Heterozygosity-Fitness Correlations and Inbreeding Depression in Two Critically Endangered Mammals

Conservation Biology

Volumn 26, Issue 6, 2012, Pages 1121-1129

  Ruiz López, María José ^a,f   Gañan, Natalia ^a   Godoy, José Antonio ^b   Del Olmo, Ana ^a   Garde, Julian ^c   Espeso, Gerardo ^d   Vargas, Astrid ^e   Martinez, Fernando ^e   Roldán, Eduardo R S ^a   Gomendio, Montserrat ^a  

^a MUSEO NACIONAL DE CIENCIAS NATURALES   (Spain)

^b DEPARTMENT OF CONSERVATION BIOLOGY   (Spain)

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

^d DEPARTAMENTO DE ECOLOGÍA FUNCIONAL Y EVOLUTIVA   (Spain)

^e Centro de Cría en Cautividad 'El Acebuche'   (Spain)

^f UNIVERSITY OF MISSOURI   (United States)

Author keywords

Endangered species; Gazella dama mhorr; HFCs; Iberian lynx; IFCs; Inbreeding; Lynx pardinus; Mohor gazelle; Semen quality

Indexed keywords

MICROSATELLITE DNA;

ANCESTRY; ENDANGERED SPECIES; FELID; FITNESS; GENEALOGY; GENETIC MARKER; GENOME; HETEROZYGOSITY; HYPOTHESIS TESTING; INBREEDING DEPRESSION; PHENOTYPE; SPERM; UNGULATE;

ANIMAL; ANTELOPE; ARTICLE; BIOLOGICAL MODEL; ENDANGERED SPECIES; ENVIRONMENTAL PROTECTION; GENETICS; HETEROZYGOTE; INBREEDING; LYNX; MALE; PEDIGREE; PHYSIOLOGY; POLYMERASE CHAIN REACTION; REPRODUCTIVE FITNESS; SEMEN ANALYSIS; SPAIN; SPERMATOZOON; STATISTICAL MODEL;

ANIMALS; ANTELOPES; CONSERVATION OF NATURAL RESOURCES; ENDANGERED SPECIES; GENETIC FITNESS; HETEROZYGOTE; INBREEDING; LINEAR MODELS; LYNX; MALE; MICROSATELLITE REPEATS; MODELS, GENETIC; PEDIGREE; POLYMERASE CHAIN REACTION; SEMEN ANALYSIS; SPAIN; SPERMATOZOA;

GAZELLA DAMA MHORR; LYNX; LYNX PARDINUS; MAMMALIA;

EID: 84868634179     PISSN: 08888892     EISSN: 15231739     Source Type: Journal    
DOI: 10.1111/j.1523-1739.2012.01916.x     Document Type: Article

References (50)

