Multiple SNP Markers Reveal Fine-Scale Population and Deep Phylogeographic Structure in European Anchovy (Engraulis encrasicolus L.)

Abstract

Geographic surveys of allozymes, microsatellites, nuclear DNA (nDNA) and mitochondrial DNA (mtDNA) have detected several genetic subdivisions among European anchovy populations. However, these studies have been limited in their power to detect some aspects of population structure by the use of a single or a few molecular markers, or by limited geographic sampling. We use a multi-marker approach, 47 nDNA and 15 mtDNA single nucleotide polymorphisms (SNPs), to analyze 626 European anchovies from the whole range of the species to resolve shallow and deep levels of population structure. Nuclear SNPs define 10 genetic entities within two larger genetically distinctive groups associated with oceanic variables and different life-history traits. MtDNA SNPs define two deep phylogroups that reflect ancient dispersals and colonizations. These markers define two ecological groups. One major group of Iberian-Atlantic populations is associated with upwelling areas on narrow continental shelves and includes populations spawning and overwintering in coastal areas. A second major group includes northern populations in the North East (NE) Atlantic (including the Bay of Biscay) and the Mediterranean and is associated with wide continental shelves with local larval retention currents. This group tends to spawn and overwinter in oceanic areas. These two groups encompass ten populations that differ from previously defined management stocks in the Alboran Sea, Iberian-Atlantic and Bay of Biscay regions. In addition, a new North Sea-English Channel stock is defined. SNPs indicate that some populations in the Bay of Biscay are genetically closer to North Western (NW) Mediterranean populations than to other populations in the NE Atlantic, likely due to colonizations of the Bay of Biscay and NW Mediterranean by migrants from a common ancestral population. Northern NE Atlantic populations were subsequently established by migrants from the Bay of Biscay. Populations along the Iberian-Atlantic coast appear to have been founded by secondary waves of migrants from a southern refuge.

Thermal adaptation and clinal mitochondrial DNA variation of European anchovy

“…The two mtDNA clades found in the European anchovy are sympatric over most of the distribution range and exhibit a remarkable latitudinal cline in the eastern Atlantic [19]. Previous studies [21,22,40,41] assumed the observed two-clade pattern as a consequence of ancient isolations followed by secondary contact. However, genetic clines may represent a balance between selection, genetic drift and dispersal, across time and space [49,50].…”

“…We compiled E. encrasicolus mitochondrial clade frequencies comprising 66 sampling sites from previous studies [19,20,[37][38][39][40][41] (electronic supplementary material, table S1) and used general linear models (GLM) of the binomial family (logit) to evaluate the correlation between clade frequencies and a variety of environmental variables. Data on temperature, salinity, apparent oxygen utilization and nutrient concentrations (phosphate, nitrate and silicate) for depths less than 10 m were obtained from the World Ocean Atlas 2009, one-degree objectively analysed climatology datasets [42] in NetCDF format and imported as geo-referenced layers into R 2.15.3 [43] using the ncdf [44] and raster [45] packages (electronic supplementary material, table S1).…”

“…Oxygen availability is of extreme importance in ectothermic small pelagic fishes, especially at higher latitudes where water temperature is low and consequently metabolism decreases. Although anchovies have high capacity for migration, environmental affinity precludes dispersal, contributing to population structure [19,40,41,52]. Temperature has been identified as one of the major selective forces acting on mtDNA [53].…”

Anchovy (<em>Engraulis encrasicolus</em>) otoliths reveal growth differences between two areas of the Spanish Mediterranean Sea

“…Various methods of stock discrimination in marine fishes have been widely used, especially spawning areas and seasons, abundance and distribution patterns, length-frequency distribution differences (Guerra-Sierra and Sánchez-Lizaso 1998), tagging and migration studies, parasites, serology (Cadrin et al 2014), biochemical-genetic differences (Zarraonaindia et al 2012, Viñas et al 2013) and otolith morphometric parameters (Cendrero and Abaunza 2001, Carvalho and Castello 2013, Jansen et al 2013. Otolith length is an ideal measurement for determining anchovy length, because a quasi-perfect linear relationship exists between them (Zengіn et al 2015).…”

Female reproductive cycle and batch fecundity in the central-southern Adriatic population ofEngraulis encrasicolus(Osteichthyes: Engraulidae)

“…Lastly, the notable differences in the European anchovy fecundity in the Mediterranean and the eastern Atlantic Ocean may also reflect the considerable genetic differences among the different populations (Bembo et al 1996;Chairi et al 2007;Bouchenak-Khelladi et al 2008;Zarraonaindia et al 2012), which are supposed to have diverged genetically since 5 million years ago, when the species entered the Mediterranean from the Eastern Atlantic, and the peculiar hydrogeographic conditions across the Strait of Gibraltar contributed to keep the populations separated (Magoulas et al 1996(Magoulas et al , 2006Chairi et al 2007). According to some authors, the high genetic variability between the anchovy populations of these two areas could conceal more than one species (Borsa 2002;Borsa et al 2004).…”