Museomics of an extinct European flat oyster population

Abstract

Understanding the factors that predispose species and populations to decline and extinction is a major challenge of biodiversity research. In the present study, we investigated the historical population genomics of an extinct population of the European oyster (Ostrea edulis L.) from the Wadden Sea collected between 1868 and 1888, and compared it to French and English populations sampled at the same time. Our museomic results indicate that the now-extinct population was genetically isolated from the French and English populations and showed signs of local adaptation in the form of Fst outlier loci between the Wadden Sea and the other two populations. Thus the Wadden Sea oysters may have been predisposed for extinction because they were not naturally replenished from other populations. A comparison of population-wide genomic diversity may hint towards a sudden population contraction of the Wadden Sea population, possibly being the result of stronger - or earlier - population decline in this population than in the others. In summary, our historical population genomic exploration hints at some potential causes of population decline in flat oysters from the Wadden Sea, which might have led to their extinction.

Fig. 1

Historical and present-day genetic population structure of the European oyster Ostrea edulis. A: historical distribution of mitochondrial genome haplogroups at the end of the 19 th century highlighting the uniqueness of the Wadden Sea population. B: present-day genetic population structure synthesized from several studies highlighting the presence of at least five distinct genetic clusters^,,–. Outlines denote clusters of genetically similar oyster populations. The map was generated with the function ‘map’ of the package ‘maps’ in the R environment.

Fig. 2

Mapping results. A: Mean read depth over the complete reference genome. B: mean read depth over the covered reference genome. C: % of the reference genome covered by at least 1 read.

Fig. 3

Nuclear population genomic structure of European oysters collected at the end of the 19 th century. A: Principal component analysis. Samples are colored based on their sampling locality. In subsequent analysis, Thames and English Channel samples are analyzed as a single “English” population. B: Admixture plot. Each bar is one individual, and the colors denote the assignment probability to K ancestral populations.

Fig. 4

Genome-wide genetic diversity. Density distributions of sliding window estimates. A: Watterson’s theta, B: π, C: Tajima’s D. Dashed lines show the mean values. Abbreviations: FR = France, GB = England, WS = Wadden Sea.

Fig. 5

Mitochondrial population genetic diversity of historical European oysters. A: phylogenetic reconstruction (maximum likelihood tree) showing at least three distinct genetic clusters. Branch to the NS clade was shortened to facilitate visualization. Clade names are taken from Hayer et al. B: mitochondrial nucleotide diversity per sampling locality indicating low mitochondrial genetic diversity in the French Atlantic population. Error bars denote confidence intervals. Asterisk indicates significantly lower nucleotide diversity in the French population.

Fig. 6

Fst sliding window genome scan to identify potential regions of local adaptation. Red bars denote large chromosomal inversions that can lead to increased Fst between populations. A: Fst between French Atlantic and English oysters. B: Fst between English and Wadden Sea oysters. C: Fst between French Atlantic and Wadden Sea oysters. Blue dots represent sliding window estimates that were outliers in both comparisons with the Wadden Sea population. Black dots represent significant outliers in one of the interpopulation comparisons.

Fig. 7

Density distribution of diversity metrics for the Fst outlier regions of the Wadden Sea population (gray line) in comparison to the genome-wide sliding window estimates (in color). Vertical lines represent the mean values. Watterson’s theta: A, D, G; Nucleotide diversity π: B, E, H; Tajima’s D: C, F, I. Wadden Sea: A, B, C; France: D, E, F; England: G, H, I.