[en] Recent climate change has triggered profound reorganization in northeast Atlantic ecosystems, with substantial impact on the distribution of marine assemblages from plankton to fishes. However, assessing the repercussions on apex marine predators remains a challenging issue, especially for pelagic species. In this study, we use Bayesian coalescent modelling of microsatellite variation to track the population demographic history of one of the smallest temperate cetaceans, the harbour porpoise (Phocoena phocoena) in European waters. Combining genetic inferences with palaeo-oceanographic and historical records provides strong evidence that populations of harbour porpoises have responded markedly to the recent climate-driven reorganization in the eastern North Atlantic food web. This response includes the isolation of porpoises in Iberian waters from those further north only approximately 300 years ago with a predominant northward migration, contemporaneous with the warming trend underway since the 'Little Ice Age' period and with the ongoing retreat of cold-water fishes from the Bay of Biscay. The extinction or exodus of harbour porpoises from the Mediterranean Sea (leaving an isolated relict population in the Black Sea) has lacked a coherent explanation. The present results suggest that the fragmentation of harbour distribution range in the Mediterranean Sea was triggered during the warm 'Mid-Holocene Optimum' period (approx. 5000 years ago), by the end of the post-glacial nutrient-rich 'Sapropel' conditions that prevailed before that time.
Alheit, J., Hagen, E., Long-term climate forcing of European herring and sardine populations (1997) Fish Oceanogr., 6, pp. 130-139. , doi:10.1046/j.1365-2419.1997.00035.x
Bandelt, H.-J., Clock debate: When times are a-changin' - Time dependency of molecular rate estimates: Tempest in a teacup (2008) Heredity, 100 (1), pp. 1-2. , DOI 10.1038/sj.hdy.6801054, PII 6801054
Beaugrand, G., Reid, P.C., Ibanez, F., Lindley, J.A., Edwards, M., Reorganization of North Atlantic marine copepod biodiversity and climate (2002) Science, 296 (5573), pp. 1692-1694. , DOI 10.1126/science.1071329
Beaugrand, G., Edwards, M., Brander, K., Luczak, C., Ibanez, F., Causes and projections of abrupt climate-driven ecosystem shifts in the North Atlantic (2008) Ecol. Lett., 11, pp. 1157-1168. , doi:10.1111/j.1461-0248.2008. 01218.x
Brinkmann, B., Klintschar, M., Neuhuber, F., Huhne, J., Rolf, B., Mutation rate in human microsatellites: Influence of the structure and length of the tandem repeat (1998) American Journal of Human Genetics, 62 (6), pp. 1408-1415. , DOI 10.1086/301869
Brook, B.W., Sodhi, N.S., Bradshaw, C.J.A., Synergies among extinction drivers under global change (2008) Trends Ecol. Evol., 23, pp. 453-460. , doi:10.1016/j.tree. 2008.03.011
Calvert, S.E., Nielsen, B., Fontugne, M.R., Evidence from nitrogen isotope ratios for enhanced productivity during formation of eastern Mediterranean sapropels (1992) Nature, 359 (6392), pp. 223-225. , DOI 10.1038/359223a0
De Bruyn, M., Hall, B.L., Chauke, L.F., Baroni, C., Koch, P.L., Hoelzel, A.R., Rapid response of a marine mammal species to Holocene climate and habitat change (2009) PLoS Genet., 5, pp. e1000554. , doi:10.1371/journal. pgen.1000554
Ellegren, H., Microsatellite mutations in the germline: Implications for evolutionary inference (2000) Trends Genet., 16, pp. 551-558. , doi:10.1016/S0168-9525(00)02139-9
