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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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Novel Microsatellite Markers for Pyura Chilensis Reveal Fine-Scale Genetic Structure Along the Southern Coast of Chile Mar Biodiv DOI 10.1007/s12526-017-0672-9 ORIGINAL PAPER Novel microsatellite markers for Pyura chilensis reveal fine-scale genetic structure along the southern coast of Chile E. C. Giles1 & C. Petersen-Zúñiga1 & S. Morales-González1 & S. Quesada-Calderón1 & Pablo Saenz-Agudelo1 Received: 25 August 2016 /Revised: 22 February 2017 /Accepted: 23 February 2017 # Senckenberg Gesellschaft für Naturforschung and Springer-Verlag Berlin Heidelberg 2017 Abstract Studying the geographic scale of gene flow and here, it seems possible that genetic structure at this spatial population structure in marine populations can be a powerful scale is driven to some extent by local population dynamics tool with which to infer patterns of larval dispersal averaged (deviations from random mating and/or a large proportion of across generations. Here, we describe the development of ten larvae settling in proximity of relatives), yet infrequent long- novel polymorphic microsatellite markers for an important distance dispersal events might also be responsible for the endemic ascidian, Pyura chilensis, of the southeastern relatively weak spatial heterogeneity between sites. Overall, Pacific, and we report the results from fine-scale genetic struc- our results both highlight the utility of this new marker set for ture analysis of 151 P. chilensis individuals sampled from five population genetic studies of this species and provide new sites constituting ∼80 km of coastline in southern Chile. All evidence regarding the complexity of the small-scale popula- microsatellite markers were highly polymorphic (number of tion structure of this species. alleles ranged from 12 to 36). Our results revealed significant deviations from Hardy–Weinberg equilibrium (HWE) for Keywords Population genetics . Ascidiacea . Isolation by most loci, suggesting the presence of either null alleles or distance . Relatedness deviations from random mating within sampled sites. However, we found a significantly higher spatial autocorrela- tion and higher mean pairwise relatedness among individuals Introduction sampled from the same sites than would be expected if sam- ples were randomly distributed across all sites; this suggests The advent of next-generation sequencing has enhanced our that spatial configuration and reproduction might not be ran- ability to develop and characterize molecular markers (such as dom within sites. Our results indicate the presence of a weak microsatellites or single-nucleotide polymorphisms [SNPs]) but significant genetic structure between sites (overall FST= for non-model species (Guichoux et al. 2011). Hyper- 0.015, p < 0.001). Despite the short pelagic larval duration of variable markers, such as microsatellites, exhibit rapid muta- this species, geographic distance does not appear to correlate tion rates and can accumulate new mutations in a much shorter with genetic distances between sites. From the results gathered time than other markers (Guichoux et al. 2011). Thus, highly variable markers are favored over more slowly evolving nu- clear or mitochondrial markers when measuring recent demo- Communicated by K. Kocot graphic events, detecting minimal genetic variability, Electronic supplementary material The online version of this article reconstructing pedigrees, identifying clones, and examining (doi:10.1007/s12526-017-0672-9) contains supplementary material, parentage (Selkoe and Toonen 2006). which is available to authorized users. Pyura chilensis Molina 1782, commonly known as piure, * Pablo Saenz-Agudelo is a solitary tunicate (Pyuridae) endemic to the southeastern [email protected] Pacific coast of South America, found from Peru (10°S) to the tenth region of Chile (44°S) (Vásquez 1983; Lancellotti and 1 Instituto de Ciencias Ambientales y Evolutivas, Universidad Austral Vasquez 2000). Pyura chilensis inhabits subtidal rocky de Chile, Valdivia, Chile shores, where it can form vast patches, creating a habitat Mar Biodiv matrix for a wide variety of organisms (Zamorano and Materials and methods Moreno 1975; Sepulveda et al. 2003; Sepúlveda et al. 2014). Pyura chilensis is a digonic, protandrous hermaphrodite, and Sample collection, DNA extraction, and sequencing though it has the ability to self-fertilize, it favors cross- fertilization when congeners are nearby (Manriquez and Total DNA was extracted from the siphon tissue of one Castilla 2005). Similar to other benthic tunicates (e.g., see P. chilensis individual from Los Molinos (−39.853, −73.396) Ben-Shlomo et al. 2010), P. chilensis produces short-lived using the High Pure PCR Template Preparation Kit (Roche, free-swimming larvae that spend 12 to 24 h in the water