Individual genetic diversity correlates with the size and spatial isolation of natal colonies in a bird metapopulation

Proceedings of the Royal Society B: Biological Sciences

Volumn 275, Issue 1646, 2008, Pages 2039-2047

  Ortego, Joaquín ^a,b   Aparicio, José Miguel ^a   Cordero, Pedro J ^a   Calabuig, Gustau ^a  

^a INSTITUTO DE INVESTIGACIÓN EN RECURSOS CINEGÉTICOS IREC CSIC UCLM JCCM   (Spain)

^b MUSEO NACIONAL DE CIENCIAS NATURALES   (Spain)

Author keywords

Dispersal; Falco naumanni; Genetic diversity; Immigration; Population isolation; Population size

Indexed keywords

BIRD; DISPERSAL; GENE FLOW; GENETIC DIFFERENTIATION; GENETIC MARKER; HETEROZYGOSITY; IMMIGRATION; ISOLATED POPULATION; MARK-RECAPTURE METHOD; METAPOPULATION; MIGRATORY SPECIES; POPULATION SIZE; POPULATION STRUCTURE;

ANIMAL EXPERIMENT; ARTICLE; BIRD; CORRELATION ANALYSIS; GENE FLOW; GENETIC VARIABILITY; HETEROZYGOSITY; IMMIGRATION; METAPOPULATION; MICROSATELLITE MARKER; NONHUMAN; POPULATION DISPERSION; POPULATION DISTRIBUTION; POPULATION DYNAMICS; POPULATION ISOLATION; POPULATION SIZE; POPULATION STRUCTURE; PRIORITY JOURNAL;

AVES; FALCO NAUMANNI; VERTEBRATA;

EID: 47249113818     PISSN: 09628452     EISSN: 14712970     Source Type: Journal    
DOI: 10.1098/rspb.2008.0475     Document Type: Article

References (70)

