Strong trans-Pacific break and local conservation units in the Galapagos shark (Carcharhinus galapagensis) revealed by genome-wide cytonuclear markers

Abstract

The application of genome-wide cytonuclear molecular data to identify management and adaptive units at various spatio-temporal levels is particularly important for overharvested large predatory organisms, often characterized by smaller, localized populations. Despite being "near threatened", current understanding of habitat use and population structure of Carcharhinus galapagensis is limited to specific areas within its distribution. We evaluated population structure and connectivity across the Pacific Ocean using genome-wide single-nucleotide polymorphisms (~7200 SNPs) and mitochondrial control region sequences (945 bp) for 229 individuals. Neutral SNPs defined at least two genetically discrete geographic groups: an East Tropical Pacific (Mexico, east and west Galapagos Islands), and another central-west Pacific (Lord Howe Island, Middleton Reef, Norfolk Island, Elizabeth Reef, Kermadec, Hawaii and Southern Africa). More fine-grade population structure was suggested using outlier SNPs: west Pacific, Hawaii, Mexico, and Galapagos. Consistently, mtDNA pairwise Φ defined three regional stocks: east, central and west Pacific. Compared to neutral SNPs (F = 0.023-0.035), mtDNA exhibited more divergence (Φ = 0.258-0.539) and high overall genetic diversity (h = 0.794 ± 0.014; π = 0.004 ± 0.000), consistent with the longstanding eastern Pacific barrier between the east and central-west Pacific. Hawaiian and Southern African populations group within the west Pacific cluster. Effective population sizes were moderate/high for east/west populations (738 and 3421, respectively). Insights into the biology, connectivity, genetic diversity, and population demographics informs for improved conservation of this species, by delineating three to four conservation units across their Pacific distribution. Implementing such conservation management may be challenging, but is necessary to achieve long-term population resilience at basin and regional scales.

Accounting for kin sampling reveals genetic connectivity in Tasmanian and New Zealand school sharks, Galeorhinus galeus

“…This study presents the first genomic study of school sharks and in theory allows a more accurate calculation of genetic diversity (Fischer et al, ). Overall, our diversity measures correspond to other genomic studies in sharks (Feutry et al, ; Maisano Delser et al, ; Pazmiño et al, ). Furthermore, Ward and Gardner () found weak evidence of genetic differentiation; however, this was based on a single allozyme and mitochondrial DNA markers.…”

Weak population structure of the Spot‐tail shark Carcharhinus sorrah and the Blacktip shark C. limbatus along the coasts of the Arabian Peninsula, Pakistan, and South Africa

“…In particular, the offspring of C. limbatus migrates from nursery grounds to offshore wintering grounds when temperatures drop below 21°C (Castro, 1996). This Future research to understand the role of philopatric behavior in generating fine-scale structure in shark populations (Momigliano et al, 2017;Pazmiño et al, 2018;Portnoy et al, 2015) in the Arabian region is warranted. Particular focus should be placed on a comparison of geographic scales of heterogeneity partition produced by neutral (both microsatellite and mtDNA) vs. non-neutral markers.…”

Oceanographic barriers, divergence, and admixture: Phylogeography and taxonomy of two putative subspecies of short‐finned pilot whale

“…The Eastern Pacific Barrier is a known barrier to many shallow, coastally‐distributed fishes, corals, and other invertebrates (Bowen et al, ; Chow et al, ; Rocha et al, ). Increasing evidence suggests it may also be an important barrier separating mobile trans‐Pacific or globally‐distributed species, such as Galapagos sharks ( Carcharhinus galapagensis ) (Pazmiño et al, ), tope sharks ( Galeorhinus galeus ) (Chabot, ), Risso's dolphins ( Grampus griseus ) (Chen et al, ), and spinner dolphins ( Stenella longirostris ) (Leslie & Morin, ). Some evidence suggests that the barrier may be semi‐permeable to some species (Lessios & Robertson, ), allowing occasional migration and mixing between the eastern and western Pacific Ocean.…”

“…Taxonomic species delineation based on morphological characteristics sometimes overlooks the existence of cryptic species, subspecies, or evolutionarily important population structure (Rosel et al, ; Taylor, Perrin, et al, ). Recent advances in genomic techniques allow researchers to describe species' taxonomy and population structure with higher resolution than was previously possible (Cammen et al, ), oftentimes revealing cryptic speciation in the absence of physical barriers to dispersal, driven by local adaptation and/or social behaviour (Leslie & Morin, ; Morin et al, ; Pazmiño et al, ; Podos, ; Rendell, Mesnick, Dalebout, Burtenshaw, & Whitehead, ; Rocha, Craig, & Bowen, ; Smith & Friesen, ; Yoshino, Armstrong, Izawa, Yokoyama, & Kawata, ).…”