Tracing early stages of species differentiation: Ecological, morphological and genetic divergence of Galápagos sea lion populations

BMC Evolutionary Biology

Volumn 8, Issue 1, 2008, Pages

  Wolf, Jochen B W ^a,b,f   Harrod, Chris ^b,c   Brunner, Sylvia ^d   Salazar, Sandie ^e   Trillmich, Fritz ^f   Tautz, Diethard ^a,b  

^a UNIVERSITY OF COLOGNE   (Germany)

^b MAX PLANCK INSTITUTE FOR EVOLUTIONARY BIOLOGY   (Germany)

^c QUEEN'S UNIVERSITY BELFAST   (United Kingdom)

^d UNIVERSITY OF ALASKA FAIRBANKS   (United States)

^e Estación Científica Charles Darwin   (Ecuador)

^f BIELEFELD UNIVERSITY   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

MICROSATELLITE DNA; MITOCHONDRIAL DNA;

ARCTOCEPHALUS GALAPAGOENSIS; ARTICLE; CULTURAL ANTHROPOLOGY; ECOSYSTEM; GENETIC VARIABILITY; ISOTOPE ANALYSIS; MITOCHONDRION; MORPHOLOGY; NONHUMAN; POPULATION RESEARCH; SEAL; SKULL; SPECIES DIFFERENTIATION; STATISTICAL SIGNIFICANCE; ZALOPHUS WOLLEBAEKI; ANIMAL; BAYES THEOREM; ECOLOGY; ECUADOR; GENETIC SELECTION; GENETICS; HAPLOTYPE; HISTOLOGY; POPULATION GENETICS; SPECIES DIFFERENCE;

ANIMALIA; ARCTOCEPHALUS GALAPAGOENSIS; MAMMALIA; OTARIIDAE; ZALOPHUS WOLLEBAEKI;

ANIMALS; BAYES THEOREM; DNA, MITOCHONDRIAL; ECOLOGY; ECUADOR; GENETIC SPECIATION; GENETICS, POPULATION; HAPLOTYPES; SEA LIONS; SELECTION (GENETICS); SPECIES SPECIFICITY; VARIATION (GENETICS);

EID: 44649139816     PISSN: None     EISSN: 14712148     Source Type: Journal    
DOI: 10.1186/1471-2148-8-150     Document Type: Article

References (78)

