Abstract
Invasive alien species are a major cause of biodiversity loss. Nevertheless, non-native species can also contribute to conservation objectives. In 1673, the red-legged partridge (Alectoris rufa), a galliform native to southwest Europe, was introduced from France (A. r. rufa) into the UK for hunting purposes. Nowadays, hunters constantly supplement natural populations of A. rufa in its native range with stocks of captive-bred individuals. Such birds are usually genetically unscreened, and human-mediated hybridization with the exotic chukar (Alectoris chukar) has undermined genomic integrity of the species. Alectoris rufa in the UK has never been genetically investigated, and birds from East Anglian estates with no modern history of supplementation offer a potential genomic backup for the highly polluted native-range A. r. rufa. We genotyped modern and ancient (1824–1934) birds at the mitochondrial DNA (mtDNA) level to determine present and past kinship between East Anglian and native-range A. rufa. We used Short Tandem Repeats (STR) and Random Amplified Polymorphic DNA (RAPD) markers to identify A. rufa × A. chukar hybrids. The kinship of East Anglian birds with A. r. rufa was confirmed. No A. chukar introgression was found in ancient East Anglian A. rufa. Among modern partridges, we found birds with A. chukar mtDNA, and both STRs and RAPDs disclosed many A. rufa × A. chukar hybrids. While the genetic analysis pointed to the increase of diversity and decline of disparity over time within and among A. rufa populations, respectively, the conservation value of the resource historically introduced to the UK proved to have been quashed by three decades of recent releases of A. chukar and its A. rufa hybrids.





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References
Aebischer NJ, Lucio AJ (1997) Alectoris rufa. In: Hagenmeijer WJM, Blair MJ (eds) The EBCC Atlas of European breeding birds: their distribution and abundance. T & AD Poyser, London, pp 208–209
Aebischer NJ, Potts GR (1994) Red-legged partridge Alectoris rufa. In: Tucker GM, Heath MF (eds) Birds in Europe, their conservation status. Birdlife conservation series no 3. BirdLife International, Cambridge, pp 214–215
Allendorf FW, Luikart G (2007) Conservation and the genetic of populations. Blackwell Publishing, Malden
Alyokhin A (2011) Non-natives: put biodiversity at risk. Nature 475:36
Balmer DE, Gillings S, Caffrey BJ, Swann RL, Downie IS, Fuller RJ (2013) Bird Atlas 2007–11: the breeding and wintering birds of Britain and Ireland. BTO Books, Thetford
Bandelt HJ, Forster P, Röhl A (1999) Median-joining networks for inferring intraspecific phylogenies. Mol Biol Evol 16:37–48
Baratti M, Ammannati M, Magnelli C, Dessì-Fulgheri F (2004) Introgression of chukar genes into a reintroduced red-legged partridge (Alectoris rufa) population in central Italy. Anim Genet 36:29–35
Barbanera F, Negro JJ, Di Giuseppe G, Bertoncini F, Cappelli F, Dini F (2005) Analysis of the genetic structure of red-legged partridge (Alectoris rufa, Galliformes) populations by means of mitochondrial DNA and RAPD markers: a study from central Italy. Biol Conserv 122:275–287
Barbanera F, Guerrini M, Hadjigerou P, Panayides P, Sokos C, Wilkinson P, Khan AA, Khan BY, Cappelli F, Dini F (2007) Genetic insight into Mediterranean chukar (Alectoris chukar, Galliformes) populations inferred from mitochondrial DNA and RAPD markers. Genetica 131:287–298
Barbanera F, Guerrini M, Khan AA, Panayides P, Hadgijerou P, Sokos C, Gombobaatar S, Samadi S, Khan BY, Tofanelli S, Paoli G, Dini F (2009a) Human-mediated introgression of exotic chukar (Alectoris chukar, Galliformes) genes from East Asia into native Mediterranean partridges. Biol Invas 11:333–348
