Integrating genomics and multivariate evolutionary quantitative genetics: a case study of constraints on sexual selection in Drosophila serrata

In evolutionary quantitative genetics, the genetic variance–covariance matrix, G , and the vector of directional selection gradients, β , are key parameters for predicting multivariate selection responses and genetic constraints. Historically, investigations of G and β have not overlapped with those dissecting the genetic basis of quantitative traits. Thus, it remains unknown whether these parameters reflect pleiotropic effects at individual loci. Here, we integrate multivariate genome-wide association study (GWAS) with G and β estimation in a well-studied system of multivariate constraint: sexual selection on male cuticular hydrocarbons (CHCs) in Drosophila serrata . In a panel of wild-derived re-sequenced lines, we augment genome-based restricted maximum likelihood to estimate G alongside multivariate single nucleotide polymorphism (SNP) effects, detecting 532 significant associations from 1 652 276 SNPs. Constraint was evident, with β lying in a direction of G with low evolvability. Interestingly, minor frequency alleles typically increased male CHC-attractiveness suggesting opposing natural selection on β . SNP effects were significantly misaligned with the major eigenvector of G , g max , but well aligned to the second and third eigenvectors g 2 and g 3 . We discuss potential factors leading to these varied results including multivariate stabilizing selection and mutational bias. Our framework may be useful as researchers increasingly access genomic methods to study multivariate selection responses in wild populations.

The genetic and social contributions to sex differences in lifespan in Drosophila serrata

Sex differences in lifespan remain an intriguing puzzle for evolutionary biologists. A possible explanation for lower lifespan in males is the unconditional expression of recessive deleterious alleles in heterogametic X chromosomes in males (the unguarded X hypothesis). Empirical evidence, however, has yielded controversial results that can be attributed to differences in both genetic and social background. Here, we test the unguarded X hypothesis in Drosophila serrata using a factorial design to quantify the effects of genotype, sex, social environment, and their interactions on phenotypic variation for lifespan. Using an experimental approach, we manipulated two inbred laboratory genotypes and their reciprocal F1s, while controlling for different levels of density and mating status to account for any potential social effects. Our results also show subtle but significant genotype dependent effects for both density and mating, but ultimately find the unguarded X hypothesis insufficient to fully explain sexual dimorphism in D. serrata lifespan.

Integrating genomics and multivariate evolutionary quantitative genetics: A case study of multivariate constraints on sexual selection in Drosophila serrata

In evolutionary quantitative genetics, the genetic variance-covariance matrix, G, and the vector of directional selection gradients, β , are key parameters for predicting multivariate selection responses and genetic constraints. Historically, investigations of G and β have not overlapped with those dissecting the genetic basis of quantitative traits. Thus, it remains unknown whether these parameters reflect pleiotropic effects at individual loci. Here, we integrate multivariate GWAS with G and β estimation in a well-studied system of multivariate constraint; sexual selection on male cuticular hydrocarbons (CHCs) in Drosophila serrata. In a panel of wild-derived resequenced lines, we augment genome-based REML, (GREML) to estimate G alongside multivariate SNP effects, detecting 532 significant associations from 1,652,276 SNPs. Constraint was evident, with β lying in a direction of G with low evolvability. Interestingly, minor frequency alleles typically increased male CHC-attractiveness suggesting opposing natural selection on β. SNP effects were significantly misaligned with the major eigenvector of G, gmax, but well aligned to the second and third eigenvectors g2 and g3. We discuss potential factors leading to these varied results including multivariate stabilising selection and mutational bias. Our framework may be useful as researchers increasingly access genomic methods to study multivariate selection responses in wild populations.

The contribution of mutation and selection to multivariate quantitative genetic variance in an outbred population of Drosophila serrata

Genetic variance is not equal for all multivariate combinations of traits. This inequality, in which some combinations of traits have abundant genetic variation while others have very little, biases the rate and direction of multivariate phenotypic evolution. However, we still understand little about what causes genetic variance to differ among trait combinations. Here, we investigate the relative roles of mutation and selection in determining the genetic variance of multivariate phenotypes. We accumulated mutations in an outbred population of Drosophila serrata and analyzed wing shape and size traits for over 35,000 flies to simultaneously estimate the additive genetic and additive mutational (co)variances. This experimental design allowed us to gain insight into the phenotypic effects of mutation as they arise and come under selection in naturally outbred populations. Multivariate phenotypes associated with more (less) genetic variance were also associated with more (less) mutational variance, suggesting that differences in mutational input contribute to differences in genetic variance. However, mutational correlations between traits were stronger than genetic correlations, and most mutational variance was associated with only one multivariate trait combination, while genetic variance was relatively more equal across multivariate traits. Therefore, selection is implicated in breaking down trait covariance and resulting in a different pattern of genetic variance among multivariate combinations of traits than that predicted by mutation and drift. Overall, while low mutational input might slow evolution of some multivariate phenotypes, stabilizing selection appears to reduce the strength of evolutionary bias introduced by pleiotropic mutation.

