Abstract
Genetic introgression from Chatham Island Red-crowned parakeet (Cyanoramphus novaezelandiae chathamensis) is a long-standing problem in the conservation of the rare Forbes’ parakeet (C. forbesi) on Mangere Island, New Zealand. Microsatellite genotypes, mitochondrial DNA sequences, and morphological markers have been applied to study the situation. An extensive history of hybridisation was detected in the single remaining Forbes’ parakeet population, where no less than 81% of all birds screened are considered hybrids. Genetic markers showed that a large proportion of birds identified as Forbes’ parakeets by crown plumage are cryptic hybrids. Only a small proportion of birds with Forbes’ parakeet morphotype were found to be genetically distinct from Chatham Island Red-crowned parakeets using microsatellite and mitochondrial DNA assignment tests, but these still represent an Evolutionarily Significant Unit (ESU) for conservation.
Article PDF
Similar content being viewed by others
Avoid common mistakes on your manuscript.
References
Allendorf FW, Leary RF, Spruell P, Wenburg JK (2001) The problems with hybrids: Setting conservation guidelines. TREE 16:613–622
Anderson E, Stebbins GL Jr (1954) Hybridization as an evolutionary stimulus. Evolution 8:377–388
Anderson EC, Thompson EA (2002) A model-based method for identifying species hybrids using multilocus genetic data. Genetics 160:1217–1229
Anderson MJ (2003) PCO: a FORTRAN computer program for principal coordinate analysis. Department of Statistics University of Auckland, New Zealand
Ballantyne KN, Chan C-H, Chambers GK (2004) A PCR-RFLP based method for assigning mitochondrial control region haplogroups in hybridizing Chatham Islands Cyanoramphus parakeets. New Zealand Natural Sciences 29:33–38
Balloux F (2001) EASYPOP (version 1.7): a computer program for population genetics simulations. J. Hered 92:301–302
Barton NH (2001) The role of hybridization in evolution. Molecular Ecology 10:551–568
Bigelow RS (1965) Hybrid zones and reproductive isolation. Evolution 19:449–458
Boecklen WJ, Howard DJ (1997) Genetic analysis of hybrid zones: Number of markers and power of resolution. Ecology 78:2611–2616
Boon WM, Kearvell JC, Daugherty CH, Chambers GK (2000) Molecular systematics of New Zealand Cyanoramphus parakeets: Conservation of Orange-fronted and Forbes’ parakeets. Bird Conservation International 10:211–239
Boon WM, Kearvell JC, Daugherty CH, Chambers GK (2001) Molecular systematics and conservation of kakariki (Cyanoramphus spp.): Science for Conservation 176. Department of Conservation, Wellington
Bowcock AM, Ruiz-Linares A, Tomfohrde J, Minch E, Kidd JR, Cavalli-Sforza LL (1994) High resolution of human evolutionary trees with polymorphic microsatellites. Nature 368:455–457
Caparroz R, Miyaki CY, Baker AJ (2003) Characterization of microsatellite loci in the Blue-and-gold Macaw, Ara ararauna (Psittaciformes: Aves). Molecular Ecology Notes 3:441–443
Chan C-H, Ballantyne KN, Lambert DM, Chambers GK (2005) Characterization of variable microsatellite loci in Forbes’ parakeet (Cyanoramphus forbesi) and their use in other parrots. Conserv. Genet., 6, 651–654
Cornuet JM, Luikart G (1996) Description and power analysis of two tests for detecting recent population bottlenecks from allele frequency data. Genetics 144:2001–2014
Crandall KA, Bininda-Emonds ORP, Mace GM, Wayne RK (2000) Considering evolutionary processes in conservation biology. TREE 15:290–295
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 91:3166–3170
Dieringer D, Schlötterer C (2002) Microsatellite analyser (MSA): a platform independent analysis tool for large microsatellite data sets. Molecular Ecology Notes 3:167–169
Dowling TE, Secor CL (1997) The role of hybridization and introgression in the diversification of animals. Annu. Rev. Ecol. Syst 28:593–619
Dyer R, Sork VL (2001) Pollen pool heterogeneity in shortleaf pine, Pinus echinata Mill. Molecular Ecology 10:859–866
Excoffier L, Smouse PE, Quattro JM (1992) Analysis of molecular variance inferred from metric distances among DNA haplotypes: application to human mitochondrial DNA restriction data. Genetics 131:479–491
Felsenstein J (1989) PHYLIP–phylogeny inference package (version 3.2). Cladistics 5:164–166
Fraser DJ, Bernatchez L (2001) Adaptive evolutionary conservation: towards a unified concept for defining conservation units. Molecular Ecology 10:2741–2752
Goldstein DB, Ruiz Linares A, Cavalli-Sforza LL, Feldman MW (1995) Genetic absolute dating based on microsatellites and the origin of modern humans. Proc. Natl. Acad. Sci. USA 92:6723–6727
Grant PR, Grant BR (1992) Hybridization of bird species. Science 256:193–197