Barbanera F, Marchi C, Guerrini M, Panayides P, Sokos C, Hadjigerou P (2009b) Genetic structure of Mediterranean chukar (Alectoris chukar, Galliformes) populations: conservation and management implications. Naturwissenschaften 96:1203–1212
Barbanera F, Pergams ORW, Guerrini M, Forcina G, Panayides P, Dini F (2010) Genetic consequences of intensive management in game birds. Biol Conserv 143:1259–1268
Barbanera F, Forcina G, Guerrini M, Dini F (2011) Molecular phylogeny and diversity of Corsican red-legged partridge: hybridization and management issues. J Zool 285:56–65
Barilani M, Bernard-Laurent A, Mucci N, Tabarroni C, Kark S, Perez Garrido JA, Randi E (2007) Hybridisation with introduced chukars (Alectoris chukar) threatens the gene pool integrity of native rock (A. graeca) and red-legged (A. rufa) partridge populations. Biol Conserv 137:57–69
Blanco-Aguiar JA, González-Jara P, Ferrero ME, Sánchez-Barbudo I, Virgós E, Villafuerte R, Dávila JA (2008) Assessment of game restocking contributions to anthropogenic hybridization: the case of the Iberian red-legged partridge. Anim Conserv 11:535–545
Blank TH, Ash JS (1955) A population of partridges (Perdix p. perdix and Alectoris r. rufa) on a Hampshire estate. In: Proceedings of the XIth international congress of ornithology, pp 424–427
Bradshaw CJA, Isagi Y, Kaneko S, Bowman DMJS, Brook BW (2006) Conservation value of non-native banteng in northern Australia. Conserv Biol 20:1306–1311
Byers SM, Burger GV (1979) Evaluation of three partridge species for put and take hunting. Wildl Soc Bull 7:17–20
Casas F, Mougeot F, Sánchez-Barbudo I, Dávila JA, Viñuela J (2012) Fitness consequences of anthropogenic hybridization in wild red-legged partridge (Alectoris rufa, Phasianidae) populations. Biol Invas 14:295–305
Clavero M, García-Berthou E (2005) Invasive species are a leading cause of animal extinctions. Trend Ecol Evol 20:110
Cottam C, Arnold LN, Saylor LW (1940) The chukar and Hungarian partridge in America. US Department Interior, Bio Survey, Wildlife Leaflets, BS-159, USA
Crandall KA, Bininda Emonds ORP, Mace GM, Wayne RK (2000) Considering evolutionary processes in conservation biology. Trends Ecol Evol 15:290–295
Davis MA, Chew MK, Hobbs RJ, Lugo AE, Ewel JJ, Vermeij GJ, Brown JH, Rosenzweig ML, Gardener MR, Carroll SP, Thompson K, Pickett STA, Stromberg JC, Del Tredici P, Suding KN, Ehrenfeld JG, Grime JP, Mascaro J, Briggs JC (2011) Don’t judge species on their origin. Nature 474:153–154
de Soland A (1861) Etude sur une nouvelle race de Perdrix (Perdix atro-rufa Soc. Linn.). Ann Soc Linn Du dep. De Maine-et-Loire IV:143–146
Dias D (1992) Rock (Alectoris graeca) and chukar (A. chukar) partridge introductions in Portugal and their possible hybridization with red-legged partridges (A. rufa): a research project. Gibier Faune Sauvage 9:781–784
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 10:564–567
Ferrero ME, González-Jara P, Blanco-Aguiar JA, Sánchez-Barbudo I, Dávila JA (2007) Sixteen new polymorphic microsatellite markers isolated for red-legged partridge (Alectoris rufa) and related species. Mole Ecol Notes 7:13491351
Ferrero ME, Blanco-Aguiar JA, Lougheed SC, Sánchez-Barbudo I, de Nova PJG, Villafuerte R, Dávila JA (2011) Phylogeography and genetic structure of the red-legged partridge (Alectoris rufa): more evidence for refugia within Iberian glacial refugium. Mol Ecol 20:2628–2642
Fraser DJ, Bernatchez L (2001) Adaptive evolutionary conservation: towards a unified concept for defining conservation units. Mol Ecol 10:2741–2752
Gonzalez EG, Castilla AM, Zardoya R (2005) Novel polymorphic microsatellites for the red-legged partridge (Alectoris rufa) and cross-species amplification in Alectoris graeca. Mol Ecol Notes 5:449–451
Goodwin D (1986) Further notes on chukar and hybrid partridges in Britain and Europe. Avic Mag 92:157–160
Gould SJ (1989) Wonderful life: the Burgess Shale and the nature of history. W.W. Norton & Company, New York
