Invasion genetics of the Pacific oyster Crassostrea gigas in the British Isles inferred from microsatellite and mitochondrial markers

Abstract

Abstract:The Pacific oyster, Crassostrea gigas, native to northeast Asia, is one of the most important cultured shellfish species. In Europe, Pacific oysters first settled along the Atlantic coasts of France at the end of the 1960s but rapidly spread and are now widely established. Twenty-two sites in the United Kingdom (UK), Ireland, Denmark, France and Spain were sampled to assess genetic diversity and differentiation. Hatcherypropagated stocks from two hatcheries located in the UK also were included. Two main genetic clusters were identified from pairwise genetic differentiation indexes, Bayesian clustering methods or neighbour-joining analysis, based on 7 microsatellite loci: (1) a Northeast cluster (including feral samples from East England, Ireland and Denmark as well as UK hatchery stocks) and (2) a Southwest cluster (including samples from South Wales, South West England, France and Spain). The Southwest cluster had significantly higher allelic richness (A) and expected heterozygosity (He) (A: 45.68, He: 0.928) than in the Northeast (A: 26.58, He: 0.883); the two diverging by a small but significant FST value (FST=0.017, 95% CI: 0.014-0.021). A 739-bp fragment of the major noncoding region of the mitochondrial genome was sequenced in 248 oysters from 12 of the studied samples in Europe and in 25 oysters from Miyagi prefecture (Japan). A total of 81 haplotypes were found. Haplotype frequency analyses identified the same two clusters observed using microsatellites. This study highlights how the number and size of introduction events, aquaculture practices, genetic bottlenecks followed by genetic drift and natural dispersal can act concurrently to shape the genetic diversity and structure of introduced populations.Response to Reviewers:The changes required by the reviewer have been made. The manuscript has been Powered by Editorial Manager® and ProduXion Manager® from Aries Systems Corporationsignificantly reduced in length. The figures 2, 3 and 5 have been modified following the reviewer's feedback.Line 199, we have specified that marine geographic distance corresponds to the nearest waterway distance.The deltaK method of Evanno has been used to determine the number of genetic clusters (see line 211). 1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 25 26 27 28 29 30 31 32 33 34 35 36 37 38 39 40 41 42 43 44 45 46 47 48 49 50 51 52 53 54 55 56 57 58 59 60 61 62 63 64 65 2 Powered by Editorial Manager® and ProduXion Manager® from Aries Systems Corporation Abstract: 34 35The Pacific oyster, Crassostrea gigas, native to northeast Asia, is one of the most important cultured 36 shellfish species. In Europe, Pacific oysters first settled along the Atlantic coasts of France at the end 37 of the 1960s but rapidly spread and are now widely established. Twenty-two sites in the United 38 Kingdom (UK), Ireland, Denmark, France and Spain were sampled to assess genetic diversity and 39 differentiation. Hatchery-propagated stocks from two hatc...

Origin and route of establishment of the invasive Pacific oyster Crassostrea gigas in Scandinavia

“…However, only weak general patterns in heterozygote deficiency across samples or populations were observed: the Irish aquaculture sample showed a pattern of consistent deficit across loci indicative of inbreeding or a Wahlund effect (when a sampled 'population' is a mixture of different subpopulations; Wahlund 1928). Although hetero zygote deficiency was observed in some of the samples, both H o and H e were relatively high for all samples across all loci, in agreement with previous studies performed on Crassostrea gigas (Li et al 2006, Kochmann et al 2012, Rohfritsch et al 2013, Lallias et al 2015. On the other hand, when considering N a and A R , higher genetic diversity was ob served in the southern group.…”

“…Several populations showed deviations from HW proportions in the form of heterozygote deficiency, consistent with previous studies of the Pacific oyster (Meistertzheim et al 2013, Rohfritsch et al 2013, Lallias et al 2015. However, only weak general patterns in heterozygote deficiency across samples or populations were observed: the Irish aquaculture sample showed a pattern of consistent deficit across loci indicative of inbreeding or a Wahlund effect (when a sampled 'population' is a mixture of different subpopulations; Wahlund 1928).…”

“…Different genetic markers have previously been applied to disentangle the Pacific oysters' complex population structure in Europe (Moehler et al 2011, Kochmann et al 2012, Rohfritsch et al 2013, Lallias et al 2015. Most of the studies identified a southern population group (stretching from Spain to south Wales) and a northern population group (from Ireland and north Germany to Sweden).…”

New insights about the introduction of the Portuguese oyster,Crassostrea angulata, into the North East Atlantic from Asia based on a highly polymorphic mitochondrial region

“…For example, it is documented that C. angulata was introduced into Morocco from Spain and Portugal in 1952(Shafee 1985cited in Fabioux et al 2002. In contrast to C. gigas in Europe, which showed a typical star-shaped haplotype phylodiversity characteristic of expanding populations (Moehler et al 2011;Lallias et al 2015), the haplotype network of C. angulata did not show such a pronounced star-shape. Significant negative Tajima's D values were only found for C. angulata samples from Asia, although Fu's F tests were significant for Mira and Keelung samples.…”

“…The nucleotide diversity of C. angulata observed in the present study was higher than that previously reported for C. gigas for the same mitochondrial region. Moehler et al (2011) and Lallias et al (2015) reported nucleotide diversity values of 0.0044 and 0.0046 for C. gigas, respectively, with samples mainly collected in Europe but also in Canada and Japan. Hsiao et al (2016) found haplotype and nucleotide diversities (using mitochondrial cytochrome oxidase I sequences) in Asia being considerably higher in C. angulata than in C. gigas.…”