Global population genetic dynamics of a highly migratory, apex predator shark

Abstract

Knowledge of genetic connectivity dynamics in the world's large-bodied, highly migratory, apex predator sharks across their global ranges is limited. One such species, the tiger shark (Galeocerdo cuvier), occurs worldwide in warm temperate and tropical waters, uses remarkably diverse habitats (nearshore to pelagic) and possesses a generalist diet that can structure marine ecosystems through top-down processes. We investigated the phylogeography and the global population structure of this exploited, phylogenetically enigmatic shark by using 10 nuclear microsatellites (n = 380) and sequences from the mitochondrial control region (CR, n = 340) and cytochrome oxidase I gene (n = 100). All three marker classes showed the genetic differentiation between tiger sharks from the western Atlantic and Indo-Pacific ocean basins (microsatellite F > 0.129; CR Φ > 0.497), the presence of North vs. southwestern Atlantic differentiation and the isolation of tiger sharks sampled from Hawaii from other surveyed locations. Furthermore, mitochondrial DNA revealed high levels of intraocean basin matrilineal population structure, suggesting female philopatry and sex-biased gene flow. Coalescent- and genetic distance-based estimates of divergence from CR sequences were largely congruent (d = 0.0015-0.0050), indicating a separation of Indo-Pacific and western Atlantic tiger sharks <1 million years ago. Mitochondrial haplotype relationships suggested that the western South Atlantic Ocean was likely a historical connection for interocean basin linkages via the dispersal around South Africa. Together, the results reveal unexpectedly high levels of population structure in a highly migratory, behaviourally generalist, cosmopolitan ocean predator, calling for management and conservation on smaller-than-anticipated spatial scales.

Evidence for environmental and ecological selection in a microbe with no geographic limits to gene flow

“…Divergence in T. rotula was similar to other phytoplankton species sampled over large distances, such as across the Baltic Sea and the NE Atlantic (maximum F ST = 0.099) (21,22) but below the maximum F ST (0.76) observed among allopatrically separated populations of the pennate diatom P. pungens (17). Divergence in T. rotula was comparable to population divergence observed in globally distributed, highly migratory marine macrofauna (maximum F ST = 0.175) (40)(41)(42). Thus, F ST observed here for T. rotula is within the range expected for cosmopolitan high-dispersal marine organisms, but lower than those exhibiting strong patterns of allopatry.…”

Population structure, connectivity, and demographic history of an apex marine predator, the bull shark Carcharhinus leucas

“…The Benguela Upwelling System may be more constraining than the closure of the Isthmus of Panama for the bull shark, which is more sensitive to cold temperatures than species for which some gene flow after the formation of this current has been highlighted (e.g., tiger shark Galeocerdo cuvier [Bernard et al, ], dusky shark Carcharhinus obscurus [Benavides et al, ], or scalloped hammerhead shark Sphyrna lewini [Duncan et al, ]). Bull sharks remain in warmer waters, favoring temperatures of 24–26°C (Smoothey et al, ), and found less frequently in waters less than 18°C (Brunnschweiler et al, ; Lea et al, ; Matich & Heithaus, ).…”

“…The Benguela Upwelling System may be more constraining than the closure of the Isthmus of Panama for the bull shark, which is more sensitive to cold temperatures than species for which some gene flow after the formation of this current has been highlighted (e.g., tiger shark Galeocerdo cuvier [Bernard et al, 2016], dusky shark…”

World without borders—genetic population structure of a highly migratory marine predator, the blue shark (Prionace glauca)

“…Environmental variability associated with the glacial‐interglacial cycles of the Late Quaternary predating the appearance of modern climatic conditions (~11.5 ky before present) have been recurrently invoked to explain present‐day phylogeographic patterns in a variety of living organisms (e.g., Maggs et al., ; Randi, ). For instance, colder water conditions around the tip of South Africa during glacial periods, and the presence of the cold Benguela current during warm interglacial periods have been proposed to explain Atlantic versus Indo‐Pacific isolation and mitochondrial lineage divergence in warm‐temperate and tropical sharks, such as in cosmopolitan oceanic epipelagic species (e.g., R. typus, Vignaud et al., ; C. falciformis, Clarke et al., ) and in many cosmopolitan coastal pelagic carcharhinoids (e.g., C. limbatus, Keeney & Heist, ; Keeney, Heupel, Hueter, & Heist, ; Carcharhinus obscurus (Lesueur, 1818) Benavides et al., ; Carcharhinus plumbeus (Nardo, 1827) , Portnoy, McDowell, Heist, Musick, & Graves, ; Carcharhinus brachyurus (Günther, 1870), Benavides et al., ; Benavides et al., ; Galeocerdo cuvier (Péron & Lesuer, 1822) Bernard et al., ; Sphyrna lewini (Griffith & Smith, 1834), Duncan, Martin, Bowen, & De Couet, ; Daly‐Engel et al., ). Lineage divergence associated with between‐ocean cessation of gene flow in temperate species with wide temperature ranges, such as the blue shark, may also have occurred during periods when water temperatures around South Africa went below their thermal tolerance limit.…”