Green RE (1983) Spring dispersal and agonistic behaviour of the Red-legged partridge (Alectoris rufa). J Zool 201:541–555
Green RE (1984) The feeding ecology and survival of partridge chicks (Alectoris rufa and Perdix perdix) on arable farmland in East Anglia. J Appl Ecol 21:817–830
Griffiths CJ, Jones CG, Hansen DM, Puttoo M, Tatayah RV, Müller CB, Harris S (2010) The use of extant non-indigenous tortoises as a restoration tool to replace extinct ecosystem engineers. Restor Ecol 18:1–7
Hochberg Y (1988) A sharper Bonferroni procedure for multiple tests of significance. Biometrika 75:800–802
Lerdau M, Wickham JD (2001) Non-natives: four risk factors. Nature 475:36–37
Lever C (1977) The naturalized animals of the British Isles. Hutchinson, London
Lever C (1987) Naturalized birds of the world. Longman Scientific & Technical, Harlow
Librado P, Rozas J (2009) DnaSP v5: a software for comprehensive analysis of DNA polymorphism data. Bioinformatics 25:1451–1452
Lockwood JL, Hoopes MF, Marchetti MP (2011) Non-natives: plusses of invasion ecology. Nature 475:36
Lodge DM, Williams S, Macisaac HJ, Hayes KR, Leung B, Reichard S, Mack RN, Moyle PB, Smith M, Andow DA, Carlton JT, McMichael A (2006) Biological invasions: recommendations for U.S. policy and management. Ecol Appl 16:2035–2054
Mack RN, Simberloff D, Lonsdale WM (2000) Biotic invasions: causes, epidemiology, global consequences and control. Ecol Appl 10:689–710
Madge S, McGowan P (2002) Pheasants, partridges and grouse. A and C Black Ltd., London
Martínez-Fresno M, Henriques-Gil N, Arana P (2008) Mitochondrial DNA sequence variability in red-legged partridge, Alectoris rufa, Spanish populations and the origins of genetic contamination from A. chukar. Conserv Genet 9:1223–1231
Masseti M, Pecchioli E, Vernesi C (2008) Phylogeography of the last surviving populations of Rhodian and Anatolian fallow deer (Dama dama dama L., 1758). Biol J Linn Soc 93:835–844
Middleton AD, Chitty H (1937) The food of adult partridges Perdix perdix and Alectoris rufa in Great Britain. J Appl Ecol 6:322–336
Mooney HA, Hobbs RJ (2000) Invasive species in a changing world. Island Press, Washington, DC
Musgrove AJ, Aebischer NJ, Eaton MA, Hearn RD, Newson SE, Noble DG, Parsons M, Risely K, Stroud DA (2013) Population estimates of birds in Great Britain and the United Kingdom. Br Birds 106:64–100
Negri A, Pellegrino I, Mucci N, Randi E, Tizzani P, Meneguz PG, Malacarne G (2013) Mitochondrial DNA and microsatellite markers evidence a different pattern of hybridization in red-legged partridge (Alectoris rufa) populations from NW Italy. Eur J Wildl Res 59:407–419
Olden DJ, Poff NL, Douglas MR, Douglas EM, Fausch KD (2004) Ecological and evolutionary consequences of biotic homogenization. Trend Ecol Evol 19:18–24
Payn WH (1991) The introduction of the Chukar. Br Birds 84:68
Peatkau D, Waits L, Clarkson PL, Craighead L, Vyse E, Ward R, Strobeck C (1998) Variation in genetic diversity across the range of North American brown bears. Conserv Biol 12:418–429
Potts GR (1980) The effects of modern agriculture, nest predation and game management on the population ecology of partridges (Perdix perdix and Alectoris rufa). Adv Ecol Res 11:1–79
Potts GR (1989) The impact of releasing hybrid partridges on wild red-legged populations. Game Conserv Rev 20:81–85
Potts GR (1991) The introduction of the Chukar. Br Birds 84:289
Potts GR (2012) Partridges. HarperCollins Publishers, London
Pritchard JK, Stephens M, Donnelly P (2000) Inference of population structure using multilocus genotype data. Genetics 155:945–959
Randi E (1996) A Mitochondrial Cytochrome B phylogeny of the Alectoris Partridges. Mol Phylogenet Evol 2:214–227
Rands MRW (1986) Effects of hedgerow characteristics on partridge breeding densities. J Appl Ecol 23:479–487
