Abstract
Genetic introgression with exotic genomes represents a major conservation concern for the red-legged partridge (Alectoris rufa, Phasianidae). In particular, massive releases of chukar partridges (Alectoris chukar) and/or red-legged × chukar partridge hybrids for hunting purposes have cast serious doubts on the Italian present-day occurrence of wild A. rufa populations not affected by introgressive hybridization. This study investigates the genetic structure of red-legged partridges populations in two ecologically different areas in Northern Italy. Analysis of maternal mitochondrial DNA and biparental microsatellite markers excluded the presence of hybridization in a typical agricultural habitat where hunting and release of reared birds are strictly banned. By contrast, signs of chukar introgression were detected in a perifluvial habitat unusual for the red-legged partridge in Italy. The present study documents the first red-legged partridge population with no genetic evidences of recent chukar introgression presently living in Italy. We recommend that urgent conservation actions are taken to preserve the genetic integrity of this population from the risk of hybridization with farm-reared birds and to support its long-term conservation.
Similar content being viewed by others
References
Allendorf F, Luikart G (2007) Conservation and the genetics of populations. Blackwell, Malden
Allendorf FW, Leary RF, Spruell P, Wenburg JK (2001) The problems with hybrids: setting conservation guidelines. Trends Ecol Evol 16:613–622
Alonso ME, Pérez JA, Gaudioso VR, Díez C, Prieto R (2005) Study of survival, dispersal and home range of autumnreleased red-legged partridges (Alectoris rufa). Br Poul Sci 46:401–406
Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ (1990) Basic local alignment search tool. J Mol Biol 215:403–410
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, Dessi-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, Khan AA, Panayides P, Hadjigerou P, Sokos C, Gombobaatar S, Samadi S, Khan BY, Tofanelli S, Paoli G, Dini F (2009) Human-mediated introgression of exotic chukar (Alectoris chukar, Galliformes) genes from East Asia into native Mediterranean partridges. Biol Invasions 11:333–348
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 the Corsican red-legged partridge: hybridization and management issues. J Zool 285:56–65
Barilani M, Bernard-Laurent A, Mucci N, Tabarroni C, Karkd S, Perez Garrido JA, Randi E (2007a) Hybridization 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
Barilani M, Sfougaris A, Giannakopoulos A, Mucci N, Tabarroni C, Randi E (2007b) Detecting introgressive hybridization in rock partridge populations (Alectoris graeca) in Greece through Bayesian admixture analyses of multilocus genotypes. Conserv Genet 8:343–354
Barton NH (2001) The role of hybridization in evolution. Mol Ecol 10:551–568
Beaumont MA, Rannala B (2004) The Bayesian revolution in genetics. Nat Rev Genet 5:251–261
Belkhir K, Borsa P, Chikhi L, Raufaste N, Bonhomme F (1996–2004) GENETIX 4.05, logiciel sous Windows TM pour la génétique des populations. Laboratoire Genome, Populations, Interactions, CNRS UMR 5000, Universite de Montpellier II Montpellier, France. Available from http://kimura.univ-montp2.fr/genetix/
Bernard-Laurent A (1984) Hybridation naturelle entre Perdrix bartavelle (Alectoris graeca saxatilis) et Perdrix rouge (Alectoris rufa rufa) dans les Alpes-Maritimes. Gibier Faune Sauvage 2:79–96
Bernard-Laurent A, Auliac P, Douvre P, Guillet D, Normand F, Roche P, Sibut P, Toja S (2001) Risques de pollution génétique des populations de perdrix bartavelle: Bilan d’une enquête sur les lâchers de perdrix rouge dans les Alpes Francaises. Gibier Faune Sauvage 254:10–15
Blanco-Aguiar JA, Virgós E, Villafuerte R (2003) Perdiz roja (Alectoris rufa). In: Martí R, del Moral JC (eds) Atlas de las aves reproductoras de Espana. DGCoNa-SEO, Madrid, pp 212–213
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
Boano G, Pulcher C (2003) Check list degli Uccelli di Piemonte e Val d’Aosta aggiornata al dicembre 2000
