Morphological and genetic evidence for two evolutionarily significant units (ESUs) in the South American fur seal, Arctocephalus gazella

Conservation Genetics

Volumn 9, Issue 6, 2008, Pages 1451-1466

  De Oliveira, Larissa Rosa ^a,b,c   Hoffman, Joseph I ^d   Hingst Zaher, Erika ^a   Majluf, Patricia ^e   Muelbert, Mônica M C ^f   Morgante, João Stenghel ^a   Amos, William ^d  

^a UNIVERSITY OF SÃO PAULO   (Brazil)

^b Grupo de Estudos de Mamiferos Aquaticos do Rio Grande do Sul   (Brazil)

^c FEDERAL UNIVERSITY OF RIO GRANDE DO SUL   (Brazil)

^d UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^e UNIVERSIDAD PERUANA CAYETANO HEREDIA   (Peru)

^f Programa de Pós Graduação Em Oceanografia Biológica   (Brazil)

Author keywords

Arctocephalus australis; Evolutionarily significant units (ESUs); Microsatellite; Skull morphometrics; South American fur seal

Indexed keywords

COMPARATIVE STUDY; EVOLUTION; GENETIC ANALYSIS; GEOGRAPHICAL VARIATION; MORPHOLOGY; MORPHOMETRY; PINNIPED; POLYMORPHISM; SHAPE; SIZE; SKULL;

ATLANTIC COAST [SOUTH AMERICA]; PACIFIC COAST [SOUTH AMERICA]; PERU; SOUTH AMERICA; URUGUAY;

ARCTOCEPHALUS AUSTRALIS; ARCTOCEPHALUS GAZELLA;

EID: 56149096453     PISSN: 15660621     EISSN: 15729737     Source Type: Journal    
DOI: 10.1007/s10592-007-9473-1     Document Type: Article

References (119)

