Abstract
BackgroundQuantifying 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).ResultsWe 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.ConclusionOur 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.
Highlights
Quantifying the amount of standing genetic variation in fitness represents an empirical challenge
In the initial diallel cross, variance in lifetime egg production came from highly significant contributions of σ2m and σ2p, representing line-specific maternal and paternal effects, respectively
Our analyses revealed sizeable additive and non-additive components of genetic variation for our most comprehensive fitness variable (F1 productivity) in C. maculatus, illustrating that the diallel cross offers a useful empirical route to provide insights into rather complex aspects of the genetic architecture of fitness
Summary
Quantifying the amount of standing genetic variation in fitness represents an empirical challenge. Models for the evolution of female choice based on indirect genetic benefits are usually grouped into good genes models, where alleles with additive effects confer fitness benefits, and compatibility models, where the combining ability of specific alleles (i.e., epistasis) of the male and female genomes determines fitness [2,9,10]. These models, rely on different types of genetic variation for fitness
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