Advertisement

Conservation Genetics

, Volume 16, Issue 5, pp 1099–1113 | Cite as

Fine-scale matrilineal population structure in the Galapagos fur seal and its implications for conservation management

  • Fernando Lopes
  • Joseph Ivan Hoffman
  • Victor Hugo Valiati
  • Sandro L. Bonatto
  • Jochen B. W. Wolf
  • Fritz Trillmich
  • Larissa R. Oliveira
Research Article

Abstract

Females of many pinniped species generally exhibit strong fine-scale philopatry, but it is unclear over what spatial scale this behavior may translate into genetic population structure. We conducted a population genetic survey in the Galapagos fur seal, Arctocephalus galapagoensis, an endangered pinniped endemic to a small geographic range in the northwest of the Galapagos archipelago. To assess patterns of genetic diversity levels and population differentiation, we analyzed part of the mitochondrial control region (mtDNA) and 18 microsatellites DNA markers. We detected similar levels of genetic diversity to many other pinniped species (h = 0.86, π = 0.012, A = 7.44) despite severe anthropogenic exploitation in the nineteenth century and recurrent population crashes due to recent climatic perturbations associated with El Niño Southern Oscillation events. We further found remarkably strong fine-scale matrilineal population structure, with 33.9 % of the mtDNA variation being partitioned among colonies separated by as little as 70 km swimming distance. In contrast, population structure inferred from nuclear markers was weak. Our findings provide further evidence that natal philopatry can translate into fine-scale genetic population structure in highly mobile species. We discuss the relevance of our results for the fine-scale conservation management of this species with a very restricted geographic range.

Keywords

Arctocephalus galapagoensis Philopatry Genetic diversity Galapagos Islands Pinnipeds 

Notes

Acknowledgments

We would like to thank the Servicio Parque Nacional Galápagos (SPNG) for the research permit and the Charles Darwin Research Station (CDRS) for the logistic support during the fieldwork. The authors are indebted to K. Acevedo-Whitehouse, M. Cruz and S. Salazar for their help with tissue sampling; to the members of Laboratory of Mammal Ecology (UNISINOS) and Center for Genomics and Molecular Biology (PUCRS), especially to Lúcia Darsie Fraga and Ana Lúcia Cypriano, for their laboratory and analytical help and to Dr. Steve Kirkman, who kindly revised the final version of the manuscript. This study was financially supported by The VW-Foundation and National Geographic 7671-04 to Fritz Trillmich and CNPq 479199/2010-8 to Larissa Rosa de Oliveira. Fernando Lopes was Granted by CNPq (process n° GM 130945/2013-7, 144580/2012-8 and 148039/2011-1). This publication is Contribution Number 2108 of the Charles Darwin Foundation for the Galapagos Islands.

Supplementary material

10592_2015_725_MOESM1_ESM.xlsx (26 kb)
Supplementary material 1 (DOCX 27 kb)