1. PJ Allen W Amos PP Pomery SD Twiss 1995 Microsatellite variation in grey seals (Halichoerus grypus) shows evidence of genetic differentiation between two British breeding colonies Mol Ecol 4 653 662
2. Amos W, Hoelzel AR (1991) Long-term preservation of whale skin for DNA analysis, In: Hoelzel AR (ed) Genetic ecology of whales and dolphins. IWC, special issue 13, Cambridge, pp 99-103
3. Arias-Schreiber M, Rivas C (1998) Distribución, tamaño y estructura de las poblaciones de lobos marinos Arctocephalus australis y Otaria byronia en el litoral Peruano, en Noviembre 1996 y Marzo 1997. Informe Progresivo del Instituto del Mar del Perú 73:17-32. Callao, Peru
4. JC Avise 1989 A role for molecular geneticists in the recognition and conservation of endangered species TREE 4 279 281
5. JC Avise RM Ball Jr 1990 Principles of genealogical concordance in species concepts and biological taxonomy Oxford Surveys Evol Biol 7 45 67
6. L Bottin J Tassin R Nasi J Bouvet 2007 Molecular, quantitative and abiotic variables for the delineation of evolutionary significant units: case of sandalwood (Santalum austrocaledonicum Vieillard) in New Caledonia Cons Gen 8 99 109
7. FL Bookstein 1984 A statistical method for biological shape comparisons J Theor Biol 107 475 520
8. FL Bookstei 1989 Size and shape: a comment on semantics Syst Zool 38 173 180
9. Bookstein FL (1991) Morphometric tools for landmark data: geometry and biology. Cambridge University Press, New York
10. JFY Brookfield 1996 A simple new method for estimating null allele frequency from heterozygote deficiency Mol Ecol 5 453 455
11. Brunner S (2000) Cranial Morphometrics of fur seals and sea lions (Family: Otariidae) - systematics, geographic variation and growth. PhD thesis, University of Sydney
12. S Brunner 2004 Fur seals and sea lions (Otariidae): identification of species and taxonomic review Syst Biod 1 339 439
13. MA Cane 1983 Oceanographic events during El Niño Science 22 1189 1195
14. Cappozzo HL, Perez F, Batalles LM (1996) Reproductive behavior of South American fur seals in Uruguay. Paper presented at the International Symposium and workshop on Otariid reproductive strategies and conservation, Smithsonian Institution, Washington, 12-16 April 1996, p 37
15. CT Carvalho 1975 Ocorrência de mamíferos marinhos no Brasil Boletim Técnico do Instituto Florestal 16 13 32
16. C Chan KN Ballantyne H Aikman D Fastier CH Daugherty GK Chambers 2006 Genetic analysis of interspecific hybridisation in the world's only Forbes' parakeet (Cyanoramphus forbesi) natural population Cons Gen 7 4 493 506
17. DW Coltman WD Bowen JM Wright 1996 PCR primers for harbour seal (Phoca vitulina concolor) microsatellites amplify polymorphic loci in other species Mol Ecol 5 161 163
18. Cracraft J (1983) Species concepts and speciation analysis. In: Johnson RF (ed) Current ornithology. Plenum Press, New York, pp 159-187
19. KA Crandall ORP Bininda-Emonds GM Mace RK Wayne 2000 Considering evolutionary processes in conservation biology TREE 15 290 295
20. GA Daneri CM Garcia Esponda LJM De Santis 1997 A record of Arctocephalus australis (Zimmermann, 1783) (Carnivora, Otariidae) south of the Antarctic Convergence Mammalia 61 3 451 454
21. TA Demére A Berta JA Peter 2003 Pinnipedimorph evolutionary biogeography Bull Am Mus Nat His 279 32 76
22. CJ Drehmer J Ferigolo 1997 Osteologia cranianacomparada entre Arctocephalus australis e A. tropicalis (Pinnipedia, Otariidae). Iheringia Série Zoologia 83 137 149
23. S Ellner NG Hairston Jr 1994 Role of overlapping generations in maintaining genetic variation in a fluctuating environment The Am Nat 143 403 417
24. SE Encalada PH Lahanas KA Bjorndal AB Bolten MM Miyamoto BW Bowen 1996 Phylogeography and population structure of the green turtle (Chelonia mydas) in the Atlantic Ocean and Mediterranean Sea: a mitochondrial DNA control region sequence assessment Mol Ecol 5 473 484
25. A Fabiani AR Hoelzel F Galimberti MMC Muelbert 2003 Long-range paternal gene flow in the Southern Elephant Seal Science 299 676
