Skip to main content

Advertisement

SpringerLink
Log in

Phylogeography of California and Galápagos sea lions and population structure within the California sea lion

  • Original Paper
  • Published:
Marine Biology Aims and scope Submit manuscript

Abstract

We investigate the phylogeography of California (Zalophus californianus) and Galápagos (Z. wollebaeki) sea lions and describe within-population structure for the California sea lion based on mitochondrial DNA. Fifty control-region haplotypes were found, 41 from Z. californianus and 9 from Z. wollebaeki, with three fixed differences between the two species. Ranked population boundaries along the range of Z. californianus were defined based on the Monmonier Maximum Difference Algorithm, resulting in five genetically distinct populations, two in the Pacific Ocean and three inside the Gulf of California. A Minimum Spanning Network showed a strong phylogeographic signal with two well-defined clusters, Z. californianus and Z. wollebaeki, separated by six base-pair differences, supporting the existence of two genetically distinct species with an estimated divergence time of ~0.8 Ma. Results are discussed in the context of the historical geologic and paleoceanographic events of the last 1 Ma in the eastern Pacific.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  • Acevedo-Whitehouse K, de la Cueva H, Gulland FMD, Aurioles-Gamboa D, Arellano-Carbajal F, Suárez-Guemes F (2003) Evidence of Leptospira interrogans infection in California sea lion pups from the Gulf of California. J Wildl Dis 39:145–151

    Article  PubMed  Google Scholar 

  • Acevedo-Whitehouse K, Spraker TR, Lyons E, Melin SR, Gulland F, Delong RL, Amos W (2006) Contrasting effects of heterozygosity on survival and hookworm resistance in California sea lion pups. Mol Ecol 15:1973–1982. doi:https://doi.org/10.1111/j.1365-294X.2006.02903.x

    Article  CAS  PubMed  Google Scholar 

  • Akst EP, Boersma PD, Fleischer RC (2002) A comparison of genetic diversity between the Galápagos penguin and the Magellanic penguin. Cons Gen 3:375–383. doi:https://doi.org/10.1023/A:1020555303124

    Article  CAS  Google Scholar 

  • Amos B, Hoelzel AR (1991) Long-term preservation of whale skin for DNA analysis. In: Hoelzel AR (ed) The genetic ecology of whales and dolphins. Special publication no. 13 of the IWC, Cambridge, pp 99–103

  • Antonelis GA, Stewart BS, Perryman WS (1990) Foraging characteristics of female northern fur seals (Callorhinus ursinus) and California sea lions (Zalophus californianus). Can J Zool 68:150–158. doi:https://doi.org/10.1139/z90-022

    Article  Google Scholar 

  • Arnason U, Johnsson E (1992) The complete mitochondrial DNA sequence of the harbor seal, Phoca vitulina. J Mol Evol 34:493–505. doi:https://doi.org/10.1007/BF00160463

    Article  CAS  PubMed  Google Scholar 

  • Aurioles-Gamboa D, Díaz-Guzmán C, Le Boeuf BJ, Casper D (2009) Temporomandibular arthritis and osteomielitis in California sea lions (Zalophus califorinianus). J Zoo Wildl Med (in press)

  • Aurioles-Gamboa D, Le Boeuf BJ (1991) Effects of the El Niño 1982–1983 on California Sea Lions in México. In: Trillmich F, Ono KA (eds) Pinnipeds and El Niño: responses to environmental stress. Ecological studies 88. Springer, New York, pp 112–118

    Chapter  Google Scholar 

  • Aurioles-Gamboa D, Zavala-González A (1994) Algunos factores ecológicos que determinan la distribución y abundancia del lobo marino Zalophus californianus, en el Golfo de California. Cienc Mar 20:535–553

    Article  Google Scholar 

  • Aurioles-Gamboa D, Sinsel F, Fox C, Alvarado E, Maravilla-Chávez O (1983) Winter migration of subadult male California sea lions Zalophus californianus in the southern part of Baja California. J Mammal 64:513–518. doi:https://doi.org/10.2307/1380369

    Article  Google Scholar 

  • Aurioles-Gamboa D, Castillo S, Contreras AI, Barnes LG (2000) Patron latitudinal en caracteres dentarios del lobo marino de California en Norteamérica (Zalophus californianus californianus). In: XXV Reunión Internacional para el Estudio de los Mamíferos Marinos. La Paz, Baja California Sur, México

