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. 2000 Aug;155(4):1981–1990. doi: 10.1093/genetics/155.4.1981

An inbreeding model of associative overdominance during a population bottleneck.

N Bierne 1, A Tsitrone 1, P David 1
PMCID: PMC1461183  PMID: 10924490

Abstract

Associative overdominance, the fitness difference between heterozygotes and homozygotes at a neutral locus, is classically described using two categories of models: linkage disequilibrium in small populations or identity disequilibrium in infinite, partially selfing populations. In both cases, only equilibrium situations have been considered. In the present study, associative overdominance is related to the distribution of individual inbreeding levels (i.e., genomic autozygosity). Our model integrates the effects of physical linkage and variation in inbreeding history among individual pedigrees. Hence, linkage and identity disequilibrium, traditionally presented as alternatives, are summarized within a single framework. This allows studying nonequilibrium situations in which both occur simultaneously. The model is applied to the case of an infinite population undergoing a sustained population bottleneck. The effects of bottleneck size, mating system, marker gene diversity, deleterious genomic mutation parameters, and physical linkage are evaluated. Bottlenecks transiently generate much larger associative overdominance than observed in equilibrium finite populations and represent a plausible explanation of empirical results obtained, for instance, in marine species. Moreover, the main origin of associative overdominance is random variation in individual inbreeding whereas physical linkage has little effect.

