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Open Access Research article

The genetic architecture of fitness in a seed beetle: assessing the potential for indirect genetic benefits of female choice

T Bilde12*, U Friberg13, AA Maklakov14, JD Fry5 and G Arnqvist1

Author Affiliations

1 Animal Ecology/Department of Ecology and Evolution, Evolutionary Biology Centre, University of Uppsala, Uppsala SE-753 32, Sweden

2 Department of Biological Sciences, Ecology and Genetics, University of Aarhus, 8000 Aarhus C, Denmark

3 Department of Ecology, Evolution and Marine Biology, University of California, Santa Barbara, California 93106-9610, USA

4 School of Biological, Earth and Environmental Sciences, The University of New South Wales, Kensington, Sydney 2052, Australia

5 University of Rochester, Department of Biology, Rochester, New York 14627-0211, USA

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BMC Evolutionary Biology 2008, 8:295  doi:10.1186/1471-2148-8-295

Published: 26 October 2008

Abstract

Background

Quantifying the amount of standing genetic variation in fitness represents an empirical challenge. Unfortunately, the shortage of detailed studies of the genetic architecture of fitness has hampered progress in several domains of evolutionary biology. One such area is the study of sexual selection. In particular, the evolution of adaptive female choice by indirect genetic benefits relies on the presence of genetic variation for fitness. Female choice by genetic benefits fall broadly into good genes (additive) models and compatibility (non-additive) models where the strength of selection is dictated by the genetic architecture of fitness. To characterize the genetic architecture of fitness, we employed a quantitative genetic design (the diallel cross) in a population of the seed beetle Callosobruchus maculatus, which is known to exhibit post-copulatory female choice. From reciprocal crosses of inbred lines, we assayed egg production, egg-to-adult survival, and lifetime offspring production of the outbred F1 daughters (F1 productivity).

Results

We used the bio model to estimate six components of genetic and environmental variance in fitness. We found sizeable additive and non-additive genetic variance in F1 productivity, but lower genetic variance in egg-to-adult survival, which was strongly influenced by maternal and paternal effects.

Conclusion

Our results show that, in order to gain a relevant understanding of the genetic architecture of fitness, measures of offspring fitness should be inclusive and should include quantifications of offspring reproductive success. We note that our estimate of additive genetic variance in F1 productivity (CVA = 14%) is sufficient to generate indirect selection on female choice. However, our results also show that the major determinant of offspring fitness is the genetic interaction between parental genomes, as indicated by large amounts of non-additive genetic variance (dominance and/or epistasis) for F1 productivity. We discuss the processes that may maintain additive and non-additive genetic variance for fitness and how these relate to indirect selection for female choice.