References

  1. Acevedo-Whitehouse K, Petetti L, Duignan P, Castinel A (2009) Hookworm infection, anaemia and genetic variability of the New Zealand sea lion. Proc Biol Sci 276:3523–3529Google Scholar
  2. Akçakaya HR, Mills G, Doncaster CP (2007) The role of metapopulations in conservation. In: Macdonald DW, Service K (eds) Key topics in conservation biology. Blackwell Publishing, Oxford, pp 64–84Google Scholar
  3. Alava JJ, Salazar S (2006) Status and conservation of Otariids in Ecuador and the Galápagos Islands. In: Trites AW, Atkinson SK, DeMaster DP, Fritz LW, Gelatt TS, Rea LD, Wynne KM (org) Sea Lions of the world—22nd Lowell Wakefield fisheries symposium. Alaska Sea Grant College Program, Anchorage, pp 495–519Google Scholar
  4. Allen PJ, Amos W, Pomery PP, Twiss SD (1995) Microsatellite variation in grey seals (Halichoerus grypus) shows evidence of genetic differentiation between two British breeding colonies. Mol Ecol 4:653–662PubMedCrossRefGoogle Scholar
  5. Andersen L, Born E, Gjertz I, Wiig O, Holm LE, Bendixen C (1998) Population structure and gene flow of the Atlantic walrus (Odobenus rosmarus rosmarus) in the eastern Atlantic Arctic based on mitochondrial DNA and microsatellite variation. Mol Ecol 7:1323–1336PubMedCrossRefGoogle Scholar
  6. Aurioles-Gamboa D, Schramm Y, Mesnick S (2004) Galapagos fur seals, Arctocephalus galapagoensis, in Mexico. LAJAM 3:77–80CrossRefGoogle Scholar
  7. Avise JC (1989) A role for molecular geneticists in the recognition and conservation of endangered species. Trends Ecol Evol 4:279–281PubMedCrossRefGoogle Scholar
  8. Bandelt HJ, Forster P, Rohl A (1999) Median-joining networks for inferring intraspecific phylogenies. Mol Biol Evol 16:37–48PubMedCrossRefGoogle Scholar
  9. Bartholomew GA (1970) A model for the evolution of pinniped polygyny. Evolution 24:546–559CrossRefGoogle Scholar
  10. Bastida R, Rodríguez D, Secchi E, Da Silva V (2007) Mamíferos Acuáticos de Sudamérica y Antártica, 2nd edn. Vázquez Manzini Editores, Buenos AiresGoogle Scholar
  11. Boness DJ (1991) Determinants of mating systems in the Otariidae (Pinnipedia). In: Renouf D (ed) The behaviour of pinnipeds. Chapman and Hall, London, pp 1–44CrossRefGoogle Scholar
  12. Bottin L, Tassin J, Nasi R, Bouvet J (2007) Molecular, quantitative and abiotic variables for the delineation of evolutionary significant units: case of sandalwood (Santalum austrocaledonicum Vieillard) in New Caledonia. Conserv Genet 8:99–109CrossRefGoogle Scholar
  13. Campagna C, Le Boeuf BJ, Capozzo HL (1988) Group raids: a mating strategy of male southern sea lions. Behaviour 105:224–249CrossRefGoogle Scholar
  14. Campbell R (2003) Demography and population genetic structure of the Australian sea lion, Neophoca cinerea. Thesis, University of Western AustraliaGoogle Scholar
  15. Campbell RA, Gales NJ, Lento GM, Baker CS (2008) Islands in the sea: extreme female natal site fidelity in the Australian sea lion, Neophoca cinerea. Biol Lett 4:139–142PubMedCentralPubMedCrossRefGoogle Scholar
  16. Capella JJ, Florez-Gonzáles L, Falk-Fernández P, Palácios DM (2002) Regular appearance of otariid pinnipeds along the Colombian Pacific coast. Aquat Mamm 28:67–72Google Scholar
  17. Chan C, Ballantyne KN, Aikman H, Fastier D, Daugherty CH, Chambers GK (2006) Genetic analysis of interspecific hybridisation in the world’s only Forbes’ parakeet (Cyanoramphus forbesi) natural population. Conserv Genet 7:493–506CrossRefGoogle Scholar
