Heterozygosity is linked to the costs of immunity in nestling great tits (Parus major)
Version of Record online: 5 NOV 2013
© 2013 The Authors. Ecology and Evolution published by John Wiley & Sons Ltd.
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Ecology and Evolution
Volume 3, Issue 14, pages 4815–4827, November 2013
How to Cite
Ecology and Evolution 2013; 3(14): 4815–4827
- Issue online: 25 NOV 2013
- Version of Record online: 5 NOV 2013
- Manuscript Accepted: 17 SEP 2013
- Manuscript Revised: 10 SEP 2013
- Manuscript Received: 2 JUL 2013
- Swiss National Science Foundation. Grant Number: 138658
- 2003. Disease susceptibility in California sea lions. Nature 422:35. , , , and .
- 2005. Genetic resistance to bovine tuberculosis in the Iberian wild boar. Mol. Ecol. 14:3209–3217. , , , , , and .
- 2010. Rhh: an R extension for estimating multilocus heterozygosity and heterozygosity-heterozygosity correlation. Mol. Ecol. Res. 10:720–722. , , and .
- 2006. What should we weigh to estimate heterozygosity, alleles or loci? Mol. Ecol. 15:4659–4665. , , and .
- 2005. Inbreeding depression in benign and stressful environments. Heredity 95:235–242. , and .
- 2004. Does heterozygosity estimate inbreeding in real populations? Mol. Ecol. 13:3021–3031. , , and .
- 2012. lme4: Linear mixed-effects models using S4 classes. R package version 0.999999-0, Available at http://CRAN.R-project.org/package=lme4. , , and .
- 2008. Carotenoid-induced maternal effects interact with ectoparasite burden and brood size to shape the trade-off between growth and immunity in nestling great tits. Funct. Ecol. 22:854–863. , , and .
- 2008. What makes a host profitable? Parasites balance host nutritive resources against immunity Am. Nat. 171:107–118. , , , and .
- 2004. Immunocompetence and its costs during development: an experimental study in blue tit nestlings. Proceed. Royal Soc. B-Biol. Sci. 271:S110–S113.
- 2009. A quantitative review of heterozygosity-fitness correlations in animal populations. Mol. Ecol. 18:2746–2765. , , , , and .
- 2009. Juveniles exposed to embryonic corticosterone have enhanced flight performance. Proceed. Royal Soc. B-Biol. Sci. 276:499–505. , , , , , and .
- 2003. Microsatellite measures of inbreeding: a meta-analysis. Evolution 57:971–983. , and .
- 1999. Parasite-mediated selection against inbred Soay sheep in a free-living, island population. Evolution 53:1259–1267. , , , and .
- 1999. Microsatellite loci reveal sex-dependent responses to inbreeding and outbreeding in red deer calves. Evolution 53:1951–1960. , , , and .
- 2006. Genetic diversity-fitness correlation revealed by microsatellite analyses in European alpine marmots (Marmota marmota). Conserv. Genet. 7:371–382. , , , , and .
- 1998. Heterozygosity-fitness correlations: new perspectives on old problems. Heredity 80:531–537.
- 2007. Reliable selfing rate estimates from imperfect population genetic data. Mol. Ecol. 16:2474–2487. , , , , and .
- 2010. New methods to identify conserved microsatellite loci and develop primer sets of high cross-species utility – as demonstrated for birds. Mol. Ecol. Res. 10:475–494. , , , , , , et al.
- 2006. Sex-specific development of cell-mediated immunity under experimentally altered rearing conditions in blue tit nestlings. Proceed. Royal Soc. B-Biol. Sci. 273:1759–1764. , , and .
- 1995. Cytokine effects on CNS biogenic amines. Neuroimmunomodulation 2:319–328. , and .
- 1996. First gene on the avian W chromosome (CHD) provides a tag for universal sexing of non-ratite birds. Proceed. Royal Soc. B-Biol. Sci. 263:1635–1641.
- 2003. Females increase offspring heterozygosity and fitness through extra-pair matings. Nature 425:714–717. , , , , and .
- 2012. Heterozygosity-fitness correlations in zebra finches: microsatellite markers can be better than their reputation. Mol. Ecol. 21:3237–3249. , , , , and .
- 2009. Cell-mediated immunity and multi-locus heterozygosity in bluethroat nestlings. J. Evol. Biol. 22:1954–1960. , , and .
- 2011. Inbreeding depression increases with environmental stress: an experimental study and meta-analysis. Evolution 65:246–258. , and .
- 1977. The distribution of the proportion of the genome which is homozygous by descent in inbred individuals. Theoret. Popul. Biol. 11:60–80.
- 2011. Temporal and spatial variations of ectoparasites on cage-reared channel catfish, Ictalurus punctatus, in Tamaulipas, Mexico. J. World Aquaculture Soc. 42:406–411. , , , , , and .
- 1995. FSTAT (Version 1.2): A computer program to calculate F-statistics. J. Hered. 86:485–486.
- 1981. Incubation during the egg-laying period in relation to clutch-size and other aspects of reproduction in the Great Tit Parus-Major. Ornis Scandinavica 12:169–185.
- 2006. Inbreeding linked to amphibian survival in the wild but not in the laboratory. J. Hered. 97:499–507. , , and .
- 2002. On the correlation between heterozygosity and fitness in natural populations. Mol. Ecol. 11:2467–2474. , and .