Endicott, P., Ho, S.Y.W., Metspalu, M., Stringer, C., Evaluating the mitochondrial timescale of human evolution (2009) Trends Ecol. Evol., 24, pp. 515-521. , doi:10.1016/j. tree.2009.04.006
Estoup, A., Angers, B., Microsatellites and minisatellites for molecular ecology: Theoretical and empirical considerations (1998) Advances in Molecular Ecology, pp. 55-86. , ed. G. Carvalho Amsterdam, The Netherlands: IOS Press
Estoup, A., Jarne, P., Cornuet, J.M., Homoplasy and mutation model at microsatellite loci and their consequences for population genetics analysis (2002) Mol. Ecol., 11, pp. 1591-1604. , doi:10.1046/j.1365-294X.2002. 01576.x
Fiùza, A.F.G., Upwelling patterns of Portugal (1983) Coastal Upwelling, Its Sedimentary Record. Part A. Responses of the Sedimentary Regime to Present Coast Upwelling, pp. 85-98. , eds E. Suess & J. Thiede New York, NY: Plenum Press
Fontaine, M.C., Baird, S.J.E., Piry, S., Ray, N., Tolley, K.A., Duke, S., Birkun Jr., J.A., Michaux, J.R., Rise of oceanographic barriers in continuous populations of a cetacean: The genetic structure of harbour porpoises in Old World waters (2007) BMC Biology, 5, p. 30. , DOI 10.1186/1741-7007-5-30
Frantzis, A., Gordon, J., Hassidis, G., Komenou, A., The enigma of harbour porpoise presence in the Mediterranean Sea (2001) Mar. Mamm. Sci., 17, pp. 937-943. , doi:10.1111/ j.1748-7692.2001.tb01307.x
Galtier, N., Enard, D., Radondy, Y., Bazin, E., Belkhir, K., Mutation hot spots in mammalian mitochondrial DNA (2006) Genome Research, 16 (2), pp. 215-222. , http://www.genome.org/cgi/reprint/16/2/215, DOI 10.1101/gr.4305906
Galtier, N., Nabholz, B., Glemin, S., Hurst, G.D.D., Mitochondrial DNA as a marker of molecular diversity: A reappraisal (2009) Mol. Ecol., 18, pp. 4541-4550. , doi:10.1111/j. 1365-294X.2009.04380.x
Grove, J.M., Little ice ages: Ancient and modern (2004) Routledge Studies in Physical Geography and Environment, , London UK: Routledge
Henn, B.M., Gignoux, C.R., Feldman, M.W., Mountain, J.L., Characterizing the time dependency of human mitochondrial DNA mutation rate estimates (2009) Mol. Biol. Evol., 26, pp. 217-230. , doi:10.1093/molbev/msn244
Herr, H., Fock, H.O., Siebert, U., Spatio-temporal associations between harbour porpoise Phocoena phocoena and specific fisheries in the German Bight (2009) Biol. Conserv., 142, pp. 2962-2972. , doi:10.1016/j.biocon. 2009.07.025
Hewitt, G., The genetic legacy of the quaternary ice ages (2000) Nature, 405 (6789), pp. 907-913. , DOI 10.1038/35016000
Hewitt, G.M., Genetic consequences of climatic oscillations in the Quaternary (2004) Phil. Trans. R. Soc. Lond. B, 359, pp. 183-195. , Discussion 195
Hey, J., Machado, C.A., The study of structured populations - New hope for a difficult and divided science (2003) Nature Reviews Genetics, 4 (7), pp. 535-543. , DOI 10.1038/nrg1112
Hey, J., Nielsen, R., Multilocus methods for estimating population sizes, migration rates and divergence time, with applications to divergence of Drosophila pseudoobscura and D. persimilis (2004) Genetics, 167, pp. 747-760
Ho, S.Y., Phillips, M.J., Cooper, A., Drummond, A.J., Time dependency of molecular rate estimates and systematic overestimation of recent divergence times (2005) Mol. Biol. Evol., 22, pp. 1561-1568. , doi:10.1093/molbev/ msi145
Ho, S.Y., Kolokotronis, S.O., Allaby, R.G., Elevated substitution rates estimated from ancient DNA sequences (2007) Biol. Lett., 3, pp. 702-705. , doi:10.1098/rsbl. 2007.0377
Hoelzel, A.R., Hancock, J.M., Dover, G.A., Evolution of the cetacean mitochondrial d-loop region (1991) Mol. Biol. Evol., 8, pp. 475-493
