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Novel microsatellite markers for Pyura chilensis reveal fine-scale genetic structure along the southern coast of Chile

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Abstract

Studying the geographic scale of gene flow and population structure in marine populations can be a powerful tool with which to infer patterns of larval dispersal averaged across generations. Here, we describe the development of ten novel polymorphic microsatellite markers for an important endemic ascidian, Pyura chilensis, of the southeastern Pacific, and we report the results from fine-scale genetic structure analysis of 151 P. chilensis individuals sampled from five sites constituting ∼80 km of coastline in southern Chile. All microsatellite markers were highly polymorphic (number of alleles ranged from 12 to 36). Our results revealed significant deviations from Hardy–Weinberg equilibrium (HWE) for most loci, suggesting the presence of either null alleles or deviations from random mating within sampled sites. However, we found a significantly higher spatial autocorrelation and higher mean pairwise relatedness among individuals sampled from the same sites than would be expected if samples were randomly distributed across all sites; this suggests that spatial configuration and reproduction might not be random within sites. Our results indicate the presence of a weak but significant genetic structure between sites (overall F ST = 0.015, p < 0.001). Despite the short pelagic larval duration of this species, geographic distance does not appear to correlate with genetic distances between sites. From the results gathered here, it seems possible that genetic structure at this spatial scale is driven to some extent by local population dynamics (deviations from random mating and/or a large proportion of larvae settling in proximity of relatives), yet infrequent long-distance dispersal events might also be responsible for the relatively weak spatial heterogeneity between sites. Overall, our results both highlight the utility of this new marker set for population genetic studies of this species and provide new evidence regarding the complexity of the small-scale population structure of this species.

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References

  • Almany GR, Hamilton RJ, Bode M, Matawai M, Potuku T, Saenz-Agudelo P, Planes S, Berumen ML, Rhodes KL, Thorrold SR, Russ GR, Jones GP (2013) Dispersal of grouper larvae drives local resource sharing in a coral reef fishery. Curr Biol 23:626–630

    Article  CAS  PubMed  Google Scholar 

  • Astorga MP, Ortiz JC (2006) Variabilidad genética y estructura poblacional del tunicado Pyura chilensis Molina, 1782, en la costa de Chile. Rev Chil Hist Nat 79:423–434. doi:10.4067/S0716-078X2006000400002

    Article  Google Scholar 

  • Benjamini Y, Hochberg Y (1995) Controlling the false discovery rate: a practical and powerful approach to multiple testing. J R Stat Soc Ser B Methodol 57:289–300

    Google Scholar 

  • Ben-Shlomo R, Paz G, Rinkevich B (2006) Postglacial-period and recent invasions shape the population genetics of Botryllid ascidians along European Atlantic coasts. Ecosystems 9:1118–1127. doi:10.1007/s10021-006-0141-y

    Article  Google Scholar 

  • Ben-Shlomo R, Reem E, Douek J, Rinkevich B (2010) Population genetics of the invasive ascidian Botryllus schlosseri from Southern American coasts. Mar Ecol Prog Ser 412:85–92. doi:10.3354/meps08688

    Article  Google Scholar 

  • Castilla JC, Fernandez M (1998) Small-scale benthic fisheries in Chile: on co-management and sustainable use of benthic invertebrates. Ecol Appl 8:S124–S132. doi:10.1890/1051-0761(1998)8[S124:SBFICO]2.0.CO;2

    Article  Google Scholar 

  • Castilla JC, Collins AG, Meyer CP, Guíñez R, Lindberg DR (2002) Recent introduction of the dominant tunicate, Pyura praeputialis (Urochordata, Pyuridae) to Antofagasta, Chile. Mol Ecol 11:1579–1584

    Article  CAS  PubMed  Google Scholar 

  • Cea G (1969) Estadios primarios de desarrollo y metamorfosis de Pyura chilensis Molina, 1782 (Tunicata, Ascidiacea, Pyuridae). Bol Soc Biol Concepción, Tomo XLII:317–331

    Google Scholar 

  • Cea G (1973) Biología del Piure (Pyura chilensis Molina, 1782; Chordata, Tunicata, Ascidiacea). Gayana Zool 28:1–65

    Google Scholar 

  • Costantini F, Fauvelot C, Abbiati M (2007) Fine-scale genetic structuring in Corallium rubrum: evidence of inbreeding and limited effective larval dispersal. Mar Ecol Prog Ser 340:109–119

    Article  CAS  Google Scholar 

  • Dias GM, Duarte LFL, Solferini VN (2006) Low genetic differentiation between isolated populations of the colonial ascidian Symplegma rubra Monniot, C. 1972. Mar Biol 148:807–815

    Article  Google Scholar 

  • Dupont L, Viard F, Dowell MJ, Wood C, Bishop JDD (2009) Fine- and regional-scale genetic structure of the exotic ascidian Styela clava (Tunicata) in southwest England, 50 years after its introduction. Mol Ecol 18:442–453. doi:10.1111/j.1365-294X.2008.04045.x