- 2001. Microsatellite diversity predicts recruitment of sibling great reed warblers. Proceed. Royal Soc. of London Series B-Biol. Sci. 268:1287–1291. , , , and .
- 2005. Genetic diversity predicts pathogen resistance and cell-mediated immunocompetence in house finches. Biol. Lett. 1:326–329. , , , and .
- 1999. Immune function and survival of great tit nestlings in relation to growth conditions. Oecologia 121:316–322. , , , and .
- 1996. Microsatellites, from molecules to populations and back. Trends Ecol. Evol. 11:424–429. , and .
- 2002. Inbreeding effects in wild populations. Trends Ecol. Evol. 17:230–241. , and .
- 2007. Mate choice and genetic quality: a review of the heterozygosity theory. Adv. Study Behav. 37:189–278.
- 2010. Determinants of ectoparasite assemblage structure on rodent hosts from South American marshlands: the effect of host species, locality and season. Med. Vet. Entomol. 24:284–292. , and .
- 2012. Heterozygosity–behaviour correlations in nine-spined stickleback (Pungitius pungitius) populations: contrasting effects at random and functional loci. Mol. Ecol. 21:4872–4884. , , , and .
- 1993. Ectoparasites – direct impact on host fitness. Parasitology Today 9:8–13.
- 2005. Environmental and population dependency of genetic variability-fitness correlations in Rana temporaria. Mol. Ecol. 14:311–323. , , , and .
- 2004. Microsatellites within genes: structure, function, and evolution. Mol. Biol. Evol. 21:991–1007. , , , and .
- 2000. Trade-offs in evolutionary immunology: just what is the cost of immunity? Oikos 88:87–98. , and .
- 1991. The genetic interpretation of inbreeding depression and outbreeding depression. Evolution 45:622–629.
- 2006. Interactive effects of environmental stress and inbreeding on reproductive traits in a wild bird population. J. Anim. Ecol. 75:1406–1415. , , , , and .
- 1996. Weather dependent effects of nest ectoparasites on their bird hosts. Ecography 19:107–113. , and .
- 2007. Effect size, confidence interval and statistical significance: a practical guide for biologists. Biol. Rev. 82:591–605. and .
- 2009. Corrigendum. Biol. Rev. 84:515. , and .
- 2003. Brood size, sibling competition, and the cost of begging in great tits (Parus major). Behav. Ecol. 14:457–462. , , , and .
- 2011. Heterozygosity and survival in blue tits (Cyanistes caeruleus): contrasting effects of presumably functional and neutral loci. Mol. Ecol. 20:4028–4041. , , and .
- 1998. Do female black-capped chickadees prefer high-ranking males as extra-pair partners? Behav. Ecol. Sociobiol. 43:25–36. , , , and .
- 1998. Antibody responses and body weights of chicken lines selected for high and low humoral responsiveness to sheep red blood cells. 1. Effect of Escherichia coli lipopolysaccharide. Poult. Sci. 77:248–255. , , and .
- 1998. Microsatellite primers from Geospiza fortis and cross-species amplification in Darwin's finches. Mol. Ecol. 7:1782–1784.
- 2010. Costs and benefits of experimentally induced changes in the allocation of growth versus immune function under differential exposure to ectoparasites. PLoS ONE 5:e10814. , , , and .
- 1993. Microsatellites and Kinship. Trends Ecol. Evol. 8, 285. , , and .
- 2007. Inbreeding effects on immune response in free-living song sparrows (Melospiza melodia). Proceed. Royal Soc. B-Biol. Sci. 274:697–706. , , , , , and .
- 1993. Effect of an ectoparasite on reproduction in great tits. J. Anim. Ecol. 62:703–710. , , and .
- 1998. Effects of a dipteran ectoparasite on immune response and growth trade-offs in barn swallow, Hirundo rustica, nestlings. Oikos 81:217–228. , , and .
- 2012. A set of 48 microsatellite loci for the great tit Parus major including 15 novel markers. Mol. Ecol. Res. 12:185–189. , and .
- 2003. Isolation and characterization of 16 microsatellite loci in the Great Tit Parus major. Mol. Ecol. Notes 3:520–522. , , , and .
- 1999. Energy expenditure, nestling age, and brood size: an experimental study of parental behavior in the great tit Parus major. Behav. Ecol. 10:598–606. , and .
- 1996. Ecological immunology: Costly parasite defences and trade-offs in evolutionary ecology. Trends Ecol. Evol. 11:317–321. , and .
- 2007. Simple sequence repeats in zebra finch (Taeniopygia guttata) expressed sequence tags: a new resource for evolutionary genetic studies of passerines. BMC Genomics 8:52. , , and .
- 2003. Trade-off between immunocompetence and growth in magpies: an experimental study. Proceed. Royal Soc. B-Biol. Sci. 270:241–248. , , , , and .
- 2011. Negative heterozygosity-fitness correlations observed with microsatellites located in functional areas of the genome. Mol. Ecol. 20:3949–3952. , and .
- 2010. Heterozygosity-fitness correlations: a time for reappraisal. Evolution 64:1202–1217. , , and .
- 2009. A simple method for distinguishing within- versus between-subject effects using mixed models. Anim. Behav. 77:753–758. , and .
- 2012. Parasites as mediators of heterozygosity–fitness correlations in the Great Tit (Parus major). J. Evol. Biol. 25:584–590. , , , and .