Skip to main content

Effects of species biology on the historical demography of sharks and their implications for likely consequences of contemporary climate change

Abstract

Climate variation is an important factor shaping the demographic histories of many marine species, though impacts likely differ depending on species life history, habitat preferences and ecology. Investigating how species responded to historic climate fluctuations may provide critical insights into a species’ response to current climate change. Despite their ecological diversity, shark species share many similar life history characteristics and may be especially vulnerable to anthropogenic and climate impacts. We compared patterns of genetic variability, mismatch distributions and demographic reconstructions from coalescence approaches among temperate and tropical shark species with differing ecological characteristics, to investigate the effect of the past glaciation cycles on population abundance. Genetic diversity at two mitochondrial DNA regions (ND2 and control region) was assayed in four North Pacific species, Pacific spiny dogfish, Pacific sleeper sharks, salmon shark, and bluntnose sixgill shark. In addition, control region sequences acquired from GenBank for five shark species [tope shark (California/Australia), white shark (California), blacktip shark (eastern and western Gulf of Mexico), lemon shark (Bahamas), and whale shark] were analyzed. General patterns in genetic diversity, mismatch analyses and Bayesian skyline plots supported our hypothesis that species biology affected the impact of climate variation on demographic history. Consequently, our results suggest that effects of contemporary climate change on sharks may be to some degree predictable from species biology, distribution, habitat and the impact of past climate events.

This is a preview of subscription content, access via your institution.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7

References

  • Ahonen H, Harcourt RG, Stow AJ (2009) Nuclear and mitochondrial DNA reveals isolation of imperilled grey nurse shark populations (Carcharias taurus). Mol Ecol 18(21):4409–4421

    Article  PubMed  CAS  Google Scholar 

  • Andrews KS, Williams GD, Levin PS (2010) Seasonal and ontogenetic changes in movement patterns of sixgill sharks. PLoS ONE 5(9):e12549

    Article  PubMed  CAS  Google Scholar 

  • Bazin E, Glémin S, Galtier N (2006) Population size does not influence mitochondrial genetic diversity in animals. Science 312(5773):570–572

    Article  PubMed  CAS  Google Scholar 

  • Beamish RJ, McFarlane GA, Weir KR, Smith MS, Scarsbrook JR, Cass AJ, Wood CC (1982) Observations on the biology of Pacific Hake, Walleye Pollock and spiny dogfish in the Strait of Georgia, Juan de Fuca Strait and off the west coast of Vancouver Island and United States, July 13–24, 1976. Can MS Rep Fish Aquat Sci 1651:150

    Google Scholar 

  • Benavides MT, Feldheim KA, Duffy CA, Winter S, Braccini JM, Boomer J, Huveneers C, Rogers P, Mangel JC, Alfaro-Shigueto J, Cartamil DP, Chapman DD (2011) Phylogeography of the copper shark (Carcharhinus brachyurus) in the southern hemisphere: implications for the conservation of a coastal apex predator. Mar Freshw Res 63:861–869

    Article  Google Scholar 

  • Bonfil R, Meÿer M, Scholl MC, Johnson R, O’Brien S, Oosthuizen H, Swanson S, Kotze D, Paterson M (2005) Transoceanic migration, spatial dynamics, and population linkages of white sharks. Science 310(5745):100–103

    Article  PubMed  CAS  Google Scholar 

  • Bremer JRA, Viñas J, Mejuto J, Ely B, Pla C (2005) Comparative phylogeography of Atlantic bluefin tuna and swordfish: the combined effects of vicariance, secondary contact, introgression, and population expansion on the regional phylogenies of two highly migratory pelagic fishes. Mol Phylogenet Evol 36(1):169–187

    Article  CAS  Google Scholar 

  • Brieuc M, Naish K (2011) Detecting signatures of positive selection in partial sequences generated on a large scale: pitfalls, procedures and resources. Mol Ecol Res 11:172–183

    Article  Google Scholar 

  • Burridge CP, Craw D, Fletcher D, Waters JM (2008) Geological dates and molecular rates: fish DNA sheds light on time dependency. Mol Biol Evol 25(4):624–633

    Article  PubMed  CAS  Google Scholar 

  • Canino MF, Spies IB, Cunningham KM, Hauser L, Grant WS (2010) Multiple ice-age refugia in Pacific cod, Gadus macrocephalus. Mol Ecol 19:4339–4351