Hofreiter, M., Stewart, J., Ecological change, range fluctuations and population dynamics during the Pleistocene (2009) Curr. Biol., 19, pp. R584-R594. , doi:10.1016/j.cub.2009.06.030
Hovelsrud, G.K., McKenna, M., Huntington, H.P., Marine mammal harvests and other interactions with humans (2008) Ecol. Appl., 18, pp. S135-S147. , doi:10.1890/06-0843.1
Howell, N., Smejkal, C.B., Mackey, D.A., Chinnery, P.F., Turnbull, D.M., Herrnstadt, C., The pedigree rate of sequence divergence in the human mitochondrial genome: There is a difference between phylogenetic and pedigree rates (2003) American Journal of Human Genetics, 72 (3), pp. 659-670. , DOI 10.1086/368264
Jimenez-Espejo, F.J., Martinez-Ruiz, F., Sakamoto, T., Iijima, K., Gallego-Torres, D., Harada, N., Paleoenvironmental changes in the western Mediterranean since the last glacial maximum: High resolution multiproxy record from the Algero-Balearic basin (2007) Palaeogeography, Palaeoclimatology, Palaeoecology, 246 (2-4), pp. 292-306. , DOI 10.1016/j.palaeo.2006.10.005, PII S0031018206005815
Johnston, D.W., Westgate, A.J., Read, A.J., Effects of fine-scale oceanographic features on the distribution and movements of harbour porpoises Phocoena phocoena in Bay of Fundy (2005) Mar. Ecol. Prog. Ser., 295, pp. 279-293. , doi:10.3354/meps295279
Kastelein, R.A., Van Der Sijs, S.J., Staal, C., Nieuwstraten, S.H., Blubber thickness in harbour porpoises (Phocoena phocoena) (1997) The Biology of Harbour Porpoise, pp. 179-199. , eds A. J. Read, P. R. Wiepkema & P. E. Nachtigall Woerden, The Netherlands: De Spil Publishers
Kerwin, M., Overpeck, J., Webb, R.S., Devernal, A., Rind, D.H., Healy, R.J., The role of oceanic forcing in Mid-Holocene northern hemisphere climatic change (1999) Paleoceanography, 14, pp. 200-210. , doi:10.1029/ 1998PA900011
Kintisch, E., As the seas warm (2006) Science, 313, pp. 776-779. , doi:10.1126/science.313.5788.776
Koopman, H.N., Iverson, S.J., Gaskin, D.E., Stratification and age-related differences in blubber fatty acids of the male harbour porpoise (Phocoena phocoena) (1996) J. Comp. Physiol. B Biochem. Syst. Environ. Physiol., 165, pp. 628-639
Koopman, H.N., Pabst, D.A., McLellan, W.A., Dillaman, R.M., Read, A.J., Changes in blubber distribution and morphology associated with starvation in the harbor porpoise (Phocoena phocoena): Evidence for regional differences in blubber structure and function (2002) Physiological and Biochemical Zoology, 75 (5), pp. 498-512. , DOI 10.1086/342799
Lambert, D.M., Ritchie, P.A., Millar, C.D., Holland, B., Drummond, A.J., Baroni, C., Rates of evolution in ancient DNA from Adélie penguins (2002) Science, 295 (5563), pp. 2270-2273. , DOI 10.1126/science.1068105
Learmonth, J.A., MacLeod, C.D., Santos, M.B., Pierce, G.J., Crick, H.Q.P., Robinson, R.A., Potential effects of climate change on marine mammals (2006) Oceanogr. Mar. Biol., 44, pp. 431-464
Lockyer, C., Harbour porpoises (Phocoena phocoena) in the North Atlantic: Biological parameters (2003) Harbour Porpoises in the North Atlantic, 5, pp. 71-90. , eds T. Haug, G. Desportes, G. A. Vikingsson & L. Witting Tromso, Norway: NAMMCO Scientific Publications
Lockyer, C., All creatures great and smaller: A study in cetacean life history energetics (2007) Journal of the Marine Biological Association of the United Kingdom, 87 (4), pp. 1035-1045. , DOI 10.1017/S0025315407054720, PII S0025315407054720
