Living in a tilted world: Climate change and geography limit speciation in Old World anchovies (Engraulis; Engraulidae)

Biological Journal of the Linnean Society

Volumn 88, Issue 4, 2006, Pages 673-689

  Grant, W Stewart ^a,c   Bowen, Brian W ^b  

^a UNIVERSITY OF THE WITWATERSRAND   (South Africa)

^b UNIVERSITY OF HAWAII   (United States)

^c UNIVERSITY OF ALASKA ANCHORAGE   (United States)

Author keywords

Colonization; Cytochrome b; Dispersal; Extinction; Milankovitch cycles; mtDNA; Phylogeography

Indexed keywords

CLIMATE CHANGE; CLIMATE OSCILLATION; DISPERSAL; EXTINCTION RISK; FAUNA; FISH; GEOGRAPHICAL VARIATION; HISTORICAL PERSPECTIVE; MARINE ECOSYSTEM; MARINE MAMMAL; MILANKOVITCH CYCLE; MITOCHONDRIAL DNA; PALEONTOLOGY; PHYLOGEOGRAPHY; RANGE EXPANSION; RNA-DNA RATIO; TEMPERATE ENVIRONMENT;

ATLANTIC OCEAN; ATLANTIC OCEAN (EAST); PACIFIC OCEAN; PACIFIC OCEAN (NORTHEAST); PACIFIC OCEAN (NORTHWEST);

ENGRAULIDAE; ENGRAULIS; ENGRAULIS JAPONICUS;

EID: 33746217870     PISSN: 00244066     EISSN: 10958312     Source Type: Journal    
DOI: 10.1111/j.1095-8312.2006.00651.x     Document Type: Article

References (104)