    Article  Google Scholar 

  • Castro ALF, Stewart BS, Wilson SG, Hueter RE, Meekan MG, Motta PJ, Bowen BW, Karl SA (2007) Population genetic structure of Earth’s largest fish, the whale shark (Rhincodon typus). Mol Ecol 16:5183–5192

    Article  PubMed  CAS  Google Scholar 

  • Chabot CL, Allen LG (2009) Global population structure of the tope (Galeorhinus galeus) inferred by mitochondrial control region sequence data. Mol Ecol 18:545–552

    Article  PubMed  CAS  Google Scholar 

  • Chevolot M, Hoarau G, Rijnsdorp AD, Stam WT, Olsen JL (2006) Phylogeography and population structure of thornback rays (Raja clavata L., Rajidae). Mol Ecol 15:3693–3705

    Article  PubMed  CAS  Google Scholar 

  • Clark PU, Dyke AS, Shakun JD, Carlson AE, Clark J, Wohlfarth B, Mitrovica JX, Hostetler SW, McCabe AM (2009) The last glacial maximum. Science 325:710–714

    Article  PubMed  CAS  Google Scholar 

  • Compagno LJV (2001) Sharks of the world. An annotated and illustrated catalogue of shark species known to date. FAO, Rome pp 269

    Google Scholar 

  • Craig MT, Eble JA, Bowen BW (2010) Origins, ages and population histories: comparative phylogeography of endemic Hawaiian butterfly fishes (genus Chaetodon). J Biogeogr 37:2125–2136

    Article  Google Scholar 

  • Crandall ED, Sbrocco EJ, DeBoer TS, Barber PH, Carpenter KE (2012) Expansion dating: Calibrating molecular clocks in marine species from expansions onto the Sunda shelf following the last glacial maximum. Mol Biol Evol 29(2):707–719

    Article  PubMed  CAS  Google Scholar 

  • Drummond AJ, Rambaut A (2007) BEAST: Bayesian evolutionary analysis by sampling trees. BMC Evol Biol 7:214

    Article  PubMed  CAS  Google Scholar 

  • Drummond AJ, Rambaut A, Shapiro B, Pybus OG (2005) Bayesian coalescent inference of past population dynamics from molecular sequences. Mol Biol Evol 22:1185–1192

    Article  PubMed  CAS  Google Scholar 

  • Drummond AJ, Ashton B, Buxton S, Cheung M, Cooper A, Heled J, Kearse M, Moir R, Stones-Havas S, Sturrock S, Thierer T, Wilson A (2010) Geneious v5.1, Available from: http://www.geneious.com. Accessed 19 Dec 2012

  • Dulvy NK, Sadovy Y, Reynolds JD (2003) Extinction vulnerability in marine populations. Fish Fish 4:25–64

    Article  Google Scholar 

  • Duncan KM, Martin AP, Bowen BW, De Couet HG (2006) Global phylogeography of the scalloped hammerhead shark (Sphyrna lewini). Mol Ecol 15:2239–2251

    Article  PubMed  CAS  Google Scholar 

  • Ebert DA, Compagno LJV, Natanson LJ (1987) Biological notes on the Pacific sleeper shark, Somniosus Pacificus (Chondrichthyes, Squalidae). Calif Fish Game 73:117–123

    Google Scholar 

  • Eckert SA, Stewart BS (2001) Telemetry and satellite tracking of whale sharks, Rhincodon typus, in the Sea of Cortez, Mexico, and the north Pacific Ocean. Environ Biol Fish 60:299–308

    Article  Google Scholar 

  • Edwards SV, Beerli P (2000) Perspective: gene divergence, population divergence, and the variance in coalescence time in phylogeographic studies. Evolution 54:1839–1854

    PubMed  CAS  Google Scholar 

  • Emerson KJ, Merz CR, Catchen JM, Hohenlohe PA, Cresko WA, Bradshaw WE, Holzapfel CM (2010) Resolving postglacial phylogeography using high-throughput sequencing. Proc Natl Acad Sci USA 107:16196–16200

    Article  PubMed  CAS  Google Scholar 

  • Excoffier L (2004) Patterns of DNA sequence diversity and genetic structure after a range expansion: lessons from the infinite-island model. Mol Ecol 13:853–864

