Exactly how the high genetic variance of traits involved in sexual selection through female mate choice is maintained is a much debated issue1,2,3. Theoretical models attempt to explain the high genetic variance of sexual traits, among others, by the evolution of condition dependence1,4, in which expression of the trait depends on physical condition. If it is costly to be choosy, then these models should also apply to female mate preference and predict that female condition affects the choice of mate. Here we allow female laboratory-bred three-spined sticklebacks, Gasterosteus aculeatus, to choose between computer animations of courting males5, and find that the choice of mate correlates well with female physical condition.
Heritability estimates of mate preference have accumulated in recent years: the average heritability (±s.d.) of mate preference in 15 species was 0.41 (±0.21) (ref. 3), which is high for a behavioural trait6. Condition dependence might explain the high heritability of costly mate preferences, as it does the high genetic variance in sexual traits1,4. Costs may include physiological as well as choice costs. Condition dependence of sexual traits is well known7, and there is some evidence for condition-dependent mate choice3,8. We have studied the covariance of condition and mate preference in a fish species that is well-known for intensive sexual selection2.
Sticklebacks were bred from wild-caught parents, and were raised and maintained under standardized laboratory conditions in full-sibling groups of similar size. Paternal effects on offspring traits were excluded by removing clutches from the fathers' nests one hour after fertilization. After reaching adult body size, fish were transferred from simulated summer to winter conditions, under which gonadal development and the development of male breeding coloration are suppressed.
Six months later, the condition factor9 of a random sample of males per full-sib group was assessed. Average male winter condition per group was taken as an index of group rearing condition because some females showed signs of egg production under the prolonged winter conditions. Male physical condition is not confounded by possible between-group variance in ovarian development. Females were randomly sampled from the full-sib groups about six months later and placed individually in 10-litre tanks under simulated summer conditions, where they became reproductive.
When females became ripe they were tested for their preference for red males by placing them in a one-litre cuvette in front of a computer monitor on which two virtual males that differed only in red breeding coloration (bright red or bright orange) were courting simultaneously5. In this preference test, males differ in only one trait, and there are no costs of choice.
Despite standardized rearing conditions, progeny from different fathers differed significantly in condition during rearing (ANOVA, F(10,67)=7.65, P<0.001) and in preference for red coloration (ANOVA, F(10,13)=3.52, P<0.02). Overall, there was no significant preference for the bright red male over the bright orange one (t-test, t=0.37, df=10, P>0.71), but average red preference and rearing condition per father correlated positively (r=0.77, N=11, P<0.01; Fig. 1). Females from groups with a high average condition factor before reproduction therefore preferred the red male, whereas those of lower rearing condition showed a preference for the orange male.
Combined with condition dependence of sexual traits, the covariance of mate preferences with condition may have consequences for the evolution of both preferences and preferred sexual traits. Experiments must show whether mate preferences have condition-dependent expression. When mate preferences appear to be condition dependent, and assuming there is high genetic variance in condition4, pleiotropic effects of genes that influence condition would be expected to lead to high genetic correlations between sexual trait and mate preference. Alternatively, the covariance of mate preference with condition may be brought about by genetic covariance of sexual male traits with both female preference10 and male condition. The consequences of these alternatives should be explored using theoretical models of sexual selection.
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