1. Agostini VN, Bakun A. 2002. 'Ocean triads' in the Mediterranean Sea: physical mechanisms potentially structuring reproductive habitat suitability (with example application to European anchovy, Engraulis encrasicolus). Fisheries Oceanography 11: 129-142.
2. Avise JC. 2000. Phylogeography, the history and formation of species. Cambridge, MA: Harvard University Press.
3. Avise JC, Walker D. 1997. Pleistocene phylogeographic effects on avian populations and the speciation process. Proceedings of the Royal Society of London Series B, Biological Sciences 265: 457-463.
4. Avise JC, Walker D, Johns GC. 1998. Speciation durations and Pleistocene effects on vertebrate phylogeography. Proceedings of the Royal Society of London Series B, Biological Sciences 265: 1707-1712.
5. Barange M, Hampton I, Roel BA. 1999. Trends in the abundance and distribution of anchovy and sardine in the South African continental shelf in the 1990s, deduced from acoustic surveys. South African Journal of Marine Science 21: 367-391.
6. Baumgartner TR, Soutar A, Ferreira-Batrina V. 1992. Reconstruction of the history of Pacific sardine and northern anchovy populations over the past two millennia from sediments of the Santa Barbara basin, California. California Cooperative Oceanic Fisheries Investigations Reports 33: 24-40.
7. Beare D, Burns F, Jones F, Peach K, Portilla E, Greig T, McKenzie E, Reid D. 2004. An increase in the abundance of anchovies and sardines in the north-western North Sea since 1995. Global Change and Biology 10: 1209.
8. Bembo DG, Carvalho GR, Cingolani N, Arneri E, Giannetti G, Pitcher TJ. 1996a. Allozymic and morphometric evidence for two stocks of the European anchovy Engraulis encrasicolus in Adriatic waters. Marine Biology 126: 529-538.
9. Bembo DG, Carvalho GR, Cingolani N, Pitcher TJ. 1996b. Electrophoretic analysis of stock structure in northern Mediterranean anchovies, Engraulis encrasicolus. ICES Journal of Marine Science 53: 115-128.
10. Bembo DG, Carvalho GR, Snow M, Cingolani N, Pitcher TJ. 1995. Stock discrimination among European anchovies, Engraulis encrasicolus, by means of PCR-amplified mitochondrial DNA analysis. Fishery Bulletin (Washington DC) 94: 31-40.
11. Bennett KD. 1990. Milankovitch cycles and their effects on species in ecological and evolutionary time. Paleobiology 16: 11-21.
12. Bennett KD. 1997. Evolution and ecology: the pace of life. Cambridge: Cambridge University Press.
13. Bermingham E, Martin AP. 1998. Comparative mtDNA phylogeography of neotropical freshwater fishes: testing shared history to infer the evolutionary landscape of lower Central America. Molecular Ecology 7: 499-517.
14. Bernatchez L, Wilson CC. 1998. Comparative phylogeography if Nearctic and Palearctic fishes. Molecular Ecology 7: 431-452.
15. Blanchon P, Shaw J. 1995. Reef drowning during the last deglaciation: evidence for catastrophic sea-level rise and deep-ocean circulation. Geology 23: 4-8.
16. Bond G, Broecker W, Johnson S, McManus J, Labeyrie L, Jouzel J, Bonani G. 1993. Correlations between climate records from North Atlantic sediments and Greenland ice. Nature 365: 143-147.
17. Bond G, Showers W, Cheseby M, Lotti R, Almasi P, deMenocal P, Priore P, Cullen H, Hajdas I, Bonani G. 1997. A pervasive millennial-scale cycle in North Atlantic Holocene and glacial climates. Science 278: 1257-1265.
18. Borsa P. 2002. Allozyme, mitochondrial-DNA, and morphometric variability indicate cryptic species of anchovy (Engraulis encrasicolus). Biological Journal of the Linnean Society 75: 261-269.
19. Borsa P, Collet A, Durand J-D. 2004. Nuclear-DNA markers confirm the presence of two anchovy species in the Mediterranean. Comptes Rendus Biologies 327: 1113-1123.
20. Bowen BW, Grant WS. 1997. Phylogeography of the sardines (Sardinops spp.): assessing biogeographic models and population histories in temperate upwelling zones. Evolution 51: 1601-1510.
21. Bowen BW, Kamezaki N, Limpus CJ, Hughes GH, Meylan AB, Avise JC. 1994. Global phylogeography of the loggerhead turtle (Caretta caretta) as indicated by mitochondrial DNA haplotypes. Evolution 48: 1820-1828.
22. Boyd AJ. 1979. A relationship between sea surface temperature variability and anchovy Engraulis capensis recruitment off South West Africa, 1970-78. Fishery Bulletin of South Africa 12: 80-84.
23. Boyd AJ, Shannon LV, Schulein FH, Taunton-Clark J. 1997. Food, transport and anchovy recruitment in the southern Benguela upwelling system off South Africa. In: Duran MH, Cury P, Mendelssohn R, Roy C, Bakun A, Pauly D, eds. Global vs local changes in upwelling systems. Paris: Editions de l'Orstom, 195-210.
24. Broeker WS, Denton GH. 1989. The role of ocean-atmosphere reorganizations in glacial cycles. Geochimica Cosmochimica Acta 53: 2465-2501.