Greene TC (2000) Forbes’ parakeet (Cyanoramphus forbesi) population on Mangere Island, Chatham Islands: Conservation Advisory Science Notes 319. Department of Conservation, Wellington
Hughes CR, Melland RR, Beissinger SR (1998) Polymorphic trinucleotide microsatellite loci for a neotropical parrot, the green-rumped parrotlet, Forpus passerinus. Molecular Ecology 7:1247–1263
Huxel GR (1999) Rapid displacement of native species by invasive species: Effects of hybridization. Biological Conservation 89:143–152
Kimura M, Crow JF (1964) The number of alleles that can be maintained in a finite population. Genetics 49:725–738
Lewontin RC, Birch LC (1966) Hybridization as a source of variation for adaptation to new environments. Evolution 20:315–336
Moritz C (1994) Defining ‘Evolutionarily Significant Units’ for conservation. TREE 9:373–375
Nielsen R (1997) A likelihood approach to population samples of microsatellite alleles. Genetics 146:711–716
Nielsen R, Palsbøll PJ (1999) Single-locus tests of microsatellite evolution: Multi-step mutations and constraints on allele size. Molecular Phylogenetics and Evolution 11:477–484
Nixon AJ (1982) Aspects of the ecology and morphology of Cyanoramphus parakeets and hybrids from Mangere Island, Chatham Islands. MSc thesis, Victoria University of Wellington, Wellington, New Zealand
Ohta T, Kimura M (1973) A model of mutation appropriate to estimate the number of electrophoretic detectable alleles in a finite population. Genet. Res 22:201–204
Prager EM, Wilson AC (1975) Slow evolutionary loss of potential for interspecific hybridization in birds: a manifestation of slow regulatory evolution. Proc. Natl. Acad. Sci. USA 72:200–204
Primmer CR, Raudsepp T, Chowdhary BP, Møller AP, Ellegren H (1997) Low frequency of microsatellites in the avian genome. Genome Research 7:471–482
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 genetic software for the exact tests and ecumenicisms. J. Hered 86:248–249
Rhymer JM, Simberloff D (1996) Extinction by hybridization and introgression. Annu. Rev. Ecol. Syst 27:83–109
Robertson BC, Minot EO, Lambert DM (2000) Microsatellite primers for the kakapo (Strigops habroptilus) and their utility in other parrots. Conservation Genetics 1:93–95
Russello M, Calcagnotto D, DeSalle R, Amato G (2001) Characterization of microsatellite loci in the endangered St. Vincent Parrot. Amazona guildingii, Molecular Ecology Notes 1:162–164
Ryder OA (1986) Species conservation and systematics: The dilemma of subspecies. TREE 1:9–10
Sainsbury JP, MacAvoy ES, Chambers GK (2004) Characterization of microsatellite loci in the Kaka,Nestor meridionalis. Molecular Ecology Notes 4:623–625
Saitou N, Nei M (1987) The neighbor-joining method: A new method for reconstructing phylogenetic trees. Mol. Bio. Evol 4:406–425
Sambrook J, Fritsch EF, Maniatis T (1989) Molecular Cloning: A Laboratory Manual, 2nd edn. Cold Spring Harbor Laboratory Press, New York
Seehausen O (2004) Hybridization and adaptive radiation. TREE 19:198–207
Slatkin M (1995) A measure of population subdivision based on microsatellite allele frequencies. Genetics 139:457–462
Taylor RH (1975) Some ideas on speciation in New Zealand parakeets. Notornis 22:110–121
Thioulouse J, Chessel D, Dolédec S, Olivier JM (1997) ADE-4: a multivariate analysis and graphical display software. Statistics and Computing 7:75–83
Triggs SJ, Daugherty CH (1996) Conservation and genetics of New Zealand parakeets. Bird Conservation International 6:89–101
Valdes AM, Slatkin M, Freimer NB (1993) Allele frequencies at microsatellite loci: the stepwise mutation model revisited. Genetics 133:737–749
Weir BS, Cockerham CC (1984) Estimating F-statistics for the analysis of population structure. Evolution 38:1358–1370
Wolf DE, Takebayashi N, Rieseberg LH (2001) Predicting the risk of extinction through hybridization. Conservation Biology 15:1039–1053
Acknowledgements
We thank the New Zealand Department of Conservation and Victoria University of Wellington for funding this research. We also thank Tertia Thurley and other field workers for sample collection, James Sainsbury, Elizabeth MacAvoy, Rod Hitchmough, and Colin Miskelly for technical assistance, and two anonymous reviewers for their comments on this manuscript.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Chan, Ch., Ballantyne, K.N., Aikman, H. et al. Genetic analysis of interspecific hybridisation in the world’s only Forbes’ parakeet (Cyanoramphus forbesi) natural population. Conserv Genet 7, 493–506 (2006). https://doi.org/10.1007/s10592-005-9060-2
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10592-005-9060-2