The Roles of Plasticity and Selection in Rapid Phenotypic Changes at the Pacific Oyster Invasion Front in Europe

Invasive species present significant management challenges worldwide due to their ability to rapidly adapt to novel environments. The Pacific oyster Crassostrea gigas, a globally distributed invasive species, arrived in western Sweden in 2006 but has not yet colonised the low salinity waters of the Baltic Sea, presumably because low salinities act as a barrier to reproduction. We used classic mating designs to investigate fertilisation rates and heritability of embryonal salinity tolerance (in 8‰-33‰) in oysters from three locations with different invasion history and salinity (established, 33‰; past invasion front, 23.5‰; and present invasion front, 16‰). We found that fertilisation rates at lower salinities increased with proximity to the range front, with a pronounced heritable component. We then used whole-genome sequencing of oysters from the present invasion front to identify genomic regions showing stronger deviations from Mendelian inheritance in larval full-sib families reared in low salinity compared to controls. These regions contained coding sequences for Histones and ribosomal DNA, with the paternal genotype explaining a significant proportion of the deviation, suggesting the involvement of sperm in modulation of low-salinity tolerance at fertilisation and early development. Furthermore, we found no evidence of recent bottlenecks along the invasion front. We conclude that the Pacific oyster has developed low-salinity tolerant reproductive phenotypes at the present invasion front through acclimation and natural selection. Given the strong heritability for tolerance to low-salinities at fertilisation, the species likely has the potential to adapt further to low-salinity conditions and may invade the Baltic Sea.