1. Speciation in the 21st century. Book review of "Speciation" by Jerry A. Coyne & H. Allen Orr. J Mallet, Heredity 2005 95 105 109 10.1038/sj.hdy.6800686
2. On the origin of species by sympatric speciation. U Dieckmann M Doebeli, Nature 1999 400 6742 354 357 10.1038/22521 10432112
3. The conditions for speciation through intraspecific competition. R Bürger KA Schneider M Willensdorfer, Evolution 2006 60 2185 2206 17236413
4. Speciation through the learning of habitat features. JB Beltman P Haccou, Theor Popul Biol 2005 67 3 189 202 10.1016/j.tpb.2005.01.001 15808336
5. Speciation along environmental gradients. M Doebeli U Dieckmann, Nature 2003 421 259 264 10.1038/nature01274 12529641
6. Ecological divergence exhibits consistently positive associations with reproductive isolation across disparate taxa. DJ Funk P Nosil WJ Etges, Proc Natl Acad Sci USA 2006 103 9 3209 3213 16492742 10.1073/pnas.0508653103
7. Adaptive Speciation. U Dieckmann M Doebeli JAJ Metz D Tautz, Cambridge, UK: Cambridge University Press 2004
8. Ecological speciation. HD Rundle P Nosil, Ecol Lett 2005 8 3 336 352 10.1111/j.1461-0248.2004.00715.x
9. The Ecology of Adaptive Radiation. D Schluter, Oxford, U.K.: Oxford Universtiy Press 2000
10. Tracing the first steps to speciation: ecological and genetic differentiation of a salamader population in a small forest. S Steinfartz M Weitere D Tautz, Mol Ecol 2007 16 21 4550 4561 10.1111/j.1365-294X.2007.03490.x 17877714
11. Phylogeography and Patterns of Incipient Speciation. D Tautz, Adaptive Speciation Cambridge: Cambridge University Press, Dieckmann U, Doebeli M, Metz JAJ, Tautz D, 2004 305 320
12. Environmental correlates of population differentiation in Atlantic herring. D Bekkevold C Andre TG Dahlgren LAW Clausen E Torstensen H Mosegaard GR Carvalho TB Christensen E Norlinder DE Ruzzante, Evolution 2005 59 12 2656 2668 16526512
13. Rapid evolution of reproductive isolation in the wild: evidence from introduced salmon. AP Hendry JK Wenburg P Bentzen EC Volk TP Quinn, Science 2000 290 516 519 10.1126/science.290.5491.516 11039932
14. The energetic cost of moving about. VA Tucker, Am Scientist 1975 63 413 419 1137237
15. Rise of oceanographic barriers in continuous populations of a cetacean: the genetic structure of harbour porpoises in Old World waters. MC Fontaine SJE Baird S Piry N Ray KA Tolley S Duke A Birkun M Ferreira T Jauniaux A Llavona, BMC Biology 2007 5 17651495
16. Reproductive character displacement and the genetics of gamete recognition in tropical sea urchins. LB Geyer SR Palumbi, Evolution 2003 57 5 1049 1060 12836822
17. Evolution of population structure in a highly social top predator, the killer whale. AR Hoelzel J Hey ME Dahlheim C Nicholson V Burkanov N Black, Mol Biol Evol 2007 24 6 1407 1415 10.1093/molbev/msm063 17400573
18. Galápagos and Californian sea lions are separate species: genetic analysis of the genus Zalophus and its implications for conservation management. JB Wolf D Tautz F Trillmich, Front Zool 2007 4 1 20 17868473 10.1186/1742-9994-4-20
19. Ambiente físico. S Banks, Reserva Marina de Galápagos Puerto Ayora, Santa Cruz, Galápagos: Fundación Charles Darwin/Servicio Parque Nacional Galápagos, Danulat E, Edgar GJ, 2002 22 35
20. Surface seawater distributions of inorganic carbon and nutrients around the Galápagos Islands: results from the PlumEx experiment using automated chemical mapping. CM Sakamoto FJ Millero WS Yao GE Friederich FP Chavez, Deep-Sea Res II 1998 45 6 1055 1071 10.1016/S0967-0645(98)00013-7
21. Population size and trends of the Galápagos Penguin Spheniscus mendiculus. H Vargas C Logheed H Snell, Ibis 2005 147 367 374 10.1111/j.1474-919x.2005.00412.x
22. Reserva Marina de Galápagos. E Danulat GJ Edgar, Puerto Ayora, Santa Cruz, Galápagos: Fundación Charles Darwin/Servicio Parque Nacional Galápagos; 2002
23. Carbon-13 enrichment in benthic compared to planktonic algae: foodweb implications. RL France, Mar Ecol - Prog Ser 1995 124 307 312 10.3354/meps124307
24. Stable isotope analysis reveals pelagic foraging by the Southern sea lion in central Chile. LA Hückstädt CP Rojas T Antezana, J Exp Mar Biol Ecol 2007
25. Determining trophic niche width: a novel approach using stable isotope analysis. S Bearhop CE Adams S Waldron RA Fuller H Macleod, J Anim Ecol 2004 73 5 1007 1012 10.1111/j.0021-8790.2004.00861.x
26. Correlation of pairwise genetic and geographic distance measures: Inferring the relative influences of gene flow and drift on the distribution of genetic variability. DW Hutchison AR Templeton, Evolution 1999 53 6 1898 1914 10.2307/2640449
27. Movement and diving behavior of male California sea lion (Zalophus californianus) during anomalous oceanographic conditions of 2005 compared to those of 2004. MJ Weise DP Costa RM Kudela, Geophys Res Lett 2006 33 22
