Population genomics shed light on the demographic and adaptive histories of European invasion in the Pacific oyster, Crassostrea gigas

Abstract

Crassostrea gigas originated from the Pacific coast of Asia, but was introduced into several European countries in the early 1970s. Natural populations have now spread across the length of the western seaboard of Europe. To elucidate the demographic and selective processes at play during this rapid expansion, genome-scan analysis was performed on different populations. High diversities and low differentiation were observed overall, but significant genetic differentiation was found among newly established populations and between the newly established northern group and a nearly panmictic group composed of southern European populations and a population from Japan. Loss of genetic diversity was also seen in the north, likely caused by founder events during colonization. The few strongly supported outlier loci revealed a genetic structure uncorrelated with the north/south differentiation, but grouping two samples from the Danish fjords (northern group) and one from the Dutch Scheldt estuary (southern group) with the one from Japan. These findings might reflect the following: (i) parallel adaptation to similar environmental pressures (fjord-like environment) within each of the two groups or (ii) a footprint of a secondary introduction of an alternative genomic background maintained by multifarious isolation factors. Our results call for a closer examination of adaptive genetic structure in the area of origin.

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

“…In contrast to the observed genetic similarities between oysters in the Danish Wadden Sea and the Limfjord in the present study, the oceanographic particle transport study by Laugen et al (2015) and data presented by Rohfritsch et al (2013) suggest that the Danish Wadden Sea and the Limfjord may not be well connected. We observed higher genetic diversity (allelic richness) in the Limfjord compared to the Danish Wadden Sea, which suggests that Pacific oysters in Denmark may have multiple sources of origin and/or that each population may have slightly evolved in response to genetic drift associated with demographic processes creating chaotic genetic patchiness (David et al 1997, Broquet et al 2013.…”

“…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).…”

“…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). Rohfritsch et al (2013) identified a northern group of Pacific oyster collected from 2 Swedish and 2 Danish locations, suggesting natural introduction of the species in Sweden by larval dispersal with oceanic currents from Danish locations. However, their analyses also showed contrasting patterns of genetic structure within this northern group, since Swedish oysters were significantly differentiated from those in Limfjord in Denmark, but not from those in the Danish Wadden Sea.…”

“…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).…”