Abstract
It is crucial to understand the genetic health and implications of inbreeding in wildlife populations, especially of vulnerable species. Using extensive demographic and genetic data, we investigated the relationships among pedigree inbreeding coefficients, metrics of molecular heterozygosity and fitness for a large population of endangered African wild dogs (Lycaon pictus) in South Africa. Molecular metrics based on 19 microsatellite loci were significantly, but modestly correlated to inbreeding coefficients in this population. Inbred wild dogs with inbreeding coefficients of ≥0.25 and subordinate individuals had shorter lifespans than outbred and dominant contemporaries, suggesting some deleterious effects of inbreeding. However, this trend was confounded by pack-specific effects as many inbred individuals originated from a single large pack. Despite wild dogs being endangered and existing in small populations, findings within our sample population indicated that molecular metrics were not robust predictors in models of fitness based on breeding pack formation, dominance, reproductive success or lifespan of individuals. Nonetheless, our approach has generated a vital database for future comparative studies to examine these relationships over longer periods of time. Such detailed assessments are essential given knowledge that wild canids can be highly vulnerable to inbreeding effects over a few short generations.
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References
Acevedo-Whitehouse K, Gulland F, Greig D, Amos W (2003) Inbreeding: disease susceptibility in California sea lions. Nature 422:35
Alexander KA, Appel MJG (1994) African wild dogs (Lycaon pictus) endangered by a canine distemper virus epizootic among domestic dogs near the Masai Mara National Reserve, Kenya. J Wildl Dis 30:481–485
Amos W, Wilmer JW, Fullard K et al (2001) The influence of parental relatedness on reproductive success. Proc R Soc Lond B 268:2021–2027
Aparicio JM, Ortego J, Cordero PJ (2007) Can a simple algebraic analysis predict markers-genome heterozygosity correlations? J Hered 98:93–96
Asa C, Miller P, Agnew M et al (2007) Relationship of inbreeding with sperm quality and reproductive success in Mexican gray wolves. Anim Conserv 10:326–331
Balloux F, Amos W, Coulson T (2004) Does heterozygosity estimate inbreeding in real populations? Mol Ecol 13:3021–3031
Bensch S, Andren H, Hansson B et al (2006) Selection for heterozygosity gives hope to a wild population of inbred wolves. PLoS One 1:e72
Bolker BM, Brooks ME, Clark CJ, Geange SW, Poulsen JR, Stevens MHH, White JS (2008) Generalized linear mixed models: a practical guide for ecology and evolution. Trends Ecol Evol 24:127–135
Buettner UK, Davies-Mostert HT, du Toit JT, Mills MGL (2007) Factors affecting juvenile survival in African wild dogs (Lycaon pictus) in Kruger National Park, South Africa. J Zool (Lond) 272:10–19
Burnham KP, Anderson DR (2002) Model selection and multimodel inference: a practical information-theoretical approach, 2nd edn. Springer-Verlag, New York
Charpentier MJE, Williams CV, Drea CM (2008) Inbreeding depression in ring-tailed lemurs (Lemur catta): genetic diversity predicts parasitism, immunocompetence and survivorship. Conserv Genet 9:1605–1615
Cleaveland S, Appel MJG, Chalmers WSK, Chillingworth C, Kaare M, Dye C (2000) Serological and demographic evidence for domestic dogs as a source of canine distemper virus infection for Serengeti wildlife. Vet Microbiol 72:217–227
Coltman D, Slate J (2003) Microsatellite measures of inbreeding: a meta-analysis. Evolution 57:971–983
Coltman DW, Pilkington JG, Smith JA, Pemberton JM (1999) Parasite-mediated selection against inbred Soay sheep in a free-living, island population. Evolution 53:1259–1267
Cornuet JM, Luikart G (1996) Description and power analysis of two tests for detecting recent population bottlenecks from allele frequency data. Genetics 144:2001–2014
Coulson T, Pemberton JM, Albon S et al (1998) Microsatellites reveal heterosis in red deer. Proc R Soc Lond B 265:489–495