28. Multiple foraging strategies in a marine apex predator, the Galápagos Sea Lion. S Villegas-Amtmann DP Costa Y Tremblay D Aurioles-Gamboa S Salazar, Mar Ecol - Prog Ser
29. Deep genetic subdivision within a continuously distributed and highly vagile marine mammal, the Steller's sea lion (Eumetopias jubatus). JI Hoffman CW Matson W Amos TR Loughlin JW Bickham, Mol Ecol 2006 15 10 2821 2832 16911203
30. Long-range paternal gene flow in southern elephant seals. A Fabiani AR Hoelzel F Galimberti MMC Muelbert, Science 2003 299 676 10.1126/science.299. 5607.676 12560542
31. Evolution of Character Displacement in Darwin's Finches. PR Grant BR Grant, Science 2006 313 224 226 10.1126/science.1128374 16840700
32. Ecological character displacement and speciation in sticklebacks. D Schluter JD McPhail, Am Nat 1992 140 1 85 108 10.1086/285404
33. Ecological Studies - Pinnipeds and El Nĩo. F Trillmich KA Ono, Berlin: Springer Verlag 1991 88
34. Males in the shade: habitat use and sexual segregation in the Galápagos sea lion (Zalophus californianus wollebaeki). JBW Wolf G Kauermann F Trillmich, Behav Ecol Sociobiol 2005 59 2 293 302 10.1007/s00265-005-0042-7
35. Dieta, tamão poblacional e interacción con desechos costeros del lobo marino Zalophus californianus wollebaeki en las islas Galápagos. Disertación previa al título de Licenciatura en Ciencias Biológicas. SK Salazar, Pontificia Universidad Católica del Ecuador 1999
36. Fish prey of the sympatric Galápagos fur seal and sea lions: seasonal variation and niche seperation. T Dellinger F Trillmich, Can J Zool 1999 77 1204 1216 10.1139/cjz-77-8-1204
37. Diving Behavior of Galápagos Sea Lions. GL Kooyman F Trillmich, Fur seals - Maternal Strategies on Land and at Sea Princeton, New Jersey: Princeton University Press, Gentry RL, Kooyman GL, 1986 209 219
38. Adaptive effects of natal experience on habitat selection by dispersers. JA Stamps JM Davis, Anim Behav 2006 72 1279 1289 10.1016/j.anbehav.2006.03.010
39. Learning the ecological niche. T Slagsvold KL Wiebe, Proc R Soc B 2007 274 1606 19 23 17015332 10.1098/rspb.2006.3663
40. Differentiation of tundra/taiga and boreal coniferous forest wolves: genetics, coat colour and association with migratory caribou. M Musiani JA Leonard HD Cluff CC Gates S Mariani PC Paquet C Vilà RK Wayne, Mol Ecol 2007 16 4149 4170 10.1111/j.1365-294X.2007.03458.x 17725575
41. Parent-offspring and sibling conflict in Galápagos fur seals and sea lions. F Trillmich JBW Wolf, Behav Ecol Sociobiol 2008 62 3 363 375 10.1007/s00265-007-0423-1
42. Long-term memory for concepts in a California sea lion (Zalophus californianus). CR Kastak RJ Schusterman, Anim Cogn 2002 5 4 225 232 10.1007/s10071-002-0153-8 12461600
43. How animals classify friends and foes. RJ Schusterman CJ Reichmuth D Kastak, Curr Dir Psychol Sci 2000 9 1 1 6 10.1111/1467-8721.00047
44. Beyond habitat requirements: individual fine-scale site fidelity in a colony of the Galapagos sea lion (Zalophus wollebaeki) creates conditions for social structuring. JBW Wolf F Trillmich, Oecologia 2007 152 553 567 10.1007/s00442-007-0665-7 17505851
45. Social structure in a colonial mammal: Unravelling hidden structural layers and their foundations by network analysis. JBW Wolf D Mawdsley F Trillmich R James, Anim Behav 2007 74 5 1293 1302 10.1016/j.anbehav.2007.02.024
46. Kin in space. Social viscosity in a spatially and genetically sub-structured network. JBW Wolf F Trillmich, Proc R Soc Lond B 2008 10.1098/rspb.2008.0356
47. Islands in the sea: extreme female natal site fidelity in the Australian sea lion, Neophoca cinerea. RA Campbell NJ Gales GM Lento CS Baker, Biol Lett 2008 4 139 142 10.1098/rsbl.2007.0487 18042512
48. Mating systems, philopatry and dispersal in birds and mammals. PJ Greenwood, Anim Behav 1980 28 1140 1162 10.1016/S0003-3472(80)80103-5
49. Social organization and territoral behavior of the Galápagos sea lion Zalophus californianus wollebaeki (Sivertsen, 1953). BD Voigt, Thesis. Kopenhagen 1979 1 75
50. Sexual conflicts in spotted hyenas: male and female mating tactics and their reproductive outcome with respect to age, social status and tenure. ML East T Burke K Wilhelm C Greig H Hofer, Proc Biol Sci 2003 270 1521 1247 1254 10.1098/rspb.2003.2363 12816637
51. Dominance, access to colonies, and queues for mating opportunities by male boat-tailed grackles. JP Poston, Behav Ecol Sociobiol 1997 41 2 89 98 10.1007/s002650050368
52. Seasonal changes of vocal rates and their relation to territorial status in male Galápagos sea lions (Zalophus wollebaeki). H Kunc JBW Wolf, Ethology 2008 114 381 388 10.1111/j.1439-0310.2008.01484.x