26. DJ Fraser L Bernatchez 2001 Adaptive evolutionary conservation: towards a unified concept for defining conservation units Mol Ecol 10 2741 2752
27. OE Gaggiotti RD Vetter 1999 Effect of life history strategy, environmental variability, and overexploitation on the genetic Can J Fish Aquat Sci 56 1376 1388
28. Glantz MH (1996) Currents of change-El Niño's impact on climate and society. Cambridge University Press, Cambridge
29. SD Goldsworthy DJ Boness RC Fleischer 1999 Mate choice among sympatric fur seals: female preference for conphenotypic males Behav Ecol Sociobiol 45 253 267
30. SJ Goodman 1998 Patterns of extensive genetic differentiation and variation among European harbour seals (Phoca vitulina vitulina) revealed using microsatellite DNA polymorphisms Mol Biol Evol 15 104 118
31. Guerra CC, Torres DN (1987) Presence of South American fur seal, Arctcephalus australis, in northern Chile. In: Croxall JP, Gentry RL (eds) Status, biology and ecology of fur seals. Proceedings of an international symposium and workshop, United Kingdom, 23-27 April 1984, pp 169-176
32. SW Guo EA Thompson 1992 Performing the exact test for Hardy-Weimberg proportion for multiple alleles Biometrics 48 361 372
33. PW Hedrick RN Lee CR Hurt 2006 The endangered Sonoran topminnow: examination of species and ESUs using three mtDNA genes Cons Gen 7 4 483 492
34. E Hingst-Zaher LF Marcus R Cerqueira 2000 Application of geometric morphometrics to the study of postnatal size and shape changes in the skull of Callomys expulsus Hystrix 11 99 114
35. Y Hochberg 1988 A sharper Bonferroni procedure for multiple tests of sign Biometrika 75 800 802
36. AR Hoelzel BJ LeBouef C Campagna J Reiter 1999 Alpha male paternity in elephant seals Behav Ecol Sociobiol 46 298 306
37. AR Hoelzel C Campagna T Arnbom 2000 Genetic and morphometric differentiation between island and mainland southern elephant seal populations Proc Royal Soc Lond Ser B 268 325 332
38. JI Hoffman IL Boyd W Amos 2003 Male reproductive strategy and the importance of maternal status in the Antarctic fur seal Arctocephalus gazella Evolution 57 1917 1930
39. JI Hoffman W Amos 2005 Microsatellite genotyping errors: detection approaches, common sources and consequences for paternal exclusion Mol Ecol 14 599 612
40. JI Hoffman CW Matson W Amos TR Loughlin JW Bickham 2006 Deep genetic subdivision within a continuously distributed and highly vagile marine mammal, the Steller's sea lion (Eumetopias jubatus) Mol Ecol 15 2821 2832
41. SA Karl BW Bowen 1999 Evolutionary significant units versus geopolitical taxonomy: molecular systematics of an endangered species Cons Biol 13 990 999
42. Kerley GIH, Robinson TJ (1987) Skull morphometrics of male Antarctic and Subantarctic fur seals, Arctocephalus gazella and A. tropicalis, and their interspecific hybrids, In: Croxall JP, Gentry RL (eds) Status, biology and ecology of fur seals. Proceedings of an international symposium and workshop, Cambridge, United Kingdom, 23-27 April 1984, pp 121-131
43. JE King 1954 The otariid seals of the Pacific Coast of America Bull Brit Mus (Natural History) 2 309 337
44. ML Lancaster NJ Gemmell S Negro S Goldsworthy P Sunnucks 2006 Ménage à trois on Macquarie Island: hybridization among three species of fur seal (Arctocephalus spp.) following historical population extinction Mol Ecol 15 3681 3692
45. M Lima E Páez 1995 Growth and reproductive patterns in the South American fur seal J Mamm 76 1249 1255
46. D Limberger F Trillmich GL Kooyman P Majluf 1983 Reproductive failure of fur seals in Galapagos and Peru in 1982-1983 Tropical Ocean-Atmosphere Newsletter 21 16 17
47. Majluf P (1987) South American fur seal, Arctocephalus australis, in Peru. In: Croxall, JP, Gentry RL (eds) Status, biology and ecology of fur seals. Proceedings of an international symposium and workshop, Cambridge, United Kingdom, 23-27 April 1984, pp 23-27