1. Acevedo-Whitehouse, K., Gulland, F., Greig, D. & Amos, W. 2003 Disease susceptibility in California sea lions. Nature 422, 35. (doi:10.1038/422035a)
2. Acevedo-Whitehouse, K., Spraker, T. R., Lyons, E., Melin, S. R., Gulland, F., Delong, R. L. & Amos, W. 2006 Contrasting effects of heterozygosity on survival and hookworm resistance in California sea lion pups. Mol. Ecol. 15, 1973-1982. (doi:10.1111/j.1365-294X.2006.02903.x)
3. Amos, W. & Balmford, A. 2001 When does conservation genetics matter? Heredity 87, 257-265. (doi:10.1046/j.1365-2540.2001.00940.x)
4. Amos, W. & Harwood, J. 1998 Factors affecting levels of genetic diversity in natural populations. Phil. Trans. R. Soc. B 353, 177-186. (doi:10.1098/rstb.1998.0200)
5. Andersen, L. W., Fog, K. & Damgaard, C. 2004 Habitat fragmentation causes bottlenecks and inbreeding in the European tree frog (Hyla arborea). Proc. R. Soc. B 271, 1293-1302. (doi:10.1098/rspb.2004.2720)
6. Aparicio, J. M., Ortego, J. & Cordero, P. J. 2006 What should we weigh to estimate heterozygosity, alleles or loci? Mol. Ecol. 15, 4659-4665. (doi:10.1111/j.1365-294X.2006.03111.x)
7. Aparicio, J. M., Bonal, R. & Munoz, A. 2007 Experimental test on public information use in the colonial lesser kestrel. Evol. Ecol. 21, 783-800. (doi:10.1007/s10682-006-9151-7)
8. Balloux, F., Amos, W. & Coulson, T. 2004 Does heterozygosity estimate inbreeding in real populations? Mol. Ecol. 13, 3021-3031. (doi:10.1111/j.1365-294X.2004.02318.x)
9. Bazin, E., Glemin, S. & Galtier, N. 2006 Population size does not influence mitochondrial genetic diversity in animals. Science 312, 570-572. (doi:10.1126/science.1122033)
10. Bonal, R. & Aparicio, J. M. 2001 Utilización del hábitat por el cernícalo primilla (Falco naumanni) en La Mancha. In Biología y conservación del cernícalo primilla (eds J. F. Garces & M. Corroto), pp. 53-63. Madrid, Spain: Consejería de Medio Ambiente de la Comunidad de Madrid.
11. Bowler, D. E. & Benton, T. G. 2005 Causes and consequences of animal dispersal strategies: relating individual behaviour to spatial dynamics. Biol. Rev. 80, 205-225. (doi:10.1017/S1464793104006645)
12. Calabuig, G., Ortego, J., Aparicio, J. M. & Cordero, P. J. 2008 Public information in selection of nesting colony by lesser kestrels: which cues are used and when are they obtained? Anim. Behav. 75, 1611-1617. (doi:10.1016/j.anbehav.2007.10.022)
13. Charlesworth, D. & Charlesworth, B. 1987 Inbreeding depression and its evolutionary consequences. Annu. Rev. Ecol. Evol. Syst. 18, 237-268. (doi:10.1146/annurev.es.18.110187.001321)
14. Dixon, J. D., Oli, M. K., Wooten, M. C., Eason, T. H., Mccown, J. W. & Cunningham, M. W. 2007 Genetic consequences of habitat fragmentation and loss: the case of the Florida black bear (Ursus americanus floridanus). Conserv. Gen. 8, 455-464. (doi:10.1007/s10592-006-9184-z)
15. Falconer, D. S. & Mackay, T. F. C. 1996 Introduction to quantitative genetics, 3rd edn. Harlow, UK: Longman.
16. Frankham, R. 1995 Inbreeding and extinction - a threshold effect. Conserv. Biol. 9, 792-799. (doi:10.1046/j.1523-1739.1995.09040792. x)
17. Frankham, R. 1996 Relationship of genetic variation to population size in wildlife. Conserv. Biol. 10, 1500-1508. (doi:10.1046/j.1523-1739. 1996.10061500.x)
18. Frankham, R. 1997 Do island populations have less genetic variation than mainland populations? Heredity 78, 311-327.
19. Frankham, R. 2005 Genetics and extinction. Biol. Conserv. 126, 131-140. (doi:10.1016/j.biocon.2005.05.002)
20. García-Ramos, G. & Kirkpatrick, M. 1997 Genetic models of adaptation and gene flow in peripheral populations. Evolution 51, 21-28. (doi:10.2307/2410956)
21. Gilpin, M. 1991 The genetic efective size of a metapopulation. Biol. J. Linn. Soc. 42, 165-175. (doi:10.1111/j.1095-8312.1991.tb00558.x)
22. Groombridge, J. J., Jones, C. G., Bruford, M. W. & Nichols, R. A. 2000 Conservation biology - 'Ghost' alleles of the Mauritius kestrel. Nature 403, 616. (doi:10.1038/35001148)
23. Hailer, F. et al. 2006 Bottlenecked but long-lived: high genetic diversity retained in white-tailed eagles upon recovery from population decline. Biol. Lett. 2, 316-319. (doi:10.1098/rsbl.2006.0453)
24. Hanfling, B. & Brandl, R. 1998 Genetic variability, population size and isolation of distinct populations in the freshwater fish Cottus gobio L. Mol. Ecol. 7, 1625-1632. (doi:10.1046/j.1365-294x.1998.00465. x)
25. Hanski, I. 1998 Metapopulation dynamics. Nature 396, 41-49. (doi:10.1038/23876)