    Article  PubMed  CAS  Google Scholar 

  • Excoffier L, Lischer HEL (2010) Arlequin suite ver 3.5: a new series of programs to perform population genetics analyses under Linux and Windows. Mol Ecol Resour 10:564–567

    Article  PubMed  Google Scholar 

  • Fauvelot C, Bernardi G, Planes S (2003) Reductions in the mitochondrial DNA diversity of coral reef fish provide evidence of population bottlenecks resulting from Holocene sea-level change. Evolution 57:1571–1583

    PubMed  CAS  Google Scholar 

  • Felsenstein J (2005) PHYLIP (phylogeny inference package) version 3.6. Distributed by the author. Department of Genome Sciences, University of Washington, Seattle

  • Fu Y-X (1997) Statistical tests of neutrality of mutations against population growth, hitchhiking, and background selection. Genetics 147:915–925

    PubMed  CAS  Google Scholar 

  • Gaggiotti OE, Bekkevold D, Jørgensen HB, Foll M, Carvalho GR, Andre C, Ruzzante DE (2009) Disentangling the effects of evolutionary, demographic, and environmental factors influencing genetic structure of natural populations: Atlantic herring as a case study. Evolution 63:2939–2951

    Article  PubMed  Google Scholar 

  • Gaither MR, Bowen BW, Bordenave T-R, Rocha LA, Newman SJ, Gomez JA, van Herwerden L, Craig MT (2011) Phylogeography of the reef fish Cephalopholis argus (Epinephelidae) indicates Pleistocene isolation across the indo-pacific barrier with contemporary overlap in the coral triangle. BMC Evol Biol 11:189

    Article  PubMed  Google Scholar 

  • Gallucci VF, Foy RJ, O’Brien SM, Aires-da-Silva A, Nesse H, Langseth B, Vega N, Taylor I, Goldman KJ (2008) Information from a pregnant salmon shark Lamna ditropis in the eastern North Pacific with observations on oophagous reproduction. J Fish Biol 73:732–739

    Article  Google Scholar 

  • Galtier N, Nabholz B, Glémin S, Hurst G (2009) Mitochondrial DNA as a marker of molecular diversity: a reappraisal. Mol Ecol 18:4541–4550

    Article  PubMed  CAS  Google Scholar 

  • Garvin MR, Bielawski JP, Gharrett AJ (2011) Positive Darwinian selection in the piston that powers proton pumps in complex I of the mitochondria of Pacific salmon. PLoS ONE 6:e24127

    Article  PubMed  CAS  Google Scholar 

  • Gilman SE, Urban MC, Tewksbury J, Gilchrist GW, Holt RD (2010) A framework for community interactions under climate change. Trends Ecol Evol 25:325–331

    Article  PubMed  Google Scholar 

  • Goldman KJ, Anderson SD, Latour RJ, Musick JA (2004) Homeothermy in adult salmon sharks, Lamna ditropis. Environ Biol Fish 71:403–411

    Article  Google Scholar 

  • Grant WS, Waples RS (2000) Spatial and temporal scales of variability in marine and anadromous species: Implications for fisheries oceanography. In: Harrison PJ, Parsons TR (eds). Fisheries oceanography an integrative approach to fisheries ecology and management, pp 347

  • Grant WS, Liu M, Gao T, Yanagimoto T (2012) Limits of Bayesian skyline plot analysis of mtDNA sequences to infer historical demographies in Pacific herring (and other species). Mol Phylogenet Evol 65:203–212

    Article  PubMed  Google Scholar 

  • Guindon S, Gascuel O (2003) A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Syst Biol 52:696–704

    Article  PubMed  Google Scholar 

  • Harpending H (1994) Signature of ancient population growth in a low-resolution mitochondrial DNA mismatch distribution. Hum Biol 66:591

    PubMed  CAS  Google Scholar 

  • Hauser L (2009) The molecular ecology of dogfish sharks. In: Gallucci VF, McFarlane GA, Bargmann GG (eds) Biology and management of dogfish sharks. American Fisheries Society, Bethesda, pp 229–252

    Google Scholar 

  • Heled J, Drummond AJ (2008) Bayesian inference of population size history from multiple loci. BMC Evol Biol 8:289

    Article  PubMed  CAS  Google Scholar 

  • Herbert TD, Peterson LC, Lawrence KT, Liu Z (2010) Tropical ocean temperatures over the past 3.5 million years. Science 328:1530–1534

