Seascape Genomics and Phylogeography of the Sailfish (Istiophorus platypterus)

Abstract

Permeable phylogeographic barriers characterize the vast open ocean, boosting gene flow and counteracting population differentiation and speciation of widely distributed and migratory species. However, many widely distributed species consists of distinct populations throughout their distribution, evidencing that our understanding of how the marine environment triggers population and species divergence are insufficient. The sailfish is a circumtropical and highly migratory billfish that inhabits warm and productive areas. Despite its ecological and socioeconomic importance as a predator and fishery resource, the species is threatened by overfishing, requiring innovative approaches to improve their management and conservation status. Thus, we presented a novel high-quality reference genome for the species and applied a seascape genomics approach to understand how marine environmental features may promote local adaptation and how it affects gene flow between populations. We delimit two populations between the Atlantic and Indo-Western Pacific oceans and detect outlier loci correlated with sea surface temperature, salinity, oxygen, and chlorophyll concentrations. However, the most significant explanatory factor that explains the differences between populations was isolation by distance. Despite recent population drops, the sailfish populations are not inbred. For billfishes in general, genome-wide heterozygosity was found to be relatively low compared to other marine fishes, evidencing the need to counteract overfishing effects. In addition, in a climate change scenario, management agencies must implement state-of-the-art sequencing methods, consider our findings in their management plans, and monitor genome-wide heterozygosity over time to improve sustainable fisheries and the long-term viability of its populations.

Keywords: demographic history; fisheries management units; genome-wide heterozygosity; reference genome assembly; whole-genome sequencing.

Fig. 1.

Sampling locations of sailfish (I. platypterus) specimens and the species known distribution (green), blue marlin (M. nigricans), white marlin (K. albida), and shortbill spearfish (T. angustirostris). Numbers show the sample size in each region.

Fig. 2.

Genome assembly completeness. (a) BUSCO assessments results for gene set completeness between our newly generated chromosome-level assembly from an ATL sailfish and the Indo-Pacific sailfish genome under GenBank assembly accession: GCA_016859345.1. (b) Synteny between our newly generated chromosome-level assembly from an ATL sailfish and the Indo-Pacific sailfish genome.

Fig. 3.

Clustering and admixture analysis. (a) DAPC from DAs 1 and 2. (b) Eigenvalues for the DAs. (c) Evanno's ΔK method. (d–f) Individual ancestral admixture proportions estimations from K = 2–4. (g) Short-term immigration rates between sampled regions using unlinked genome-wide SNPs. (h) Long-term immigration rates between sampled regions using the mitogenomes. Numbers indicate the migration rates between regions.

Fig. 4.

Phylogenetic inference. (a) ML phylogenetic tree estimated from genome-wide SNPs. Node color gradient displays the ultrafast bootstraps approximation (UFBoot) values from 96 to 100. (b) Fossil-calibrated Bayesian phylogenetic inference estimated from the mitogenomes. Node numbers show the age estimation; red bars indicate the 95% highest posterior density (HPD) intervals. Color names display the respective ocean basin where individuals belong: blue for the ATL Ocean and purple for the Indo-Pacific. Dashed lines represent the lower boundaries between the Cenozoic epochs, Pleistocene (2.58 M), Pliocene (5.33 M), and Miocene (23.03 M), respectively. SFA, I. platypterus; BUM, M. nigricans; WHM, K. albida; SPF, T. angustirostris. Names in blue are from the ATL lineage, while purple names are for the Indo-Pacific lineage.

Fig. 5.

Redundancy Analysis (RDA). (a and b) RDAs displaying the correlation between variables, axes numbers show the percentage of the explanation of variance. (c–f) chlo, mean chlorophyll concentration; sst, mean sea surface temperature; ssal, mean sea surface salinity; sdO₂, mean concentration of surface dissolved molecular oxygen. MEM, Moran's Eigenvector Maps. adj.R², the adjusted R² adjusted for the number of explanatory variables and P-values.

Fig. 6.

Demographic history. (a) Stairway plot from the ATL Ocean. (b) Stairway plot from the IDWP. (c) GONE. N_e, effective population size. ATL population: blue; IDWP population: purple.

Fig. 7.

Heterozygosity and inbreeding. (a) Box plots of heterozygosity per population. (b) Box plots of heterozygosity per sampled region. (c) Box plots of the proportion of the genome covered by RoH (F_RoH) per population. (d) Box plots of the proportion of the genome covered by RoH (F_RoH) per sampled region. (e) Gradients of the length distribution of RoHs fragments per individual.

Fig. 8.

Mitogenomic analyses. (a) DAPC. (b) Posterior probability of cluster membership for sampled individuals with K = 2 (not admixture coefficients). (c and d) eBSP. N_e, effective population sizes.