48. Majluf P (1991) El Niño Effects on Pinnipeds in Peru. In: Trillmich F, Ono KA (eds) Pinniped and El Niño, Responses to Environmental stress. Springer-Verlag Press, pp 55-65
49. P Majluf 1992 Timing of births and juvenile mortality in the South American fur seal in Peru J Zool Lond 227 367 383
50. a Reunião de Trabalho de Especialistas em Mamíferos Aquáticos da América do Sul e 2° Congresso da Sociedade Latinoamericana de Especialistas em Mamíferos Aquáticos de América do Sul, Olinda, 25-29 October 1998, p 120
51. P Majluf F Trillmich 1981 Distribution and abundance of sea lions (Otaria byronia) and fur seal (Arctocephalus australis) in Peru Z.f.Säugetierkunde 46 384 393
52. P Majluf ME Goebel 1992 The capture and handling of female South American fur seals and their pups Mar Mamm Sci 8 187 190
53. Majluf P, Riveros JC, Parlane S (1996) Cool spots as "hot spots": The evolution of lekking in the South American fur seal. In: Croxall JP, Gentry RL (eds) International symposium and workshop on Otariid reproductive strategies and conservation, Washington, p 26
54. Majluf P, Boness D, Insley S, Paredes R (2000) Determinantes de la estructura del sistema social en el lobo fino sudamericano Arctocephalus australis - resultados de un experimento natural. Paper presented at the 9a Reunión de Trabajo de Especialistas en Mamíferos Acuáticos de América del Sur y 3° Congresso de la Sociedad Latinoamericana de Especialistas en Mamíferos Acuáticos de América del Sur, Buenos Aires, 30 October-03 November 2000, p 81
55. Marcus LF (1990) Traditional morphometrics. In: Rohlf FJ, Bookstein FL (eds) Proceedings of the Michigan morphometrics workshop. The University of Michigan, Michigan, pp 77-122
56. Marcus L, Bello E, García-Valdecasas A (1993) Contributions to morphometrics. Monografias del Museu Nacional de Ciencias Naturales 8, Madrid, Spain, p 240
57. AR Martin SK Katona D Matilla D Hembree TD Waters 1984 Migration of Humpback Whales between the Caribbean and Iceland J Mamm 65 330 333
58. BR Mate BA Lagerquist J Calambokidis 1999 Movements of North Pacific Blue whales during the feeding season off Southern California and their Southern fall migration Mar Mamm Sci 15 1246 1257
59. J Matthiopoulos B Mcconnell C Duck M Fedak 2004 Using satellite telemetry and aerial counts to estimate space use by grey seals around the British Isles J Appl Ecol 41 476 491
60. AL McMillen-Jackson TM Bert H Cruz-Lopez S Seyoum T Orsoy RE Crabtree 2005 Molecular genetic variation in tarpon (Megalops atlanticus Valenciennes) in the northern Atlantic Ocean Mar Biol 146 253 261
61. ELA Monteiro-Filho LR Monteiro SF Reis 2002 Skull shape and size divergence in dolphins of the genus Sotalia: a tridimensional morphometric analysis J Mamm 83 125 134
62. C Moritz 1994 Defining evolutionary significant units for conservation TREE 9 373 375
63. C Moritz 1994 Applications of mitochondrial DNA analysis in conservation: critical review Mol Ecol 3 401 411
64. Moritz C, Lavery S, Slade R (1995) Using allele frequency and phylogeny to define units for conservation and management. In: Nielsen JL, Powers GA (eds) Evolution and the aquatic ecosystem: defining unique units in population conservation, symposium 17. American Fisheries Society, Bethesda, Maryland, pp 249-262
65. Neff NA, Marcus LF (1980) A survey of multivariate methods for systematics. American Society of Mammalogy, p 243
66. Nielsen JL, Powers GA (1995) Evolution and the aquatic ecosystem: defining unique units in population conservation. American Fisheries Society, Bethesda, Maryland
67. Oliveira LR (2004) Variação geográfica do lobo-marinho sulamericano, Arctocephalus australis (Zimmermann, 1783) com base em dados morfológicos e moleculares. PhD thesis, Universidade de São Paulo
68. LR Oliveira LR Malabarba P Majluf 1999 Variação geográfica em crânios do lobo-marinho sul-americano Arctocephalus australis (Zimmermann, 1783) das populações do Brasil e Peru Comunicações do Museu de Ciências e Tecnologia da PUCRS 12 179 192