25. Butler JL. 1989. Growth during the larval and juvenile stages of the northern anchovy, Engraulis mordax, in the California Current during 1980-84. Fishery Bulletin (Washington DC) 87: 645-652.
26. Charlesworth D, Charlesworth B, Morgan MT. 1995. The pattern of neutral molecular variation under the background selection model. Genetics 141: 1619-1632.
27. Chenoweth SF, Hughes HM, Keenan CP, Lavery S. 1998. When oceans meet: a teleost shows secondary intergradation at an Indian-Pacific interface. Proceedings of the Royal Society of London B265: 415-420.
28. Clark WG. 1976. The lessons of the Peruvian anchoveta fishery. California Cooperative Oceanic Fisheries Investigations Reports 19: 57-63.
29. Clement M, Posada D, Crandall KA. 2000. TCS: a computer program to estimate gene genealogies. Molecular Ecology 9: 1657-1660.
30. Crandall KA, Templeton AR. 1993. Empirical tests of some predictions from coalescent theory with applications to intraspecific phylogeny reconstruction. Genetics 134: 959-969.
31. Cronin TM. 1999. Principles of paleoclimatology. New York, NY: Columbia University Press.
32. Cronin TM, Raymo ME. 1997. Orbital forcing of the deep-sea benthic species diversity. Nature 385: 624-627.
33. DeVries TJ, Pearcy WG. 1982. Fish debris in sediments of the upwelling zone off central Peru: a late Quaternary record. Deep-Sea Research 29: 87-109.
34. Dodson JJ, Colombani F, Ng PKL. 1995. Phylogeographic structure in mitochondrial DNA of a South-east Asian freshwater fish, Hemibagrus nemurus (Siluroidei; Bagridae) and Pleistocene sea-level changes on the Sunda shelf. Molecular Ecology 4: 331-346.
35. Dutton PH, Bowen BW, Owens DW, Barragan A, Davis SK. 1999. Global phylogeography of the leatherback turtle, Dermochelys coriacea. Journal of Zoology 248: 397-409.
36. Ewens WJ. 1972. The sampling theory of selectively neutral alleles. Theoretical Population Biology 3: 87-112.
37. Excoffier L, Smouse PE, Quattro JM. 1992. Analysis of molecular variance inferred from metric distances among DNA haplotypes: application to human mitochondrial restriction data. Genetics 131: 479-491.
38. Felsenstein J. 1992. Estimating effective population size from samples of sequences: inefficiency of pairwise and segregating sites as compared to phylogenetic estimates. Genetical Research 59: 139-147.
39. Fitch JE. 1969. Fossil records of certain schooling fishes of the California Current System. California Cooperative Oceanic Fisheries Investigations Reports 13: 71-80.
40. Fu Y-X. 1997. Statistical tests of neutrality of mutations against population growth, hitchhiking and background selection. Genetics 147: 915-925.
41. Fu Y-X, Li W-H. 1993. Statistical tests of neutrality of mutations. Genetics 133: 693-709.
42. Fujio Y, Kato Y. 1979. Genetic variation in fish populations. Bulletin of the Japanese Society of Scientific Fisheries 45: 1169-1178.
43. Godfrey JS, Hirst AC, Wilkin J. 1993. Why does the Indonesian throughflow appear to originate from the North Pacific? Journal of Physical Oceanography 23: 1087-1098.
44. Gordon AL, Fine RA. 1996. Pathways of water between the Pacific and Indian Oceans in the Indonesian Seas. Nature 379: 146-149.
45. Grande L, Nelson G. 1985. Interrelationships of fossil and recent anchovies (Teleostei: Engraulidae) and description of a new species from the Miocene of Cyprus. American Museum of Natural History, Noviates 2826: 1-16.
46. Grant WS. 1985. Biochemical genetic stock structure of the southern African anchovy, Engraulis capensis Gilchrist. Journal of Fish Biology 27: 23-29.
47. Grant WS, Bowen BW. 1998. Shallow population histories in deep evolutionary lineages of marine fishes: insights from sardines and anchovies and lessons for conservation. Journal of Heredity 89: 415-426.
48. Grant WS, Leslie RW, Bowen BW. 2005. Molecular genetic assessment of bipolarity in the anchovy genus Engraulis. Journal of Fish Biology 67: 1242-1265.
49. Hays JD, Imbrie J, Shackleton NJ. 1976. Variations in the Earth's orbit: pacemaker of the ice ages. Science 194: 1121-1132.
50. Hayward TL. 1997. Pacific Ocean climate change: atmospheric forcing, ocean circulation and ecosystem response. Trends in Ecology and Evolution 12: 150-154.
51. Hedgecock D, Hutchinson ES, Li G, Sly FL, Nelson K. 1989. Genetic and morphometric variation in the Pacific sardine, Sardinops sagax caerulea: comparisons and contrast with historical data and the variability in the northern anchovy, Engraulis mordax. Fishery Bulletin (Washington DC) 87: 653-671.
52. Hewitt GM. 1996. Some genetic consequences of ice ages, and their role in divergence and speciation. Biological Journal of the Linnean Society 58: 247-276.
53. Hewitt GM. 2000. The genetic legacy of the Quaternary ice ages. Nature 405: 907-913.