  • Baker AR, Loughlin TR, Burkanov V, Matson CW, Trujillo RG, Calkins DG, Wickliffe JK, Bickham JW (2005) Variation of mitochondrial control region sequences of Steller sea lions: the three-stock hypothesis. J Mammal 86:1075–1084. doi:https://doi.org/10.1644/04-MAMM-A-113R1.1

    Article  Google Scholar 

  • Bartholomew GA (1967) Seal and sea lion populations of the Channel Islands. In: Philbrick RN (ed) Proceedings of the symposium on the biology of the Calif. Islands, Santa Barbara Botanic Garden. Santa Barbara, CA, pp 229–243

  • Beheregaray LB, Havill N, Gibbs J, Fritts T, Powell JR, Caccone G (2004) Giant tortoises are not so slow: rapid diversification and biogeographic consensus in the Galápagos. Proc Natl Acad Sci USA 101:6514–6519. doi:https://doi.org/10.1073/pnas.0400393101

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bernardi G, Findley L, Rocha-Olivares A (2003) Vicariance and dispersal across Baja California in disjunct marine fish populations. Evol Int J Org Evol 57:1599–1609

    Article  Google Scholar 

  • Bickham JW, Patton JC, Loughlin TR (1996) High variability for control-region sequences in a marine mammal: implications for conservation and biogeography of Steller sea lion (Eumetopias jubatus). J Mammal 77:95–108. doi:https://doi.org/10.2307/1382712

    Article  Google Scholar 

  • Boness DJ, Oftedal OT, Ono KA (1991) The effect of El Niño on pup development in the California Sea Lion (Zalophus californianus) I. Early postnatal growth. In: Trillmich F, Ono KA (eds) Pinnipeds and El Niño: responses to environmental stress. Ecological studies 88. Springer, New York, pp 173–179

    Chapter  Google Scholar 

  • Bowen L, Aldridge BM, DeLong R, Melin S, Godínez C, Zavala A, Gulland F, Lowenstine L, Stott JL, Johnson ML (2006) MHC gene configuration variation in geographically disparate populations of California sea lions (Zalophus californianus). Mol Ecol 15:529–533. doi:https://doi.org/10.1111/j.1365-294X.2005.02612.x

    Article  CAS  PubMed  Google Scholar 

  • Brassel KE, Reif D (1979) A procedure to generate Thiessen polygons. Geogr Anal 11:289–303

    Article  Google Scholar 

  • Browne RA, Anderson DJ, Houser JN, Cruz F, Glasgow KJ, Hodges CN, Massey G (1997) Genetic diversity and divergence of endangered Galápagos and Hawaiian petrel populations. Condor 99:812–815. doi:https://doi.org/10.2307/1370494

    Article  Google Scholar 

  • Brunner S (2004) Fur seals and sea lions (Otariidae): identification of species and taxonomic review. Syst Biodivers 1:339–439. doi:https://doi.org/10.1017/S147720000300121X

    Article  Google Scholar 

  • Capella JJ, Flórez-González L, Falk-Fernández P, Palacios DM (2002) Regular appearance of otariid pinnipeds along the Colombian Pacific coast. Aquat Mamm 28:67–72

    Google Scholar 

  • Cenami Spada E, Hanggi EB, Schusterman RJ (1991) Variation in vocalizations and individual recognition in two subspecies of California sea lions. In: Abstracts of the 9th Biennial conference on the biology of marine mammals. Chicago, Illinois

  • Christie DM, Duncan RA, McBirney AR, Richards MA, White WM, Harp KS, Fox CG (1992) Drowned islands downstream from the Galapagos hotspot imply extended speciation times. Nature 355:246–248. doi:https://doi.org/10.1038/355246a0

    Article  Google Scholar 

  • Clark PU, Archer D, Pollard D, Blum JD, Rial JA, Brovkin V, Mix AC, Pisias NG, Roy M (2006) The middle Pleistocene transition: characteristics, mechanisms, and implications for long-term changes in atmospheric pCO2. Quat Sci Rev 25:3,150–153,184, doi:https://doi.org/10.1016/j.quascirev.2006.07.008

    Article  Google Scholar 

  • Crandall KA, Templeton AR (1993) Empirical tests of some predictions from coalescent theory with applications to intraspecific phylogeny reconstruction. Genetics 134:959–969

