Abstract
Introgressive hybridization occurs when closely related taxa overlap in distribution and is often associated with historically isolated populations coming into contact as a result of anthropogenic disturbance. There is evolutionary and conservation interest in detecting hybridization to determine its implications on future species composition, especially for threatened and recovering taxa such as subantarctic (Arctocephalus tropicalis) and Antarctic (A. gazella) fur seals, which were driven to the brink of extinction by human exploitation. Hybridization between these species has been reported at two locations and they breed sympatrically at a third site, Iles Crozet. While hybrid individuals have previously been identified based on phenotype, individuals can be difficult to classify based on these characteristics alone. Genotypic hybrid identification has been successful in several species, including fur seals. In this study we conducted an assignment test using microsatellite data to identify hybrids and to measure the frequency of hybridization at Iles Crozet. Samples were collected from 372 individuals and screened with 6 polymorphic microsatellite markers. MtDNA genotypes were also determined for individuals identified as hybrids or backcrosses based on microsatellite genotype. Phenotype, microsatellite and mtDNA genotype were then compared in order to identify hybrids. The results indicate that 1% of the population have hybrid genotypes and at a minimum, 2.4% of the population are backcrossed to parental species. We found that the two species are genetically distinct from one another and given the low rate of hybridization it is unlikely that they will fuse. These results suggest that there is a mechanism for species recognition that acts as a barrier to hybridization. It therefore seems unlikely that fur seals are threatened by significant introgression. Further investigation of fur seal mating systems would provide valuable insight into the mechanisms governing hybridization and species recognition in mate choice.
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References
Adams JR, Kelly BT, Waits LP (2003) Using faecal DNA sampling and GIS to monitor hybridization between red wolves (Canis rufus) and coyotes (Canis latrans). Mol Ecol 12:2175–2186
Allen PJ, Amos W, Pomeroy PP, Twiss SD (1995) Microsatellite variation in grey seals (Halichoerus grypus) shows evidence of genetic differentiation between two British breeding colonies. Mol Ecol 4:653–662
Allendorf FW, Leary RF, Spruell P, Wenburg JK (2001) The problems with hybrids setting conservation guidelines. Trends Ecol Evol 16:613–622
Anderson E, Hubricht L (1938) Hybridization in Tradescantia III The evidence for introgressive hybridization. Am J Bot 25:396–402
Arnold ML (1992) Natural hybridization as an evolutionary process. Ann Rev Ecol Syst 23:237–261
Arnold ML (1997) Natural hybridization and evolution. Oxford University Press, Oxford
Arnould JPY, Boyd IL, Warneke RM (2003) Historical dynamics of the Australian fur seal population:evidence of regulaton by man? Can J Zool 81:1428–1436
Barton NH (2001) The role of hybridization in evolution. Mol Ecol 10:551–568
Beaumont M, Barratt EM, Gottelli D, Kitchener AC, Daniels MJ, Pritchard JK, Bruford MW (2001) Genetic diversity and introgression in the Scottish wildcat. Mol Ecol 10:319–336
Bensch S, Helbig AJ, Salomon M, Seibold I (2002) Amplified fragment length polymorphism analysis identifies hybrids between two subspecies of warblers. Mol Ecol 11:473–481
Bester MN (1987) Subantarctic fur seal, Arctocephalus tropicalis, at Gough Island (Tristan da Cunha Group). In: Croxall JP, Gentry RL (eds) Status, biology, and ecology of fur seals. US Dept. of Commerce
Bester MN, Wilkinson IS (1989) Field identification of Antarctic and subantarctic fur seal pups. S Afr J Wildl Res 19:140–144
