Abstract
Pocillopora verrucosa is a branching, reef-building coral, and a simultaneous hermaphrodite that reproduces sexually and asexually by fragmentation. In the Gulf of California, local P. verrucosa populations have mixed modes of reproduction which vary in frequency by site. Sexual and asexual reproductions were assessed using multi-locus genotypes deriving from six microsatellite loci at every location. Clone frequencies varied from 0.30 at Loreto to 0.96 in the San Lorenzo Channel. Isla Espíritu Santo and the San Lorenzo Channel were mostly asexual subpopulations, presented the lowest genotypic richness (N g /N = 0.1–0.12) and genotypic diversity (G o /G e = 0.04), and were dominated by one or two multi-loci genotypes (G o /N g = 0.35–0.45). Loreto, El Portugués, and Cabo Pulmo were mostly sexual with high Ng/N (0.80–0.74) and G o /G e (0.52–0.58) and did not show domination by a single multi-locus genotype (G o /N g = 0.70–0.74). There was a significant relationship (P < 0.05) between tropical storm frequency and the genotypic indexes of richness and diversity modeling an inverted U-shape, which indicates that the sites where storm frequencies were the highest had mostly clonal populations; sites exposed to intermediate or low storm frequencies had mostly sexual populations. The study included a restored area (San Lorenzo Channel) where genotypic analyses showed a high level of clonality similar to natural conditions occurring in a nearby subpopulation (Isla Espíritu Santo), which demonstrates the low natural genetic diversity of the area. This study showed that a species with mixed reproduction modes has different maintenance strategies at a regional and even local level among populations indicating the crucial role that storms play in population structure.
References
Adjeroud M, Tsuchiya M (1999) Genetic variation and clonal structure in the scleractinian coral Pocillopora damicornis in the Ryukyu Archipelago, southern Japan. Mar Biol 134:753–760
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
Ayre DJ, Miller KJ (2004) Where do clonal larvae go? Adult genotypic diversity conflicts with reproductive effort in the brooding coral Pocillopora damicornis. Mar Ecol Prog Ser 277:95–105
Ayre DJ, Willis BL (1988) Population structure in the coral Pavona cactus: clonal genotypes show little phenotypic plasticity. Mar Biol 99:495–505
Balart EF, Reyes Bonilla H, De León González JA, Serviere Zaragoza E, Hernández Moreno LG, Cabral Tena R, Mazariegos A, Ortega Rubio A (2010) Proyecto CT001 Programa de monitoreo de la restauración de arrecife coralino afectado por el Buque Tanque Lázaro Cárdenas II, y de las comunidades arrecifales de la región del Parque de Loreto, Baja California Sur. Informe Final para CONABIO. Centro de Investigaciones Biológicas del Noroeste, S.C., La Paz, B.C.S., México, p 80
Baums IB (2008) A restoration genetics guide for coral reef conservation. Mol Ecol 17:2796–2811
Baums IB, Miller MW, Hellberg ME (2005) Regionally isolated populations of an imperiled Caribbean coral, Acropora palmata. Mol Ecol 14:1377–1390
Baums IB, Miller MW, Hellberg ME (2006) Geographic variation in clonal structure in a reef building Caribbean coral, Acropora palmata. Ecol Monogr 76:503–519
Carpizo-Ituarte E, Vizcaíno-Ochoa V, Chi-Barragán G, Tapia-Vázquez O, Cupul-Magaña AL, Medina-Rosas P (2011) Evidence of sexual reproduction in the hermatypic corals Pocillopora damicornis, Porites panamensis, and Pavona gigantea in Banderas Bay, Mexican Pacific. Cienc Mar 37: 97–112
Chávez-Romo HE, Reyes-Bonilla H (2007) Sexual reproduction of the coral Pocillopora damicornis in the southern Gulf of California, México. Cienc Mar 33:495–501
Chávez-Romo HE, Correa-Sandoval F, Paz-García DA, Reyes-Bonilla H, López-Pérez RA, Medina-Rosas P, Hernández-Cortés MP (2008) Genetic structure of a scleractinia coral, Pocillopora damicornis, in the Mexican Pacific. Proc 11th Int Coral Reef Symp:429–433