    CAS  PubMed  PubMed Central  Google Scholar 

  • Davies JL (1958) The Pinnipedia: an essay in zoogeography. Geogr Rev 48:474–493. doi:https://doi.org/10.2307/211670

    Article  Google Scholar 

  • Del Toro L, Heckel G, Camacho-Ibar VF, Schramm Y (2006) California sea lion (Zalophus californianus californianus) have lower chlorinated hydrocarbon contents in Baja California, México than in Southern California, USA. Environ Pollut 142:83–92. doi:https://doi.org/10.1016/j.envpol.2005.09.019

    Article  CAS  PubMed  Google Scholar 

  • DeLong RL, Antonelis GA, Oliver CW, Stewart BS, Lowry MC, Yochem PK (1991) Effects of the 1982–83 El Niño on several population parameters and diet of California Sea Lions on the California Channel Islands. In: Trillmich F, Ono KA (eds) Pinnipeds and El Niño: responses to environmental stress. Ecological studies 88. Springer, New York, pp 166–172

    Chapter  Google Scholar 

  • Deméré TA, Berta A, Adam PJ (2003) Pinnipedimorph evolutionary biogeography. Bull Am Mus Nat Hist 279:32–76. doi:https://doi.org/10.1206/0003-0090(2003)279<0032:C>2.0.CO;2

    Article  Google Scholar 

  • Dickerson BR, Ream RR, Vignieri SN, Bentzen P, Antonelis GA (2008) Population Structure as Revealed by mtDNA and Microsatellites in Northern Fur Seals, Callorhinus ursinus. In: Alaska Marine Science Symposium, Anchorage, AK

  • Eibl-Eibesfeldt I (1984) The Galapagos seals. Part 1. Natural history of the Galapagos sea lion (Zalophus californianus wollebaeki, Siverstsen). In: Perry R (ed) Key environments: Galapagos. Pergamon Press, Oxford, pp 207–214

    Google Scholar 

  • Elorriaga-Verplancken F, Aurioles-Gamboa D (2008) Trace metal concentrations in the hair of Zalophus californianus pups and their relation to feeding habits. Biol Trace Elem Res 126:148–164. doi:https://doi.org/10.1007/s12011-008-8186-8

    Article  CAS  PubMed  Google Scholar 

  • Espinosa de los Reyes MG (2007) Variabilidad espacial de la dieta del lobo marino de California (Zalophus californianus californianus, Lesson 1828). MSc thesis, CICESE, Ensenada, BC, México

  • Espinosa-Carreón TL, Strub PT, Beier E, Ocampo-Torres F, Glaxiola-Castro G (2004) Seasonal and interannual variability of satellite-derived chlorophyll pigment, surface height, and temperature off Baja California. J Geophys Res 109(C03039). doi:https://doi.org/10.1029/2003JC002105

  • Excoffier L, Smouse P (1994) Using allele frequencies and geographic subdivision to reconstruct gene genealogies within a species. Molecular variance parsimony. Genetics 136:343–359

    CAS  PubMed  PubMed Central  Google Scholar 

  • Excoffier L, Smouse P, Quattro J (1992) Analysis of molecular variance inferred from metric distances among DNA haplotypes: application to human mitochondrial DNA restriction data. Genetics 131:479–491

    CAS  PubMed  PubMed Central  Google Scholar 

  • Francis JM, Heath CB (1991) Population abundance, pup mortality, and copulation frequency in the California sea lion in relation to the 1983 El Niño on San Nicolas Island. In: Trillmich F, Ono KA (eds) Pinnipeds and El Niño: responses to environmental stress. Ecological studies 88. Springer, New York, pp 119–128

    Chapter  Google Scholar 

  • Friesen VL, Anderson DJ, Steeves TE, Jones H, Schreiber EA (2002) Molecular support for species status of the Nazca booby (Sula granti). Auk 119(3):820–826. doi:https://doi.org/10.1642/0004-8038(2002)119[0820:MSFSSO]2.0.CO;2

    Article  Google Scholar 

  • Gallo-Reynoso JP, Solórzano-Velasco JL (1991) Two new sightings of California sea lions on the southern coast of México. Mar Mamm Sci 7:96. doi:https://doi.org/10.1111/j.1748-7692.1991.tb00557.x

