Retrospective genomics highlights changes in genetic composition of tiger sharks (Galeocerdo cuvier) and potential loss of a south-eastern Australia population

Abstract

Over the last century, many shark populations have declined, primarily due to overexploitation in commercial, artisanal and recreational fisheries. In addition, in some locations the use of shark control programs also has had an impact on shark numbers. Still, there is a general perception that populations of large ocean predators cover wide areas and therefore their diversity is less susceptible to local anthropogenic disturbance. Here we report on temporal genomic analyses of tiger shark (Galeocerdo cuvier) DNA samples that were collected from eastern Australia over the past century. Using Single Nucleotide Polymorphism (SNP) loci, we documented a significant change in genetic composition of tiger sharks born between ~1939 and 2015. The change was most likely due to a shift over time in the relative contribution of two well-differentiated, but hitherto cryptic populations. Our data strongly indicate a dramatic shift in the relative contribution of these two populations to the overall tiger shark abundance on the east coast of Australia, possibly associated with differences in direct or indirect exploitation rates.

Figure 1

Sampling locations and distribution through time and space. (a) Samples distribution along the east coast of Australia. Samples are grouped by decades of birth (1910–1960, 1970–1990 and 2000) as explained in the text and the colours identify the three time-periods. Group names refer to the three major regions where samples were collected: Gulf of Carpentaria (GCA), Coral Sea (CRS) and Tasman Sea (TAS). (b) The histogram shows the difference between decade of catch and calculated decade of birth and associated sample numbers, as reported above each bar. Grey bars identify the calculated years of birth, while black numbers refer to the years of catch.

Figure 2

Principal Coordinates Analysis (PCoA) of mean pairwise FST’s between spatiotemporal tiger shark samples from eastern Australia. Groups are based on back-calculated ages and refer to: Gulf of Carpentaria (GCA), Coral Sea (CRS) and Tasman Sea (TAS). The axes report the percentage of variance explained.

Figure 3

Principal Component Analysis (PCA) by time periods and locations. (a) PCA of all individual genotypes for the samples with back-calculated age of birth and (b) PCA of contemporary samples based on decade of catch (2000–2010) covering the Gulf of Carpentaria (GCA), Coral Sea (CRS) and Tasman Sea (TAS).

Figure 4

Discriminant Analysis of Principal Components (DAPC) for K = 2. The plot illustrates the spatiotemporal occurrence of individuals from the two hypothesized clusters in time and space. Samples grouped by time and space are labelled along the x-axis, only collections encompassing more than six samples were included. The y-axis reports the membership probability of each sample to belong of either clusters (‘1’ in blue and ‘2’ in green).

Figure 5

Boxplot of the average proportion of heterozygous SNPs loci for the two clusters. Average proportion of heterozygous SNP loci over total loci genotyped for the two identified clusters. Cluster 1 is composed of mainly contemporary and northern samples, while cluster 2 individuals are almost exclusively found in southern historical samples (see Fig. 4 for explanation).