Brichetti P, Fracasso G (2004) Ornitologia Italiana. Vol. 2, Tetraonidae-Scolopacidae. Alberto Perdisa Ed., Bologna
Burke JM, Arnold ML (2001) Genetics and the fitness of hybrids. Annu Rev Genet 35:31–52
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, Sanchez-Barbudo I, Davila JA, Vinuela J (2012) Fitness consequences of anthropogenic hybridization in wild red-legged partridge (Alectoris rufa, Phasianidae) populations. Biol Invasions 14:295–305
Cramp S, Simmons KEL (1980) The birds of the Western Palearctic, vol. II. Oxford University Press, Oxford
DeHaan P, Schwabe L, Ardren W (2010) Spatial patterns of hybridization between bull trout, Salvelinus confluentus, and brook trout, Salvelinus fontinalis in an Oregon stream network. Conserv Genet 11:935–949
Dragoev V (1974) On the population of the rock partridge (Alectoris graeca Meisner) in Bulgaria and methods of census. Acta Ornithol 14:251–255
Evanno G, Regnault S, Goudet J (2005) Detecting the number of clusters of individuals using the software. Mol Ecol 14(8):2611–2620
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
Excoffier L, Laval G, Schneider S (2005) Arlequin ver. 3.0: an integrated software package for population genetics data analysis. Evol Bio Online 1:47–50
Falush D, Stephens M, Pritchard JK (2003) Inference of population structure using multilocus genotype data: linked loci and correlated allele frequencies. Genet 164:1567–1587
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 the Iberian glacial refugium. Mol Ecol 20:2628–2642
Ford MJ (2002) Selection in captivity during supportive breeding may reduce fitness in the wild. Conserv Biol 16:815–825
Frankham R (2008) Genetic adaptation to captivity in species conservation programs. Mol Ecol 17:325–333
Goudet J (2001) FSTAT, a program to estimate and test gene diversities and fixation indices (version 2.9.3). Available from http://www2.unil.ch/popgen/softwares/fstat.htm. Updated from Goudet (1995)
Grant PR, Grant RB (1992) Hybridization of bird species. Science 256:193–197
Guerrini M, Barbanera (2009) Noninvasive genotyping of the red-legged partridge (Alectoris rufa, Phasianidae): semi-nested PCR of mitochondrial DNA from feces. Biochem Genet 47:873–883
Hall TA (1999) BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symp Ser 41:95–98
Jiguet F, Devictor V, Ottvall R, Van Turnhout C, Van der Jeugd H, Lindström Å (2010) Bird population trends are linearly affected by climate change along species thermal ranges. Proc R Soc B 277:3601–3608
Johnsgard PA (1988) The quails, partridges, and francolins of the world. Oxford University Press, New York
Kalinowski ST (2005) HP-RARE 1.0: a computer program for performing rarefaction on measures of allelic richness. Mol Ecol Notes 5:187–189
Keane A, de Brooke ML, McGowan PJK (2005) Correlates of extinction risk and hunting pressure in gamebirds (Galliformes). Biol Conserv 126:216–233
Khromov-Borisov NN, Rogozin IB, Henriques JAP, de Serres FJ (1999) Similarity pattern analysis in mutational distributions. Mutat Res 163:55–74
Koskinen MT, Hirvonen H, Landry PA, Primmer CR (2004) The benefits of increasing the number of microsatellites utilized in genetic population studies: an empirical perspective. Hereditas 141:61–67
Latch EK, Harveson LA, King JS, Hobson MD, Rhodes OE (2006) Assessing hybridization in wildlife populations using molecular markers: a case study in wild turkeys. J Wildl Manag 70:485–492
Librado P, Rozas J (2009) DnaSP v5: A software for comprehensive analysis of DNA polymorphism data. Bioinformatics 25:1451–1452
Longmire JL, Maltbie M, Baker RJ (1997) Use of “lysis buffer” in DNA isolation and its implication for museum collections. Occasional Papers. Mus Texas Tech Univ 163:1–4
Lucchini V, Randi E (1998) Mitochondrial DNA sequence variation and phylogeographical structure of rock partridge (Alectoris graeca) populations. Heredity 81:528–536
Mack RN, Simberloff D, Lonsdale WM, Evans H, Clout M, Bazzaz FA (2000) Biotic invasions: causes, epidemiology, global consequences, and control. Ecol Appl 10:689–710
Mallet J (2005) Hybridization as an invasion of the genome. Trends Ecol Evol 20:229–237