    Article  Google Scholar 

  • García-Rodríguez FJ, Aurioles-Gamboa D (2004) Spatial and temporal variation in the diet of the California sea lion (Zalophus californianus) in the Gulf of California, México. Fish Bull (Washington, DC) 102:47–62

    Google Scholar 

  • Geist D (1996) On the emergence and submergence of the Galápagos Islands. Not Galap 56:5–9

    Google Scholar 

  • González-Suárez M, McCluney K, Aurioles-Gamboa D, Gerber LR (2006) Incorporating uncertainty in spatial structure for viability predictions: a case study of California sea lions. Anim Conserv 9:219–227. doi:https://doi.org/10.1111/j.1469-1795.2006.00022.x

    Article  Google Scholar 

  • Grehan J (2001) Biogeography and evolution of the Galapagos: integration of the biological and geological evidence. Biol J Linn Soc Lond 74(3):267–287. doi:https://doi.org/10.1006/bijl.2001.0576

    Article  Google Scholar 

  • Guo S, Thomson E (1992) Performing the exact test of Hardy–Weinberg proportion for multiple alleles. Biometrics 48:361–372. doi:https://doi.org/10.2307/2532296

    Article  CAS  PubMed  Google Scholar 

  • Harlin-Cognato A, Bickham JW, Loughlin TR, Honeycutt RL (2006) Glacial refugia and the phylogeography of Steller’s sea lion (Eumetopias jubatus) in the North Pacific. J Evol Biol 19:955–969. doi:https://doi.org/10.1111/j.1420-9101.2005.01052.x

    Article  CAS  PubMed  Google Scholar 

  • Heath CB (2002) California, Galapagos, and Japanese Sea Lions. In: Perrin WF, Würsig B, Thewissen JGM (eds) Enciclopedia of Marine Mammals. Academic Press, San Diego, pp 180–186

    Google Scholar 

  • Hernández-Camacho C, Aurioles-Gamboa D, Laake J, Gerber L (2008a) Survival rates of the California sea lion, Zalophus californianus, in México. J Mammal 89:1059–1066. doi:https://doi.org/10.1644/07-MAMM-A-404.1

    Article  Google Scholar 

  • Hernández-Camacho C, Aurioles-Gamboa D, Gerber L (2008b) Age-specific birth rates of California sea lions (Zalophus californianus) in the Gulf of California, México. Mar Mamm Sci 24:664–676. doi:https://doi.org/10.1111/j.1748-7692.2008.00199.x

    Article  Google Scholar 

  • Hey J (1991) The structure of genealogies and the distribution of fixed differences between DNA sequence samples from natural populations. Genetics 128:831–840

    CAS  PubMed  PubMed Central  Google Scholar 

  • Hickey BM (1998) Coastal oceanography of western North America from the tip of Baja California to Vancouver Island, coastal segment (8,E). In: Robinson AR, Brink KH (eds) The sea, vol 11, pp 345–393. Wiley, New York, pp 345–393

  • 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. doi:https://doi.org/10.1093/molbev/msi145

    Article  CAS  PubMed  Google Scholar 

  • Jacobs DK, Haney TA, Louie KD (2004) Genes, diversity, and geologic process on the Pacific coast. Annu Rev Earth Planet Sci 32:601–652. doi:https://doi.org/10.1146/annurev.earth.32.092203.122436

    Article  CAS  Google Scholar 

  • Kahru M, Marinone SG, Lluch-Cota SE, Parés-Sierra A, Mitchell BG (2004) Ocean-color variability in the Gulf of California: scales from days to ENSO. Deep Sea Res Part II Top Stud Oceanogr 51:139–146. doi:https://doi.org/10.1016/j.dsr2.2003.04.001

    Article  CAS  Google Scholar 

  • Kannan K, Kajiwara N, Le Boeuf BJ, Tanabe S (2004) Organochlorine pesticides and polychlorinated biphenyls in California sea lions. Environ Pollut 131:425–434. doi:https://doi.org/10.1016/j.envpol.2004.03.004

    Article  CAS  PubMed  Google Scholar 

  • King JE (1983) Seals of the World. National History British Museum. Cornell University Press, New York