Coulson T, Albon S, Slate J, Pemberton JM (1999) Microsatellite loci reveal sex-dependent responses to inbreeding and outbreeding in red deer calves. Evolution 53:1951–1960
Courchamp F, Grenfell B, Clutton-Brock T (1999) Population dynamics of obligate cooperators. Proc R Soc Lond B 266:557–563
Creel S, Creel NM (2002) The African wild dog: behavior, ecology and conservation. Princeton University Press, Princeton
DaSilva A, Luikart G, Yoccoz NG, Cohas A, Allaine D (2006) Genetic diversity-fitness correlation revealed by microsatellite analyses in European marmots (Marmota marmota). Conserv Genet 7:371–382
Davies-Mostert HT, Mills MGL, Macdonald DW (2009) A critical assessment of South Africa’s managed metapopulation recovery strategy for African wild dogs. In: Somers MJ, Hayward MW (eds) Reintroduction of top-order predators. Wiley-Blackwell, London
Fitzpatrick JL, Evans JP (2009) Reduced heterozygosity impairs sperm quality in endangered mammals. Biol Lett 25:320–323
Frankham R (2009) Genetic considerations in reintroduction programmes for large terrestrial predators. In: Somers MJ, Hayward MW (eds) Reintroduction of top-order predators. Wiley-Blackwell, London
Frankham R, Ballou JD, Briscoe DA (2002) Introduction to conservation genetics. Cambridge University Press, Cambridge
Fredrickson RJ, Siminski P, Woolf M, Hedrick P (2007) Genetic rescue and inbreeding depression in Mexican wolves. Proc R Soc Lond B 274:2365–2371
Gascoyne SC, Laurenson MK, Lelo S, Borner M (1993) Rabies in African wild dogs (Lycaon pictus) in the Serengeti region, Tanzania. J Wildl Dis 29:396–402
Girman JG, Mills MGL, Geffen E, Wayne RK (1997) A molecular genetic analysis of social structure, dispersal and interpack relationships of the African wild dog (Lycaon pictus). Behav Ecol Sociobiol 40:187–198
Girman DJ, Vila C, Geffen E et al (2001) Patterns of population subdivisión, gene flow and genetic variability in the African wild dog (Lycaon pictus). Mol Ecol 10:1703–1723
Grafen A (1982) How not to measure inclusive fitness. Nature 298:425–426
Grueber CE, Wallis GP, Jamieson IG (2008) Heterozygosity-fitness correlations and their relevance to studies on inbreeding depression in threatened species. Mol Ecol 17:3978–3984
Gusset M, Slotow R, Somers MJ (2006) Divided we fail: the importance of social integration for the re-introduction of endangered African wild dogs (Lycaon pictus). J Zool (Lond) 270:502–511
Hansson B, Westerberg L (2008) Heterozygosity-fitness correlations within inbreeding classes: local or genome-wide effects? Conserv Genet 9:73–83
Hedrick P, Fredrickson R (2008) Captive breeding and the reintroduction of Mexican and red wolves. Mol Ecol 17:344–350
Hedrick P, Fredricskon R, Ellegren H (2001) Evaluation of mean d2, a microsatellite measure of inbreeding and outbreeding, in wolves with a known pedigree. Evolution 55:1256–1260
Jensen H, Bremset EM, Ringsby TH, Saether BE (2007) Multilocus heterozygosity and inbreeding depression in an insular house sparrow metapopulation. Mol Ecol 16:4066–4078
Kalinowski S, Hedrick PW (1999) Detecting inbreeding depression is difficult in captive endangered species. Anim Conserv 2:131–136
Keller LF (1998) Inbreeding and its fitness effects in an insular population of song sparrows (Melospiza melodia). Evolution 52:240–250
Keller LF, Waller DM (2002) Inbreeding effects in wild populations. Trends Ecol Evol 17:230–241
Laikre L, Ryman N (1991) Inbreeding depression in a captive wolf (Canis lupus) population. Conserv Biol 5:33–40
Liberg O, Andren H, Pedersen HC et al (2005) Severe inbreeding depression in a wild wolf population. Biol Lett 1:17–20
Lindsey P, du Toit JT, Mills MGL (2004) The distribution and population status of African wild dogs (Lycaon pictus) outside protected areas in South Africa. S Afr J Wildl Res 34:143–161
Marsden CD, Mable BK, Woodroffe R et al (2009) Highly endangered African wild dogs (Lycaon pictus) lack variation at the major histocompatibility complex. J Hered. doi: 10.1093/jhered/esp031
