs (2012) 31:765–777

investigations using DNA markers may confound inter- pretations, both approaches indicate that the relative

) importance of sexual versus asexual processes in main- o H 0.38–0.62 Observed heterozygosity ( taining Pocillopora populations may ultimately depend on the region, locality, and/or habitat. One challenge is to determine whether and/or how local patterns and processes inﬂuence larger regional processes.

(mean) The present body of work on the clonal structure, st F population connectivity, and life history strategies per- 0.01–0.18 0.00–0.23 (0.05) Total 0.05 connectivity Range of ceived among populations of Pocillopora in the wider Paciﬁc may be confounded by inaccurate taxonomic res- (mean) Population

e olution. The incongruence between genetic and morpho- G / o

G logical data suggests that the current morphospecies designations of Pocillopora need revision (Flot et al. 2010; Souter 2010; Pinzo´n 2011; Pinzo´n and LaJeunesse 2011). For example, colonies that appear to be P. damicornis in one region may not be a member of the same evolutionary

(mean) Range of lineage at another location, and colonies that appear N / g

N morphologically different may actually be the same species while colonies that appear similar may represent cryptic taxa (Souter 2010; Pinzo´n and LaJeunesse 2011). 0.35–0.85 0.09–0.71 0.03 0.26–0.50 0.82–1.00 Pairwise Range of In certain regions, such as the ETP where morphology does not relate to species identity (Pinzo´n and LaJeunesse 2011), samples should be pre-screened by sequencing (7) (7) (5) Genetic Marker (# loci) phylogenetically informative markers to identify the genetic lineage of a colony so that population level analyses are correctly applied and results between studies are

Range (km) directly comparable. For example, Combosch and Vollmer (2011) appear to have combined two morphologically cryptic species (presumably types 1 and 3, sensu Pinzo´n and LaJeunesse 2011) in their investigation of population genetic structure along the coast of Panama. Indeed 3 m) 10 Microsats 3 m) 5,000 Microsats 3 m) 300 Microsats \ \ \ Bayesian analyses using the software Structure (Pritchard et al. 2000) unambiguously identify two lineages (K = 2) that when analyzed separately reveal no population Reef Crest ( structure over the geographic range of their study sites. The use of multiple molecular markers with differing amounts of genetic resolution ultimately improves accu- racy in assessing Scleractinian biodiversity, ecology, and

Southern Mexico, Clipperton, Panama, and Galapagos evolution, and should be incorporated in all future research La Paz Bay Reef Crest ( La Paz Bay, Panama Reef Crest ( (e.g., Budd et al. 2010; Pinzoń and LaJeunesse 2011). Finally, reef coral populations are under significant pressure from a variety of disturbances related to local and global stressors (Pandolfi et al. 2003, Hoegh-Guldberg et al. California Pacific Pacific Gulf of Eastern Tropical Eastern Tropical Region Location Habitat Geographic 2007). How these animals will respond ecologically may depend on numerous factors including their rate and mode of reproduction (Edinger and Risk 1995; Kerr et al. 2011). Among the Pocillopora spp., the dominant mode of repro- Type 1 Type 1 damicornis Pocillopora morphospecies duction in a particular population or species may influence their responsiveness and/or long-term persistence and must continued