    Article  PubMed  CAS  Google Scholar 

  • Hewitt GM (2004) Genetic consequences of climatic oscillations in the quaternary. Philos Trans R Soc B 359:183–195

    Article  CAS  Google Scholar 

  • Hewitt GM (2011) Quaternary phylogeography: the roots of hybrid zones. Genetica 139:617–638

    Article  PubMed  Google Scholar 

  • Ho SYW, Larson G (2006) Molecular clocks: when times are a-changin’. Trends Genet 22:79–83

    Article  PubMed  CAS  Google Scholar 

  • Ho SYW, Phillips MJ, Cooper A, Drummond AJ (2005) Time dependency of molecular rate estimates and systematic overestimation of recent divergence times. Mol Biol Evol 22:1561–1568

    Article  PubMed  CAS  Google Scholar 

  • Ho SYW, Shapiro B, Phillips MJ, Cooper A, Drummond AJ (2007) Evidence for time dependency of molecular rate estimates. Syst Biol 56(3):515–522

    Article  PubMed  Google Scholar 

  • Ho SYW, Saarma U, Barnett R, Haile J, Shapiro B (2008) The effect of inappropriate calibration: three case studies in molecular ecology. PLoS ONE 3(2):e1615

    Article  PubMed  Google Scholar 

  • Ho SYW, Lanfear R, Bromham L, Phillips MJ, Soubrier J, Rodrigo AG, Cooper A (2011) Time-dependent rates of molecular evolution. Mol Ecol 20:3087–3101

    Article  PubMed  Google Scholar 

  • Hoelzel AR, Shivji MS, Magnussen J, Francis MP (2006) Low worldwide genetic diversity in the basking shark (Cetorhinus maximus). Biol Lett 2:639–642

    Article  PubMed  CAS  Google Scholar 

  • Hoenig JM, Gruber SH (1990) Life-history patterns in the elasmobranchs: implications for fisheries management. In: Pratt HL Jr, Gruber SH, Taniuchi T (eds) Elasmobranchs as living resources: advances in biology, ecology, systematics and the status of the fisheries. U.S. Department of Commerce, NOAA Tech. Rep. NMFS 90

  • Hulbert LB, Aires-da-Silva AM, Gallucci VF, Rice JS (2005) Seasonal foraging movements and migratory patterns of female Lamna ditropis tagged in Prince William Sound, Alaska. J Fish Biol 67:490–509

    Article  Google Scholar 

  • Hulbert LB, Sigler MF, Lunsford CR (2006) Depth and movement behaviour of the Pacific sleeper shark in the north-east Pacific Ocean. J Fish Biol 69:406–425

    Article  Google Scholar 

  • Janko K, Lecointre G, DeVries A, Couloux A, Cruaud C, Marshall C (2007) Did glacial advances during the Pleistocene influence differently the demographic histories of benthic and pelagic Antarctic shelf fishes?—inferences from intraspecific mitochondrial and nuclear DNA sequence diversity. BMC Evol Biol 7:220

    Article  PubMed  CAS  Google Scholar 

  • Jeffreys H (1961) Theory of probability. Oxford University Press, Oxford

    Google Scholar 

  • Jorgensen SJ, Reeb CA, Chapple TK, Anderson S, Perle C, Van Sommeran SR, Fritz-Cope C, Brown AC, Klimley AP, Block BA (2010) Philopatry and migration of Pacific white sharks. Proc R Soc B 277:679–688

    Article  PubMed  Google Scholar 

  • Karl SA, Castro ALF, Lopez JA, Charvet P, Burgess GH (2011) Phylogeography and conservation of the bull shark (Carcharhinus leucas) inferred from mitochondrial and microsatellite DNA. Conserv Genet 12:371–382

    Article  Google Scholar 

  • Keeney DB, Heist EJ (2006) Worldwide phylogeography of the blacktip shark (Carcharhinus limbatus) inferred from mitochondrial DNA reveals isolation of western Atlantic populations coupled with recent Pacific dispersal. Mol Ecol 15:3669–3679

    Article  PubMed  CAS  Google Scholar 

  • Kumar S (2005) Molecular clocks: four decades of evolution. Nat Rev Genet 6:654–662

    Article  PubMed  CAS  Google Scholar 

  • Lambeck K, Esat TM, Potter E (2002) Links between climate and sea levels for the past three million years. Nature 419:199–206