Raymond M, Rousset F (1995) GENEPOP (version 1.2): population genetics software for exact tests and ecumenicism. J Hered 86:248–249
Rhymer JM, Simberloff D (1996) Extinction by hybridization and introgression. Annu Rev Ecol Syst 27:83–109
Rodríguez García MJ, Galián J (2014) Lack of mitochondrial genetic structure in the red-legged partridge Alectoris rufa (Phasianidae). J Zoolog Syst Evol Res 52:59–64
Salm R, Feder L, Jardim MAG, Hass N, Jalles-Filho E, Costa AM (2009) Conservation value of an exotic species: the case of coconuts on the Kayapo indigenous lands, south-eastern Amazonia. Environ Dev Sustain 11:161–173
Schlaepfer MA, Sax DF, Olden JD (2011) The potential conservation value of non native species. Conserv Biol 25:428–437
Schlaepfer MA, Sax DF, Olden JD (2012) Toward a more balanced view of non-native species. Conserv Biol 26:1156–1158
Simberloff D (2011) Non-natives: 141 scientists object. Nature 475:36
Tejedor MT, Monteagudo LV, Mautner, Hadjisterkotis H, Arruga MV (2007) Introgression of Alectoris chukar genes into a Spanish wild Alectoris rufa population. J Hered 98:179–182
Thompson JD, Higgins DG, Gibson TJ (1994) CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, positions-specific gap penalties and weight matrix choice. Nucleic Acids Res 22:4673–4680
Tompkins DM, Parish DMB, Hudson PJ (2002) Parasite mediated competition among red-legged partridges and other lowland gamebirds. J Wildl Manag 66:445–450
True GH (1937) The chukar partridge of Asia. Calif Fish Game 23:229–231
Vaha J-P, Primmer CR (2006) Efficiency of model-based Bayesian methods for detecting hybrid individuals under different hybridization scenarios and with different numbers of loci. Mol Ecol 15:63–72
Valière N (2002) Gimlet: a computer program for analyzing genetic individual identification data. Mol Ecol Notes 2:377–379
Vitule JRS, Freire CA, Vazquez DP, Nunez MA, Simberloff D (2012) Revisiting the potential conservation value of non-native species. Conserv Biol 26:1153–1155
Waits LP, Luikart G, Taberlet P (2001) Estimating the probability of identity among genotypes in natural populations: cautions and guidelines. Mol Ecol 10:249–256
Wiens JA, Goble DD, Scott JM (2012) Time to accept conservation triage. Nature 488:281
Wilkinson P (1987) Red-legged impostors. BTO News 152:1–2
Wright S (1951) The genetical structure of populations. Ann Eugen 15:323–354
Acknowledgments
Authors wish to thank M. Adams (The Natural History Museum, Tring, UK) for his valuable support in the loan of the A. rufa museum specimens, and R.A.H. Draycott, J.A. Ewald, R. Burrell, C.J. Wheatley (Game & Wildlife Conservation Trust) and the Norfolk gamekeepers for A. rufa sampling in the UK. For A. rufa sampling outside the UK: J.A. Dávila (Instituto de Investigación en Recursos Cinegéticos, Ciudad Real), J.J. Negro (Estación Biológica de Doñana, Seville), C. Pietri (Fédération Départemental des Chasseurs de Haute-Corse, Bastia), C. Cherbonnel (Laboratoire d’Analyses Génétiques Genindexe, La Rochelle), Fédération Départemental des Chasseurs de Charente-Maritime (Saint Jean d’Angély), R.S. Ceia (Sociedade Portuguesa para o Estudo das Aves, Lisboa), A. Gregoire (Centre d’Ecologie Fonctionnelle et Evolutive, Montpellier), and M. Nobili (Unité Mixte de Recherche, CNRS/UMII 5587, Montpellier). The authors are grateful to F.P. Frontini (University of Pisa, Italy) for his support in the laboratory work.
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Barbanera, F., Forcina, G., Cappello, A. et al. Introductions over introductions: the genomic adulteration of an early genetically valuable alien species in the United Kingdom. Biol Invasions 17, 409–422 (2015). https://doi.org/10.1007/s10530-014-0739-5
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DOI: https://doi.org/10.1007/s10530-014-0739-5