69. LR Oliveira D Danilewicz MB Martins P Ott IB Moreno G Caon 2001 New records of the Antarctic fur seal, Arctocephalus gazella (Peters, 1875) to the Brazilian coast Comunicações do Museu de Ciências e Tecnologia da PUCRS 14 201 207
70. LR Oliveira E Hingst-Zaher JS Morgante 2005 Size and shape sexual dimorphism in the skull of the South American fur seal, Arctocephalus australis (Zimmermann, 1783) (Carnivora: Otariidae) LAJAM 4 27 40
71. LR Oliveira M Arias-Schreiber D Meyer JS Morgante 2006 Effective population size in a bottlenecked fur seal population Biol Cons 131 505 509
72. JR Ovenden J Salini S O'connor R Street 2004 Pronounced genetic population structure in a potentially vagile fish species (Pristipomoides multidens, Teleostei: Perciformes: Lutjanidae) from the East Indies triangle Mol Ecol 13 1991 1999
73. D Paetkau W Calvert I Stirling C Strobeck 1995 Microsatellite analysis of population structure in Canadian polar bears Mol Ecol 4 347 354
74. KM Parsons JW Durban DE Claridge DL Herzing KC Balcomb LR Noble 2006 Population genetic structure of coastal bottlenose dolphins (Tursiops truncatus) in the Northern Bahamas Mar Mamm Sci 22 276 298
75. Peters RH (1983) The ecological implications of body size. Cambridge studies in ecology. Cambridge Academic Press, Cambridge
76. MC Pinedo 1990 Ocorrência de Pinípedes na costa brasileira Garcia de Orta, Serie Zoologia 15 37 48
77. S Piry A Alapetite J-M Cornuet D Paetkau L Baudouin A Estoup 2004 GeneClass2: a software for genetic assignment and first generation migrants detection J Her 95 536 539
78. JK Pritchard M Stephens P Donnelly 2000 Inference of population structure using multilocus genotype data Genetics 155 945 959
79. M Raymond F Rousset 1995 genepop (version 1.2): Population genetics software for exact tests and ecumenicism J Her 86 248 249
80. Repenning CA, Peterson RS, Hubbs CL (1971) Contributions to the systematics of the southern fur seals, with particular reference to the Juan Fernández and Guadalupe species. In: Burt WH (ed) Antarctic Pinnipedia, vol 18. Antarctic Research, American Geophysical Union, pp 1-34
81. Rice DW (1998) Marine Mammals of the World. Special Publication No. 4. Society for Marine Mammalogy
82. 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. Cons Gen (in press). doi: 10.1007/s10592-006-9275-x
83. Rohlf FJ (1993) Relative warps analysis and an example of its application to mosquito wings. Contributions to morphometrics. Monografias del Museu Nacional de Ciencias Naturales 8. Madrid, Spain, p 240
84. Rohlf FJ (2000) Tps Regr, ver. 1.25 © 2000. Dept. Ecology and Evolution, State University of New York at Stony Brook
85. Rohlf FJ (2002) TpsRelW, ver. 1.25. © 2002. Dept. Ecology and Evolution, State University of New York at Stony Brook
86. Rohlf FJ (2003) TpsDig, ver. 1.32 © 2003. Dept. Ecology and Evolution, State University of New York at Stony Brook
87. FJ Rohlf LF Marcus 1993 A revolution in morphometrics TREE 8 129 132
88. FCW Rosas MC Pinedo M Marmontel M Haimovici 1994 Seasonal movements of the South American sea lion (Otaria flavescens, Shaw) off the Rio Grande do Sul coast, Brazil Mammalia 58 51 59
89. OA Ryder 1986 Species conservation and systematics: the dilemma of subspecies TREE 1 9 10
90. Seal Conservation Society (2006) South American Fur Seal. Available via http://www.pinnipeds.org/species/samfursl.htm. Accessed 30 March 2006
91. PC Simões-Lopes CJ Drehmer PH Ott 1995 Nota sobre os Otariidae e Phocidae (Mammalia: Carnivora) da costa norte do Rio Grande do Sul e Santa Catarina, Brasil Biociências 3 173 181
92. M Slatkin 1995 A measure of population subdivision based on microsatellite allele frequencies Genetics 139 457 462
93. Slice DE (1994) GRF-ND, Generalized rotational fitting of n-dimensional landmark data. Dept. Ecology and Evolution, State University of New York at Stony Brook
94. Sokal RR, Rohlf, FJ (1981) Biometry, the principals and practice of statistics in biological research, 3rd edn. New York