    Google Scholar 

  • Kooyman GL, Trillmich F (1986) Diving behavior of Galapagos sea lions. In: Gentry RL, Kooyman GL (eds) Fur seals—maternal strategies on land and at sea. Princeton University Press, Princeton, pp 209–220

    Google Scholar 

  • Koutavas A, Sachs JP (2008) Northern timing of deglaciation in the eastern equatorial Pacific from alkenone paleothermometry. Paleoceanography 23:PA4205. doi:https://doi.org/10.1029/2008PA001593

    Article  Google Scholar 

  • Kumar S, Tamura K, Jakobsen IB, Nei M (2001) Mega, version 2.1. Molecular Evolutionary Genetics Analysis software. Arizona State University, Tempe

    Google Scholar 

  • Labrada MV, Aurioles-Gamboa D, Castro-González MI (2007) Relation of dental wear to the concentrations of essential minerals in teeth of the California sea lion Zalophus californianus californianus. Biol Trace Elem Res 114:107–126

    Article  Google Scholar 

  • Lawrence KT, Liu Z, Herbert TD (2006) Evolution of the eastern tropical Pacific through Plio-Pleistocene glaciation. Science 321:79–83. doi:https://doi.org/10.1126/science.1120395

    Article  Google Scholar 

  • Le Boeuf BJ, Aurioles-Gamboa D, Condit R, Fox C, Gisiner R, Romero R, Sincel F (1983) Size and distribution of the California sea lion in México. Proc Calif Acad Sci 43:77–85

    Google Scholar 

  • Lea DW, Pak DK, Belanger CL, Spero HJ, Hall MA, Shackleton NJ (2006) Paleoclimate history of Galápagos surface waters over the last 135,000 yr. Quat Sci Rev 25:1152–1167. doi:https://doi.org/10.1016/j.quascirev.2005.11.010

    Article  Google Scholar 

  • Lesson RP (1828) Phoque. In: Bory de Sanint-Vicent JBGM (ed) Dictionaire Classique d’Histoire Naturelle. Paris Rey et Gravier, Paris

    Google Scholar 

  • Lluch-Belda D (1969) El lobo marino de California, Zalophus californianus (Lesson, 1828). Allen 1880; observaciones sobre su ecología y explotación. Instituto Mexicano de Recursos Naturales Renovables, México

    Google Scholar 

  • Lowry MS, Maravilla-Chávez MO (2002) Abundancia de lobos marinos de California (Zalophus californianus) en Baja California, México y Estados Unidos de America durante julio y agosto del 2000. In: XXVII Reunión Internacional para el estudios de los Mamíferos Marinos. Veracruz, Ver. México

  • Lowry MS, Boveng P, DeLong RJ, Oliver CW, Stewart BS, De Anda-Delgado H, Barlow J (1992) Status of the California sea lion (Zalophus californianus californianus) population in 1992. NOAA-TM-NMFS-SWFSC-LJ-92–32, La Jolla, pp 1–24

  • Maldonado JE, Orta-Dávila F, Stewart BS, Geffen E, Wayne RK (1995) Intraspecific genetic differentiation in California sea lions (Zalophus californianus) from Southern California and the Gulf of California. Mar Mamm Sci 11:46–58. doi:https://doi.org/10.1111/j.1748-7692.1995.tb00273.x

    Article  Google Scholar 

  • Manel S, Schwartz MK, Luikart G, Taberlet P (2003) Landscape genetics: combining landscape ecology and population genetics. Trends Ecol Evol 18:189–197. doi:https://doi.org/10.1016/S0169-5347(03)00008-9

    Article  Google Scholar 

  • Maniscalco JM, Wynne K, Pitcher KW, Hanson MB, Melin SR, Atkinson S (2004) The occurrence of California sea lions in Alaska. Aquat Mamm 30:427–433. doi:https://doi.org/10.1578/AM.30.3.2004.427

    Article  Google Scholar 

  • Manni F, Guérard E, Heyer E (2004) Geographic patterns of (genetic, morphologic, linguistic) variation: how barriers can be detected by “Monmonier’s algorithm”. Am J Hum Biol 76:173–190. doi:https://doi.org/10.1353/hub.2004.0034

    Article  Google Scholar 

  • Melin SR, DeLong RL (1999) At-sea distribution and diving behavior of California sea lion females from San Miguel Island, California. In: Browne DR, Mitchell KL, Chaney HW (eds) Proceeding of the fifth California islands symposium. Santa Barbara Museum of Natural History, Santa Barbara, pp 402–407