54. Hudson RR. 1990. Gene genealogies and the coalescent process. In: Futuyama D Antonovics J, eds. Oxford surveys in evolutionary biology. Oxford: Oxford University Press, 1-44.
55. Huntley B, Webb T III. 1989. Migration: species' response to climatic variations caused by changes in the earth's orbit. Journal of Biogeography 16: 5-19.
56. James AG. 1987. Feeding ecology, diet and field-based studies on feeding selectivity of the Cape anchovy Engraulis capensis Gilchrist. South African Journal of Marine Science 5: 673-692.
57. Jansson R, Dynesius M. 2002. The fate of clades in a world of recurrent climatic change: Milankovitch oscillations and evolution. Annual Review of Ecology and Systematics 33: 741-777.
58. Kawahata H. 2002. Shifts in oceanic and atmospheric boundaries in the Tasman Sea (Southwest Pacific) during the Late Pleistocene: evidence from organic carbon and lithogenic fluxes. Palaeogeography Palaeoclimatology Palaeoecology 184: 225-249.
59. Kawasaki T, Omori M. 1995. Possible mechanisms underlying fluctuations in the far eastern sardine population inferred from time series of two biological traits. Fisheries Oceanography 4: 238-242.
60. Kimura M. 1980. A simple method for estimating evolutionary rates of base substitutions through comparative studies of nucleotide sequences. Journal of Molecular Evolution 16: 111-120.
61. Kotilainen AT, Shackleton NJ. 1995. Rapid climate variability in the North Pacific Ocean during the past 95 000 years. Nature 377: 323-326.
62. Kuhner M, Yamato J, Felsenstein J. 1995. Estimating effective population size and mutation rate from sequence data using Metropolis-Hastings sampling. Genetics 140: 1421-1430.
63. Kuhner M, Yamato J, Felsenstein J. 1998. Maximum likelihood estimation of population growth rates based on the coalescent. Genetics 149: 429-434.
64. Lasker R. 1975. Field criteria for survival of anchovy larvae: the relation between inshore chlorophyll maximum layers and successful first feeding. Fishery Bulletin (Washington DC) 73: 453-462.
65. Lecomte F, Grant WS, Dodson JJ, Rodriguez-Sanchez R, Bowen BW. 2004. Living with uncertainty: genetic imprints of climate shifts in East Pacific anchovy (Engraulis mordax) and sardine (Sardinops sagax). Molecular Ecology 13: 2169-2182.
66. Lehman SJ, Keigwin LD. 1992. Sudden changes in North Atlantic circulation during the last glaciation. Nature 356: 757-762.
67. Lluch-Belda D, Crawford RJM, Kawasaki T, MacCall AD, Parrish RH, Schwartzlose RA, Smith PE. 1989. World-wide fluctuations of sardine and anchovy stocks: the regime problem. South African Journal of Marine Science 8: 195-205.
68. Lluch-Belda D, Schwartzlose RA, Serra R, Parrish R, Kawasaki T, Hedgecock D, Crawford RJM. 1992. Sardine and anchovy regime fluctuations of abundance in four regions of the world oceans: a workshop report. Fisheries Oceanography 1: 339-347.
69. Magoulas A, Tsimenides N, Zouros E. 1996. Mitochondrial DNA phylogeny and the reconstruction of the population history of a species: the case of the European anchovy (Engraulis encrasicolus). Molecular Biology and Evolution 13: 178-190.
70. Murphy GI. 1966. Population biology of the Pacific sardine (Sardinops caerulea). Proceedings of the California Academy of Science 34: 1-84.
71. Nei M. 1987. Molecular evolutionary genetics. New York, NY: Columbia University Press.
72. Plounevez S, Champalbert G. 1999. Feeding behaviour and tropic environment of Engraulis encrasicolus (L.) in the Bay of Biscay. Estuarine and Coastal Shelf Sciences 49: 177-191.
73. Posada D, Crandall KA. 1998. MODELTEST: testing the model of DNA substitution. Bioinformatics 14: 817-818.
74. Posada D, Crandall KA. 2001. Intraspecific gene genealogies: trees grafting into networks. Trends in Ecology and Evolution 16: 37-45.
75. Posada D, Crandall KA, Templeton AR. 2000. GeoDis: a program for the cladistic nested analysis of the geographical distribution of genetic haplotypes. Molecular Ecology 9: 487-488.
76. Rand DM. 1996. Neutrality tests of molecular markers and the connection between DNA polymorphism, demography, and conservation biology. Conservation Biology 10: 665-671.
77. Rogers AR, Harpending H. 1992. Population growth makes waves in the distribution of pairwise genetic differences. Molecular Biology and Evolution 9: 552-569.
78. Rozas J, Rozas R. 1999. Dnasp, Version 3: an integrated program for molecular population genetics and molecular evolution analysis. Bioinformatics 15: 174-175.
79. Saitou N, Nei M. 1987. The neighbor-joining method: a new method for reconstructing phylogenetic trees. Molecular Biology and Evolution 4: 406-425.
80. Schneider S, Excoffier L. 1999. Estimation of demographic parameters from the distribution of pairwise differences when the mutation rates vary among sites: application to human mitochondrial DNA. Genetics 152: 1079-1089.