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Selected References

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  1. Bataillon T., Kirkpatrick M. Inbreeding depression due to mildly deleterious mutations in finite populations: size does matter. Genet Res. 2000 Feb;75(1):75–81. doi: 10.1017/s0016672399004048. [DOI] [PubMed] [Google Scholar]
  2. Bierne N., Launey S., Naciri-Graven Y., Bonhomme F. Early effect of inbreeding as revealed by microsatellite analyses on Ostrea edulis larvae. Genetics. 1998 Apr;148(4):1893–1906. doi: 10.1093/genetics/148.4.1893. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Charlesworth B., Charlesworth D. The genetic basis of inbreeding depression. Genet Res. 1999 Dec;74(3):329–340. doi: 10.1017/s0016672399004152. [DOI] [PubMed] [Google Scholar]
  4. Clark A. G. Mutation-selection balance and metabolic control theory. Genetics. 1991 Nov;129(3):909–923. doi: 10.1093/genetics/129.3.909. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Coltman D. W., Bowen W. D., Wright J. M. Birth weight and neonatal survival of harbour seal pups are positively correlated with genetic variation measured by microsatellites. Proc Biol Sci. 1998 May 7;265(1398):803–809. doi: 10.1098/rspb.1998.0363. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Coulson T. N., Pemberton J. M., Albon S. D., Beaumont M., Marshall T. C., Slate J., Guinness F. E., Clutton-Brock T. H. Microsatellites reveal heterosis in red deer. Proc Biol Sci. 1998 Mar 22;265(1395):489–495. doi: 10.1098/rspb.1998.0321. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. David P. A quantitative model of the relationship between phenotypic variance and heterozygosity at marker loci under partial selfing. Genetics. 1999 Nov;153(3):1463–1474. doi: 10.1093/genetics/153.3.1463. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. David P., Delay B., Berthou P., Jarne P. Alternative models for allozyme-associated heterosis in the marine bivalve Spisula ovalis. Genetics. 1995 Apr;139(4):1719–1726. doi: 10.1093/genetics/139.4.1719. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. David P. Heterozygosity-fitness correlations: new perspectives on old problems. Heredity (Edinb) 1998 May;80(Pt 5):531–537. doi: 10.1046/j.1365-2540.1998.00393.x. [DOI] [PubMed] [Google Scholar]
  10. García-Dorado A., López-Fanjul C., Caballero A. Properties of spontaneous mutations affecting quantitative traits. Genet Res. 1999 Dec;74(3):341–350. doi: 10.1017/s0016672399004206. [DOI] [PubMed] [Google Scholar]
  11. KIMURA M., MARUYAMA T., CROW J. F. THE MUTATION LOAD IN SMALL POPULATIONS. Genetics. 1963 Oct;48:1303–1312. doi: 10.1093/genetics/48.10.1303. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Keightley P. D., Eyre-Walker A. Terumi Mukai and the riddle of deleterious mutation rates. Genetics. 1999 Oct;153(2):515–523. doi: 10.1093/genetics/153.2.515. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Koehn R. K., Diehl W. J., Scott T. M. The differential contribution by individual enzymes of glycolysis and protein catabolism to the relationship between heterozygosity and growth rate in the coot clam, Mulinia lateralis. Genetics. 1988 Jan;118(1):121–130. doi: 10.1093/genetics/118.1.121. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Latter B. D., Mulley J. C., Reid D., Pascoe L. Reduced genetic load revealed by slow inbreeding in Drosophila melanogaster. Genetics. 1995 Jan;139(1):287–297. doi: 10.1093/genetics/139.1.287. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Morton N. E., Crow J. F., Muller H. J. AN ESTIMATE OF THE MUTATIONAL DAMAGE IN MAN FROM DATA ON CONSANGUINEOUS MARRIAGES. Proc Natl Acad Sci U S A. 1956 Nov;42(11):855–863. doi: 10.1073/pnas.42.11.855. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Ohta T., Kimura M. Behavior of neutral mutants influenced by asociated overdominant loci in finite populations. Genetics. 1971 Oct;69(2):247–260. doi: 10.1093/genetics/69.2.247. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Ohta T., Kimura M. Development of associative overdominance through linkage disequilibrium in finite populations. Genet Res. 1970 Oct 2;16(2):165–177. doi: 10.1017/s0016672300002391. [DOI] [PubMed] [Google Scholar]
  18. Ota T., Cockerham C. C. Detrimental genes with partial selfing and effects on a neutral locus. Genet Res. 1974 Apr;23(2):191–200. doi: 10.1017/s0016672300014816. [DOI] [PubMed] [Google Scholar]
  19. Pamilo P., Pálsson S. Associative overdominance, heterozygosity and fitness. Heredity (Edinb) 1998 Oct;81(Pt 4):381–389. doi: 10.1046/j.1365-2540.1998.00395.x. [DOI] [PubMed] [Google Scholar]
  20. Pogson G. H., Zouros E. Allozyme and RFLP heterozygosities as correlates of growth rate in the scallop Placopecten magellanicus: a test of the associative overdominance hypothesis. Genetics. 1994 May;137(1):221–231. doi: 10.1093/genetics/137.1.221. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Pálsson S., Pamilo P. The effects of deleterious mutations on linked, neutral variation in small populations. Genetics. 1999 Sep;153(1):475–483. doi: 10.1093/genetics/153.1.475. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Rumball W., Franklin I. R., Frankham R., Sheldon B. L. Decline in heterozygosity under full-sib and double first-cousin inbreeding in Drosophila melanogaster. Genetics. 1994 Mar;136(3):1039–1049. doi: 10.1093/genetics/136.3.1039. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Strauss S. H. Heterosis at Allozyme Loci under Inbreeding and Crossbreeding in PINUS ATTENUATA. Genetics. 1986 May;113(1):115–134. doi: 10.1093/genetics/113.1.115. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Strobeck C. Partial selfing and linkage: the effect of a heterotic locus on a neutral locus. Genetics. 1979 May;92(1):305–315. doi: 10.1093/genetics/92.1.305. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Weir B. S., Cockerham C. C. Group inbreeding with two linked loci. Genetics. 1969 Nov;63(3):711–742. doi: 10.1093/genetics/63.3.711. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Weir B. S., Cockerham C. C. Mixed self and random mating at two loci. Genet Res. 1973 Jun;21(3):247–262. doi: 10.1017/s0016672300013446. [DOI] [PubMed] [Google Scholar]
  27. Zouros E., Foltz D. W. The use of allelic isozyme variation for the study of heterosis. Isozymes Curr Top Biol Med Res. 1987;13:1–59. [PubMed] [Google Scholar]
  28. Zouros E. On the relation between heterozygosity and heterosis: an evaluation of the evidence from marine mollusks. Isozymes Curr Top Biol Med Res. 1987;15:255–270. [PubMed] [Google Scholar]

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