Global phylogeography and seascape genetics of the lemon sharks (genus Negaprion)

Authors

  • J. K. SCHULTZ,

    1. Hawaii Institute of Marine Biology, University of Hawaii at Manoa, PO Box 1346, Kaneohe, HI 96744, USA,
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  • K. A. FELDHEIM,

    1. Pritzker Laboratory for Molecular Systematics and Evolution, The Field Museum, 1400 S. Lake Shore Drive, Chicago, IL 60605, USA,
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  • S. H. GRUBER,

    1. Division of Marine Biology and Fisheries, Rosenstiel School of Marine and Atmospheric Science, 4600 Rickenbacker Causeway, Miami, FL 33149, USA and Bimini Biological Field Station, 15 Elizabeth Drive, South Bimini, Bahamas and 9300 SW 99 Street Miami, FL 33176, USA,
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  • M. V. ASHLEY,

    1. Department of Biological Sciences, University of Illinois at Chicago, 845 West Taylor Street, Chicago, IL 60608, USA,
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  • T. M. MCGOVERN,

    1. Ocean Technology Group, University of Hawaii at Manoa, 1 Sand Island Access Road, Honolulu, HI 96819, USA
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  • B. W. BOWEN

    1. Hawaii Institute of Marine Biology, University of Hawaii at Manoa, PO Box 1346, Kaneohe, HI 96744, USA,
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Jennifer K. Schultz, Fax: (808) 236-7443; E-mail: jschultz@hawaii.edu

Abstract

Seascapes are complex environments, and populations are often isolated by factors other than distance. Here we investigate the role of coastal habitat preference and philopatry in shaping the distribution and population structure of lemon sharks. The genus Negaprion comprises the amphiatlantic lemon shark (N. brevirostris), with a relict population in the eastern Pacific, and its Indo-West Pacific sister species, the sicklefin lemon shark (N. acutidens). Analyzing 138 individuals throughout the range of N. brevirostris (N = 80) and N. acutidens (N = 58) at microsatellite loci (nine and six loci, respectively) and the mitochondrial control region, we find evidence of allopatric speciation corresponding to the Tethys Sea closure (10–14 million years ago) and isolation of the eastern Pacific N. brevirostris population via the emergence of the Isthmus of Panama (~3.5 million years ago). There is significant isolation by oceanic distance (R2 = 0.89, P = 0.005), defined as the maximum distance travelled at depths greater than 200 m. We find no evidence for contemporary transatlantic gene flow (m, M = 0.00) across an oceanic distance of ~2400 km. Negaprion acutidens populations in Australia and French Polynesia, separated by oceanic distances of at least 750 km, are moderately differentiated (FST = 0.070–0.087, P≤ 0.001; ΦST = 0.00, P = 0.99), with South Pacific archipelagos probably serving as stepping stones for rare dispersal events. Migration between coastally linked N. brevirostris populations is indicated by nuclear (m = 0.31) but not mitochondrial (m < 0.001) analyses, possibly indicating female natal site fidelity. However, philopatry is equivocal in N. acutidens, which has the lowest control region diversity (h = 0.28) of any shark yet studied. Restricted oceanic dispersal and high coastal connectivity stress the importance of both local and international conservation efforts for these threatened sharks.

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