    Article  CAS  PubMed  Google Scholar 

  • Earl DA, vonHoldt BM (2012) STRUCTURE HARVESTER: a website and program for visualizing STRUCTURE output and implementing the Evanno method. Conserv Genet Resour 4:359–361. doi:10.1007/s12686-011-9548-7

    Article  Google Scholar 

  • Faircloth BC (2008) Msatcommander: detection of microsatellite repeat arrays and automated, locus-specific primer design. Mol Ecol Resour 8:92–4. doi:10.1111/j.1471-8286.2007.01884.x

    Article  CAS  PubMed  Google Scholar 

  • Galindo HM, Pfeiffer-Herbert AS, McManus MA, Chao Y, Chai F, Palumbi SR (2010) Seascape genetics along a steep cline: using genetic patterns to test predictions of marine larval dispersal. Mol Ecol 19:3692–3707. doi:10.1111/j.1365-294X.2010.04694.x

    Article  PubMed  Google Scholar 

  • Giles EC, Saenz-Agudelo P, Hussey NE, Ravasi T, Berumen ML (2015) Exploring seascape genetics and kinship in the reef spong Stylissa carteri in the Red Sea. Ecol Evol 5:2487–2502. doi:10.1002/ece3.1511

    Article  PubMed  PubMed Central  Google Scholar 

  • Guichoux E, Lagache L, Wagner S et al (2011) Current trends in microsatellite genotyping. Mol Ecol Resour 11:591–611. doi:10.1111/j.1755-0998.2011.03014.x

    Article  CAS  PubMed  Google Scholar 

  • Guillot G, Santos F, Estoup A (2008) Analysing georeferenced population genetics data with Geneland: a new algorithm to deal with null alleles and a friendly graphical user interface. Bioinformatics 24:1406–1407. doi:10.1093/bioinformatics/btn136

    Article  CAS  PubMed  Google Scholar 

  • Haye PA, Muñoz-Herrera NC (2013) Isolation with differentiation followed by expansion with admixture in the tunicate Pyura chilensis. BMC Evol Biol 13:252. doi:10.1186/1471-2148-13-252

    Article  PubMed  PubMed Central  Google Scholar 

  • Jones GP, Srinivasan M, Almany GR (2007) Population connectivity and conservation of marine biodiversity. Oceanography 20:100–111

    Article  Google Scholar 

  • Kearse M, Moir R, Wilson A et al (2012) Geneious basic: an integrated and extendable desktop software platform for the organization and analysis of sequence data. Bioinformatics 28:1647–9. doi:10.1093/bioinformatics/bts199

    Article  PubMed  PubMed Central  Google Scholar 

  • Lambert G (2007) Invasive sea squirts: a growing global problem. J Exp Mar Biol Ecol 342(1):3–4

    Article  Google Scholar 

  • Lambert CC, Lambert G (2003) Persistence and differential distribution of nonindigenous ascidians in harbors of the Southern California Bight. Mar Ecol Prog Ser 259:145–161

    Article  Google Scholar 

  • Lancellotti DA, Vasquez JA (2000) Zoogeografía de macroinvertebrados bentónicos de la costa de Chile: contribución para la conservación marina. Rev Chil Hist Nat 73:99–129. doi:10.4067/S0716-078X2000000100011

    Article  Google Scholar 

  • Lynch M, Ritland K (1999) Estimation of pairwise relatedness with molecular markers. Genetics 152(4):1753–1766

    CAS  PubMed  PubMed Central  Google Scholar 

  • Manriquez PH, Castilla JC (2005) Self-fertilization as an alternative mode of reproduction in the solitary tunicate Pyura chilensis. Mar Ecol Prog Ser 305:113–125. doi:10.3354/meps305113

    Article  Google Scholar 

  • Meeker ND, Hutchinson SA, Ho L, Trede NS (2007) Method for isolation of PCR-ready genomic DNA from zebrafish tissues. Biotechniques 43:610–614. doi:10.2144/000112619

    Article  CAS  PubMed  Google Scholar 

  • Nóbrega R, Solé-Cava AM, Russo CAM (2004) High genetic homogeneity of an intertidal marine invertebrate along 8000 km of the atlantic coast of the Americas. Journal of Experimental Marine Biology and Ecology 303(2):173-181

  • Palumbi SR (2004) Marine reserves and ocean neighborhoods: the spatial scale of marine populations and their management. Annu Rev Env Resour 29:31–68

    Article  Google Scholar 

  • Peakall R, Smouse PE (2012) GenAlEx 6.5: genetic analysis in excel. Population genetic software for teaching and research—an update. Bioinformatics 28:2537–9. doi:10.1093/bioinformatics/bts460

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Pérez-Portela R, Turon X (2008) Cryptic divergence and strong population structure in the colonial invertebrate Pycnoclavella communis (Ascidiacea) inferred from molecular data. Zoology 111(2):163–178

    Article  PubMed  Google Scholar 

  • Pritchard JK, Stephens M, Donnelly P (2000) Inference of population structure using multilocus genotype data. Genetics 155(2):945–959

    CAS  PubMed  PubMed Central  Google Scholar 

  • Rousset F (2008) genepop’007: a complete re-implementation of the genepop software for Windows and Linux. Mol Ecol Resour 8:103–6. doi:10.1111/j.1471-8286.2007.01931.x