  18. CITES: Convention on International Trade in Endangered Species of Wild of Fauna and Flora (2013). http://www.cites.org. Accessed 1 Sep 2014
  19. Coltman DW, Bowen WD, Wright JM (1996) PCR primers for harbour seal (Phoca vitulina concolour) microsatellites amplify polymorphic loci in other species. Mol Ecol 5:161–163PubMedCrossRefGoogle Scholar
  20. Corl A, Ellegren H (2012) The genomic signature of sexual selection in the genetic diversity of the sex chromosomes and autosomes. Evolution 66:2138–2149PubMedCrossRefGoogle Scholar
  21. Cornuet JM, Luikart G (1996) Description and power analysis of two tests for detecting recent population bottlenecks from allele frequency data. Genetics 144:2001–2014PubMedCentralPubMedGoogle Scholar
  22. Dasmahapatra KK, Hoffman JI, Amos W (2009) Pinniped phylogenetic relationships inferred using AFLP markers. Heredity 103:168–177. doi: 10.1038/hdy.2009.25 PubMedCrossRefGoogle Scholar
  23. Davis CS, Stirling I, Strobeck C, Coltman DW (2008) Population structure of ice-breeding seals. Mol Ecol 17:3078–3094PubMedCrossRefGoogle Scholar
  24. De Vries TJ (1987) A review of geological evidence for ancient El Niño activity in Peru. J Geophys Res 92:14471–14479CrossRefGoogle Scholar
  25. Dekinger J, Salazar S (2010) Possible effects of climate change in the populations of Galápagos pinnipeds. Not Galápagos 67:45–49Google Scholar
  26. Di Rienzo A, Peterson AC, Garza JC, Valdes AM, Slatkin M, Freimer NB (1994) Mutational processes of simple-sequence repeat loci in human populations. Proc Natl Acad Sci USA 1:3166–3170CrossRefGoogle Scholar
  27. Dickerson BR, Ream RR, Vignieri SN, Bentzen P (2010) Population structure as revealed by mtDNA and microsatellites in Northern fur seals, Callorhinus ursinus, throughout their range. PLoS ONE 5(1–9):e10671. doi: 10.1371/journal.pone.0010671 PubMedCentralPubMedCrossRefGoogle Scholar
  28. Drummond A, Suchard MA, Xie D, Rambaut A (2012) Bayesian phylogenetics with BEAUti and the BEAST 1.7. Mol Biol Evol 29:1969–1973PubMedCentralPubMedCrossRefGoogle Scholar
  29. 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 Res 10:564–567CrossRefGoogle Scholar
  30. Excoffier L, Laval G, Schneider S (2005) Arlequin (version 3.0): an integrated software package for population genetics data analysis. Evol Bioinform Online 1:47–50PubMedCentralGoogle Scholar
  31. Fabiani A, Hoelzel R, Galimberti F, Muelbert MMC (2003) Long-range paternal gene flow in the Southern elephant seal. Science 229:676. doi: 10.1126/science.299.5607.676 CrossRefGoogle Scholar
  32. Félix F, Lento G, Davis J, Chiluizal D (2001) El lobo fino de Galápagos Arctocephalus galapagoensis (Pinnipedia, Otariidae) en la costa continental de Ecuador, primeros registros confirmados mediante análises morfológicos y genéticos. Estud Oceanol 20:61–66Google Scholar
  33. Fietz K, Graves JA, Olsen MT (2013) Control control control: a reassessment and comparison of GenBank and chromatogram mtDNA sequence variation in Baltic grey seals (Halichoerus grypus). PLoS ONE 8(1–7):e72853PubMedCentralPubMedCrossRefGoogle Scholar
  34. Forcada J, Hoffman JI (2014) Climate change selects for heterozygosity in a declining fur seal population. Nature 511:462–465PubMedCrossRefGoogle Scholar
  35. Frankham R, Balou JD, Briscoe DA (2002) Introduction to conservation genetics. Cambridge University Press, CambridgeCrossRefGoogle Scholar
  36. Fu YX (1997) Statistical Tests of neutrality of mutations against population growth, hitchhiking and background selection. Genetics 147:915–925PubMedCentralPubMedGoogle Scholar