81. Schneider S, Roessli D, Excoffier L. 2000. ARLEQUIN, version 2.000 a software for population genetics data analysis. Geneva: University of Geneva. Available at http://anthro.unige.ch/arlequin.
82. Schwartlose RA, Alheit J, Bakun A, Baumgartner TR, Cloete R, Crawford RJM, Fletcher WJ, Green-Ruiz Y, Hagen E, Kawasaki T, Lluch-Belda D, Lluch-Cota SE, MacCall AD, Matsuura Y, Nevarez-Martinez MO, Parrish RH, Roy C, Serra R, Shust KV, Ward MN, Zuzunaga JZ. 1999. Worldwide large-scale fluctuations of sardine and anchovy populations. South African Journal of Marine Science 21: 289-347.
83. Shackleton LY. 1987. A comparative study of fossil fish scales from three upwelling regions. South African Journal of Marine Science 5: 79-84.
84. Shackleton NJ. 1988. Oxygen isotopes, ice volume, and sea level. Quaternary Science Reviews 6: 183-190.
85. Shannon LV. 1985. The Benguela ecosystem. 1. Evolution of the Benguela, physical features and processes. Oceanography and Marine Biology: An Annual Review 23: 105-182.
86. Shannon LV, Crawford RJM, Brundrit GB, Underhill LG. 1988. Responses of fish populations in the Benguela ecosystem to environmental change. Journal du Conseil Permanent Inernational Pour l'Exploration de la Mer 45: 5-12.
87. Shelton PA, Hutchings L. 1982. Transport of anchovy, Engraulis capensis Gilchrist, eggs and early larvae by a frontal jet current. Journal du Conseil Permanent Inernational Pour l'Exploration de la Mer 40: 185-198.
88. Shelton PA, Hutchings L. 1990. Ocean stability and anchovy spawning in the southern Benguela Current region. Fishery Bulletin (Washington DC) 88: 323-338.
89. Slatkin M, Hudson RR. 1991. Pairwise comparisons of mitochondrial DNA sequences in stable and exponentially growing populations. Genetics 129: 555-562.
90. Spanakis E, Tsimenides N, Zouros E. 1989. Genetic differences between populations of sardine, Sardina pilchardus, and anchovy, Engraulis encrasicolus, in the Aegean and Ionean seas. Journal of Fish Biology 35: 417-437.
91. Stanley DJ, Wezel FC, eds. 1985. Geological evolution of the Mediterranean basin. New York, NY: Springer.
92. Steininger FF, Rögl F. 1984. Paleogeography and palinspatic construction of the Neogene of the Mediterranean and Paratethys. In: Dix JE Robertson AHF, eds. The geological evolution of the Eastern Mediterranean. Geological Society Special Publication No. 17. Oxford: Blackwell Scientific, 659-668.
93. Swofford DL. 2002. PAUP* phylogenetic analysis using parsimony (*and other methods), Version 4. Sunderland, MA: Sinauer Associates.
94. Tamura K, Nei M. 1993. Estimation of the number of nucleotide substitutions in the control region of mitochondrial DNA in humans and chimpanzees. Molecular Biology and Evolution 10: 512-526.
95. Taunton-Clark J, Shannon LV. 1988. Annual and interannual variability in the southeast Atlantic during the 20th century. South African Journal of Marine Science 6: 97-106.
96. Templeton AR. 2004. Statistical phylogeography: methods of evaluating and minimizing inference errors. Molecular Ecology 13: 789-809.
97. Templeton AR, Sing CF. 1993. A cladistic analysis of phenotypic associations with haplotypes inferred from restriction endonuclease mapping. IV. Nested analyses with cladogram uncertainty and recombination. Genetics 134: 659-669.
98. Templeton AR, Boerwinkle E, Sing CF. 1987. A cladistic analysis of phenotypic associations with haplotypes inferred from restriction endonuclease mapping. I. Basic theory and an analysis of alcohol dehydrogenase activity in Drosophila. Genetics 117: 343-351.
99. Templeton AR, Crandall KA, Sing CF. 1992. A cladistic analysis of phenotypic association with haplotypes inferred from restriction endonuclease mapping and DNA sequence data. III. Cladogram estimation. Genetics 132: 619-633.
100. Templeton AR, Routman E, Phillips C. 1995. Separating population structure from population history: a cladistic analysis of the geographical distribution of mitochondrial DNA haplotypes in the tiger salamander, Ambystoma tigrinum. Genetics 140: 767-782.
101. Watterson GA. 1978. The homozygosity test of neutrality. Genetics 88: 405-417.
102. Whitehead PJP, Nelson GJ, Wongratana T. 1988. FAO species catalogue, vol. 7. Clupeoid fishes of the world (suborder Clupeoidei). Rome: UNDP FAO.
103. Williams DF, Peck J, Karabanov EB, Prokopenko AA, Kravchinsky V, King J, Kuzmin MI. 1997. Lake Baikal record of continental climate response to orbital insolation during the past five million years. Science 278: 1114-1117.
104. Yu Z-N, Kong X-Y, Guo T-H, Jiang Y-Y, Zhuang Z-M, Jin X-S. 2005. Mitochondrial DNA sequence variation of Japanese anchovy Engraulis japonicus from the Yellow Sea and East China Sea. Fisheries Science 71: 299-307.