95. MA Stevens DJ Boness 2003 Influences of habitat features and human disturbance on use of breeding sites by a declining population of southern fur seals (Arctocephalus asutralis) J Zool Lond 260 154 152
96. KA Tolley GA Vikingsson P Rosel 2001 Mitochondrial DNA sequencevariation and phylogeographic patterns in harbour porpoises (Phocoena phocoena) from the North Atlantic Cons Gen 2 349 361
97. JI Túnez D Centrón HL Cappozzo MH Cassini 2007 Geographic distribution and diversity of mitochondrial DNA haplotypes in South American sea lions (Otaria flavescens) and fur seals (Arctocephalus australis) Mamm Biol 72 193 203
98. C Van Oosterhout WF Hutchinson DPM Wills P Shipley 2004 MICRO-CHECKER: software for identifying and correcting genotyping errors in microsatellite data Mol Ecol Notes 4 535 538
99. Vaz-Ferreira R (1982) Arctocephalus australis Zimmerman, South American fur seal. In: Mammals in the seas. FAO Fisheries series, Small cetaceans, seals, sirenians and otters, vol 4, pp 497-508
100. a Reunião de Trabalho de Especialistas em Mamíferos Aquáticos da América do Sul e 2° Congresso da Sociedade Latinoamericana de Especialistas em Mamíferos Aquáticos de América do Sul, Olinda, 25-29 October 1998, p 221
101. CC Vieira 1955 Lista remissiva dos mamíferos do Brasil Arquivos Zoologia do Estado de São Paulo 8 341 474
102. AP Vogler R DeSalle 1994 Diagnosing units of conservation management Cons Biol 6 170 178
103. S Wada O Masayuki T Yamada 2003 A newly discovered species of living baleen whale Nature 426 278 281
104. PS Walsh DA Metzger R Higuchi 1991 Chelex100 as a medium for simple extraction of DNA for PCR-based typing from forensic material Biotech 10 506 513
105. PS Walsh HA Ehrlich R Higuchi 1992 Preferential amplification of alleles: mechanisms and solutions PCR Meth Appl 1 241 250
106. JY Wang LS Chou BN White 1999 Mitochondrial DNA analysis of sympatric morphotypes of bottlenose dolphins (genus: Tursiops) in Chinese waters Mol Ecol 8 1603 1612
107. JY Wang LS Chou BN White 2000 Differences in the external morphology of two sympatric species of bottlenose dolphins (genus Tursiops) in the waters of China J Mamm 81 1157 1165
108. RS Waples 1991 Pacific Salmon, Oncorhynchus spp. and the definition of species under the endangered species act Mar Fish Rev 53 11 22
109. Waples RS (1995) Evolutionary significant units and the conservation of biological diversity under the Endangered Species Act. In: Nielsen JL, Powers GA (eds) Evolution and the aquatic ecosystem: defining unique units in population conservation. American Fisheries Society, Bethesda, pp 8-27
110. RS Waples 1998 Evolutionarily significant units, distinct population segments, and the endangered species act: reply to Pennock and Dimmick Cons Biol 12 718 721
111. RR Warner PL Chesson 1985 Coexistence mediated by recruitment fluctuations: a field guide to the storage effect The Am Nat 125 769 787
112. PM Waser C Strobeck 1998 Genetic signatures of interpopulation dispersal TREE 13 43 44
113. RK Wayne 1992 On the use of molecular genetic characters to investigate species status Cons Biol 6 590 592
114. BS Weir CC Cockerham 1984 Estimating F-statistics for the analysis of population structure Evolution 38 1358 1370
115. CJ Wood 1998 Movement of bottlenose dolphins around the south-west coast of Britain J Zool 246 155 163
116. S Wright 1965 The interpretation of population structure by statistics with special regard to systems of mating Evolution 19 395 420
117. LP Wynen SD Goldsworthy SJ Insley M Adams J.W Bickham J Francis JP Gallo AR Hoelzel P Majluf RWG White R Slade 2001 Phylogenetic Relationships within the Eared Seals (Otariidae: Carnivora): Implications for the Historical Biogeography of the Family Mol Phyl Evol 21 270 284
118. Zelditch M, Swiderski D, Sheets DH, Fink W (2004) Geometric Morphometrics For Biologists: a primer. Elsevier Academic Press, San Diego
119. EAW Von Zimmerman 1783 Geographische Geshichte des Menschen, und der Allgemeiss Verbreiteten Vierfüssigen Thiere Leipzig 3 1778 1783