  37. Garza JC, Williamson EG (2001) Detection of reduction in population size using data from microsatellite loci. Mol Ecol 10:305–318PubMedCrossRefGoogle Scholar
  38. Gemmell NJ, Allen PJ, Goodman SJ, Reed JZ (1997) Interspecific microsatellite markers for the study of pinniped populations. Mol Ecol 6:661–666PubMedCrossRefGoogle Scholar
  39. Goldsworthy SD, Page BC (2007) A risk-assessment approach to evaluating the significance of seal bycatch in two Australian fisheries. Biol Conserv 139:269–285CrossRefGoogle Scholar
  40. Goldsworthy S, Francis J, Boness D, Fleischer R (2000) Variation in the mitochondrial control region in the Juan Fernnandez fur seal. J Hered 91:371–377PubMedCrossRefGoogle Scholar
  41. Grant WS, Bowen BW (1998) Shallow population histories in deep evolutionary lineages of marine fishes: insights from sardines and anchovies and lessons for conservation. J Hered 89:415–426CrossRefGoogle Scholar
  42. Greenwood PJ (1980) Mating Systems, philopatry and dispersal in birds and mammals. Anim Behav 28:1140–1162CrossRefGoogle Scholar
  43. Hedrick PW, Lee RN, Hurt CR (2006) The endangered Sonoran top minnow: examination of species and ESUs using three mtDNA genes. Conserv Genet 7:483–492CrossRefGoogle Scholar
  44. Hernández-Velazquez FD, Galindo-Sanchez E, Taylor MI, De la Rosa-Velez J, Cote IM, Schramm Y, Aurioles-Gamboa D, Rico C (2005) New polymorphic microsatellite markers for California sea lions (Zalophus californianus). Mol Ecol Notes 5:140–142CrossRefGoogle Scholar
  45. Hoban SM, Gaggiotti OE, Bertorelle G (2013) The number of markers and samples needed for detecting bottlenecks under realistic scenarios, with and without recovery: a simulation-based study. Mol Ecol 22:3444–3450PubMedCrossRefGoogle Scholar
  46. Hoelzel AR, Halley J, O’Brien SJ, Campagna C, Arnborn T, Le Boeuf B, Ralls K, Dover GA (1993) Elephant seal genetic variation and the use of simulation models to investigate historical population bottlenecks. J Hered 84:443–449PubMedGoogle Scholar
  47. Hoelzel RA, Le Boeuf BJ, Reiter J, Campagna C (1999) Alpha-male paternity in elephant seals. Behav Ecol Sociobiol 46:298–306CrossRefGoogle Scholar
  48. Hoffman IJ (2009) A panel of new microsatellite loci for genetic studies of Antarctic fur seals and other otariids. Conserv Genet 10:989–992CrossRefGoogle Scholar
  49. Hoffman JI, Amos W (2005) Microsatellite genotyping errors: detection approaches, common sources and consequences for paternal exclusion. Mol Ecol 14:599–612Google Scholar
  50. Hoffman JI, Forcada J (2012) Extreme natal philopatry in female Antarctic fur seals (Arctocephalus gazella). Mamm Biol 77:71–73. doi: 10.1016/j.mambio.2011.09.002 Google Scholar
  51. Hoffman JI, Trathan PN, Amos W (2006a) Genetic tagging reveals extreme site fidelity in territorial male Antarctic fur seals Arctocephalus gazella. Mol Ecol 15:3841–3847. doi: 10.1111/j.1365-294X.2006.03053.x PubMedCrossRefGoogle Scholar
  52. Hoffman JI, Matson C, Amos W, Loughlin TR, Bickham JW (2006b) Deep genetic subdivision within a continuously distributed and highly vagile marine mammal, the Steller’s sea lion Eumetopias jubatus. Mol Ecol 15:2821–2832PubMedCrossRefGoogle Scholar
  53. Hoffman IJ, Steinfartz S, Wolf JBW (2007) Ten novel dinucleotide microsatellite loci cloned from the Galápagos sea lion (Zalophus californianus wollebaeki) are polymorphic in other pinniped species. Mol Ecol Notes 7:103–105CrossRefGoogle Scholar