    Google Scholar 

  • Moritz C (1994) Defining “Evolutionarily Significant Units” for conservation. Trends Ecol Evol 9:373–375. doi:https://doi.org/10.1016/0169-5347(94)90057-4

    Article  CAS  PubMed  Google Scholar 

  • Morris PA, Oliver GW, Elliott J, Melin SR, DeLong RL (1999) El Niño 1998 and changes in California sea lion, Zalophus californianus, use of Año Nuevo island. In: Abstracts of the 13th Biennial Conference on the Biology of Marine Mammals, Wailea, Hawaii

  • Newsome SD, Etnier MA, Koch PL, Aurioles-Gamboa D (2006) Using Carbon and Nitrogen isotopes to investigate reproductive strategies in Northeast Pacific otariids. Mar Mamm Sci 22:556–572. doi:https://doi.org/10.1111/j.1748-7692.2006.00043.x

    Article  Google Scholar 

  • Palacios DM, Félix F, Flórez-González L, Capella JJ, Chiluiza D, Haase BJM (1997) Sightings of Galápagos sea lions (Zalophus californianus wollebaeki) on the coasts of Colombia and Ecuador. Mammalia 61:114–116

    Google Scholar 

  • Peterson RS, Bartholomew GA (1967) The natural history and behavior of the California sea lion. Special publication no. 1. The American society of mammalogists, pp 1–79

  • Porras-Peters H, Aurioles-Gamboa D, Cruz-Escalona VH, Koch PL (2008) Position, breadth and trophic overlap of sea lions (Zalophus californianus) in the Gulf of California, México. Mar Mamm Sci 24:554–576. doi:https://doi.org/10.1111/j.1748-7692.2008.00197.x

    Article  Google Scholar 

  • Rassmann K (1997) Evolutionary age of the Galapagos iguanas predates the age of the present Galapagos Islands. Mol Phylogenet Evol 7:158–172. doi:https://doi.org/10.1006/mpev.1996.0386

    Article  CAS  PubMed  Google Scholar 

  • Repenning CA, Ray CE, Grigourescou D (1979) Pinniped biogeography. In: Gray J, Boucot AJ (eds) Historical biogeography, plate tectonics, and the changing environment. Proceedings of the 37th Annual Biology Colloquium, and selected papers. Oregon State University, Corvallis, Oregon, pp 357-369

  • Riedman M (1990) The Pinnipeds. Seals, sea lions, and walruses. University of California Press, Berkeley/Los Angeles

    Google Scholar 

  • Salazar S (2002) Lobo Marino y Lobo Peletero. In: Danulat E, Edgar GJ (eds) Reserva Marina de Galápagos. Linea Base de la biodiversidad. Fund Charles Darwin/Ser Par Nac Galap, Santa Cruz, Galápagos, Ecuador, pp 267–290

  • Salazar S, Bustamante RH (2003) Effects of the 1997–98 El Niño on population size and diet of the Galápagos sea lion (Zalophus wollebaeki). Not Galap 62:40–45

    Google Scholar 

  • Salazar S, Michuy V (2008) Estado poblacional y conservación de los pinnípedos de las islas Galápagos. XIII Reunión de Trabajo de Especialístas en Mamíferos Acuáticos de América del Sur y 7˚ Congreso SOLAMAC. Montevideo, Uruguay, p 196

    Google Scholar 

  • Sambrook J, Fritsch EF, Maniatis T (1989) Molecular cloning: a laboratory manual. Cold Spring Harbor Laboratory Press, Cold Spring Harbor

    Google Scholar 

  • Santamaría del Ángel E, Millán-Nuñez R, González-Silvera A, Müller-Karger F (2002) The color signature of the Ensenada Front and its seasonal and interannual variability. CCOFI Rep 43:155–161

    Google Scholar 

  • Schneider S, Roessli D, Excoffier L (2001) Arlequin, version 2. A software for population genetic data analysis. Genetic and Biometry Laboratory, University of Geneva, Switzerland

  • Sivertsen E (1953) A new species of sea lion, Zalophus wollebaeki from the Galapagos Islands. Det Kong Nor Videnskaps Selsk Forh 26:1–3