26. Hansson, B., Bensch, S., Hasselquist, D., Lillandt, B. G., Wennerberg, L. & von Schantz, T. 2000 Increase of genetic variation over time in a recently founded population of great reed warblers (Acrocephalus arundinaceus) revealed by microsatellites and DNA fingerprinting. Mol. Ecol. 9, 1529-1538. (doi:10.1046/j.1365-294x.2000.01028.x)
27. Harper, G. L., Maclean, N. & Goulson, D. 2003 Microsatellite markers to assess the influence of population size, isolation and demographic change on the genetic structure of the UK butterfly Polyommatus bellargus. Mol. Ecol. 12, 3349-3357. (doi:10.1016/j.biocon.2005.05.002)
28. Hedrick, P. W. 1996 Bottleneck(s) or metapopulation in cheetahs. Conserv. Biol. 10, 897-899. (doi:10.1046/j.1523-1739.1996. 10030897.x)
29. Hedrick, P. W. 2000 Genetics of populations. Sudbury, Canada: Jones and Bartlett Publishers.
30. Hoffman, J. I., Boyd, I. L. & Amos, W. 2004 Exploring the relationship between parental relatedness and male reproductive success in the Antarctic fur seal Arctocephalus gazella. Evolution 58, 2087-2099. (doi:10.1554/04-099)
31. Hoglund, J., Larsson, J. K., Jansman, H. A. H. & Segelbacher, G. 2007 Genetic variability in European black grouse (Tetrao tetrix). Conserv. Gen. 8, 239-243. (doi:10.1007/s10592-006-9158-1)
32. Hutchison, D. W. 2003 Testing the central/peripheral model: analyses of microsatellite variability in the eastern collared lizard (Crotaphytus collaris collaris). Am. Midland Nat. 149, 148-162. (doi:10.1674/0003-0031(2003)149[0148:TTCPMA]2.0.CO;2)
33. Kaeuffer, R., Coltman, D. W., Chapuis, J. L., Pontier, D. & Reale, D. 2007 Unexpected heterozygosity in an island mouflon population founded by a single pair of individuals. Proc. R. Soc. B 274, 527-533. (doi:10.1098/rspb.2006.3743)
34. Kirkpatrick, M. & Barton, N. H. 1997 Evolution of a species' range. Am. Nat. 150, 1-23. (doi:10.1086/286054)
35. Krackow, S. & Tkadlec, E. 2001 Analysis of brood sex ratios: implications of offspring clustering. Behav. Ecol. Sociobiol. 50, 293-301. (doi:10.1007/s002650100366)
36. Lammi, A., Siikamaki, P. & Mustajarvi, K. 1999 Genetic diversity, population size, and fitness in central and peripheral populations of a rare plant Lychnis viscaria. Conserv. Biol. 13, 1069-1078. (doi:10.1046/j.1523-1739.1999.98278.x)
37. Levins, R. 1969 Some demographic and genetic consequences of environmental heterogeneity for biological control. Bull. Entomol. Soc. Am. 15, 237-240.
38. Madsen, T., Shine, R., Olsson, M. & Wittzell, H. 1999 Conservation biology - restoration of an inbred adder population. Nature 402, 34-35. (doi:10.1038/46941)
39. Markert, J. A., Grant, P. R., Grant, B. R., Keller, L. F., Coombs, J. L. & Petren, K. 2004 Neutral locus heterozygosity, inbreeding, and survival in Darwin's ground finches (Geospiza fortis and G. scandeus). Heredity 92, 306-315. (doi:10.1038/sj.hdy.6800409)
40. Negro, J. J., Hiraldo, F. & Donazar, J. A. 1997 Causes of natal dispersal in the lesser kestrel: inbreeding avoidance or resource competition? J. Anim. Ecol. 66, 640-648. (doi:10.2307/5917)
41. Nesje, M., Roed, K. H., Lifjeld, J. T., Lindberg, P. & Steen, O. F. 2000 Genetic relationships in the peregrine falcon (Falco peregrinus) analysed by microsatellite DNA markers. Mol. Ecol. 9, 53-60. (doi:10.1046/j.1365-294x.2000.00834.x)
42. Nevo, E., Bieles, A. & Ben-Shlomo, R. 1984 The evolutionary significance of genetic diversity: ecological, demographic and life history correlates. In Evolutionary dynamics of genetic diversity (ed. G. S. Mani), pp. 13-213. Berlin, Germany: Springer.
43. Nieminen, M., Singer, M. C., Fortelius, W., Schops, K. & Hanski, I. 2001 Experimental confirmation that inbreeding depression increases extinction risk in butterfly populations. Am. Nat. 157, 237-244. (doi:10.1086/318630)
44. Ortego, J., Aparicio, J. M., Calabuig, G. & Cordero, P. J. 2007a Risk of ectoparasitism and genetic diversity in a wild lesser kestrel population. Mol. Ecol. 16, 3712-3720. (doi:10.1111/j.1365- 294X.2007.03406.x)
45. Ortego, J., Calabuig, G., Cordero, P. J. & Aparicio, J. M. 2007b Egg production and individual genetic diversity in lesser kestrels. Mol. Ecol. 16, 2383-2392. (doi:10.1111/j.1365-294X.2007.03322.x)
46. Ortego, J., Aparicio, J. M., Calabuig, G. & Cordero, P. J. 2007c Increase of heterozygosity in a growing population of lesser kestrels. Biol. Lett. 3, 585-588. (doi:10.1098/rsbl.2007.0268)
47. Ortego, J., Gonzalez, E. G., Sanchez-Barbudo, I., Aparicio, J. M. & Cordero, P. J. 2007d New highly polymorphic loci and cross-amplified microsatellites for the lesser kestrel Falco naumanni. Ardeola 54, 101-108.