  54. Hoffman JI, Dasmahapatra KK, Amos W, Phillips CD, Gelatti TS, Bickham JW (2009) Contrasting patterns of genetic diversity at three different genetic markers in a marine mammal metapopulation. Mol Ecol 18:2961–2978Google Scholar
  55. Hoffman JI, Grant SM, Forcada J, Phillips CD (2011) Bayesian inference of a historical genetic bottleneck in a heavily exploited marine mammal. Mol Ecol 20:3989–4008. doi: 10.1111/j.1365-294X.2011.05248 PubMedCrossRefGoogle Scholar
  56. Hulesenbeck JP, Andolfatto P (2007) Inference of population structure under a Dirichlet process model. Genetics 175:1787–1802CrossRefGoogle Scholar
  57. IUCN (2014) IUCN red list of threatened species. http://www.iucnredlist.org/apps/redlist/details/2057/0. Accessed 1 Oct 2014
  58. Jeglinski J, Goetz KT, Werner C, Costa DP, Trillmich F (2013) Same size–same niche? Foraging niche separation between sympatric juvenile Galapagos sea lions and adult Galapagos fur seals. J Anim Ecol 82:694–706. doi: 10.1111/1365-2656.12019 PubMedCrossRefGoogle Scholar
  59. Kimura M, Crow JF (1964) The number of alleles that can be maintained in a finite population. Genetics 49:725–738PubMedCentralPubMedGoogle Scholar
  60. Klimova A, Fietz K, Olsen MT, Harwood J, Amos W, Hoffman JI (2014) Global population structure and demographic history of the grey seal. Mol Ecol 23:3999–4017PubMedCrossRefGoogle Scholar
  61. Kocher TD, Thomas WK, Meyer A, Edwards SV, Pääbo S, Villablanca FX, Wilson AC (1989) Dynamics of mitochondrial DNA evolution in animals: amplification and sequencing with conserved primers. Proc Natl Acad Sci USA 86:6196–6200PubMedCentralPubMedCrossRefGoogle Scholar
  62. Lancaster ML, Arnould JPY, Kirkwood (2010) Genetic status of an endemic marine mammal, the Australian fur seal, following historical harvesting. Anim Conserv 13:247–255Google Scholar
  63. Librado P, Rozas J (2009) DnaSP v5: a software for comprehensive analysis of DNA polymorphism data. Bioinformatics 25:1451–1452PubMedCrossRefGoogle Scholar
  64. Luikart G, Cornuet JM (1998) Empirical evaluation of a test for identifying recently bottlenecked populations from allele frequency data. Conserv Biol 12:228–237CrossRefGoogle Scholar
  65. Lynch M, Ritland K (1999) Estimation pairwise relatedness with molecular markers. Genetics 152:1753–1766PubMedCentralPubMedGoogle Scholar
  66. Majluf P (1987) Reproductive ecology of female South American fur seals at Punta San Juan. PhD Thesis, University of CambridgeGoogle Scholar
  67. Majluf P, Goebel ME (1992) The capture and handling of female South American fur seals and their pups. Mar Mamm Sci 8:187–190CrossRefGoogle Scholar
  68. Maldonado JE, Davila FO, Stewart BS, Geffen E (1995) Intraspecific genetic differentiation in California sea lions (Zalophus californianus) from southern California and the Gulf of California. Mar Mamm Sci 11:46–58CrossRefGoogle Scholar
  69. Mathee CA, Fourie F, Oosthuizen WH, Meyër MA, Tolley KA (2006) Mitochondrial DNA sequence data of the Cape fur seal (Arctocephalus pusillus pusillus) suggest that population numbers may be affected by climatic shifts. Mar Biol 148:899–905CrossRefGoogle Scholar
  70. Matthiopoulos J, Harwood J, Thomas L (2005) Metapopulation consequences of site fidelity for colonially breeding mammals and birds. J Anim Ecol 74:716–727CrossRefGoogle Scholar