    Google Scholar 

  • Sivertsen E (1954) A survey of the eared seals (family Otariidae) with remarks on the Antarctic seals collected by M/K “Norwegian” in 1928–1929. Det Nor Videnskaps—Akad Oslo

  • Stewart DT, Baker AJ (1994) Patterns of sequence variation in the mitochondrial D-loop region of shrews. Mol Biol Evol 11:9–21

    CAS  PubMed  Google Scholar 

  • Szteren D (2006) Regionalización ecológica de las colonias reproductivas de Zalophus c. californianus en el Golfo de California, México. PhD thesis, CICIMAR-IPN, La Paz, BCS México

  • Szteren D, Aurioles D, Gerber LR (2006) Population status and trends of the California sea lion (Zalophus californianus californianus) in the Gulf of California, México. In: Trites AW, Atkinson SK, DeMaster DP, Fritz LW, Gelatt TS, Rea LD, Wynne KM (eds) Sea Lions of the World. Alaska Sea Grant College Program, Lowell Wakefield Fisheries Symposium Series, Rhode Island, pp 369–384

  • Trillmich F, Dellinger T (1991) The effects of El Niño on Galapagos Pinnipeds. In: Trillmich F, Ono KA (eds) Pinnipeds and El Niño: Responses to environmental stress. Ecological Studies 88. Springer, New York, pp 66–74

    Chapter  Google Scholar 

  • Trillmich F, Limberger D (1985) Drastic effects of El Niño on Galapagos pinnipeds. Oecologia 67:19–22. doi:https://doi.org/10.1007/BF00378445

    Article  PubMed  Google Scholar 

  • Villegas-Amtmann S, Costa DP, Tremblay Y, Salazar S, Aurioles-Gamboa D (2008) Multiple foraging strategies in a marine apex predator, the Galapagos sea lion Zalophus wollebaeki. Mar Ecol Prog Ser 363:209–299. doi:https://doi.org/10.3354/meps07457

    Article  Google Scholar 

  • Walker PL, Craig S (1979) Archaeological evidence concerning the prehistoric occurrence of sea mammals at Point Bennet, San Miguel Island. Calif Fish Game 65:50–54

    Google Scholar 

  • Walker PL, Kennett DJ, Jones TL, DeLong R (1999) Archaeological investigations at the Point Bennett pinniped rookery on San Miguel Island. In: Brown DR, Mitchell KC, Chaney HW (eds) Proceedings of the fifth California Islands symposium. US Department of the Interior Minerals Management Service, Pacific OCS Region, pp 628-632

  • Weber DS, Stewart BS, Lehman N (2004) Genetic consequences of a severe population bottleneck in the Guadalupe fur seal (Arctocephalus townsendi). J Hered 95:144–153. doi:https://doi.org/10.1093/jhered/esh018

    Article  CAS  PubMed  Google Scholar 

  • Werner R, Hoernle K, van den Bogaard P, Ranero C, von Huene R, Korich D (1999) Drowned 14-m.y.-old Galápagos Archipelago off the coast of Costa Rica: Implications for tectonic and evolutionary models. Geology 27:499–502. doi:0.1130/0091-7613(1999)027<0499:DMYOGP>2.3.CO;2

    Article  CAS  Google Scholar 

  • Wolf JBW, Tautz D, Trillmich F (2007) Galápagos and California sea lions are separate species: genetic analysis of the genus Zalophus and its implications for conservation management. Front Zool 4:20. doi:https://doi.org/10.1186/1742-9994-4-20

    Article  PubMed  PubMed Central  Google Scholar 

  • Wolf JBW, Harrod C, Brunner S, Salazar S, Trillmich F, Tautz D (2008) Tracing early stages of species differentiation: ecological, morphological and genetic divergence of Galápagos sea lion populations. BMC Evol Biol 8:150. doi:https://doi.org/10.1186/1471-2148-8-150

    Article  PubMed  PubMed Central  Google Scholar 

  • Wynen LP, Goldsworthy SD, Insley SJ, Adams M, Bickham JW, Francis J, Gallo-Reynoso JP, Hoelzel AR, Majluf P, White RWG, Slade R (2001) Phylogenetic relationships within the eared seals (Otariidae: Carnivora): Implications for the historical biogeography of the Family. Mol Phylogenet Evol 21:270–284. doi:https://doi.org/10.1006/mpev.2001.1012