    Article  PubMed  CAS  Google Scholar 

  • Lanfear R, Welch JJ, Bromham L (2010) Watching the clock: studying variation in rates of molecular evolution between species. Trends Ecol Evol 25:495–503

    Article  PubMed  Google Scholar 

  • Larkin MA, Blackshields G, Brown NP, Chenna R, McGettigan PA, McWilliam H, Valentin F, Wallace IM, Wilm A, Lopez R, Thompson JD, Gibson TJ, Higgins DG (2007) Clustal W and clustal X version 2.0. Bioinformatics 23:2947–2948

    Article  PubMed  CAS  Google Scholar 

  • Larson S, Christiansen J, Griffing D, Ashe J, Lowry D, Andrews K (2011) Relatedness and polyandry of sixgill sharks, Hexanchus griseus, in an urban estuary. Conserv Genet 12:679–690

    Article  Google Scholar 

  • Last PR, White WT, Gledhill DC, Hobday AJ, Brown R, Edgar GJ, Pecl G (2011) Long-term shifts in abundance and distribution of a temperate fish fauna: a response to climate change and fishing practices. Glob Ecol Biogeogr 20:58–72

    Article  Google Scholar 

  • Librado P, Rozas J (2009) DnaSP v5: a software for comprehensive analysis of DNA polymorphism data. Bioinformatics 25:1451–1452

    Article  PubMed  CAS  Google Scholar 

  • Liu J-X, Tatarenkov A, Beacham TD, Gorbachev V, Wildes S, Avise JC (2011) Effects of Pleistocene climatic fluctuations on the phylogeographic and demographic histories of Pacific herring (Clupea pallasii). Mol Ecol 20:3879–3893

    Article  PubMed  Google Scholar 

  • Lourie SA, Green DM, Vincent ACJ (2005) Dispersal, habitat differences, and comparative phylogeography of Southeast Asian seahorses (Syngnathidae: Hippocampus). Mol Ecol 14:1073–1094

    Article  PubMed  CAS  Google Scholar 

  • Maggs CA, Castilho R, Foltz D, Henzler C, Jolly M, Kelly J, Olsen J, Perez KE, Stam W, Vainola R, Viard F, Wares J (2008) Evaluating signatures of glacial refugia for North Atlantic benthic marine taxa. Ecology 89:108–122

    Article  Google Scholar 

  • Marko PB, Hoffman JM, Emme SA, Mcgovern TM, Keever CC, Cox LN (2010) The ‘expansion–contraction’ model of Pleistocene biogeography: rocky shores suffer a sea change? Mol Ecol 19:146–169

    Article  PubMed  CAS  Google Scholar 

  • Martin AP, Naylor GJP, Palumbi SR (1992) Rates of mitochondrial DNA evolution in sharks are slow compared with mammals. Nature 357:153–155

    Article  PubMed  CAS  Google Scholar 

  • McCusker MR, Bentzen P (2010) Positive relationships between genetic diversity and abundance in fishes. Mol Ecol 19:4852–4862

    Article  PubMed  Google Scholar 

  • McFarlane GA, King JR (2003) Migration patterns of spiny dogfish (Squalus acanthias) in the North Pacific Ocean. Fish Bull 101:358–367

    Google Scholar 

  • Mulligan CJ, Kitchen A, Miyamoto MM (2006) Comment on “population size does not influence mitochondrial genetic diversity in animals”. Science 314:1388a–1390a

    Article  CAS  Google Scholar 

  • Murray BW, Wang JY, Yang S, Stevens JD, Fisk A, Svavarsson J (2008) Mitochondrial cytochrome b variation in sleeper sharks (Squaliformes: Somniosidae). Mar Biol 153:1015–1022

    Article  CAS  Google Scholar 

  • Nabholz B, Glémin S, Galtier N (2008) Strong variations of mitochondrial mutation rate across mammals—the longevity hypothesis. Mol Biol Evol 25:120–130

    Google Scholar 

  • Nabholz B, Glémin S, Galtier N (2009) The erratic mitochondrial clock: variations of mutation rate, not population size, affect mtDNA diversity across birds and mammals. BMC Evol Biol 9:54

