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Efficiency of selection, as measured by single nucleotide polymorphism variation, is dependent on inbreeding rate in Drosophila melanogaster

Authors

  • DITTE DEMONTIS,

    1. Department of Biological Sciences, Ecology and Genetics, Aarhus University, Ny Munkegade, Building 1540, DK-8000 Århus C, Denmark
    2. Institute of Human Genetics, Aarhus University, Wilhelm Meyers Allé, Building 1240, DK-8000 Århus C, Denmark
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  • CINO PERTOLDI,

    1. Department of Biological Sciences, Ecology and Genetics, Aarhus University, Ny Munkegade, Building 1540, DK-8000 Århus C, Denmark
    2. Mammal Research Institute, Polish Academy of Sciences, Waszkiewicza 1c, 17-230 Białowieża, Poland
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  • VOLKER LOESCHCKE,

    1. Department of Biological Sciences, Ecology and Genetics, Aarhus University, Ny Munkegade, Building 1540, DK-8000 Århus C, Denmark
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  • KARINA MIKKELSEN,

    1. Department of Biological Sciences, Ecology and Genetics, Aarhus University, Ny Munkegade, Building 1540, DK-8000 Århus C, Denmark
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  • TOMAS AXELSSON,

    1. Molecular Medicine, Department of Medical Sciences, Uppsala University, University Hospital, Entrance 70, 75185 Uppsala, Sweden
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  • TORSTEN NYGAARD KRISTENSEN

    1. Department of Biological Sciences, Ecology and Genetics, Aarhus University, Ny Munkegade, Building 1540, DK-8000 Århus C, Denmark
    2. Department of Genetics and Biotechnology, Aarhus University, Blichers Allé 20, DK-8830 Tjele, Denmark
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  • Ditte Demontis is a postdoc at Department of Human Genetics, Aarhus University, Denmark. Currently she works with genome wide association studies in humans in order to identify risk alleles involved in various psychiatric diseases. Cino Pertoldi is associate professor at Department of Biological Sciences, Ecology and Genetics, Aarhus University, Denmark. He is primarily interested in conservation genetics and evolutionary ecology. Volker Loeschcke is professor in evolutionary genetics and head of the Aarhus Center of Environmental Stress Research, Department of Biological Sciences, Aarhus University, Denmark. His research aims at relating variation at the DNA level to variation in function and phenotype. Karina Mikkelsen is a master student at Department of Biological Sciences, Aarhus University, Denmark. She is interested in inbreeding depression and uses ecologically relevant assays in her studies of associations between inbreeding and stress resistance. Tomas Axelsson is a senior scientist and manager of the SNP technology platform, Uppsala University, Sweden. His research focus is on technologies for determining genetic variation and its applications in natural science. Torsten Nygaard Kristensen is a senior scientist at Department of Genetics and Biotechnology, Aarhus University, Denmark. He works with small populations and tries to identify causes and consequences of inbreeding using omic technologies.

Ditte Demontis, Fax: +45 8942 1672; E-mail: ditte@humgen.au.dk

Abstract

It is often hypothesized that slow inbreeding causes less inbreeding depression than fast inbreeding at the same absolute level of inbreeding. Possible explanations for this phenomenon include the more efficient purging of deleterious alleles and more efficient selection for heterozygote individuals during slow, when compared with fast, inbreeding. We studied the impact of inbreeding rate on the loss of heterozygosity and on morphological traits in Drosophila melanogaster. We analysed five noninbred control lines, 10 fast inbred lines and 10 slow inbred lines; the inbred lines all had an expected inbreeding coefficient of approximately 0.25. Forty single nucleotide polymorphisms in DNA coding regions were genotyped, and we measured the size and shape of wings and counted the number of sternopleural bristles on the genotyped individuals. We found a significantly higher level of genetic variation in the slow inbred lines than in the fast inbred lines. This higher genetic variation was resulting from a large contribution from a few loci and a smaller effect from several loci. We attributed the increased heterozygosity in the slow inbred lines to the favouring of heterozygous individuals over homozygous individuals by natural selection, either by associative over-dominance or balancing selection, or a combination of both. Furthermore, we found a significant polynomial correlation between genetic variance and wing size and shape in the fast inbred lines. This was caused by a greater number of homozygous individuals among the fast inbred lines with small, narrow wings, which indicated inbreeding depression. Our results demonstrated that the same amount of inbreeding can have different effects on genetic variance depending on the inbreeding rate, with slow inbreeding leading to higher genetic variance than fast inbreeding. These results increase our understanding of the genetic basis of the common observation that slow inbred lines express less inbreeding depression than fast inbred lines. In addition, this has more general implications for the importance of selection in maintaining genetic variation.

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