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
McCarthy EM (2006) Handbook of avian hybrids of the world. Oxford Uni. Press, Oxford
McKinney ML, Lockwood JL (1999) Biotic homogenization: a few winners replacing many losers in the next mass extinction. Tree 14:450–453
Meriggi A, Mazzoni della Stella R (2004) Dynamics of a reintroduced population of red-legged partridges Alectoris rufa in central Italy. Wildl Biol 10:1–9
Meriggi A, Mazzoni della Stella R, Brangi A, Ferloni M, Masseroni E, Merli E, Pompilio L (2007) The reintroduction of grey and red-legged partridges (Perdix perdix and Alectoris rufa) in central Italy: a metapopulation approach. Ital J Zool 74:215–237
Millais JG (1894) Game birds and shooting-sketches illustrating the habits, modes of capture, stages of plumage and the hybrids and varieties which occur amongst them. Henry, London
Mooney HA, Cleland EE (2001) The evolutionary impact of invasive species. Proc Nat Acad Sci USA 98:5446–5451
Morin PA, Luikart G, Wayne RK, the SNP workshop group (2004) SNPs in ecology, evolution and conservation. Trends Ecol Evol 19:208–216
Negro JJ, Torres MJ, Godoy JA (2001) RAPD analysis for detection and eradication of hybrid partridges (Alectoris rufa × A. graeca) in Spain. Biol Conserv 98:19–24
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
Pellegrino I (2011) Filogeografia e analisi della variabilità genetica in popolazioni naturali di Athene noctua a Alectoris rufa. PhD thesis. University of Piemonte Orientale, Italy
Pérez JA, Alonso ME, Gaudioso VR, Olmedo JA, Díez C, Bartolomé D (2004) Use of radiotracking techniques to study a summer repopulation with red-legged partridge (Alectoris rufa) chicks. Poult Sci 86:882–888
Pérez JA, Alonso ME, Prieto R, Bartolomé D, Gaudioso VR (2010) Influence of the breeding system on the escape response of red-legged partridges (Alectoris rufa). Poult Sci 89:5–12
Porkert J, Solheim R, Flor A (1997) Behaviour of hybrid male Tetrao tetrix males × T. urogallus females on black grouse leks. Wildl Biol 3:169–176
Potts GR (1989) The impact of releasing hybrid partridges on wild red-legged populations. The Game Conservancy Annual Review, 81–85
Pritchard JK, Stephens M, Donnelly PJ (2000) Inference of population Structure using multilocus genotype data. Genetics 155:945–959
Quintela M, Thulin CG, Höglund J (2010) Detecting hybridization between willow grouse (Lagopus lagopus) and rock ptarmigan (L. muta) in central Sweden through Bayesian admixture analyses and mtDNA screening. Conserv Genet 11:557–569
Randi E (2005) Management of wild ungulate populations in Italy: captive-breeding, hybridization and genetic consequences of translocations. Vet Res Commun 29:71–75
Randi E (2008) Detecting hybridization between wild species and their domesticated relatives. Mol Ecol 17:285–293
Randi E, Bernard-Laurent A (1999) Population genetics of a hybrid zone between the red-legged partridge and rock partridge. Auk 116:324–337
Randi E, Lucchini V (1998) Organisation and evolution of the mitochondrial DNA control-region in the avian genus Alectoris. J Mol Evol 47:449–462
Randi E, Tabarroni C, Rimondi S, Lucchini V, Sfougaris A (2003) Phylogeography of the rock partridge (Alectoris graeca). Mol Ecol 12:2201–2214
Rice WR (1989) Analysing tables of statistical tests. Evolution 43:223–225
Romagosa CM, Guyer C, Wooten MC (2009) Contribution of the live-vertebrate trade toward taxonomic homogenization. Conserv Biol 23:1001–1007
Scandura M, Iacolina L, Apollonio M, Dessì-Fulgheri F, Baratti M (2010) Current status of the Sardinian partridge (Alectoris barbara) assessed by molecular markers. Eur J Wild Res 56:33–42
Seehausen O (2004) Hybridization and adaptive radiation. Trends Ecol Evol 19:198–207
Sevane N, Cortés O, Garcĺa D, Cañón J, Dunner S (2009) New single nucleotide polymorphisms in Alectoris identified using chicken genome information allow Alectoris introgression detection. Mol Ecol Res 10:205–213
Sokos CK, Birtsas PK, Tsachalidis EP (2009) The aims of galliforms release and choice of techniques. Wildl Biol 14:412–422
