Using major histocompatibility complex markers to assign the geographic origin of migratory birds: Examples from the threatened lesser kestrel

Animal Conservation

Volumn 14, Issue 3, 2011, Pages 306-313

  Rodriguez A ^a   Alcaide, M ^b   Negro, J J ^a   Pilard, P ^c  

^a DEPARTMENT OF CONSERVATION BIOLOGY   (Spain)

^b HARVARD UNIVERSITY   (United States)

^c LPO Mission Rapaces   (France)

Author keywords

Intrinsic marker; Major histocompatibility complex; Migratory connectivity; Migratory stopover; Non invasive sampling

Indexed keywords

BREEDING POPULATION; CONSERVATION MANAGEMENT; GENETIC DIFFERENTIATION; MIGRATORY SPECIES; POLYMORPHISM; SPECIES CONSERVATION; STOPOVER; WADER;

SENEGAL; SOUTH AFRICA;

AVES; FALCO NAUMANNI;

EID: 79957561559     PISSN: 13679430     EISSN: 14691795     Source Type: Journal    
DOI: 10.1111/j.1469-1795.2010.00431.x     Document Type: Article

References (56)

1. Anmarkrud, J.A., Johnsen, A., Bachmann, L. & Lifjeld, J.T. (2010). Ancestral polymorphism in exon 2 of bluethroat (Luscinia svecica) MHC class II B genes. J. Evol. Biol. 23, 1206-1217.
2. Alcaide, M. (2010). On the relative roles of selection and genetic drift shaping MHC variation. Mol. Ecol. 19, 3842-3844.
3. Alcaide, M., Edwards, S.V., Cadahía, L. & Negro, J.J. (2009). MHC class I genes of birds of prey: isolation, polymorphism and diversifying selection. Conserv. Genet. 10, 1349-1355.
4. Alcaide, M., Edwards, S.V. & Negro, J.J. (2007). Characterization, polymorphism and evolution of MHC class II B genes in birds of prey. J. Mol. Evol. 65, 541-554.
5. Alcaide, M., Edwards, S.V., Negro, J.J., Serrano, D. & Tella, J.L. (2008). Extensive polymorphism and geographical variation at a positively selected MHC class IIB gene of the lesser kestrel (Falco naumanni). Mol. Ecol. 17, 2652-2665.
6. Alcaide, M., Lemus, J.A., Blanco, G., Tella, J.L., Serrano, D., Negro, J.J., Rodríguez, A. & García-Montijano, M. (2010). MHC diversity and differential exposure to pathogens in kestrels (Aves: Falconidae). Mol. Ecol. 19, 691-705.
7. Babik, W. (2010). Methods for MHC genotyping in non-model vertebrates. Mol. Ecol. Res. 10, 237-251.
8. Ballard, J.W.O. & Whitlock, M.C. (2004). The incomplete natural history of mitochondria. Mol. Ecol. 13, 729-744.
9. Banguera-Hinestroza, E., Cárdenas, H., Ruiz-García, M., Marmontel, M., Gaitán, E., Váquez, R. & García-Vallejo, F. (2002). Molecular identification of evolutionarily significant units in the Amazon River dolphin Inia sp (Cetacea: Iniidae). J. Hered. 93, 312-322.
10. Beacham, T.D., Candy, J.R., Supernault, K.J., Ming, T., Deagle, B., Schulze, A., Tuck, D., Kaukinen, K.H., Irvine, J.R., Miller, K.M. & Withler, R.E. (2001). Evaluation and application of microsatellite and major histocompatibility complex variation for stock identification of coho salmon in British Columbia. Trans. Am. Fish. Soc. 130, 1116-1149.
11. Beacham, T.D., Lapointe, M., Candy, J.R., Miller, K.M. & Withler, R.E. (2004). DNA in action: rapid application of DNA variation to sockeye salmon fisheries management. Conserv. Genet. 5, 411-416.
12. BirdLife International. (2010). Falco naumanni. Birdlife species factsheet. Available at (1 March 2010).
13. Boulet, M. & Norris, D.R. (eds) (2006). Patterns of migratory connectivity in two Nearctic-Neotropical songbirds: new insights from intrinsic markers. Ornithological Monographs. Vol. 61. Washington: American Ornithologists' Union.
14. Burri, R., Niculita-Hirzel, H., Roulin, A. & Fumagalli, L. (2008). Isolation and characterization of major histocompatibility complex (MHC) class II B genes in the barn owl (Aves: Tyto alba). Immunogenetics 60, 543-550.