Coffroth MA, Lasker HR (1998) Population structure of a clonal gorgonian coral: the interplay between clonal reproduction and disturbance. Evolution 52:379–393
Connell JH (1979) Tropical rain forests and coral reefs as open non-equilibrium systems. In: Anderson R, Turner B, Taylor L (eds) Population dynamics. Blackwell, Oxford, pp 141–163
D’Croz L, Mate JL (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
Excoffier L, Laval G, Schneider S (2005) Arlequin 3.0: An integrated software package for population genetics data analysis. Evol Bioinformatics Online 1:47–50
Fautin DG (2002) Reproduction of Cnidaria. Can J Zool 80:1735–1754
Foster NL, Baums IB, Mumby PJ (2007) Sexual vs. asexual reproduction in an ecosystem engineer: the massive coral Montastraea annularis. J Anim Ecol 76:384–391
Glynn PW (1997) Bioerosion and coral reef grow: a dynamic balance. In: Birkeland C (ed) Life and death of coral reefs. Chapman and Hall, New York, pp 68–95
Glynn PW, Gassman NJ, Eakin CM, Cortés J, Smith DB, Guzmán HM (1991) Reef coral reproduction in the eastern Pacific: Costa Rica, Panama, and Galapagos Islands (Ecuador), Part I- Pocilloporidae. Mar Biol 109:355–368
Guo S, Thompson E (1992) Performing the exact test of Hardy-Weinberg proportion for multiple alleles. Biometrics 48:361–372
Harper JL (1977) Population biology of plants. Academic Press, London
Hellberg ME, Burton SE, Neigel JE, Palumbi SR (2002) Genetic assessment of connectivity among marine populations. Bull Mar Sci 70:273–290
Hernández L, Reyes-Bonilla H, Balart EF (2010) Efecto del blanqueamiento del coral por baja temperatura en los crustáceos decápodos asociados a arrecifes del suroeste del golfo de California. Revista Mexicana de Biodiversidad 81:S113–S119
Highsmith RC (1982) Reproduction by fragmentation in corals. Mar Ecol Prog Ser 7:207–226
Hughes TP, Ayre D, Connell JH (1992) The evolutionary ecology of corals. Trends Ecol Evol 7:292–295
Hunter CL (1993) Genotypic variation and clonal structure in coral populations with different disturbance histories. Evolution 47:1213–1228
LaJeunesse TC, Smith R, Walther M, Pinzón J, Pettay DT, McGinley M, Aschaffenburg M, Medina-Rosas P, Cupul-Magaña AL, López Pérez A, Reyes-Bonilla H, Warner ME (2010) Host–symbiont recombination versus natural selection in the response of coral–dinoflagellate symbioses to environmental disturbance. Proc R Soc B 277:2925–2934
Lirman D (2000) Fragmentation in the branching coral Acropora palmata (Lamarck): growth, survivorship, and reproduction of colonies and fragments. J Exp Mar Biol Ecol 251:41–57
Magalon H, Samadi S, Richard M, Adjerou M, Veuille M (2004) Development of coral and zooxanthella-specific microsatellites in three species of Pocillopora (Cnidaria, Scleractinia) from French Polynesia. Mol Ecol Notes 4:206–208
Magalon H, Adjeroud M, Veuille M (2005) Patterns of genetic variation do not correlate with geographical distance in the reef-building coral Pocillopora meandrina in the South Pacific. Mol Ecol 14:1861–1868
Miller KJ, Ayre DJ (2004) The role of sexual and asexual reproduction in structuring high latitude populations of the reef coral Pocillopora damicornis. Heredity 92:557–568
Nei M, Maruyama T, Chakraborty R (1975) The bottleneck effect and genetic variability in populations. Evolution 29:1–10
Nishikawaa A, Kinzie RA, Sakaia K (2009) Fragmentation and genotypic diversity of the scleractinian coral Montipora capitata in Kaneohe Bay, Hawaii. J Mar Biol Assoc U K 89:101–107
Paz-García Chávez-Romo HE, Correa-Sandoval F, Reyes-Bonilla H, López-Pérez A, Medina-Rosas P, Hernández-Cortés MP (2012) Genetic connectivity patterns of corals Pocillopora damicornis and Porites panamensis (Anthozoa: Scleractinia) along the west coast of México. Pac Sci 66:43–61
Pérez-Vivar TL, Reyes-Bonilla H, Padilla C (2006) Corales pétreos (Scleractinia) de las Islas Marías, Pacífico de México. Cienc Mar 32:259–270