1. Balloux, F., W. Amos, and T. Coulson 2004. Does heterozygosity estimate inbreeding in real populations? Molecular Ecology 13:3021-3031.
2. Barbosa, A., and G. Espeso, editors. 2005. International studbook of Gazella dama mhorr. Parque de Rescate de Fauna Sahariana, Estacion Experimental de Zonas Aridas, Consejo Superior de Investigaciones Cientificas, Almeria, Spain.
3. Boyce, A. J. 1983. Computation of inbreeding and kinship coefficients on extended pedigrees. Journal of Heredity 74:400-404.
4. Chapman, J. R., S. Nakagawa, D. W. Coltman, J. Slate, and B. C. Sheldon 2009. A quantitative review of heterozygosity-fitness correlations in animal populations. Molecular Ecology 18:2746-2765.
5. Charlesworth, B., and D. Charlesworth 1999. The genetic basis of inbreeding depression. Genetical Research 74:329-340.
6. Coltman, D. W, W. Don Bowen, and J. M. Wright 1998. Birth weight and neonatal survival of harbour seal pups are positively correlated with genetic variation measured by microsatellites. Proceedings of the Royal Society of London Series B-Biological Sciences 265:803-809.
7. Crnokrak, P., and D. A. Roff 1999. Inbreeding depression in the wild. Heredity 83:260-270.
8. David, P. 1998. Heterozygosity-fitness correlations: new perspectives on old problems. Heredity 80:531-537.
9. David, P., B. Pujol, F. Viard, V. Castella, and J. Goudet 2007. Reliable selfing rate estimates from imperfect population genetic data. Molecular Ecology 16:2474-2487.
10. Excoffier, L., G. Laval, S., Scheneider 2006. Arlequin. Version 3.1. An integrated software package for population genetics data analysis. University of Bern, Bern, Switzerland.
11. Ferrer, M., and J. J. Negro 2004. The near extinction of two large european predators: super specialists pay a price. Conservation Biology 18:344-349.
12. Gañan, N., R. González, J. J. Garde, F. Martínez, A. Vargas, M. Gomendio, and E. R. S. Roldan 2009. Semen quality, sperm cryopreservation and heterologous in vitro fertilisation in the critically endangered Iberian lynx (Lynx pardinus). Reproduction, Fertility and Development 21: 848-859.
13. Gañan, N., et al. 2010. Reproductive traits in captive and free-ranging males of the critically endangered Iberian lynx (Lynx pardinus). Reproduction 139:275-285.
14. Garde, J. J., A. J. Soler, J. Cassinello, C. Crespo, A. F. Malo, G. Espeso, A. Gomendio, and E. R. S. Roldan 2003. Sperm Cryopreservation in three species of endangered gazelles (Gazella cuvieri, G.dama mhorr, and G.dorcas neglecta). Biology of Reproduction 69:602-611.
15. Godoy, J. A., M. Casas-Marce, and J. Fernandez 2009. Genetic issues in the implementation of the Iberian lynx ex situ conservation programme. Pages 86-99 in A. Vargas, C. Breitenmoser and U. Breitenmoser, editors. Iberian lynx ex situ conservation: an interdisciplinary approach. Fundacion Biodiversidad, Madrid.
16. Gomendio, M., J. Cassinello, and E. R. S. Roldan 2000. A comparative study of ejaculate traits in three endangered ungulates with different levels of inbreeding: fluctuating asymmetry as an indicator of reproductive and genetic stress. Proceedings of the Royal Society of London Series B-Biological Sciences 267:875-882.
17. Gomendio, M., A. F. Malo, J. Garde, and E. R. S. Roldan 2007. Sperm traits and male fertility in natural populations. Reproduction 134:19-29.
18. Gómez Montoto, L., C. Magaña, M. Tourmente, J. Martín-Coello, C. Crespo, J. J. Luque-Larena, M. Gomendio, and E. R. S. Roldan 2011. Sperm competition, sperm numbers and sperm quality in muroid rodents. Public Library of Science ONE 6 DOI:10.1371/journal.pone.0018173.
19. Gotelli, N. J., and A. Ellison 2004. A primer of Ecological Statistics. Sinauer Associates, Sunderland, Massachusetts.
20. Grueber, C. E., G. P. Wallis, and I. G. Jamieson 2008. Heterozygosity-fitness correlations and their relevance to studies on inbreeding depression in threatened species. Molecular Ecology 17:3978-3984.
21. Grueber, C. E., J. M. Waters, and I. G. Jamieson 2011. The imprecision of heterozygosity-fitness correlations hinders the detection of inbreeding and inbreeding depression in a threatened species. Molecular Ecology 20:67-79.
22. Hansson, B., and L. Westerberg 2002. On the correlation between heterozygosity and fitness in natural populations. Molecular Ecology 11:2467-2474.
23. 2, a microsatellite measure of inbreeding and outbreeding, in wolves with a known pedigree. Evolution 55:1256-1260.
24. IUCN (International Union for Conservation of Nature). 2011. IUCN red list of threatened species. Version 2011.2. IUCN, Gland, Switzerland.
25. Johnson, W. E., J. A. Godoy, F. Palomares, M. Delibes, M. Fernandes, E. Revilla, and S. J. O'Brien 2004. Phylogenetic and phylogeographic analysis of Iberian lynx populations. Journal of Heredity 95:19-28.
26. Keller, L. F., and D. M. Waller 2002. Inbreeding effects in wild populations. Trends in Ecology & Evolution 17:230-241.