  71. McCarthy MA, Menkhorst PW, Quin BR, Smales IJ, Burgman MA (2004) Helmeted Honeyeater (Lichenostomus melanops cassidix) in Southern Australia: assessing options for establishing a new wild population. In: Akçakaya HR, Burgman MA, Kindvall O, Wood CC, Sjögren-Gulve P, Hatfield JS, McCarthy MA (eds) Species conservation and management: case studies. Oxford University Press, Oxford, pp 410–420Google Scholar
  72. Montero-Cordero A, Fernández DM, Hernández-Mora G (2010) Mammalia, Carnivora, Otariidae, Arctocephalus galapagoensis Heller, 1904: first continental record for Costa Rica. Checkl J 6:630–632Google Scholar
  73. Moritz C (1994) Defining “Evolutionarily Significant Units” for conservation. Trends Ecol Evol 9:373–375PubMedCrossRefGoogle Scholar
  74. Oliveira LR (2011) Vulnerability of South American pinnipeds under El Niño Southern Oscillation events: 14:237–252. In: Casalengo S (ed) Global warming impacts—case studies on the economy, human health, and on urban and natural environments. InTech, pp 1–17. doi: 10.5772/25204
  75. Oliveira LR, Arias-Schreiber M, Meyer D, Morgante JS (2006) Effective population size in a bottlenecked fur seal population. Biol Conserv 131:505–509CrossRefGoogle Scholar
  76. Oliveira LR, Hoffman JI, Hingst-Zaher E, Majluf P, Muelbert MMC, Morgante JS, Amos Q (2008) Morphological and genetic evidence for two evolutionarily significant units (ESUs) in the South American fur seal, Arctocephalus australis. Conserv Genet 9:1451–1466Google Scholar
  77. Oliveira LR, Meyer D, Hoffman JI, Majluf P, Morgante JS (2009) Evidence of a genetic bottleneck in an El Niño affected population of South American fur seals, Arctocephalus australis. J Mar Biol Assoc UK 89:1717–1725. doi: 10.1017/S0025315409000162 CrossRefGoogle Scholar
  78. Otha T, Kimura M (1973) A model of mutation appropriate to estimate the number of electrophoretically detectable alleles in a finite population. Genet Res 22:201–204CrossRefGoogle Scholar
  79. Peakall R, Smouse PE (2006) GENALEX 6: genetic analysis in Excel. Population genetic software for teaching and research. Mol Ecol Notes 6:288–295CrossRefGoogle Scholar
  80. Peakall R, Smouse PE (2012) GenAlEx 6.5: genetic analysis in Excel. Population genetic software for teaching and research—an update. Bioinformatics 28:2537–2539PubMedCentralPubMedCrossRefGoogle Scholar
  81. Pella J, Masuda M (2006) The Gibbs and split-merge sampler for population mixture analysis from genetic data with incomplete baselines. Can J Fish Aquat Sci 63:576–596CrossRefGoogle Scholar
  82. Perrin N, Mazalov V (2000) Local Competition, inbreeding, and the evolution of sex-biased dispersal. Am Nat 155:116–127PubMedCrossRefGoogle Scholar
  83. Philander SFH (1983) El Niño Southern Oscillation phenomena. Nature 302:295–301CrossRefGoogle Scholar
  84. Pimm SL, Gittleman JL, MaCracken GF, Gilpin M (1989) Plausible alternatives to bottlenecks to explain reduced genetic diversity. Trends Ecol Evol 4:176–178PubMedCrossRefGoogle Scholar
  85. Piry S, Luikart G, Cornuet JM (1999) BOTTLENECK: a computer program for detecting recent reductions in the effective population size using allele frequency data. J Hered 90:502–503CrossRefGoogle Scholar
  86. Pomeroy P, Twiss S, Redman P (2000) Philopatry, site fidelity and local kin associations within grey seal breeding colonies. Ethology 106:899–919. doi: 10.1046/j.1439-0310.2000.00610.x CrossRefGoogle Scholar
  87. Pritchard JK, Stephens M, Donnely PJ (2000) Inference of population structure using multilocus genotype data. Genetics 155:945–959PubMedCentralPubMedGoogle Scholar
  88. Rice WR (1989) Analyzing tables of statistical tests. Evolution 43:223–225CrossRefGoogle Scholar