MacLeod, C.D., Santos, M.B., Reid, R.J., Scott, B.E., Pierce, G.J., Linking sandeel consumption and the likelihood of starvation in harbour porpoises in the Scottish North Sea: Could climate change mean more starving porpoises? (2007) Biol. Lett., 3, pp. 185-188. , doi:10.1098/ rsbl.2006.0588
Major, C., Ryan, W., Lericolais, G., Hajdas, I., Constraints on Black Sea outflow to the Sea of Marmara during the last glacial-interglacial transition (2002) Marine Geology, 190 (1-2), pp. 19-34. , DOI 10.1016/S0025-3227(02)00340-7, PII S0025322702003407
Marx, F.G., Uhen, M.D., Climate, critters, and cetaceans: Cenozoic drivers of the evolution of modern whales (2010) Science, 327, pp. 993-996. , doi:10.1126/science.1185581
Moritz, C., Defining 'evolutionary significant unit' for conservation (1994) Trends Ecol. Evol., 9, pp. 373-375. , doi:10. 1016/0169-5347(94) 90057-4
Moritz, C., Strategies to protect biological diversity and the evolutionary processes that sustain it (2002) Systematic Biology, 51 (2), pp. 238-254. , DOI 10.1080/10635150252899752
Nabholz, B., Glemin, S., Galtier, N., Strong variations of mitochondrial mutation rate across mammals: The longevity hypothesis (2008) Mol. Biol. Evol., 25, pp. 120-130. , doi:10.1093/molbev/msm248
Nabholz, B., Mauffrey, J.-F., Bazin, E., Galtier, N., Glemin, S., Determination of mitochondrial genetic diversity in mammals (2008) Genetics, 178, pp. 351-361. , doi:10. 1534/genetics.107.073346
O'Corry-Crowe, G., Climate change and the molecular ecology of Arctic marine mammals (2008) Ecol. Appl., 18, pp. S56-S76. , doi:10.1890/06-0795.1
Osborn, T.J., Briffa, K.R., The spatial extent of 20th-century warmth in the context of the past 1200 years (2006) Science, 311 (5762), pp. 841-844. , DOI 10.1126/science.1120514
(2000) Quality Status Report 2000: Region IV-Bay of Biscay and Iberian Coast, , OSPAR Commission OSPAR Commission, London, UK
Pakendorf, B., Stoneking, M., Mitochondrial DNA and human evolution (2005) Annual Review of Genomics and Human Genetics, 6, pp. 165-183. , DOI 10.1146/annurev.genom.6.080604.162249
Pastene, L.A., Goto, M., Kanda, N., Zerbini, A.N., Kerem, D., Watanabe, K., Bessho, Y., Palsboll, P.J., Radiation and speciation of pelagic organisms during periods of global warming: The case of the common minke whale, Balaenoptera acutorostrata (2007) Molecular Ecology, 16 (7), pp. 1481-1495. , DOI 10.1111/j.1365-294X.2007.03244.x
Perry, A.L., Low, P.J., Ellis, J.R., Reynolds, J.D., Ecology: Climate change and distribution shifts in marine fishes (2005) Science, 308 (5730), pp. 1912-1915. , DOI 10.1126/science.1111322
Phillips, C.D., Trujillo, R.G., Gelatt, T.S., Smolen, M.J., Matson, C.W., Honeycutt, R.L., Patton, J.C., Bickham, J.W., Assessing substitution patterns, rates and homoplasy at HVRI of Steller sea lions, Eumeto-pias jubatus (2009) Mol. Ecol., 18, pp. 3379-3393. , doi:10.1111/j. 1365-294X.2009.04283.x
Pimm, S.L., Biodiversity: Climate Change or Habitat Loss - Which Will Kill More Species? (2008) Current Biology, 18 (3), pp. R117-R119. , DOI 10.1016/j.cub.2007.11.055, PII S096098220702341X
Pimm, S.L., Climate disruption and biodiversity (2009) Curr. Biol., 19, pp. R595-R601. , doi:10.1016/j.cub.2009.05.055
Poulard, J.-C., Blanchard, F., The impact of climate change on the fish community structure of the eastern continental shelf of the Bay of Biscay (2005) ICES Journal of Marine Science, 62 (7), pp. 1436-1443. , DOI 10.1016/j.icesjms.2005.04.017, PII S105431390500086X, Influence of Climate Change on North Atlantic Fish Stocks