15. Canal, D., Alcaide, M., Anmarkrud, J.A. & Potti, J. (2010). Towards the simplification of MHC typing protocols: targeting classical MHC class II genes in a passerine, the pied flycatcher Ficedula hypoleuca. BMC Res. Notes 3, 236.
16. Coiffait, L., Redfern, C.P.F., Bevan, R.M., Newton, J. & Wolff, K. (2009). The use of intrinsic markers to study bird migration. Ring. Migrat. 24, 169-174.
17. Crawford, N.G. (2010). SMOGD: software for the measurement of genetic diversity. Mol. Ecol. Res. 10, 556-557.
18. Ekblom, R., Sæther, S.A., Jacobson, P., Fiske, P., Sahlman, T., Grahn, M., Kalas, J.A. & Höglund, J. (2007). Spatial patterns of MHC class II variation in the great snipe (Gallinago media). Mol. Ecol. 16, 1439-1451.
19. Faaborg, J., Holmes, R.T., Anders, A.D., Bildstein, K.L., Dugger, K.M., Gauthreaux, S.A., Heglund, P., Hobson, K.A., Jahn, A.E., Johnson, D.H., Latta, S.C., Levey, D.J., Marra, P.P., Merkord, C.L., Nol, E., Rothstein, S.I., Sherry, T.W., Sillett, T.S., Thompson, F.R. III & Warnock, N. (2010). Conserving migratory land birds in the new world: do we know enough? Ecol. Appl. 20, 398-418.
20. Hall, T.A. (1999). BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucl. Acids Symp. Ser. 41, 95-98.
21. Heim de Balsac, H. & Mayaud, N. (1962). Les oiseaux du nord ouest de L'Afrique: distribution geográphique, ecologie, migrations, reproduction. Paris: Ed. Paul Lechavalier.
22. Hobson, K.A. (2005). Stables isotopes and the determination of avian migratory connectivity and seasonal interactions. Auk 122, 1037-1048.
23. Horváth, M.B., Martinez-Cruz, B., Negro, J.J., Kalmar, L. & Godoy, J.A. (2005). An overlooked DNA source for non-invasive genetic analysis in birds. J. Avian Biol. 36, 84-88.
24. Hudson, R.R., Slatkin, M. & Maddison, W.P. (1992). Estimation of levels of gene flow from DNA sequence data. Genetics 132, 583-589.
25. Hurst, G.D.D. & Jiggins, F.M. (2005). Problems with mitochondrial DNA as a marker in population, phylogeographic and phylogenetic studies: the effects of inherited symbionts. Proc. Roy. Soc. B 272, 1525-1534.
26. ST and its relatives do not measure differentiation. Mol. Ecol. 17, 4015-4026.
27. Librado, P. & Rozas, J. (2009). DnaSP v5: a software for comprehensive analysis of DNA polymorphism data. Bioinformatics 25, 1451-1452.
28. Loiseau, C., Richard, M. & Garnier, S., Chastel, O., Julliard, R., Zoorob, R. & Sorci, G. (2009). Diversifying selection on MHC class I in the house sparrow (Passer domesticus). Mol. Ecol. 18, 1331-1340.
29. Lopes, R.J., Hortas, F. & Wennerberg, L. (2008). Geographical segregation in Dunlin Calidris alpina populations wintering along the East Atlantic migratory flyway - evidence from mitochondrial DNA analysis. Divers. Distrib. 14, 732-741.
30. Lovette, I.J., Clegg, S.M. & Smith, T.B. (2004). Limited utility of mtDNA markers for determining connectivity among breeding and overwintering locations in three neotropical migrant birds. Conserv. Biol. 18, 156-166.
31. LPO (2010). Ligue pour la Protection des Oiseaux. Dernieres nouvelles des faucons crecerellettes au Senegal. In: Faucon crecerellette. Ligue pour la Protection des Oiseaux. Available at (1 March 2010).
32. Manel, S., Gaggiotti, O.E. & Waples, R.S. (2005). Assignment methods: matching biological questions techniques with appropriate. Trends Ecol. Evol. 20, 136-142.
33. Mank, J.E. & Avise, J.C. (2003). Microsatellite variation and differentiation in North Atlantic eels. J. Hered. 94, 310-314.
34. Marra, P.P., Norris, D.R., Haig, S.M., Webster, M. & Royle, J.A. (2006). Migration connectivity. In Connectivity conservation: 157-183. Crooks, K.R. & Sanjayan, M. (Eds). New York: Cambridge University Press.
35. Mihoub, J-B., Gimenez, O., Pilard, P. & Sarrazin, F. (2010). Challenging conservation of migratory species: Sahelian rainfalls drive first-year survival of the vulnerable Lesser Kestrel Falco naumanni. Biol. Conserv. 143, 839-847.
