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Putative Selected Markers in the Chionodraco Genus Detected by Interspecific Outlier Tests

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Putative Selected Markers in the Chionodraco Genus Detected by Interspecific Outlier Tests View metadata, citation and similar papers at core.ac.uk brought to you by CORE provided by Electronic Publication Information Center Polar Biol DOI 10.1007/s00300-013-1370-0 ORIGINAL PAPER Putative selected markers in the Chionodraco genus detected by interspecific outlier tests Cecilia Agostini • Chiara Papetti • Tomaso Patarnello • Felix C. Mark • Lorenzo Zane • Ilaria A. M. Marino Received: 14 March 2013 / Revised: 20 June 2013 / Accepted: 27 June 2013 Ó Springer-Verlag Berlin Heidelberg 2013 Abstract The identification of loci under selection (out- Three outlier loci were identified, detecting a higher dif- liers) is a major challenge in evolutionary biology, being ferentiation between species than did neutral loci. Outliers critical to comprehend evolutionary processes leading to showed sequence similarity to a calmodulin gene, to an population differentiation and speciation, and for conser- antifreeze glycoprotein/trypsinogen-like protease gene and vation purposes, also in light of recent climate change. to nonannotated fish mRNAs. Selective pressures acting on However, detection of selected loci can be difficult when outlier loci identified in this study might reflect past evo- populations are weakly differentiated. This is the case of lutionary processes, which led to species divergence and marine fish populations, often characterized by high levels local adaptation in the Chionodraco genus. Used loci will of gene flow and connectivity, and particularly of fish provide a valuable tool for future population genetic living in the Antarctic marine environment, characterized studies in Antarctic notothenioids. by a complex and strong circulating system promoting individual dispersal all around the continent. With the final Keywords Genome-wide selection scan Á Genetic aim of identifying outlier loci putatively under selection in differentiation Á Local adaptation Á EST-linked the Chionodraco genus, we used 21 microsatellites, microsatellites Á Standardized FST Á Antarctic icefish including both genomic (Type II) and EST-linked loci (Type I), to investigate the genetic differentiation among the three recently derived Chionodraco species that are Introduction endemic to the freezing Antarctic waters. Neutrality tests were applied in interspecific comparisons in order to The idea that marine species are genetically homogeneous identify candidate loci showing high levels of genetic dif- throughout their range of distribution is traditionally ferentiation, which might reveal imprints of past selection. assumed. Large population sizes and wide spatial distri- butions, associated with an extensive potential for dis- persal, in the absence of evident barriers to gene flow, are Electronic supplementary material The online version of this supposed to limit genetic structuring among local popula- article (doi:10.1007/s00300-013-1370-0) contains supplementary tions (Ward et al. 1994). Typically, genetic studies of material, which is available to authorized users. natural populations employ neutral molecular markers, like C. Agostini Á C. Papetti Á L. Zane (&) Á I. A. M. Marino SNPs and microsatellites, which permit to elucidate various Department of Biology, University of Padova, Padua, Italy aspects of species biology. These loci also allow the esti- e-mail: [email protected] mation of demographic parameters, such as effective T. Patarnello population size and migration rate, the inference of which Department of Comparative Biomedicine and Food Science, would be biased by the effects of natural selection acting in University of Padova, Agripolis, Legnaro, Padua, Italy a locus-specific manner (Avise 1994). The growing interest in understanding the genetic bases of ecologically impor- F. C. Mark Integrative Ecophysiology, Alfred Wegener Institute for Polar tant traits and in studying local adaptation has, however, and Marine Research, Bremerhaven, Germany gradually shifted the attention to genetic markers 123 Polar Biol influenced by natural selection, as revealed by the devel- morphological differences and molecular data (Fischer and opment of several methods aimed at detecting putative Hureau 1985; Patarnello et al. 2003), are thought to have selected loci from genome-wide scans (Bowcock et al. diverged between 2 and 1.8 millions of years ago (addi- 1991; Beaumont and Nichols 1996; Vitalis et al. 2001; tional result not reported in Near et al. 2012). Furthermore, Schlo¨tterer 2002; Porter 2003; Beaumont and Balding we performed an FST-based survey to search for loci 2004; Foll and Gaggiotti 2008). showing a high level of genetic differentiation between the In fish, genome scan studies accomplished so far, in three