Solberg EJ, Jensen H, Ringsby TH, Sæther BE (2006) Fitness consequences of hybridization between house sparrows (Passer domesticus) and tree sparrows (P. montanus). J Ornithol 147:504–506
Spagnesi M, Serra L (2004) Uccelli d‘Italia. Quad. Cons. Natura, 21. Min. Ambiente. Ist. Naz. Fauna Selvatica
Spanò S (2010) La Pernice Rossa, ed. Il Piviere, Gavi
Spanò S, Traverso G, Truffi G, Zacchetti D (1987) La pernice rossa Alectoris rufa (L.) in Italia. Boll Mus Ist Biol Univ Genova 53:5–33
Tejedor MT, Monteagudo LV, Mautner S, Hadjisterkotis E, Arruga MV (2007) Introgression of Alectoris chukar genes into a Spanish wild Alectoris rufa population. J Hered 98:179–182
Tejedor MT, Monteagudo LV, Arruga MV (2008) Microsatellite markers for the analysis of genetic variability and relatedness in red-legged partridge (Alectoris rufa) farms in Spain. Res Vet Sci 85:62–67
Templeton AR (1986) Coadaptation and outbreeding depression. In: ME Soulé (eds) Conservation biology: the science of scarcity and diversity. Sinauer: Sunderland, MA. pp 105–116
Thomas CD, Cameron A, Green RE, Bakkenes M, Beaumont LJ, Collingham YC, Erasmus BFN, de Siqueira MF, Grainger A, Hannah L, Hughes L, Huntley B, van Jaarsveld AS, Midgley GF, Miles L, Ortega-Huerta MA, Townsend Peterson A, Phillips OL, Williams SE (2004) Extinction risk from climate change. Nature 427:145–148
Tizzani P, Negri E, Silvano F, Malacarne G, Meneguz PG (2012) Does the use of playback affect the estimated numbers of red-legged partridge Alectoris rufa? Anim Biodivers Conserv 35(2):429–435
Vähä J-P, Primmer CR (2006) Efficiency of model based Bayesian methods for detecting hybrid individuals under different hybridization scenarios and with different number of loci. Mol Ecol 15:63–72
Väli Ü, Dombrovski V, Treinys R, Bergmanis U, Daróczi SJ, Dravecky M, Ivanovski V, Lontkowski J, Maciorowski G, Meyburg BU, Mizera T, Zeitz R, Ellegren H (2010) Widespread hybridization between the Greater Spotted Eagle Aquila clanga and the Lesser Spotted Eagle Aquila pomarina (Aves: Accipitriformes) in Europe. Biol J Linn Soc 100:725–736
Vallance M, Queney G, Soyez D, Ricci JC (2006) Mise au point et validation d'un système de marqueurs génétiques pour les perdrix hybrides. Rapport scientifique, ONCFS: 76–81
VV.AA (2007) Linne guida per l’immissione di specie faunistiche. Quad. Cons. Natura 27, Min. Ambiente-Ist. Naz. Fauna Selvatica
Wahlund S (1928) Zusammensetzung von Populationen und Korrelationserscheinungen vom Standpunkt der Vererbungslehre aus betrachtet. Hereditas 11:65–106
Williams CL, Brust RC, Fendley TT, Tiller GR, Rhodes OE (2005) A comparison of hybridization between Mottled Ducks (Anas fulvigula) and Mallards (A. platyrhynchos) in Florida and South Carolina using microsatellite DNA analysis. Conserv Genet 6:445–453
Woodworth LM, Montgomery ME, Briscoe DA, Frankham R (2002) Rapid genetic deterioration in captive populations: causes and conservation implications. Conserv Genet 3:277–288
Wright S (1965) The interpretation of population structure by F statistics with special regards to systems of mating. Evolution 19:395–420
Acknowledgments
We are very grateful to F. Silvano (Natural History Museum of Stazzano, Alessandria, Italy), E. Negri (Associazione Ambiente Territorio e Formazione, Alessandria), A. Repetto, and E. Migliora without whom collaboration field operations would not have been possible. Authors also thank M. Brustia for help during laboratory analyses and M. Cucco for having provided useful comments on an early draft of the manuscript. The study was supported by ATF (Agenzia Ambiente Territorio e Formazione, Alessandria) and MIUR60 grants.
Author information
Authors and Affiliations
Corresponding author
Additional information
Communicated by C. Gortázar
Alessandro Negri and Irene Pellegrino contributed equally to this work.
Rights and permissions
About this article
Cite this article
Negri, A., Pellegrino, I., Mucci, N. et al. 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 (2013). https://doi.org/10.1007/s10344-012-0686-3
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10344-012-0686-3