    Article  PubMed  CAS  Google Scholar 

  • Nance HA, Klimley P, Galván-Magaña F, Martínez-Ortíz J, Marko PB (2011) Demographic processes underlying subtle patterns of population structure in the scalloped hammerhead shark, Sphyrna lewini. PLoS ONE 6:e21459

    Article  PubMed  Google Scholar 

  • Orlov AM, Moiseev SI (1999) Some biological features of Pacific sleeper shark, Somniosus pacificus (Bigelow et Schroeder, 1944) (Squalidae) in the Northwestern Pacific Ocean. Oceanol St 28:3–16

    Google Scholar 

  • Peltier WR (1994) Ice age paleotopography. Science 265:195

    Article  PubMed  CAS  Google Scholar 

  • Perry AL, Low PJ, Ellis JR, Reynolds JD (2005) Climate change and distribution shifts in marine fishes. Science 308:1912

    Article  PubMed  CAS  Google Scholar 

  • Planque B, Fromentin J-M, Cury P, Drinkwater KF, Jennings S, Perry RI, Kifani S (2010) How does fishing alter marine populations and ecosystems sensitivity to climate? J Mar Syst 79:403–417

    Article  Google Scholar 

  • Portnoy DS, McDowell JR, Heist EJ, Musick JA, Graves JE (2010) World phylogeography and male-mediated gene flow in the sandbar shark, Carcharhinus plumbeus. Mol Ecol 19:1994–2010

    Article  PubMed  CAS  Google Scholar 

  • Posada D (2008) jModelTest: phylogenetic model averaging. Mol Biol Evol 25:1253–1256

    Article  PubMed  CAS  Google Scholar 

  • Pulquerio MJF, Nichols RA (2007) Dates from the molecular clock: how wrong can we be? Trends Ecol Evol 22:180–184

    Article  PubMed  Google Scholar 

  • Rambaut A, Drummond AJ (2007) Tracer v1.4, Available from: http://beast.bio.ed.ac.uk/Tracer. Accessed 19 Dec 2012

  • Ramirez-Macias D, Vazquez-Juarez R, Galvan-Magana F, Munguia-Vega A (2007) Variations of the mitochondrial control region sequence in whale sharks (Rhincodon typus) from the Gulf of California, Mexico. Fish Res 84:87–95

    Article  Google Scholar 

  • Reum JCP, Essington TE (2011) Season- and depth-dependent variability of a demersal fish assemblage in a large fjord estuary (Puget Sound, Washington). Fish Bull 109:186–197

    Google Scholar 

  • Rogers A, Harpending H (1992) Population growth makes waves in the distribution of pairwise genetic differences. Mol Biol Evol 9:552–569

    PubMed  CAS  Google Scholar 

  • Rosa A, Brehm A (2011) African human mtDNA phylogeography at-a-glance. J Anthropol Sci 89:25–58

    PubMed  Google Scholar 

  • Rozen S, Skaletsky H (2000) Primer3 on the WWW for general users and for biologist programmers. In: Krawetz S, Misener S (eds) Bioinformatics methods and protocols: methods in molecular biology. Humana Press, Totowa, pp 365–386 Source code available at http://fokker.wi.mit.edu/primer3/

  • Salzburger W, Ewing GB, Von Haeseler A (2011) The performance of phylogenetic algorithms in estimating haplotype genealogies with migration. Mol Ecol 20:1952–1963

    Article  PubMed  Google Scholar 

  • Sancetta C (1983) Effect of Pleistocene glaciation upon oceanographic characteristics of the North Pacific Ocean and Bering Sea. Deep Sea Res 30:851–869

    Article  Google Scholar 

  • Schultz JK, Feldheim KA, Gruber SH, Ashley MV, Mcgovern TM, Bowen BW (2008) Global phylogeography and seascape genetics of the lemon sharks (genus Negaprion). Mol Ecol 17:5336–5348

    Article  PubMed  CAS  Google Scholar 

  • Shepherd T, Page F, Macdonald B (2002) Length and sex-specific associations between spiny dogfish (Squalus acanthias) and hydrographic variables in the Bay of Fundy and Scotian Shelf. Fish Oceanogr 11:78–89

    Article  Google Scholar 

  • Slatkin M, Hudson RR (1991) Pairwise comparisons of mitochondrial DNA sequences in stable and exponentially growing populations. Genetics 129:555–562