Bettles CM, Docker MF, Dufour B, Heath DD (2005) Hybridization dynamics between sympatric species of trout: loss of reproductive isolation. J Evol Biol 18:1220–1233
Bigelow RS (1965) Hybrid zones and reproductive isolation Evolution 19:449–458
Boness DJ (1991) Determinants of mating systems in the Otariidae (Pinnipedia). In: Renouf D (ed) Behaviour of pinnipeds. Chapman and Hall, London
Bonner WN, Laws RM (1964) Seals and sealing. In: Priestly R, Adie RJ, Robin GDQ (eds) Antarctic research. Butterworths, London, pp 163–190
Boyd IL (1989) Spatial and temporal distribution of Antarctic fur seals Arctocephalus gazella on the breeding grounds at Bird Island, South Georgia, South Atlantic Ocean. Polar Biol 10:179–186
Boyd IL (1991) Environmental and physiological factors controlling the reproductive cycles of pinnipeds. Can J Zool 69:1135–1148
Campton DE (1987) Natrual hybridization and introgression in fishes: methods of detection and genetic interpretations. In: Ryman N, Utter F (eds) Population genetics and fishery management. University of Washington Press, pp 161–192
Coltman DW, Bowen WD, Wright JM (1996) PCR primers for harbour seal (Phoca vitulina concolour) microsatellites amplify polymorphic loci in other pinniped species. Mol Ecol 5:161–163
Condy PR (1978) Distribution, abundance and annual cycle of fur seals (Arctocephalus spp.) on the Prince Edward Islands. S Afr J Wildl Res 8:159–168
Dowling TE, Secor CL (1997) The role of hybridization and introgression in the diversification of animals. Ann Rev Ecol Syst 28:593–619
Fisher HS, Wong BBM, Rosenthal GG (2006) Alteration of the chemical environment disrupts communication in a freshwater fish. Proc R Soc Lond B 273:1187–1193
Flamand JRB, Vankan D, Gairhe KP, Duong H, Barker JSF (2003) Genetic identification of wild Asian water buffalo in Nepal. Anim Conserv 6:265–270
Fredrickson RJ, Hedrick PW (2006) Dynamics of hybridization and introgression in red wolves and coyotes. Conserv Biol 20:1272–1283
Goldsworthy SD, Boness DJ, Fleischer RC (1999) Mate choice among sympatric fur seals: female preference for conphenotypic males. Behav Ecol Sociobiol 45:253–267
Goodman SJ, Barton NH Swanson G Abernethy K, Pemberton JM (1999) Introgression through rare hybridization: A genetic study of a hybrid zone between red and sika deer (genus Cervus) in Argyll Scotland. Genetics 152:355–371
Goudet J (1995) FSTAT (vers: 1.2) a computer program to calculate F-statistics. J Hered 86:485–486
Guinet C, Jouventin P, Georges JY (1994) Long term population changes of fur seals Arctocephalus gazella and Arctocephalus tropicalis on subantarctic (Crozet) and subtropical (St. Paul and Amsterdam) islands and their possible relationship to El Niño southern oscillation. Antarct Sci 6:473–478
Gwilliam J (2005) Detecting hybridisation in a sympatric population of fur seals. In: Department of biological sciences. Macquarie University, Sydney, Australia
Hoelzel AR, Campagna C, Arnbom T (2001) Genetic and morphometric differentiation between island and mainland southern elephant seal populations. Proc R Soc Lond B 268:325–332
Hofmeyr GJG, Bester MN, Jonker FC (1997) Changes in population sizes and distribution of fur seals at Marion Island. Polar Bio 17:150–158
Hofmeyr GJG, Bester MN, Makhado AB, Pistorius PA (2006) Population changes in subantarctic and Antarctic fur seals at Marion Island. S Afr J Wildl Res 36:55–68
Hubbs CL (1955) Hybridization between fish species in nature. Syst Zoo 4:1–20
Jouventin P, Stahl JC, Weimerskirch H (1982) La recolonisation des Iles Crozet par les otaries (Arctocephalus tropicalis et A. gazella). Mammalia 46:505–514
Kelly BT, Miller PS, Seal US (1999) Population and habitat viability assessment workshop for the red wolf (Canis rufus). (ed (SSC/IUCN) CBSG), Apple Valley, MN, 88 pp