Chionodraco species and thus possibly influenced by which many individuals were screened using randomly selective forces acting during their shallow evolutionary selected molecular markers, reported very few instances of history. To allow future investigations at the population outlier detection; these cases include several members of level, we used a panel of loci, including both microsatellites the Salmonidae family (e.g., Freamo et al. 2011; Seeb et al. originally isolated from genomic DNA and EST-linked 2011), which are well known to be highly structured, some loci, that cross-amplified in all the three species. Cross- coral reef fishes (e.g., Fauvelot et al. 2007), and a number amplified molecular markers, such as microsatellites, have of other economically important species like Atlantic cod proven to be valuable tools for species discrimination and (e.g., Nielsen et al. 2009) and Atlantic herring (e.g. Andre´ individual assignment to nominal species also in the noto- et al. 2010). Difficulties in finding selected loci in marine thenioid family Trematominae (Van de Putte et al. 2009). fishes may be referred to the limited power of available programs to identify outlier loci when population differ- entiation is weak. Most of the existing statistical methods Materials and methods for detecting recent signatures of selection from allele frequency data are based on the original idea developed by Sample collection and DNA extraction Lewontin and Krakauer (1973), according to which loci showing a significantly higher or lower level of genetic Population samples of C. hamatus, C. myersi, and C. ra- differentiation than expected under an appropriate neutral strospinosus were collected between 1988 and 2007 at four population-genetics model can be considered candidates different locations: the Weddell Sea, the Ross Sea (Terra- for being influenced by directional (adaptive) or balancing nova Bay), and the Antarctic Peninsula (Elephant Island selection, respectively. The level of genetic differentiation and Joinville Island) (Table 1). A small piece of muscle is typically described by the FST index, which summarizes tissue was collected from each specimen and preserved at differences in allele frequency distribution between popu- -80 °C or in ethanol 90 % until molecular analysis. lations. The main difficulty of these methods is to obtain by Total genomic DNA for each individual was extracted simulations the expected FST distribution under neutrality, from 10 to 100 mg of muscle tissue following a standard which should depict the expected variance of FST values salting out protocol (Patwary et al. 1994). DNA solutions across loci with different levels of genetic variability. From were stored at -20 °C before PCR amplification. a statistical standpoint, outlier detection is particularly difficult when population structuring is weak and then Genetic and statistical analysis: DNA amplification neutral mean FST values are low (Beaumont and Balding and genotyping 2004; Foll and Gaggiotti 2008). The identification of outlier loci in marine fish is par- Twenty-one microsatellite loci were amplified in 108 ticularly challenging when environmental settings favor specimens: 10 loci originally isolated from C. rastrospi- gene flow across populations with a consequent homoge- nosus, Chaenocephalus aceratus, and Pleuragramma ant- nizing effect. This is the case of Antarctic waters, where arcticum genomic DNA (Papetti et al. 2006, 2011; Susana the complex ocean circulating system, which promotes et al. 2007), and 11 EST-linked loci isolated from about dispersal and connectivity all around Antarctica, contrib- 24,000 contigs obtained by a high-throughput sequencing utes to limit genetic differentiation among populations of a normalized cDNA library from C. hamatus muscle (Matschiner et al. 2009; Papetti et al. 2009, 2012 Damerau (Molecular Ecology Resources Primer Development Con- et al. 2012). sortium et al. 2011; Coppe et al. 2013). According to In this study, we analyzed the genetic differentiation O’Brien et al. (1993), microsatellite loci isolated from between the three recently derived species of the Chiono- genomic DNA, which are anonymous genomic sequences, draco genus (Notothenioidei, Channichthyidae), namely will be called Type II loci, while EST-linked loci, which Chionodraco hamatus, Chionodraco myersi, and Chiono- are found inside or flanking coding gene sequence, will be draco rastrospinosus, using a panel of 21 microsatellite defined as Type I loci. For the sake of simplicity, final loci. The three species, which are endemic to the Southern conditions for all the loci used in this study are reported in Ocean and whose taxonomical status is based on few Table S1 (supplementary materials). 123 Polar Biol Table 1 Summary of samples analyzed in this study Species Population sample Collection cruise Sample acronym Sample size C. hamatus Weddell Sea ANT-VII/4a
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