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Adaptive Evolution of Mutual Mate Preferences in Nature

Final Report Summary - AEMMPN (Adaptive Evolution of Mutual Mate Preferences in Nature)

Main results achieved so far:

Due to the delays and failures to establish laboratory populations representing the latitudinal range of Drosophila serrata, as a result of the extreme weather conditions, the estimation of the among-population adaptive divergence in mate preferences was not possible. Despite the delays, the experimental test of within population mate preferences has been achieved and analysis focusing on male and female preferences is still on going. The large quantitative genetic experiment of male and female mating preferences was carried out mid-2011 and consisted of over 2200 mating trials and processing over 4500 gas chromatography samples for data analysis, to empirically test key predictions of the correlated response hypothesis. First, within the context of a quantitative genetic breeding design we estimated the degree to which the trait values favoured by male and female choice are similar both phenotypically and genetically. The direction of sexual selection on male and female CHCs differed statistically, and the trait combinations that maximised male and female mating success were not genetically correlated, suggesting that male and female preferences target genetically different signals. Second, despite detecting significant genetic variance in female preferences, we found no evidence for genetic variance in male preferences and, as a consequence, no detectable correlation between male and female mating preferences. Combined, these findings are inconsistent with the idea that male mate choice in D. serrata is simply a correlated response to female choice. Our results suggest that male and female preferences are genetically distinct traits in this species and may therefore have arisen via different evolutionary processes.
Since it became impossible to carry out the geographic work, we addressed several other questions regarding preferences, the evolution of sexual dimorphism and sexual selection that related to the objectives outlined in the original project proposal. The first involved examining sex-specific differences in fitness consequences resulting from dietary preferences. The aims of the experiment where to determine 1) how adult consumption of protein and carbohydrate influences sex-specific fitness and 2) the genetic (co)variance of adult dietary preferences between the sexes. Combing two approaches and using population level estimates of evolvability for male and female dietary preferences, by applying a recently developed theoretical framework, it was possible to estimate the macronutrient blends that maximize sex-specific fitness and the degree of shared genetic variance between males and females; thereby uncovering the potential for constraint in the evolution of sex-specific dietary preferences. These experiments demonstrated a significant influence of diet composition on fitness in males and females, but found the shape of the response surface differs between the sexes. We found the genetic variance for dietary preference is, to a large extent, shared between the sexes, with the shared genetic basis of the preference being for macronutrients rather than mating traits. However, despite finding a large degree of shared genetic variance and differences in the shape of the response surfaces, the predicted responses to selection in each sex are sufficiently similar that only limited constraints may operate on evolution of dietary preferences.

We have also worked towards understanding how the degree of constraint on sexual dimorphism within a population by testing the impact of between-sex between-trait genetic covariances using an extended version of the genetic variance-covariance matrix, G, that includes Lande’s (1980) between-sex covariance matrix, B. We find that including B greatly reduces the degree to which male and female traits are predicted to diverge in the face of divergent phenotypic selection. However, the degree to which B alters the response to selection differs between the sexes. The overall rate of male trait evolution is predicted to decline, but its direction remains relatively unchanged, whereas the opposite is found in females. We used this finding to emphasise the importance of considering the B-matrix in microevolutionary studies of constraints on the evolution of sexual dimorphism. We then took this further by statistically comparing orientation divergence of within-sex (G) to cross-sex (B) covariance matrices. In line with a previous theoretical prediction, we found that the cross-sex covariance matrix, B, is more variable than either within-sex G matrix. Decomposition of B matrices into their symmetrical and nonsymmetrical components revealed that instability is linked to the degree of asymmetry. We also find that the degree of asymmetry correlates with latitude suggesting a role for spatially varying natural selection in shaping genetic constraints on the evolution of sexual dimorphism.

We also have several other manuscripts at different levels of preparation. One of the key papers relates to examining differences in allele frequencies relating to male mating success, within a Genome-Wide Association Study (GWAS). This experiment addresses a fundamental question regarding the degree to which alleles that confer higher male mating success segregate within a population. The experimental design used binomial mating trials, with both the chosen and rejected males kept for genotyping and phenotyping, using a lab adapted population of Drosophila serrata. Over 4000 individuals were phenotyped for their mating pheromones and subsequently stored for DNA extraction. From this samples were randomly divided into two blocks, each block consisting of 2000 individuals. Within each of the blocks, the estimated selection vector was used to score all males in the dataset, resulting in a trait representing the linear combination of traits under sexual selection, β. Flies in the top and bottom 10% for β have been pooled for DNA extraction. The preliminary results from this experiment have highlighted underlying alleles responsible for male attractiveness and the frequency of these alleles within a stable population near its adaptive peak and will be submitted to Proceedings of the National Academy of Sciences.

During the return phase, we have implemented many of these advanced statistical approaches to testing barriers to gene flow in natural populations of damselflies (resubmitted to Proceedings of the Royal Society B: Biological Sciences), looking at the stability of morph frequencies in I. elegans (Resubmitted to American Naturalist), and fluctuations in selection, both linear and non-linear, across several populations in Southern Sweden (in preparation). We have also applied many of the techniques to a new study looking for genetic variation in wing interference patterns in Drosophila melanogaster.

In summary, despite several obstacles hampering the projects progress, the work achieved is exceptional, and included several large-scale projects, which have involved fieldwork, large quantitative genetic experiments, high throughput genotyping and gas chromatography and advanced statistical modeling, much of which falls directly under the project objectives of the proposal. The reintegration and transfer of knowledge at Lund University has been extremely successful, particularly in regard to using advanced statistical modeling integrated into a non-model field organism learned during the outgoing phase. We expect the final results from the work will have important consequences for the application of different statistical approaches for testing and measuring sexual selection in non-model field organisms. Furthermore, the continued collaboration between the University of Queensland, Australia and Lund University, Sweden will benefit all concerned, including the research profile of European research in general.