53. Genetic tagging reveals extreme site fidelity in territorial male Antarctic fur seals Arctocephalus gazella. JI Hoffman PN Trathan W Amos, Mol Ecol 2006 15 12 3841 3847 10.1111/j.1365-294X.2006.03053.x 17032279
54. Male reproductive strategy and the importance of maternal status in the antarctic fur seal Arctocephalus gazella. JI Hoffman IL Boyd W Amos, Evolution 2003 57 8 1917 1930 14503632
55. Selection against migrants contributes to the rapid evolution of ecologically dependent reproductive isolation. AP Hendry, Evol Ecol Res 2004 6 1219 1236
56. Reproductive isolation caused by natural selection against immigrants from divergent habitats. P Nosil TH Vines DJ Funk, Evolution 2005 59 705 719 15926683
57. Geology of Galápagos Islands. T Simkin, Key environments - Galápagos Oxford: Pergamon Press, Perry R, 1984 15 43
58. Eruption rates at Fernandina volcano, Galápagos archipelago, from cosmogenic helium surficial laval flows. MD Kurz S Rowland J Curtice A Saal T Naumann, Eos Trans AGU 2005 86 52 Fall Meet. Suppl., Abstract U33A-0016
59. Physical volcanology and structural development of Cerro Azul volcano, Isabela island, Galápagos: implications for the development of Galápagos-type shield volcanoes. T Naumann D Geist, Bull Volcanol 2000 61 497 514
60. Isotopic variation complicates analysis of trophic relations within the fish community of Plußsee: a small, deep, stratifying lake. C Harrod J Grey, Archiv für Hydrobiologie 2006 167 281 299 10.1127/0003-9136/2006/ 0167-0281
61. Stable isotope analyses provide new insights into ecological plasticity in a mixohaline population of European eel. C Harrod J Grey TK McCarthy M Morrissey, Oecologia 2005 144 673 683 10.1007/s00442-005-0161-x 16025352
62. Cranial ontogeny of otariid seals. S Brunner MM Bryden PD Shaughnessy, Syst Biodivers 2004 2 1 83 110 10.1017/S1477200004001367
63. EMBL Align database. http://www.ebi.ac.uk/embl/Submission/alignment.html OR http://srs.ebi.ac.uk OR ftp://ftp.ebi.ac.uk/pub/databases/embl/align/
64. Arlequin ver. 3.0: An integrated software package for population genetics data analysis. L Excoffier G Laval S Schneider, Evol Bioinformatics Online 2005 1 47 50
65. The microevolution of the Galápagos marine iguana Amblyrhynchus cristatus assessed by nuclear and mitochondrial genetic analyses. K Rassmann D Tautz F Trillmich C Gliddon, Mol Ecol 1997 6 5 437 452 10.1046/j.1365-294X.1997. 00209.x
66. Development of new microsatellite loci and evaluation of loci from other pinniped species for the Galápagos sea lion (Zalophus californianus wollebaeki). JBW Wolf D Tautz A Caccone S Steinfartz, Conserv Genet 2006 7 3 461 465 10.1007/s10592-005-9045-1
67. Ten novel dinucleotide microsatellite loci cloned from the Galápagos sea lion (Zalophus californianus wollebaeki) are polymorphic in other pinniped species. JI Hoffman S Steinfartz JBW Wolf, Mol Ecol Notes 2007 7 1 103 105 10.1111/j.1471-8286.2006.01544.x
68. Inference of population structure using multilocus genotype data: Linked loci and correlated allele frequencies. D Falush M Stephens JK Pritchard, Genetics 2003 164 4 1567 1587 12930761
69. Detecting the number of clusters of individuals using the software STRUCTURE: a simulation study. G Evanno S Regnaut J Goudet, Mol Ecol 2005 14 2611 2620 10.1111/j.1365-294X.2005.02553.x 15969739
70. Inference of population structure using multilocus genotype data. JK Pritchard M Stephens P Donnelly, Genetics 2000 155 2 945 959 10835412
71. Estimating F-statistics for the analysis of population structure. BS Weir CC Cockerham, Evolution 1984 38 1358 1370 10.2307/2408641
72. R-ST Calc: a collection of computer programs for calculating estimates of genetic differentiation from microsatellite data and determining their significance. SJ Goodman, Mol Ecol 1997 6 9 881 885 10.1111/j.1365-294X.1997. tb00143.x
73. FSTAT: a program to estimate and test gene diversities and fixation indices (version 2.9.3). J Goudet, 2001 http://www.unil.ch/izea/softwares/fstat. html
74. Testing differentiation in diploid populations. J Goudet M Raymond T De Meeüs F Rousset, Genetics 1996 144 1933 1949 8978076
75. Microsat (version 1.5d): a program for calculating various statistics on microsatellite allele data. E Minch A Ruiz-Linares DB Goldstein M Feldman LL Cavalli-Sforza, Stanford, CA: Stanford University 1997
76. PHYLIP (Phylogeny Inference Package) version 3.6. J Felsenstein, Distributed by the author Department of Genome Sciences, University of Washington, Seattle 2004
77. Genetic differentiation between individuals. F Rousset, J Evol Biol 2000 13 1 58 62 10.1046/j.1420-9101.2000.00137.x
78. R: a language for data analysis and graphics. R Ihaka R Gentleman, J Comput Graph Stat 1996 5 299 314 10.2307/1390807