* * be considered when developing management strategies for ) ) n and

´ their protection and conservation (Baums 2008). As pre- 2011 2011 Vollmer ( LaJeunesse ( Combosch and This work Pinzo Table 3 Paper sented here, data generated using a standardized approach to 123 Coral Reefs (2012) 31:765–777 775 evaluate these populations over various spatial scales Cha´vez-Romo HE, Reyes-Bonilla H (2007) Reproduccioń sexual del improves our comprehension of underlying ecological pro- coral Pocillopora damicornis al sur del Golfo de California, Me´xico. Cienc Mar 33:495–501 cesses. Ideally, the further application of this sampling and Cha´vez-Romo HE, Correa-Sandoval F, Paz-Garcıá D, Reyes-Bonilla genetic analysis may help with local and regional conser- H, Lo´pez-Pe´rez RA, Medina-Rosas P, Hernańdez-Corte´sMP vation efforts. (2009) Genetic structure of the scleractinian coral, Pocillopora damicornis, from the Mexican Pacific. Proc 11th Int Coral Reef Acknowledgments We thank Tye Pettay and Mark Warner for Symp 1:429–433 assistance in the field and the Penn State Genomics Core Facility— Combosch D, Vollmer S (2011) Population genetics of an ecosystem- University Park, PA. Comments of three anonymous reviewers help defining reef coral Pocillopora damicornis in the Tropical in the final version of the manuscript. This research was funded in part Eastern Pacific. PLoS ONE 6(8):e21200 by The Pennsylvania State University, the National Science Foun- Cortes J (1997) Biology and geology of eastern Pacific coral reefs. dation (IOB 544854 and OCE 09287664), and an Alfred P. Sloan Coral Reefs 16:S39–S46 Scholarship to JP. Crow J (1992) An advantage of sexual reproduction in a rapidly changing environment. J Hered 83:169–173 David P, Pujol B, Viard F, Castella V, Goudet J (2007) Reliable selfing rate estimates from imperfect population genetic data. Mol Ecol 16:2474–2487 Delmotte F, Leterme N, Gauthier JP, Rispe C, Simon JC (2002) References Genetic architecture of sexual and asexual populations of the aphid Rhopalosiphum padi based on allozyme and microsatellite Adjeroud M, Tsuchiya M (1999) Genetic variation and clonal markers. Mol Ecol 711–723 structure in the scleractinian coral Pocillopora damicornis in Dorken ME, Eckert C (2001) Severely reduced sexual reproduction in the Ryukyu Archipelago, southern Japan. Mar Biol 134:753–760 northern populations of a clonal plant, Decodon verticillatus Arnaud-Haond S, Belkhir K (2007) GENCLONE: a computer (Lythraceae). J Ecol 89:339–350 program to analyse genotypic data, test for clonality and Drummond A, Ashton B, Cheung M, Heled J, Kearse M, Moir R, describe spatial clonal organization. Mol Ecol Notes 7:15–17 Stones S, Thiere T, Wilson A (2009) Geneious v4.8, Available Arnaud-Haond S, Alberto F, Teixeira S, Procaccini G, Serrao E, from http://www.geneious.com/ Duarte C (2005) Assessing genetic diversity in clonal organisms: Earl DA (2009) Structure Harvester v0.3, website: http://users.soe. low diversity or low resolution? Combining power and cost ucsc.edu/*dearl/software/struct_harvest/ efficiency in selecting markers. J Hered 96:434 Eckert C (2002) The loss of sex in clonal plants. Evol Ecol Arnaud-Haond S, Duarte C, Alberto F, Serrao E (2007) Standardizing 15:501–520 methods to address clonality in population studies. Mol Ecol Eckert C, Samis K, Lougheed S (2008) Genetic variation across 16:5115–5139 species’ geographical ranges: the central-marginal hypothesis Ayre DJ (1984) The effects of sexual and asexual reproduction on and beyond. Mol Ecol 17:1170–1188 geographic variation in the sea anemone Actinia tenebrosa. Edinger E, Risk MJ (1995) Preferential survivorship of brooding Oecologia 62:222–229 corals in a regional extinction. Paleobiology 21(2):200–219 Ayre DJ, Miller KJ (2004) Where do clonal coral larvae go? Adult Flot J, Magalon H, Cruaud C, Couloux A, Tillier S (2008) Patterns of genotypic diversity conflicts with reproductive effort in the genetic structure among Hawaiian corals of the genus Pocillo- brooding coral Pocillopora damicornis. Mar Ecol Prog Ser pora yield clusters of individuals that are compatible with 277:95–105 morphology. Comptes Rendus Biologies 331:239–247 Ayre DJ, Hughes TP, Standish RJ (1997) Genetic differentiation, Flot J-F, Couloux A, Tillier S (2010) Haplowebs as a graphical tool reproductive mode, and gene flow in the brooding coral for delimiting species: a revival of Doyle’s ‘‘field for recombi- Pocillopora damicornis along the Great Barrier Reef, Australia. nation’’ approach and its application to the coral genus Mar Ecol Prog Ser 159:175–187 Pocillopora in Clipperton. BMC Evol Biol 10:372 Baird A, Guest J, Willis B (2009) Systematic and biogeographical Gaston KJ (2009) Geographic range limits: achieving synthesis. Proc patterns in the reproductive biology of scleractinian corals. Annual R Soc B 276:1395–1406 Review of Ecology, Evolution and Systematics 40:552–571 Glynn PW (1976) Some physical and biological determinant of coral Baums IB (2008) A restoration genetics guide for coral reef community structure in the Eastern Pacific. Ecol Monogr conservation. Mol Ecol 17:2796–2811 46:431–456 Baums IB, Miller MW, Hellberg ME (2006) Geographic variation in Glynn PW, Gassman N, Eakin C, Cortes J, Smith DB, Guzman H clonal structure in a reef-building Caribbean coral, Acropora (1991) Reef coral reproduction in the eastern Pacific: Costa Rica, palmata. Ecol Monogr 76:503–519 Panama, and Galapagos Islands (Ecuador). Mar Biol 109:355–369 Benzie JAH, Haskell A, Lehman H (1995) Variation in the genetic Halkett F, Simon J, Balloux F (2005) Tackling the population composition of coral (Pocillopora damicornis and Acropora genetics of clonal and partially clonal organisms. Trends Ecol palifera) populations from different reef habitats. Mar Biol Evol 20:194–201 121:731–739 Harrison PL (2011) Sexual reproduction of scleractinian corals. In: Birkeland C (1977) The importance of rate biomass accumulation on Dubinsky Z, Stambler N (eds) Coral reefs: An ecosystem in successional stages of benthic communities survival of coral transition. Springer, London, pp 59–85 recruits. Proc 3rd Int Coral Reef Symp 1:15–21 Harrison PL, Wallace CC (1990) Reproduction, dispersal and recruit- Brown J (1984) On the relationship between abundance and ment of scleractinian corals. In: Dubinsky Z (ed) Coral reefs distribution of species. Am Nat 124:255–279 Ecosystems of the world 25. Elsevier, Amsterdam, pp 133–207 Budd A, Romano S, Smith N, Barbeitos M (2010) Rethinking the Hernańdez L, Balart EF, Reyes-Bonilla H (2009a) Checklist of reef phylogeny of scleractinian corals: A review of morphological decapod crustaceans (Crustacea: Decapoda) in the southern Gulf and molecular data. Intgr Comp Biol 50:411–427 of California, Me´xico. Zootaxa 2119:39–50