col- Germany), following the manufacturer’s instructions. DNA umn before settling (Cea 1973). This short pelagic larval du- concentration and purity were assessed using the Quant-iT ration (PLD) most likely limits the dispersal potential of PicoGreen dsDNA Assay Kit (Thermo Fisher Scientific) and P. chilensis. Despite this, populations of other ascidians, such a DQ300 fluorometer (Hoefer, Inc., Holliston, MA, USA) as Symplegma rubra and Ciona intestinalis,havebeenfound available at the AUSTRAL-omics core facility of the to be highly connected across large geographic scales (Dias Department of Science at the Austral University of Chile et al. 2006;Zhanetal.2010); human-mediated transport has (www.australomics.cl). The DNA was then used to construct long been thought to facilitate long-range dispersal of ascid- a shotgun library sequenced on a Roche Genome Sequencer ians with naturally low dispersal potential (Lambert 2007). (GS) Junior (Basel, Switzerland). Briefly, 500 ng of genomic In addition to the ecological importance of P. chilensis as a DNA was randomly sheared via nebulization. Double- provider of habitat for many species, it is an important target in stranded adaptors were then blunt-ligated to the sheared Chilean coastal fisheries (Castilla and Fernandez 1998)andis DNA using the GS FLX Titanium Rapid Library Adaptor an important food source for another highly valued fished Kit. The library was then cleaned using magnetic beads abalone, the loco (Concholepas concholepas). Information (Agencourt AMPure XP; Beckman Coulter), and size selec- on larval dispersal and population connectivity is critical for tion of DNA fragments between 400 and 600 bp was visual- the effective management of both of these resources. Others ized using an Agilent Bioanalyzer and the High Sensitivity have shown that knowledge of the spatial scale of dispersal DNA Analysis Kit (Agilent Technologies). The resulting li- can determine which conservation strategies are plausible and brary was then quantified using the DQ300 Hoefer fluorome- how reserves should be spatially arranged to produce sustain- ter. Genomic shotgun library molecules were then clonally able fisheries (Russ 2002, Palumbi 2004, Sale et al. 2005, amplified via emulsion polymerase chain reaction (PCR) fol- Jones et al. 2007). lowing the emPCR Amplification Method Manual Lib-L. To date, only two studies have measured the genetic After emulsion PCR, beads containing sufficient copies of structure of this species, and they used either partial se- clonally amplified library fragments were selected via the quences of nuclear and mitochondrial genes (Haye and specified enrichment procedure and counted using a GS Muñoz-Herrera 2013) or allozyme assays (Astorga and Junior Bead Counter (Roche, Germany) prior to sequencing. Ortiz 2006). Both studies reported significant population Following emulsion PCR enrichment, beads were deposited structure among the sampled locations, and the authors into the wells of a PicoTiterPlate device, and sequencing was suggest that the extent of gene flow at evolutionary time performed. Image analysis, signal processing and base calling scales is more important than was previously thought, were performed using the GS Junior System software (454 given the low dispersal potential of the species. Life Sciences/Roche). Furthermore, it is postulated that connectivity between geographically distant sites could be facilitated by mari- Characterization of microsatellite loci time transport (hitchhiking). While these results shed light on the connectivity of this organism at evolutionary time Using Geneious v6.1.8 software (Kearse et al. 2012), the scales, to our knowledge, the more recent demographic resulting sequence data were filtered to eliminate low-quality gene flow of P. chilensis has yet to be studied, most likely reads or to trim reads at both ends when the chance of a base due to a lack of available molecular markers. calling error was higher than 5%. The trimmed read files were Here we describe the development of ten polymorphic mi- then loaded into the MSATCOMMANDER software program crosatellite markers from next-generation sequencing data and (Faircloth 2008) to identify reads containing uninterrupted small test their application on samples from five sites in southern tandem repeats (minimum of eight repeats) of di-, tri-, and Chile that span approximately 80 km of coastline. These tetranucleotides. MSATCOMMANDER was also used to de- microsatellites are the first reported for this ascidian, and our sign primer pairs on flanking regions of the sequences contain- results reveal the presence of a fine-scale genetic structure in ing microsatellites (optimal annealing temperature = 60 °C, op- this species. These markers will be extremely useful for fur- timal length 20 nt, GC clamp, and remaining default parameters ther study of the genetic structure
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