Read, A.J., Harbour porpoise (Phocoena phocoena) (1999) Handbook of Marine Mammals, pp. 323-350. , eds S. H. Ridgway & R. Harrison London, UK: Academic Press
Read, A.J., Hohn, A.A., Life in the fast lane: The life history of harbour porpoises from the Gulf of Maine (1995) Mar. Mamm. Sci., 11, pp. 423-440. , doi:10.1111/j. 1748-7692.1995.tb00667.x
Richardson, A.J., Schoeman, D.S., Climate impact on plankton ecosystems in the Northeast Atlantic (2004) Science, 305 (5690), pp. 1609-1612. , DOI 10.1126/science.1100958
Rohling, E.J., Abu-Zieb, R., Casford, J.L.S., Hayes, A., Hoogakker, B.A.A., The marine environment: Present and past (2009) The Physical Geography of the Mediterranean, pp. 33-67. , ed. J. C. Woodward Oxford, UK: Oxford University Press
Rosel, P., Dizon, A.E., Haygood, M.G., Variability of the mitochondrial control region in populations of the harbour porpoise, Phocoena phocoena, on interoceanic and regional scales (1995) Con. J. Fish. Aquat. Sci., 52, pp. 1210-1219
Ryther, J.H., Photosynthesis and fish production in the sea (1969) Science, 166, pp. 72-76. , doi:10.1126/science.166.3901.72
Santos, M.B., Pierce, G.J., The diet of harbour porpoise (Phocoena phocoena) in the northeast Atlantic (2003) Oceanogr. Mar. Biol., 41, pp. 355-390
Santos, M.B., Pierce, G.J., Learmonth, J.A., Reid, R.J., Ross, H.M., Patterson, I.A.P., Reid, D.G., Beare, D., Variability in the diet of harbor porpoises (Phocoena phocoena) in Scottish waters 1992-2003 (2004) Mar. Mamm. Sci., 20, pp. 1-27. , doi:10.1111/j.1748-7692.2004. tb01138.x
Southward, A.J., Hawkins, S.J., Burrows, M.T., Seventy years' observations of changes in distribution and abundance of zooplankton and intertidal organisms in the western English Channel in relation to rising sea temperature (1995) J. Therm. Biol., 20, pp. 127-155. , doi:10.1016/ 0306-4565(94) 00043-I
Springer, G.S., Rowe, H.D., Hardt, B., Edwards, R.L., Cheng, H., Solar forcing of Holocene droughts in a stalagmite record from West Virginia in east-central North America (2008) Geophys. Res. Lett., 35, pp. L17703. , doi:10. 1029/2008GL034971
Stenson, G.B., Harbour porpoise (Phocoena phocoena) in the North Atlantic: Abundance, removals, and sustainability of removals (2003) Harbour Porpoises in the North Atlantic, 5, pp. 271-302. , eds T. Haug, G. Desportes, G. A. Vikingsson & L. Witting Tromso, Norway: NAMMCO Scientific Publications
Strasburg, J.L., Rieseberg, L.H., How robust are 'isolation with migration' analyses to violations of the im model? (2010) A Simulation Study. Mol. Biol. Evol., 27, pp. 297-310. , doi:10.1093/molbev/msp233
Sun, J.X., Mullikin, J.C., Patterson, N., Reich, D.E., Microsatellites are molecular clocks that support accurate inferences about history (2009) Mol. Biol. Evol., 26, pp. 1017-1027. , doi:10.1093/molbev/msp025
Tolley, K.A., Rosel, P.E., Population structure and historical demography of eastern North Atlantic harbour porpoises inferred through mtDNA sequences (2006) Mar. Ecol. Prog. Ser., 327, pp. 297-308. , doi:10.3354/ meps327297
Viaud-Martinez, K.A., Morphological and genetic differentiation of the Black Sea harbour porpoise Phocoena phocoena (2007) Mar. Ecol. Prog. Ser., 338, pp. 281-294. , doi:10. 3354/meps338281
Worm, B., Impacts of biodiversity loss on ocean ecosystem services (2006) Science, 314, pp. 787-790. , doi:10.1126/ science.1132294
Worm, B., Rebuilding global fisheries (2009) Science, 325, pp. 578-585. , doi:10.1126/science.1173146