123 776 Coral Reefs (2012) 31:765–777

Hernańdez L, Balart EF, Reyes-Bonilla H (2009b) Effect of hurricane Pritchard JK, Stephens M, Donnelly P (2000) Inference of population John (2006) on the invertebrates associated with corals in Bahıá structure using multilocus genotype data. Genetics 155:945–959 de La Paz, Gulf of California. Proc 11th Int Coral Reef Symp: Raymond M, Rousset F (1995) GENEPOP (version1.2): population 301–304 genetics software for exact tests and ecumenicism. J Hered 86: Hernańdez L, Reyes-Bonilla H, Balart EF (2010) Efecto del 248–249 blanqueamiento del coral por baja temperatura en los crustaćeos Reyes-Bonilla H (1992) New records for hermatypic corals(Anthozoa: deca´podos asociados a arrecifes del suroeste del golfo de Scleractinia) in the Gulf of California, Mexico, with an historical California. Revista Mexicana de Biodiversidad: 1–7 and biogeographical discussion. J Nat Hist 26:1163–1175 Highsmith R (1982) Reproduction by fragmentation in corals. Mar Reyes-Bonilla H (1993) Estructura de la comunidad, influencia de la Ecol Prog Ser 7:207–226 depredacioń y biologıá poblacional de corales hermatı´picos en el Hoegh-Guldberg O, Mumby PJ, Hooten H, Steneck, Greenfield P, arrecife de Cabo Pulmo, B.C.S. MSc Thesis, Centro de Gomez E, C. Harvell CD, Sale P, Edwards A, Caldeira K, Investigacioń Cientı´fica y de Educacioń Superior de Ensenada, Knowlton N, Eakin CM, Iglesias-Prieto R, Muthiga N, Bradbury Departamento de Ecologıá, p 169 B, Dubi A, Hatziolos M (2007) Coral reefs under rapid climate Richmond R (1985) Variations in the population biology of Pocil- change and ocean acidification. Science 318:1737–1742 lopora damicornis across the Pacific. Proc 5th Int Coral Reef Honnay O, Bossuyt B (2005) Prolonged clonal growth: escape route Symp 1:101–107 or route to extinction? Oikos 108:427–432 Richmond R (1987a) Energetics, competency, and long-distance Hurlbert S (1971) Nonconcept of species diversity—critique and dispersal of planula larvae of the coral Pocillopora damicornis. alternative parameters. Ecology 52:577–586 Mar Biol 93:527–533 Jackson JBC (1986) Modes of dispersal of clonal benthic inverte- Richmond RH (1987b) Energetic relationships and biogeographical brates: consequences for species’ distributions and genetic differences among fecundity, growth and reproduction in the reef structure of local populations. Bull Mar Sci 39:588–606 coral Pocillopora damicornis. Bull Mar Sci 41:594–604 Jakobsson M, Rosenberg N (2007) CLUMPP: a cluster matching and Ridgway T, Hoegh-Guldberg O, Ayre DJ (2001) Panmixia in permutation program for dealing with label switching and Pocillopora verrucosa from South Africa. Mar Biol 139:175 multimodality in analysis of population structure. Bioinformatics Rosenberg N (2004) DISTRUCT: a program for the graphical display 23:1801–1806 of population structure. Mol Ecol Notes 4:137–138 Jimeńez-Illescaz AR (1996) Ana´lisis de procesos barotro´picos y Rousset F (2008) Genepop’007: a complete re-implementation of the baroclıńicos en la Bahıá de La Paz. ICML-UNAM, B. C. S. 168 genepop software for Windows and Linux. Mol Ecol Resources Kapralov M (2004) Genotypic variation in populations of the clonal 8:103–106 plant Saxifraga cernua in the Central and Peripheral Regions of Seutin G, White BN, Boag PT (1991) Preservation of avian blood and the species range. Russ J Ecol 35:413–416 tissue samples for DNA analyses. Can J Zool 69:82–90 Kerr AM, Baird AH, Hughes TP (2011) Correlated evolution of sex Sherman CDH, Ayre DJ, Miller KJ (2006) Asexual reproduction does and reproductive mode in corals (Anthozoa: Scleractinia). Proc not produce clonal populations of the brooding coral Pocillopora R Soc B 278:75–81 damicornis on the Great Barrier Reef, Australia. Coral Reefs Knowlton N (2001) The future of coral reefs. Proc Natl Acad Sci 25:7–18 USA 96:5419–5425 Smouse P, Peakall R (1999) Spatial autocorrelation analysis of LaJeunesse TC, Low WKW, von Woesik R, Hoegh-Guldbery O, individual multiallele and multilocus genetic