Kerley GIH (1983a) Comparison of seasonal haul-out patterns of fur seals Arctocephalus tropicalis and A gazella on subantarctic Marion Island. S Afr J Wildl Res 13:71–77
Kerley GIH (1983b) Relative population sizes and trends, and hybridization of fur seals Arctocephalus tropicalis and A gazella at the Prince Edward Islands, Southern Ocean. S Afr Zool 18:388–392
Kimura M (1980) A simple method for estimating evolutionary rate of base substitutions through comparative studies of nucleotide sequences. J Mol Evol 16:111–120
Kingston JJ (2006) Hybridisation, female mate choice and male reproductive success in sympatrically breeding fur seals. In: Department of biological sciences. Macquarie University
Kumar S, Tamura K, Nei M (2004) MEGA3: Integrated software for Molecular Evolutionary Genetics Analysis and sequence alignment. Brief Bioinform 5:150–163
Kyle CJ, Johnson AR, Patterson BR, Wilson PJ, Shami K, Grewal SK, White BN (2006) Genetic nature of eastern wolves: Past, present and future. Conserv Genet 7:273–287
Lancaster ML, Gemmell NJ, Negro S, Goldsworthy SD, Sunnucks P (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
Leary RF, Allendorf FW, Forbes SH (1993) Conservation genetics of bull trout in the Columbia and Klamath River Drainages. Conserv Biol 7:856–865
Lehman N, Eisenhawer A, Hansen K, Mech LD, Peterson RO, Gogan PJP, Wayne RK (1991) Introgression of coyote mitochondrial DNA into sympatric North American gray wolf populations. Evolution 45:104–119
Lento GM, Haddon M, Chambers GK, Baker CS (1997) Genetic variation of southern hemisphere fur seals (Arctocephalus spp.): investigation of population structure and species identity. J Hered 88:202–208
Lento GM, Mattlin RH, Chambers GK, Baker CS (1994) Geographic distribution of mitochondrial cytochrome b DNA haplotypes in New Zealand fur seals (Arctocephalus forsteri). Can J Zool, 72:293–299
Mayr E (1963) Animal species and evolution. Harvard University Press, Cambridge
Nijman IJ, Otsen M, Verkaar ELC, de Ruijter C, Hanekamp E, Ochieng JW, Shamshad S, Rege JEO, Hanotte O, Barwegen MW, Sulawati T, Lenstra JA (2003) Hybridization of banteng (Bos javanicus) and zebu (Bos indicus) revealed by mitochondrial DNA, satellite DNA, AFLP and microsatellites. Heredity 90:10–16
Nowak RM (2002) The original status of wolves in eastern North America. Southeastern Nat 1:95–130
Olden JD, LeRoy Poff N, Douglas MR, Douglas ME, Fausch KD (2004) Ecological and evolutionary consequences of biotic homogenization. Trends Ecol Evol 19:18–24
Paetkau D, Calvert W, Stirling I, Strobeck C (1995) Microsatellite analysis of population structure in Canadian polar bears. Mol Ecol 4:347–354
Page B, Goldsworthy SD, Hindell MA (2001) Vocal traits of hybrid fur seals: intermediate to their parental species. Anim Behav 61:959–967
Page B, Goldsworthy SD, Hindell MA, McKenzie J (2002) Interspecific differences in male vocalizations of three sympatric fur seals (Arctocephalus spp.). J Zool 258:49–56
Pritchard JK, Stephens M, Donnelly P (2000) Inference of population structure using multilocus genotype data. Genetics 155:945–959
Raymond M, Rousset F (1995) GENEPOP (version 1.2): population genetics software for exact test and ecumenism. J Hered 86:248–249
Rhymer JM, Simberloff D (1996) Extinction by hybridization and introgression. Ann Rev Ecol Syst 27:83–109
Rhymer JM, Williams MJ, Braun MJ (1994) Mitochondrial analysis of gene flow between New Zealand mallards (Anas Platyrhynchos) and grey ducks (A. superciliosa). Auk 111:970–978
Rice WR (1989) Analysing tables of statistical tests. Evolution 43:223–225
Roux JP (1987) Subantarctic fur seal, Arctocephalus tropicalis, in French subantarctic territories. In: Croxall JP, Gentry RL (eds) Status, biology, and ecology of fur seals. US Dept. of Commerce