    Article  CAS  PubMed  Google Scholar 

  • Zavala-González A, Mellink E (2000) Historical exploitation of the California sea lion, Zalophus californianus, in México. Mar Fish Rev 62:35–40

    Google Scholar 

  • Zavaleta-Lizárraga L (2003) Variaciones geográficas en morfometría craneal en machos adultos de lobo marino de California (Zalophus californianus) en México. MSc thesis, CICIMAR-IPN, México

Download references

Acknowledgments

Tissue samples were collected in México under permit No. DOO750.8106-97 from the Instituto Nacional de Ecología; in California under permit No. 1026 from the US Department of Commerce; and in Galápagos, Ecuador, under permit No. PC-009-99 from the Galápagos National Park (and permit No. 017-00 for sample export). Additional sea lion samples from San Miguel Island were kindly provided by S. Melin (US National Marine Fisheries Service) and from Galápagos by S.K. Salazar (Charles Darwin Research Station). Work in México was facilitated by A. Zavala and O. Maravilla and carried out on Mexican Navy ships. G. Heckel, L. Inclán and M.L. Anoge participated during the cruise. We acknowledge the invaluable logistical support provided by the Charles Darwin Research Station in Galápagos (through P. Robayo). Thanks to the welcome provided by A. Dizon and staff at the SWFSC Marine Mammal Genetics Laboratory and to C. Le Duc, K. Robertson and J. Hyde for their assistance in the lab. Y.S. had grants from the Mexican National Science Foundation (CONACyT), Alstom Power (Rosarito, México), and the Universidad Autónoma de Baja California. D.M.P. was supported by award No. N00014-05-1-0045 from the US Office of Naval Research, National Oceanographic Partnership Program. Supplemental funding for Galápagos sample export was provided by the Protected Resources Division of the SWFSC (through R.L. Brownell Jr.). Earlier drafts of the manuscript benefited from comments by G. Heckel. We thank to two anonymous reviewers for their valuable suggestions and comments. The experiments comply with the current laws of the USA, México and Ecuador.

Author information

Author notes

  1. H. M. Snell

    Present address: Museum of Southwestern Biology, Department of Biology, University of New México, Albuquerque, NM, 87131, USA

Authors and Affiliations

  1. Facultad de Ciencias Marinas, Universidad Autónoma de Baja California, Km 103 Carretera Tijuana-Ensenada s/n, 22830, Ensenada, Baja California, Mexico

    Yolanda Schramm & J. de la Rosa

  2. Protected Resources Division, Southwest Fisheries Science Center, NOAA Fisheries, 8604 La Jolla Shores Drive, La Jolla, CA, 92037, USA

    S. L. Mesnick & M. S. Lowry

  3. Joint Institute for Marine and Atmospheric Research, University of Hawaii, 1000 Pope Road, Marine Sciences Building, Room 312, Honolulu, HI, 96822, USA

    D. M. Palacios

  4. Environmental Research Division, Southwest Fisheries Science Center, NOAA Fisheries, 1352 Lighthouse Avenue, Pacific Grove, CA, 93950-2097, USA

    D. M. Palacios

  5. Centro Interdisciplinario de Ciencias Marinas, Instituto Politécnico Nacional. Ave. IPN s/n, Colonia Playa Palo de Santa Rita, 23000, La Paz, Baja California Sur, Mexico

    D. Aurioles-Gamboa

  6. Charles Darwin Research Station, Charles Darwin Foundation, Puerto Ayora, Isla Santa Cruz, Galápagos, Ecuador

    H. M. Snell

  7. Department of Biological Sciences, California State University Los Angeles, Los Angeles, CA, 90032-8201, USA

    S. Escorza-Treviño

Authors
  1. Yolanda Schramm
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. S. L. Mesnick
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. J. de la Rosa
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. D. M. Palacios
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. M. S. Lowry
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. D. Aurioles-Gamboa
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. H. M. Snell
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. S. Escorza-Treviño
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Yolanda Schramm.

Additional information

Communicated by M.I. Taylor.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Schramm, Y., Mesnick, S.L., de la Rosa, J. et al. Phylogeography of California and Galápagos sea lions and population structure within the California sea lion. Mar Biol 156, 1375–1387 (2009). https://doi.org/10.1007/s00227-009-1178-1

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00227-009-1178-1

Keywords

Search

Navigation