    PubMed  CAS  Google Scholar 

  • Stevens JD (2007) Whale shark (Rhincodon typus) biology and ecology: a review of the primary literature. Fish Res 84:4–9

    Article  Google Scholar 

  • Stevens JD, Bonfil R, Dulvy NK, Walker PA (2000) The effects of fishing on sharks, rays, and chimaeras (chondrichthyans), and the implications for marine ecosystems. ICES J Mar Sci 57:476–494

    Article  Google Scholar 

  • Stewart JR, Lister AM, Barnes I, Dalen L (2010) Refugia revisited: individualistic responses of species in space and time. Proc R Soc B 277:661–671

    Article  PubMed  Google Scholar 

  • Suchard MA, Weiss RE, Sinsheimer JS (2001) Bayesian selection of continuous-time Markov chain evolutionary models. Mol Biol Evol 18:1001–1013

    Article  PubMed  CAS  Google Scholar 

  • Tanaka S, Takahashi K (2005) Late quaternary paleoceanographic changes in the Bering Sea and the western subarctic Pacific based on radiolarian assemblages. Deep Sea Res Part II 52:2131–2149

    Article  Google Scholar 

  • Tribuzio CA, Gallucci VF, Bargmann GG (2009) Reproduction biology and management implications for spiny dogfish in Puget Sound, Washington. In: Gallucci VF, McFarlane GA, Bargmann GG (eds) Biology and Management of dogfish sharks. 435 pp

  • van der Hammen T, Hooghiemstra H (2000) Neogene and quaternary history of vegetation, climate, and plant diversity in Amazonia. Quatern Sci Rev 19:725–742

    Article  Google Scholar 

  • Veríssimo A, Mcdowell JR, Graves JE (2010) Global population structure of the spiny dogfish Squalus acanthias, a temperate shark with an antitropical distribution. Mol Ecol 19:1651–1662

    Article  PubMed  CAS  Google Scholar 

  • Weng KC, Castilho PC, Morrissette JM, Landeira-Fernandez AM, Holts DB, Schallert RJ, Goldman KJ, Block BA (2005) Satellite tagging and cardiac physiology reveal niche expansion in salmon sharks. Science 310:104–106

    Article  PubMed  CAS  Google Scholar 

  • Weng KC, Foley DG, Ganong JE, Perle C, Shillinger GL, Block BA (2008) Migration of an upper trophic level predator, the salmon shark Lamna ditropis, between distant ecoregions. Mar Ecol Prog Ser 372:253–264

    Article  Google Scholar 

  • Wright SD, Ross HA, Keeling DJ, Mcbride P, Gillman LN (2011) Thermal energy and the rate of genetic evolution in marine fishes. Evol Ecol 25:525–530

    Article  Google Scholar 

  • Yang ZH (2007) PAML 4: a program package for phylogenetic analysis by maximum likelihood. Mol Biol Evol 24:1586–1591

    Article  PubMed  CAS  Google Scholar 

  • Yang ZH, Nielsen R, Goldman N, Pedersen AMK (2000) Codon-substitution models for heterogeneous selection pressure at amino acid sites. Genetics 155:431–449

    PubMed  CAS  Google Scholar 

Download references

Acknowledgments

This project was supported by a Graduate Student Award from the North Pacific Research Board (NPRB), by the H. Mason Keeler Endowment for Excellence scholarship awarded through the School of Aquatic and Fishery Sciences, University of Washington, Seattle, USA and by a grant from the Pollock Conservation Cooperative Research Center (PCCRC). We thank W Stewart Grant (Alaska Dept. of Fish and Game) for critical comments on an earlier draft of the manuscript. We also thank two anonymous reviewers for their comments on the manuscript and many people, who collected and provided samples for this research, including the Washington Department of Fish and Wildlife, the Alaska Fishery Science Center and National Marine Fisheries Service at-sea Observers, Peter Smith, National Institute of Water and Atmospheric Research, New Zealand, and Fausto Tinti, University of Bologna, Italy.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Shannon M. O’Brien.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOCX 200 kb)

Rights and permissions

Reprints and Permissions

About this article

Cite this article

O’Brien, S.M., Gallucci, V.F. & Hauser, L. Effects of species biology on the historical demography of sharks and their implications for likely consequences of contemporary climate change. Conserv Genet 14, 125–144 (2013). https://doi.org/10.1007/s10592-012-0437-8

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10592-012-0437-8

Keywords