Roux JP, Hes AD (1984) The seasonal haul-out cycle of the fur seal Arctocephalus tropicalis (Gray, 1872) on Amsterdam Island. Mammalia 48:377–389
SCAR Status of Stocks. Blix AS. University of TromsØ, http://www.seals.scar.org/docs/scar.htm
Seehausen O (2004) Hybridization and adaptive radiation. Trends Ecol Evol 19:198–207
Shaughnessy PD, Goldsworthy SD (1990) Population size and breeding season of the Antarctic fur seal Arctocephalus gazella at Heard Island-1987/1988. Mar Mammal Sci 6:292–304
Shaughnessy PD, Shaughnessy GL, Fletcher L (1988) Recovery of the fur seal population at Macquarie Island. Pap Proc R Soc Tasmania 122:177–187
Sunnucks P, Hales D (1996) Numerous transposed sequences of mitochondrial cytochrome oxidase I-II in aphids of the genus Sitobion (Hemiptera: aphididae). Mol Biol Evol 13:510–524
Taylor AC, Sherwin WB, Wayne RK (1994) Genetic variation of microsatellite loci in a bottlenecked species: the northern hairy-nosed wombat Lasiorhinus krefftii. Mol Eco 3:277–290
United States Fish and Wildlife Service (1990) Red wolf recovery/species survival plan. (ed. USFWS). Atlanta, GA, 110 pp
Vähä J-P, Primmer CR (2005) Efficiency of model-based Bayesian methods for detecting hybrid individuals under different hybridisation scenarios and with different numbers of loci. Mol Ecol 15:63–72
van Oosterhout C, Hutchinson WF, Wills DPM, Shipley P (2004) MICRO-CHECKER: software for identifying and correcting genotyping errors in microsatellite data. Mol Ecol Notes 4:535–538
Vila C, Walker C, Sundqvist AK, Flagstad O, Andersone Z, Casulli A, Kojola I, Valdmann H, Halverson J, Ellegren H (2003) Combined use of maternal, paternal and bi-parental genetic markers for the identification of wolf-dog hybrids. Heredity 90:17–24
Wayne RK, Jenks SM (1991) Mitochondrial DNA analysis implying extensive hybridization of the endangered Red Wolf Canis rufus. Nature 351:565–568
Weir BS, Cockerham CC (1984) Estimating F-statistics for the analysis of population structure. Evolution 38:1358–1370
Wickens P, York AE (1997) Comparative population dynamics of fur seals [Review]. Mar Mammal Sci 13:241–292
Wynen L (2002) Phylogenetic relationships, population genetics and hybridisation of two species of southern fur seal (Arctocephalus spp.). University of Tasmania
Wynen LP, Goldsworthy SD, Guinet C, Bester MN, Boyd IL, Gjertz I, Hofmeyr GJG, White RG, Slade R (2000) Postsealing genetic variation and population structure of two species of fur seal (Arctocephalus gazella and A. tropicalis). Mol Ecol 9:299–314
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 21:270–284
Acknowledgements
We would like to thank Des Cooper, Rob Harcourt, Simon Goldsworthy & Christophe Guinet for their continued support and supervision provided to complete this study. We would also like to thank the editor of Conservation Genetics, Rus Hoelzel, and two anonymous reviewers for their helpful comments on this manuscript. Thanks to S. Goldsworthy for providing Heard Island samples and M. Lancaster and L. Wynen for Heard Island DNA extractions. We are indebted to Laurent Dubroca, Sebastian Luque, John Arnould and the 37th mission to Crozet for their assistance in the field. Special thanks to Mark Eldridge for providing valuable comments on this manuscript. This study was made possible by funding and support from TAAF, IPEV, Virbac Australia, SeaWorld, Linnean Society, PADI AWARE Foundation and Macquarie University.
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Kingston, J.J., Gwilliam, J. Hybridization between two sympatrically breeding species of fur seal at Iles Crozet revealed by genetic analysis. Conserv Genet 8, 1133–1145 (2007). https://doi.org/10.1007/s10592-006-9269-8
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DOI: https://doi.org/10.1007/s10592-006-9269-8