structure. Heredity Schmidt GW, Fitt WR (2003) Low symbiont diversity in 82:561–573 southern Great Barrier Reef corals relative to those in the Souter P (2010) Hidden genetic diversity in a key model species of Caribbean. Limnol Oceangr 48:2046–2054 coral. Mar Biol 157:875–885 Magalon H, Adjeroud M, Vauille M (2005) Patterns of genetic Starger CJ, Yeoh SSR, Dai C-F, Baker AC, DeSalle R (2007) Ten variation do not correlate with geographical distance in the reef- polymorphic STR loci in the cosmopolitan reef coral, Pocillo- building coral Pocillopora meandrina in the south Pacific. Mol pora damicornis. Mol Ecol Resourc 8:619–621 Ecol 14:1861–1868 Starger CJ, Barber PH, Ambariyanto, Baker AC (2010) The recovery Marsh L (1993) The occurrence and growth of Acropora in extra- of coral genetic diversity in the Sunda Strait following the 1883 tropical waters off Perth, Western Australia. Proc 7th Int Coral eruption of Krakatau. Coral Reefs 29:547–565 Reef Symp 2:1233–1238 Stoddart JA (1983) Asexual production of planulae in the coral Miller KJ, Ayre DJ (2004) The role of sexual and asexual Pocillopora damicornis. Mar Biol 76:279–284 reproduction in structuring high latitude populations of the reef Stoddart JA (1984a) Biochemical genetics of Pocillopora damicornis coral Pocillopora damicornis. Heredity 92:557–568 in Kaneobe Bay, Oahu, Hawaii. Hawaii Inst Mar Biol, Tech Pandolfi JM, Bradbury RH, Sala E, Hughes TP, Bjorndal KA, Cooke Report 37:133–150 RG, Mcardle D, McClenachan L, Newman MJH, Paredes G, Stoddart JA (1984b) Genetical structure within populations of the Warner RR, Jackson JB (2003) Global trajectories of the long- coral Pocillopora damicornis. Mar Biol 81:19–30 term decline of coral reef ecosystems. Science 301:955–958 Stoddart JA (1984c) Genetic differentiation amongst populations of Peakall R, Smouse PE (2006) Genalex 6: genetic analysis in Excel. the coral Pocillopora damicornis off Southwestern Australia. Population genetic software for teaching and research. Mol Ecol Coral Reefs 3:149–156 Notes 6:288–295 Tatarenkov A, Bergstrom L, Jonsson R, Serraõ E, Kautsky L, Johannes- Pinzoń JH (2011) Phylogenetics, population genetics and ecology to son K (2005) Intriguing asexual life in marginal populations of the understand the evolution of coral-algal mutualisms. Ph.D brown seaweed Fucus vesiculosus. Mol Ecol 14:647–651 dissertation, The Pennsylvania State University, p 154 van Oosterhout C, Hutchinson WF, Wills DPM, Shipley P (2004) Pinzoń JH, LaJeunesse TC (2011) Species delimitation of reef Micro-checker: software for identifying and correcting genotyp- building corals using nucleotide sequence phylogenies, popula- ing errors in microsatellite data. Mol Ecol Notes 4:535–538 tion genetics, and symbiosis ecology. Mol Ecol 20:311–325 Vargas-Angel B, Thomas JD, Hoke SM (2003) High-latitude Precht WF, Aronson RB (2004) Climate flickers and range shifts of Acropora cervicornis thickets off Fort Lauderdale, Florida, reef corals. Front Ecol Environ 2:307–314 USA. Coral Reefs 22:465–473

123 Coral Reefs (2012) 31:765–777 777

Whitaker K (2006) Genetic evidence for mixed modes of reproduc- temperatures. Geophys Res Lett 38: L04601, p 6. doi:10.1029/ tion in the coral Pocillopora damicornis and its effect on 2010GL046474 population structure. Mar Ecol Prog Ser 306:115–124 Yeoh S-R, Dai C-F (2010) The production of sexual and asexual Widen B, Cronberg N, Widen M (1994) Genotypic diversity, larvae within single broods of the scleractinan coral, Pocillopora molecular markers and spatial distribution of genets in clonal damicornis. Mar Biol 157:351–359 plants, a literature review. Folio Geobot Phytotax 29:245–263 Zaytsev O, Rabinovich AB, Thomson RE, Silverberg N (2010) Williams G (1975) Sex and evolution. Princetown University Press, Intense diurnal surface currents in the Bay of La Paz, Mexico. Princetown, NJ Cont Shelf Res 608–619 Yamano H, Sugihara K, Nomura K (2011) Rapid poleward range expansion of tropical reef corals in response to rising sea surface

123