36. Mindell, D.P. (ed.) (1997). Avian molecular evolution and systematics. San Diego: Academic Press.
37. MKP (2010). Migrating kestrel project. Available at (1 March 2010).
38. Moreau, R.E. (1972). The palearctic-African bird migration systems. London: Academic Press.
39. Newton, I. (2004). Population limitation in migrants. Ibis 146, 197-226.
40. van Oosterhout, C., Joyce, D.A., Cummings, S.M., Blais, J., Barson, N.J., Ramnarine, I.W., Mohammed, R.S., Persad, N. & Cable, J. (2006). Balancing selection, random genetic drift, and genetic variation at the major histocompatibility complex in two wild populations of guppies (Poecilia reticulata). Evolution 60, 2562-2574.
41. Perego, U.A., Achilli, A., Angerhofer, N., Accetturo, M., Pala, M., Olivieri, A., Kashani, B.H., Ritchie, K.H., Scozzari, R., Kong, Q.-P., Myres, N.M., Salas, A., Semino, O., Bandelt, H.-J. Woodward, S.R. & Torroni, A. (2009). Distinctive paleo-Indian migration routes from beringia marked by two rare mtDNA haplogroups. Curr. Biol. 19, 1-8.
42. Piertney, S.B. & Oliver, M.K. (2006). The evolutionary ecology of the major histocompatibility complex. Heredity 96, 7-21.
43. Piry, S., Alapetite, A., Cornuet, J.M., Paetkau, D., Baudouin, L. & Estoup, A. (2004). GENECLASS2: a software for genetic assignment and first-generation migrant detection. J. Hered. 95, 536-539.
44. Queney, G., Ferrand, N., Weiss, S., Mougel, F. & Monnerot, M. (2001). Stationary distributions of microsatellite loci between divergent population groups of the European rabbit (Oryctolagus cuniculus). Mol. Biol. Evol. 18, 2169-2121.
45. Rodríguez, A., Negro, J.J., Bustamante, J., Fox, J.W. & Afanasyev, V. (2009). Geolocators map the wintering grounds of threatened lesser kestrels in Africa. Divers. Distrib. 15, 1010-1016.
46. Rubinoff, D. & Holland, B.S. (2005). Between two extremes: mitochondrial DNA is neither the panacea nor the nemesis of phylogenetic and taxonomic inference. Syst. Biol. 54, 952-961.
47. Segelbacher, G. (2002). Noninvasive genetic analysis in birds: testing reliability of feather samples. Mol. Ecol. Notes 2, 367-369.
48. Sommer, S. (2005). The importance of immune gene variability in evolutionary ecology and evolution. Front. Zool. 2, 16.
49. Spurgin, L.G. & Richardson, D.S. (2010). How pathogens drive genetic diversity: MHC, mechanisms and misunderstandings. Proc. Roy. Soc. B 277, 979-988.
50. Stefanni, S. & Thorley, J.L. (2003). Mitochondrial DNA phylogeography reveals the existence of an Evolutionarily Significant Unit of the sand goby Pomatoschistus minutus in the Adriatic (Eastern Mediterranean). Mol. Phyl. Evol. 28, 601-609.
51. Stephens, M. & Donnelly, P. (2003). A comparison of Bayesian methods for haplotype reconstruction from population genotype data. Am. J. Hum. Genet. 73, 1162-1169.
52. Taberlet, P., Waits, L.P. & Luikart, G. (1999). Noninvasive genetic sampling: look before you leap. Trends Ecol. Evol. 14, 323-327.
53. Truett, G.E. (2006). Preparation of genomic DNA from animal tissues. In DNA sequencing II: optimizing preparation and cleanup: 33-46. Kieleczawa, J. (Ed). Sudbury: Jones and Bartlett.
54. Webster, M.S., Marra, P.P., Haig, S.M., Bensch, S. & Holmes, R.T. (2002). Links between worlds: unravelling migratory connectivity. Trends Ecol. Evol. 17, 76-83.
55. Wink, M. (2006). Use of DNA markers to study bird migration. J. Ornithol. 147, 234-244.
56. Wink, M., Sauer-Gürth, H. & Pepler, D. (2004). Phylogeographic relationships of the Lesser Kestrel (Falco naumanni) in breeding and wintering quarters inferred from nucleotide sequences of the mitochondrial cytochrome b gene. In Raptors worldwide. Chancelor, R.D. & Meyburg, B.-U. (Eds). Berlin: WWGBP.