  89. Robalo JI, Doadrio I, Valente A, Almada VC (2007) Identification of ESUs in the critically endangered Portuguese minnow Chondrostoma lusitanicum Collares-Pereira 1980, based on a phylogeographical analysis. Conserv Genet 8:1225–1229CrossRefGoogle Scholar
  90. Robertson BC, Chilvers BL (2011) The population decline of the New Zealand sea lion Phocarctos hookeri: a review of possible causes. Mamm Rev 41:253–275Google Scholar
  91. Rozas J, Sánchez-DelBarrio JC, Messeguer X, Rozas R (2003) DnaSP, DNA polymorphisms analyses by the coalescent and other methods. Bioinformatics 19:2496–2497PubMedCrossRefGoogle Scholar
  92. Ryder OA (1986) Species Conservation and systematics: the dilemma of subspecies. Trends Ecol Evol 1:9–10CrossRefGoogle Scholar
  93. Sambrook J, Fritsch EF, Maniatis T (1989) Molecular cloning: a laboratory manual. Cold Spring Harbor Laboratory, New YorkGoogle Scholar
  94. Sandweiss DH, Richardson JB III, Reitz EJ, Rollins HB, Maasch KA (1996) Geoarchaeological evidence from Peru for a 5000 years BC onset of El Niño. Science 273:1531–1533CrossRefGoogle Scholar
  95. Seal Conservation Society (2010) Galapagos Fur Seal. http://www.pinnipeds.org/species/galfursl.htm. Accessed 30 Sep 2010
  96. Shafer AB, Gattepaille LM, Stewart RE, Wolf JB (2015) Demographic inferences using short-read genomic data in an approximate Bayesian computation framework: in silico evaluation of power, biases and proof of concept in Atlantic walrus. Mol Ecol 24:328–345Google Scholar
  97. Shields WM (1982) Philopatry, inbreeding and the evolution of sex. State University of New York Press, New YorkGoogle Scholar
  98. Slade RW, Moritz C, Heidman A (1994) Multiple nuclear-gene phylogenies: application to pinnipeds and comparison with a mitochondrial DNA gene phylogeny. Mol Biol Evol 11:341–356PubMedGoogle Scholar
  99. Stanley H, Casey S, Carnahan J, Goodman S, Harwood J, Wayne RK (1996) Worldwide patterns of mitochondrial DNA differentiation in the harbor seal (Phoca vitulina). Mol Biol Evol 13:368–382PubMedCrossRefGoogle Scholar
  100. Swofford DL (2002) PAUP*. Phylogenetic analysis using parsimony (*and other methods). Version 4. Sinauer Associates, SunderlandGoogle Scholar
  101. Tajima F (1989) Statistical method for testing the neutral mutation hypothesis by DNA polymorphism. Genetics 123:585–595PubMedCentralPubMedGoogle Scholar
  102. Tajima F (1993) Simple methods for testing molecular clock hypothesis. Genetics 135:599–607PubMedCentralPubMedGoogle Scholar
  103. Thompson J, Gibson TJ, Plewniak F, Jeanmouguin F, Higgins DG (1997) The ClustalX windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res 24:4876–4882CrossRefGoogle Scholar
  104. Trillmich F (1987) Galápagos fur seal: Arctocephalus galapagoensis. In: Croxal PL, Gentry RL (eds) Status, biology and ecology of fur seals. Proceedings of an international symposium and workshop, Cambridge, pp 23–27Google Scholar
  105. Trillmich F (1990) The behavioral ecology of maternal effort in fur seals and sea lions. Behaviour 114:1–20CrossRefGoogle Scholar
  106. Trillmich F, Dellinger T (1991) The effects of El Niño on Galápagos pinnipeds. In: Trillmich F, Ono KA (eds) Pinnipeds and El Niño: responses to environmental stress. Springer, Berlin, pp 66–74CrossRefGoogle Scholar
  107. Trillmich F, Kooyman GL (2001) Field metabolic rate of lactating female Galápagos fur seal (Arctocephalus galapagoensis): the influence of offspring age and environment. Comp Biochem Physiol 129:741–749CrossRefGoogle Scholar