Pinzón JH, Reyes-Bonilla H, Baums IB, LaJeunesse TC (2012) Contrasting clonal structure among Pocillopora (Scleractinia) communities at two environmentally distinct sites in the Gulf of California. Coral Reefs. doi:10.1007/s00338-012-0887-y
Reyes-Bonilla H, Calderón-Aguilera LE, Cruz-Piñón G, Medina-Rosas P, López-Pérez RA, Herrero-Perezrul MD, Leyte-Morales GE, Cupul-Magaña AL, CarriquiryBeltrán JD (2006) Atlas de corales pétreos (Anthozoa: Scleractinia) del Pacífico mexicano. Triciclo, México, p 124
Ridgway T, Hoegh-Guldberg O, Ayre DJ (2001) Panmixia in Pocillopora verrucosa from South Africa. Mar Biol 139:175–181
Ridgway T, Riginos C, Davis J, Hoegh-Guldberg O (2008) Genetic connectivity patterns of Pocillopora verrucosa in southern African Marine Protected Areas. Mar Ecol Prog Ser 354:161–168
Rogers CS (1993) Hurricanes and coral reefs: the intermediate disturbance hypothesis revisited. Coral Reefs 12:127–137
Sherman CDH, Ayre DJ, Miller KJ (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
Smith LD, Hughes TP (1999) An experimental assessment of survival, re-attachment and fecundity of coral fragments. J Exp Mar Biol Ecol 235:147–164
Souter P, Henriksson O, Olsson N, Grahn M (2009) Patterns of genetic structuring in the coral Pocillopora damicornis on reefs in East Africa. BMC Ecol 26:9–19
Starger CJ, Yeoh SSR, Dai CF, Baker AC, Desalles R (2008) Ten polymorphic STR loci in the cosmopolitan reef coral, Pocillopora damicornis. Mol Ecol Resources 8:619–621
Stoddart JA (1983) Asexual production of planulae in the coral Pocillopora damicornis. Mar Biol 76:279–284
Stoddart JA, Taylor JF (1988) Genotypic diversity: estimation and prediction in samples. Genetics 118:705–711
Szmant AM (1986) Reproductive ecology of Caribbean reef coral. Coral Reefs 5:43–47
Underwood JN, Smith LD, van Oppen MJH, Gilmour J (2007) Multiple scales of genetic connectivity in a brooding coral on isolated reefs following catastrophic bleaching. Mol Ecol 16:771–784
Valière N (2002) Gimlet: a computer program for analyzing genetic individual identification data. Mol Ecol Notes 2:377–379
Vermeij MJA, Sandin SA, Samhouri JF (2007) Local habitat distribution determines the relative frequency and interbreeding potential for two Caribbean coral morphospecies. Evol Ecol 21:27–47
Waits LP, Luikart G, Taberlet P (2001) Estimating the probability of identity among genotypes in natural populations: cautions and guidelines. Mol Ecol 10:249–256
Whitaker K (2006) Genetic evidence for mixed modes of reproduction in the coral Pocillopora damicornis and its effect on population structure. Mar Ecol Prog Ser 306:115–124
Williams GC (1975) Sex and evolution. Princeton University, Princeton, NJ
Yoshida K, Nakagawa M, Wada S (2005) Multiplex PCR system applied for analysing microsatellite loci of Schlegel’s black rockfish, Sebastes schlegeli. Mol Ecol Notes 5:416–418
Acknowledgments
We thank J. J. Ramírez-Rosas, M. Cota-Castro, and R. Cabral-Tena from CIBNOR and L. F. Drew-Morales, J. Rabadan-Sotelo, and D. Vazquez-Arce from UABCS for their enthusiastic assistance in the field. Ira Fogel, Diana Fischer from CIBNOR and Rubén E. García Gomez from CICMAR provided important editorial services. This research was supported by the Comisión Nacional para el Conocimiento y Uso de la Biodiversidad of México (CONABIO grant GD001). Partial funding came from the Consejo Nacional de Ciencia y Technología of México (CONACYT grant 83339). F.A.G. was a recipient of a graduate fellowship from CONACYT.
Author information
Authors and Affiliations
Corresponding author
Additional information
Communicated by Biology Editor Dr. Ruth Gates
Rights and permissions
About this article
Cite this article
Aranceta-Garza, F., Balart, E.F., Reyes-Bonilla, H. et al. Effect of tropical storms on sexual and asexual reproduction in coral Pocillopora verrucosa subpopulations in the Gulf of California. Coral Reefs 31, 1157–1167 (2012). https://doi.org/10.1007/s00338-012-0941-9
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00338-012-0941-9