Causes of variability in estimates of mutational variance from mutation accumulation experiments

Characteristics of the new phenotypic variation introduced via mutation have broad implications in evolutionary and medical genetics. While many estimates of this mutational variance have been published, factors contributing to their range, spanning two orders of magnitude, remain poorly resolved. In this study, we first apply a meta-analytic approach to assess how previously implicated factors affect variability in estimates. While estimates of mutational variance are available from a range of taxa, and quantitative trait type over a range of timescales, these factors are confounded with one another, precluding a clear resolution of causes of observed variability. We call for further directly comparable empirical data to address this question. We then applied a modified mutation accumulation experimental design to generate independent repeated estimates of mutational variance for a single taxon (the vinegar fly, Drosophila serrata), and for a single trait type (wing morphology) under the same experimental conditions. Analyses revealed that, in this tightly controlled experiment, variability in among-line (mutational) variance was largely the consequence of sampling error. Micro-environmental variation in mutational effects was supported as a cause of low levels of variability in mutational variance for two of 11 traits analysed. Further, there was no evidence that variation in segregating mutations, as the realisation of the mutation-drift process, impacted estimates. This investigation demonstrates the utility of short-term repeated measures to be broadly applied to improve estimates of mutational variance, consequently expanding our understanding of the dynamics of mutations in natural populations.

No support for intra-nor inter-locus sexual conflict over mating latency and copulation duration in a polyandrous fruit fly

The total strength of sexual selection on males depends on the relationship between various components of pre- and post-copulatory fitness. Misalignment between male and female interests creates inter-locus sexual conflict, where the fitness of one sex is increased at the expense of the other. Although rarely considered, mating behaviours can also be genetically correlated between males and females, creating intra-locus sexual conflict, where beneficial alleles in one sex are costly when expressed in the other sex. How inter- and intra-locus sexual conflicts operate on the expression of mating behaviours remains little understood. Here, we study male attractiveness, mating latency and copulation duration in two populations of the polyandrous Drosophila serrata. Univariate analyses show little genetic variance in mating latency, and that males, but not females, contribute to copulation duration genetic variance. Further, multivariate analyses revealed little covariance between the studied traits. However, analyses considering male and female contribution in a single framework supported genetic contributions from both sexes for mating behaviours and complex patterns of between sexes correlations. Finally, our study did not find any association between those mating behaviours and fitness component, specifically (i) no phenotypic covariance between male attractiveness and mating latency and, (ii) longer copulations did not result in the production of more offspring. With no detectable fitness benefits in any sexes for shorter mating latency or longer copulation duration, our results do not support the presence of inter-nor intra-locus sexual conflict for these mating traits.

The transposable elements of the Drosophila serrata reference panel

Transposable elements are an important element of the complex genomic ecosystem, proving to be both adaptive and deleterious - repressed by the piRNA system and fixed by selection. Transposable element insertion also appears to be bursty – either due to invasion of new transposable elements that are not yet repressed, de-repression due to instability of organismal defense systems, stress, or genetic variation in hosts. Here, we characterize the transposable element landscape in an important model Drosophila, D. serrata, and investigate variation in transposable element copy number between genotypes and in the population at large. We find that a subset of transposable elements are clearly related to elements annotated in D. melanogaster and D. simulans, suggesting they spread between species more recently than other transposable elements. We also find that transposable elements do proliferate in particular genotypes, and that often if an individual is host to a proliferating transposable element, it is host to more than one proliferating transposable element. In addition, if a transposable element is active in a genotype, it is often active in more than one genotype. This suggests that there is an interaction between the host and the transposable element, such as a permissive genetic background and the presence of potentially active transposable element copies. In natural populations an active transposable element and a permissive background would not be held in association as in inbred lines, suggesting the magnitude of the burst would be much lower. Yet many of the inbred lines have actively proliferating transposable elements suggesting this is an important mechanism by which transposable elements maintain themselves in populations.