27. Luquet, E., P. David, J. P. Lena, P. Joly, L. Konecny, C. Dufresnes, N. Perrin, and S. Plenet 2011. Heterozygosity-fitness correlations among wild populations of European tree frog (Hyla arborea) detect fixation load. Molecular Ecology 20:1877-1887.
28. Malo, A. F., J. J. Garde, A. J. Soler, A. J. García, M. Gomendio, and E. R. S. Roldan 2005. Male fertility in natural populations of red deer is determined by sperm velocity and the proportion of normal spermatozoa. Biology of Reproduction 72:822-829.
29. Markert, J., P. Grant, B. Grant, L. Keller, J. Coombs, and K. Petren 2004. Neutral locus heterozygosity, inbreeding, and survival in Darwin's ground finches (Geospiza fortis and G.scandens). Heredity 92:306-315.
30. Oosterhout van, C., W. F. Hutchinson, D. P. M. Wills, and P. Shipley 2004. MICRO-CHECKER: software for identifying and correcting genotyping errors in microsatellite data. Molecular Ecology Notes 4:535-538.
31. Overall, A. D. J., K. A. Byrne, J. G. Pilkington, and J. M. Pemberton 2005. Heterozygosity, inbreeding and neonatal traits in Soay sheep on St Kilda. Molecular Ecology 14:3383-3393.
32. Palomares, F. 2009. Life history and ecology of the Iberian lynx. Pages 4-11 in A. Vargas, C. Breitenmoser-Wursten, and U. Breitenmoser, editors. Iberian lynx ex situ conservation: an interdisciplinary approach. Fundacion Biodiversidad, Madrid.
33. Palomares, F., J. A. Godoy, A. Piriz, and S. J. O'Brien 2002. Faecal genetic analysis to determine the presence and distribution of elusive carnivores: design and feasibility for the Iberian lynx. Molecular Ecology 11:2171-2182.
34. Pemberton, J. 2004. Measuring inbreeding depression in the wild: the old ways are the best. Trends in Ecology & Evolution 19:613-615.
35. Ralls, K., K. Brugger, and J. Ballou 1979. Inbreeding and juvenile mortality in small populations of ungulates. Science 206:1101-1103.
36. Raymond, M., and F. Rousset 1995. GENEPOP (Version 1.2): population genetics software for exact tests and ecumenicism. Journal of Heredity 86: 248-249.
37. Rodríguez, A., and M. Delibes 1992. Current range and status of the Iberian lynx Felis pardina Temminck, 1824 in Spain. Biological Conservation 61:189-196.
38. Roldan, E. R. S., J. Cassinello, T., Abaigar, and M. Gomendio 1998. Inbreeding, fluctuating asymmetry, and ejaculate quality in an endangered ungulate. Proceedings of the Royal Society B-Biological Sciences 265:243-248.
39. Roldan, E. R. S., M. Gomendio, J. J. Garde, N. Gañan, R. Gonzalez, C. Crespo, and L. Arregui 2009. A genetic resource bank and assited reproduction for the critically endangered Iberian lynx. Pages 304-314 in A. Vargas, C. Breitenmoser, and U. Breitenmoser, editors. Iberian lynx ex situ conservation: an interdisciplinary approach. Fundacion Biodiversidad, Madrid.
40. Ruiz-López, M. J., E. R. S. Roldan, G. Espeso, and M. Gomendio 2009. Pedigrees and microsatellites among endangered ungulates: What do they tell us? Molecular Ecology 18:1352-1364.
41. Sambrook, J., E. F. Fritsch, and T. Maniatis, editors. 1989. Molecular cloning: a laboratory manual. Cold Spring Harbor Laboratory Press, New York.
42. Simon, M. A., R. Cadenas, J. M. Gil-Sanchez, M. López-Parra, J. Garcia, L. Fernandez, G. Ruiz, and G. López 2009. Conservation of free-ranging Iberian lynx (Lynx pardinus) populations in Andalusia. Pages 42-55 in A. Vargas, C. Breitenmoser-Wursten, and U. Breitenmoser, editors. Iberian lynx ex situ conservation: an interdisciplinary approach. Fundacion Biodiversidad, Madrid.
43. Slate, J., and J. Pemberton 2006. Does reduced heterozygosity depress sperm quality in wild rabbits (Oryctolagus cuniculus)? Current Biology 16:R790-R791.
44. Slate, J., P. David, K. G. Dodds, B. A. Veenvliet, B. C. Glass, T. E. Broad, and J. C. McEwan 2004. Understanding the relationship between the inbreeding coefficient and multilocus heterozygosity: theoretical expectations and empirical data. Heredity 93:255-265.
45. Spiering, P., M. Szykman Gunther, M. Somers, D. Wildt, M. Walters, A. Wilson, and J. Maldonado 2011. Inbreeding, heterozygosity and fitness in a reintroduced population of endangered African wild dogs (Lycaon pictus). Conservation Genetics 12:401-412.
46. Szulkin, M., N. Bierne, and P. David 2010. Heterozygosity-fitness correlations: a time for reappraisal. Evolution 64:1202-1217.
47. Valverde, J. A., editor. 2004. Memorias de un biólogo heterodoxo. Tomo III. Sáhara, Guinea, Marruecos. Expediciones Africanas Quercus, VandV, Madrid.
48. Von Arx, M., and C. Breitenmoser-Wursten 2008. Lynx pardinus. IUCN red list of threatened species. Version 2011.1. International Union for Conservation of Nature, Gland, Switzerland. Available from http://www.iucnredlist.org (accessed July 2011).
49. Weir, B., and C. Cockerham 1973. Mixed self and random mating at two loci. Genetical research 21:247-262.
50. Wright, S. 1922. Coefficients of inbreeding and relationship. The American Naturalist 56:330-338.