    Article  PubMed  Google Scholar 

  • Russ GR (2002) Yet another review of marine reserves as reef fishery management tools. In Coral Reef Fishes: Dynamics and Diversity in a Complex Ecosystem, PF Sale, ed. 421–443

  • Saenz-Agudelo P, Dibattista JD, Piatek MJ, Gaither MR, Harrison HB, Nanninga GB, Bermuen ML (2015) Seascape genetics along environmental gradients in the Arabian Peninsula: insights from ddRAD sequencing of anemonefishes. Mol Ecol 24:6241–6255, 10.111/mec.13471

    Article  PubMed  Google Scholar 

  • Sale PF, Cowen RK, Danilowicz BS, Jones G, Kritzer J, Lindeman K, Planes S, Polunin N, Russ G, Sadovy Y (2005) Critical science gaps impede use of no-take fishery reserves. Trends Ecol Evol 20:74–80. doi:10.1016/j.tree.2004.11.007

    Article  PubMed  Google Scholar 

  • Selkoe KA, Toonen RJ (2006) Microsatellites for ecologists: a practical guide to using and evaluating microsatellite markers. Ecol Lett 9:615–629. doi:10.1111/j.1461-0248.2006.00889.x

    Article  PubMed  Google Scholar 

  • Selkoe KA, Watson JR, White C, Horin TB, Iacchei M, Mitarai S, Siegel DA, Gaines SD, Toonen RJ (2010) Taking the chaos out of genetic patchiness: seascape genetics reveals ecological and oceanographic drivers of genetic patterns in three temperate reef species. Mol Ecol. doi:10.1111/j.1365-294X.2010.04658.x

    Article  PubMed  Google Scholar 

  • Sepulveda R, Cancino JM, Thiel M (2003) The peracarid epifauna associated with the ascidian Pyura chilensis (Molina, 1782) (Ascidiacea: Pyuridae). J Nat Hist 37:1555–1569. doi:10.1080/00222930110099615

    Article  Google Scholar 

  • Sepúlveda RD, Rozbaczylo N, Ibáñez CM et al (2014) Ascidian-associated polychaetes: ecological implications of aggregation size and tube-building chaetopterids on assemblage structure in the Southeastern Pacific Ocean. Mar Biodivers 45:733–741. doi:10.1007/s12526-014-0283-7

    Article  Google Scholar 

  • Untergasser A, Cutcutache I, Koressaar T, Ye J, Faircloth BC, Remm M, Rozen SG (2012) Primer3 - new capabilities and interfaces. Nucleic Acids Res 40(15):e115

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Vásquez J (1983) Pyura chilensis Molina 1782 en el Norte del Perú (Ascidacea, Pyuridae). Bol Soc Biol Concepc 54:171–172

    Google Scholar 

  • Vekemans X, Hardy OJ (2004) New insights from fine-scale spatial genetic structure analyses in plant populations. Mol Ecol 13:921–935

    Article  CAS  PubMed  Google Scholar 

  • Weir BS, Cockerham CC (1984) Estimating F-statistics for the analysis of population structure. Evolution 1358–1370

  • Zamorano J, Moreno C (1975) Comunidades bentónicas del sublitoral rocoso de Bahía Corral, 1: Area mínima de muestreo y descripción cuantitativa de la asociación de Pyura chilensis Molina. Medio Ambient 1:58–66

    Google Scholar 

  • Zhan A, Macisaac HJ, Cristescu ME (2010) Invasion genetics of the Ciona intestinalis species complex: from regional endemism to global homogeneity. Mol Ecol 19(21):4678–4694

    Article  CAS  PubMed  Google Scholar 

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Acknowledgements

This study was supported by CONICYT, programa FONDECYT grant no. 11140121 to P.S-A. All sampling was performed with authorization from the Subsecretaria de Pesca y Acuicultura de Chile (permit: P.INV 241/2014). In addition, we thank The Nature Conservancy, Marcelo Antillanca, the Sindicato de Pescadores de Chaihuín, and Jose Martel from Los Molinos for facilitating sample collection in Chaihuín and Los Molinos.

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  1. Instituto de Ciencias Ambientales y Evolutivas, Universidad Austral de Chile, Valdivia, Chile

    E. C. Giles, C. Petersen-Zúñiga, S. Morales-González, S. Quesada-Calderón & Pablo Saenz-Agudelo

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  1. E. C. Giles
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  2. C. Petersen-Zúñiga
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  3. S. Morales-González
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  4. S. Quesada-Calderón
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  5. Pablo Saenz-Agudelo
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Correspondence to Pablo Saenz-Agudelo.

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Communicated by K. Kocot

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Giles, E.C., Petersen-Zúñiga, C., Morales-González, S. et al. Novel microsatellite markers for Pyura chilensis reveal fine-scale genetic structure along the southern coast of Chile. Mar Biodiv 48, 1777–1786 (2018). https://doi.org/10.1007/s12526-017-0672-9

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  • DOI: https://doi.org/10.1007/s12526-017-0672-9

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