48. Ortego, J., Calabuig, G., Aparicio, J. M. & Cordero, P. J. 2008 Genetic consequences of natal dispersal in the colonial lesser kestrel. Mol. Ecol. 17, 2051-2059. (doi:10.1111/j.1365-294X.2008.03719.x)
49. Pemberton, J. 2004 Measuring inbreeding depression in the wild: the old ways are the best. Trends Ecol. Evol. 19, 613-615. (doi:10.1016/j.tree.2004.09.010)
50. Pritchard, J. K., Stephens, M. & Donnelly, P. 2000 Inference of population structure using multilocus genotype data. Genetics 155, 945-959.
51. Rowe, G., Beebee, T. J. C. & Burke, T. 1999 Microsatellite heterozygosity, fitness and demography in natterjack toads Bufo calamita. Anim. Conserv. 2, 85-92. (doi:10.1111/j.1469-1795.1999.tb00053.x)
52. Saccheri, I., Kuussaari, M., Kankare, M., Vikman, P., Fortelius, W. & Hanski, I. 1998 Inbreeding and extinction in a butterfly metapopulation. Nature 392, 491-494. (doi:10.1038/33136)
53. SAS Institute 2004 SAS/STAT 9.1 user's guide. Cary, NC: SAS Institute Inc.
54. Segelbacher, G., Hoglund, J. & Storch, I. 2003 From connectivity to isolation: genetic consequences of population fragmentation in capercaillie across Europe. Mol. Ecol. 12, 1773-1780. (doi:10.1046/j.1365-294X. 2003.01873.x)
55. Seppa, P. & Laurila, A. 1999 Genetic structure of island populations of the anurans Rana temporaria and Bufo bufo. Heredity 82, 309-317. (doi:10.1038/sj.hdy.6884900)
56. Serrano, D. & Tella, J. L. 2003 Dispersal within a spatially structured population of lesser kestrels: the role of spatial isolation and conspecific attraction. J. Anim. Ecol. 72, 400-410. (doi:10.1046/j.1365-2656.2003.00707.x)
57. Serrano, D., Tella, J. L., Forero, M. G. & Donazar, J. A. 2001 Factors affecting breeding dispersal in the facultatively colonial lesser kestrel: individual experience vs. conspecific cues. J. Anim. Ecol. 70, 568-578. (doi:10.1046/j.1365-2656.2001.00512.x)
58. Serrano, D., Forero, M. G., Donazar, J. A. & Tella, J. L. 2004 Dispersal and social attraction affect colony selection and dynamics of lesser kestrels. Ecology 85, 3438-3447. (doi:10.1890/04-0463)
59. Singer, J. D. 1998 Using SAS PROC MIXED to fit multilevel models, hierarchical models, and individual growth models. J. Educat. Behav. Stat. 23, 323-355.
60. Slatkin, M. 1993 Isolation by distance in equilibrium and nonequilibrium populations. Evolution 47, 264-279. (doi:10.2307/2410134)
61. Soulè, M. E. 1976 Allozyme variation, its determinants in space and time. In Molecular evolution (ed. F. J. Ayala), pp. 60-77. Sunderland, MA: Sinauer Associates.
62. Spielman, D., Brook, B. W. & Frankham, R. 2004 Most species are not driven to extinction before genetic factors impact them. Proc. Natl Acad. Sci. USA 101, 15 261-15 264. (doi:10.1073/pnas.0403809101)
63. Swart, M. K. J., Ferguson, J. W. H., Dutoit, R. & Flamand, J. R.B. 1994 Substantial genetic-variation in southern African black rhinoceros (Diceros bicornis). J. Hered. 85, 261-266.
64. Taylor, S. S., Jamieson, I. G. & Wallis, G. P. 2007 Historic and contemporary levels of genetic variation in two New Zealand passerines with different histories of decline. J. Evol. Biol. 20, 2035-2047. (doi:10.1111/j.1420-9101.2007.01362.x)
65. Vucetich, J. A. & Waite, T. A. 2003 Spatial patterns of demography and genetic processes across the species' range: null hypotheses for landscape conservation genetics. Conserv. Gen. 4, 639-645. (doi:10.1023/A:1025671831349)
66. Westemeier, R. L., Brawn, J. D., Simpson, S. A., Esker, T. L., Jansen, R. W., Walk, J. W., Kershner, E. L., Bouzat, J. L. & Paige, K. N. 1998 Tracking the long-term decline and recovery of an isolated population. Science 282, 1695-1698. (doi:10.1126/science.282.5394.1695)
67. White, T. A. & Searle, J. B. 2007 Genetic diversity and population size: island populations of the common shrew, Sorex araneus. Mol. Ecol. 16, 2005-2016. (doi:10.1111/j.1365-294X.2007.03296.x)
68. Whiteman, N. K., Matson, K. D., Bollmer, J. L. & Parker, P. G. 2006 Disease ecology in the Galapagos hawk (Buteo galapagoensis): host genetic diversity, parasite load and natural antibodies. Proc. R. Soc. B. 273, 797-804. (doi:10.1098/rspb.2005.3396)
69. Willi, Y., Van Buskirk, J. & Hoffmann, A. A. 2006 Limits to the adaptive potential of small populations. Annu. Rev. Ecol. Evol. Syst. 37, 433-458. (doi:10.1146/annurev.ecolsys.37.091305.110035)
70. Wright, S. 1943 Isolation by distance. Genetics 28, 139-156.