McNutt JW (1996) Sex-biased dispersal in African wild dogs, Lycaon pictus. Anim Behav 52:1067–1077
McNutt JW, Silk JB (2008) Pup production, sex ratios, and survivorship in African wild dogs, Lycaon pictus. Behav Ecol Sociobiol 62:1061–1067
Mills MGL, Ellis S, Woodroffe R et al (1998) Population and habitat viability assessment for the African wild dog (Lycaon pictus) in Southern Africa. Conservation Breeding Specialist Group. IUCN/Species Survival Commission, Apple Valley
O’Brien SJ, Evermann JF (1988) Interactive influence of infectious disease and genetic diversity in natural populations. Trends Ecol Evol 3:254–259
O’Grady J, Reed DH, Brook BW, Frankham R (2008) Extinction risk scales better to generations than to years. Anim Conserv 11:442–451
Raikkonen J, Bignert A, Mortensen P, Fernholm B (2006) Congenital defects in a highly inbred wild wolf population (Canis lupus). Mamm Biol 71:65–73
Ralls K, Brugger K, Ballou J (1979) Inbreeding and juvenile mortality in small populations of ungulates. Science 206:1101–1103
Slate J, David P, Dodds KG et al (2004) Understanding the relationship between the inbreeding coefficient and multilocus heterozygosity: theoretical expectations and empirical data. Heredity 93:255–265
Somers M, Maddock A (1999) Painted dogs of Zululand. Afr Wildl 53:24–26
Somers MJ, Graf JA, Szykman M, Slotow R, Gusset M (2008) Dynamics of a small re-introduced population of endangered wild dogs over 25 years: Allee effects and the implications of sociality for conservation. Oecologia 158:239–247
Spiering PA, Szykman Gunther M, Wildt DE, Somers MJ, Maldonado JE (2009) Sampling error in non-invasive genetic analyses of an endangered social carnivore. Conserv Genet 10:2005–2007
Spiering PA, Somers MJ, Maldonado JE, Wildt DE, Szykman Gunther M (2010) Reproductive sharing and proximate factors mediating cooperative breeding in the African wild dog (Lycaon pictus). Behav Ecol Sociobiol 64:583–592
Szulkin M, Bierne N, David P (2010) Heterozygosity-fitness correlations: a time for reappraisal. Evolution 64:1202–1217
Valdes AM, Slatkin M, Freimer NB (1993) Allele frequencies at microsatellite loci: the stepwise mutation model revisited. Genetics 133:737–749
Woodroffe R, Ginsberg JR, Macdonald DW (1997) The African wild dog-status survey and conservation action plan. IUCN, Gland
Acknowledgments
We thank Ezemvelo KwaZulu-Natal Wildlife, especially the management teams at Hluhluwe-iMfolozi Park and the uMkhuze section of iSimangaliso Wetland Park. We also appreciate the assistance of Thanda Private Game Reserve and the wildlife management team. We are grateful to Rob Fleischer, Emily Latch, Sarah Haas, Kalon Armstrong and Nancy Rotzel of the Smithsonian’s Conservation Biology Institute for help with laboratory protocols and procedures. Sarah Arnoff, Jan Graf, Gabriella Flacke, Mariana Venter, Carla Naude-Graaff, Sboniso (Zama) Zwane, Brendan Whittington-Jones, Chris Kelly and Warren Becker provided invaluable assistance in the field. We thank Robert Sivinski and Scott Wilson of the Smithsonian’s Migratory Bird Center for statistical advice. This research was supported by the Smithsonian Institution Undersecretary for Science Endowment Fund, the University of Pretoria, Rotterdam Zoo Thandiza Fund, Humboldt State University Sponsored Program Foundation, Conservation Endowment Fund of the Association of Zoos and Aquariums, Disney Wildlife Conservation Fund, Knowsley Safari Park, DST-NRF Centre of Excellence for Invasion Biology, Khaki Fever Work Wear, Pittsburgh Zoo Conservation Fund and the Morris Animal Foundation. International travel was generously provided by British Airways.
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Spiering, P.A., Szykman Gunther, M., Somers, M.J. et al. Inbreeding, heterozygosity and fitness in a reintroduced population of endangered African wild dogs (Lycaon pictus). Conserv Genet 12, 401–412 (2011). https://doi.org/10.1007/s10592-010-0147-z
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DOI: https://doi.org/10.1007/s10592-010-0147-z