  108. Trillmich F, Limberger D (1985) Drastic effects of El Niño on Galapagos pinnipeds. Oecologia 67:19–22CrossRefGoogle Scholar
  109. Trillmich F, Trillmich KGK (1984) The mating systems of pinnipeds and marine iguanas: convergent evolution of polygyny. Biol J Linn Soc 21:209–216CrossRefGoogle Scholar
  110. Trillmich F, Wolf JBW (2008) Parent–offspring and sibling conflict in the Galápagos fur seals and sea lions. Behav Ecol Sociobiol 62:363–375CrossRefGoogle Scholar
  111. Weber DS, Stewart BS, Garza JC, Lehman N (2000) An empirical genetic assessment of the severity of the northern elephant seal population bottleneck. Curr Biol 10:1287–1290PubMedCrossRefGoogle Scholar
  112. Weber DS, Stewart BS, Lehman N (2004) Genetic consequences of a severe population bottleneck in the Guadalupe fur seal (Arctocephalus townsendi). J Hered 95:144–153PubMedCrossRefGoogle Scholar
  113. Weir BS, Cockerham CC (1984) Estimating F-statistics for the analysis of population structure. Evolution 38:1358–1370CrossRefGoogle Scholar
  114. Wolf JBW, Trillmich F (2007) Beyond habitat requirements: individual fine-scale site fidelity in a colony of the Galapagos sea lion (Zalophus wollebaeki) creates conditions for social structuring. Oecologia 152:553–567PubMedCrossRefGoogle Scholar
  115. Wolf JBW, Trillmich F (2008) Kin in space. Social viscosity in a spatially and genetically sub-structured network. Proc R Soc Lond B 275:2063–2069CrossRefGoogle Scholar
  116. Wolf JBW, Tautz D, Caccone A, Steinfartz S (2006) Development of new microsatellite loci and evaluation of loci from other pinnipeds species for the Galápagos Sea Lion (Zalophus californianus wollebaeki). Conserv Genet 7:461–465CrossRefGoogle Scholar
  117. Wolf JBW, Tautz D, Trillmich F (2007) Galápagos and Californian sea lions are separate species: genetic analysis of the genus Zalophus and its implications for conservation management. Front Zool 4:20PubMedCentralPubMedCrossRefGoogle Scholar
  118. 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 8:1–14CrossRefGoogle Scholar
  119. Worthington-Wilmer J, Allen PJ, Pomeroy PP, Twiss SD, Amos W (1999) Where have all the fathers gone? An extensive microsatellite analysis of paternity in the grey seal (Halichoerus grypus). Mol Ecol 8:1417–1429Google Scholar
  120. Wynen LP, Goldsworthy SD, Insley SJ, Adams M, Bickham JW, Francis J, Gallo 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 21:270–284PubMedCrossRefGoogle Scholar
  121. Wyrtki K (1982) The Southern Oscillation, ocean–atmosphere interaction and El Niño. Mar Technol Soc J 16:3–10Google Scholar
  122. Yonezawa T, Kohno N, Hasegawa M (2009) The monophyletic origin of sea lion and fur seals (Carnivora; Otariidae) in the southern hemisphere. Gene 441:89–99PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media Dordrecht 2015

Authors and Affiliations

  • Fernando Lopes
    • 1
    • 2
  • Joseph Ivan Hoffman
    • 3
  • Victor Hugo Valiati
    • 1
  • Sandro L. Bonatto
    • 2
  • Jochen B. W. Wolf
    • 4
  • Fritz Trillmich
    • 3
  • Larissa R. Oliveira
    • 1
    • 5
  1. 1.Universidade do Vale do Rio dos Sinos (UNISINOS)São LeopoldoBrazil
  2. 2.Pontifícia Universidade Católica do Rio Grande do Sul - PUCRSPorto AlegreBrazil
  3. 3.University of BielefeldBielefeldGermany
  4. 4.Uppsala UniversityUppsalaSweden
  5. 5.Grupo de Estudos de Mamiferos Aquaticos do Rio Grande do Sul (GEMARS)ImbéBrazil

Personalised recommendations