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

2021 ◽  
Vol 288 (1960) ◽  
Author(s):  
Adam J. Reddiex ◽  
Stephen F. Chenoweth

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.

2021 ◽  
Author(s):  
Adam J Reddiex ◽  
Stephen Chenoweth

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.


Genetics ◽  
2003 ◽  
Vol 164 (4) ◽  
pp. 1615-1626
Author(s):  
D Waxman ◽  
J R Peck

Abstract A model is presented in which alleles at a number of loci combine to influence the value of a quantitative trait that is subject to stabilizing selection. Mutations can occur to alleles at the loci under consideration. Some of these mutations will tend to increase the value of the trait, while others will tend to decrease it. In contrast to most previous models, we allow the mean effect of mutations to be nonzero. This means that, on average, mutations can have a bias, such that they tend to either increase or decrease the value of the trait. We find, unsurprisingly, that biased mutation moves the equilibrium mean value of the quantitative trait in the direction of the bias. What is more surprising is the behavior of the deviation of the equilibrium mean value of the trait from its optimal value. This has a nonmonotonic dependence on the degree of bias, so that increasing the degree of bias can actually bring the mean phenotype closer to the optimal phenotype. Furthermore, there is a definite maximum to the extent to which biased mutation can cause a difference between the mean phenotype and the optimum. For plausible parameter values, this maximum-possible difference is small. Typically, quantitative-genetics models assume an unconstrained model of mutation, where the expected difference in effect between a parental allele and a mutant allele is independent of the current state of the parental allele. Our results show that models of this sort can easily lead to biologically implausible consequences when mutations are biased. In particular, unconstrained mutation typically leads to a continual increase or decrease in the mean allelic effects at all trait-controlling loci. Thus at each of these loci, the mean allelic effect eventually becomes extreme. This suggests that some of the models of mutation most commonly used in quantitative genetics should be modified so as to introduce genetic constraints.


Author(s):  
Bruce Walsh ◽  
Michael Lynch

One of the major unresolved issues in quantitative genetics is what accounts for the amount of standing genetic variation in traits. A wide range of models, all reviewed in this chapter, have been proposed, but none fit the data, either giving too much variation or too little apparent stabilizing selection.


2009 ◽  
Vol 36 (1) ◽  
pp. 37-56 ◽  
Author(s):  
Neus Martínez-Abadías ◽  
Carolina Paschetta ◽  
Soledad de Azevedo ◽  
Mireia Esparza ◽  
Rolando González-José

2012 ◽  
Vol 2 (2) ◽  
pp. 287-297 ◽  
Author(s):  
Ann J. Stocker ◽  
Bosco B. Rusuwa ◽  
Mark J. Blacket ◽  
Francesca D. Frentiu ◽  
Mitchell Sullivan ◽  
...  

1989 ◽  
Vol 54 (1) ◽  
pp. 45-58 ◽  
Author(s):  
Peter D. Keightley ◽  
William G. Hill

SummaryA model of genetic variation of a quantitative character subject to the simultaneous effects of mutation, selection and drift is investigated. Predictions are obtained for the variance of the genetic variance among independent lines at equilibrium with stabilizing selection. These indicate that the coefficient of variation of the genetic variance among lines is relatively insensitive to the strength of stabilizing selection on the character. The effects on the genetic variance of a change of mode of selection from stabilizing to directional selection are investigated. This is intended to model directional selection of a character in a sample of individuals from a natural or long-established cage population. The pattern of change of variance from directional selection is strongly influenced by the strengths of selection at individual loci in relation to effective population size before and after the change of regime. Patterns of change of variance and selection responses from Monte Carlo simulation are compared to selection responses observed in experiments. These indicate that changes in variance with directional selection are not very different from those due to drift alone in the experiments, and do not necessarily give information on the presence of stabilizing selection or its strength.


2014 ◽  
Vol 369 (1649) ◽  
pp. 20130255 ◽  
Author(s):  
Geir H. Bolstad ◽  
Thomas F. Hansen ◽  
Christophe Pélabon ◽  
Mohsen Falahati-Anbaran ◽  
Rocío Pérez-Barrales ◽  
...  

If genetic constraints are important, then rates and direction of evolution should be related to trait evolvability. Here we use recently developed measures of evolvability to test the genetic constraint hypothesis with quantitative genetic data on floral morphology from the Neotropical vine Dalechampia scandens (Euphorbiaceae). These measures were compared against rates of evolution and patterns of divergence among 24 populations in two species in the D. scandens species complex. We found clear evidence for genetic constraints, particularly among traits that were tightly phenotypically integrated. This relationship between evolvability and evolutionary divergence is puzzling, because the estimated evolvabilities seem too large to constitute real constraints. We suggest that this paradox can be explained by a combination of weak stabilizing selection around moving adaptive optima and small realized evolvabilities relative to the observed additive genetic variance.


Behaviour ◽  
2004 ◽  
Vol 141 (3) ◽  
pp. 327-341 ◽  
Author(s):  
Wolf Blanckenhorn ◽  
Claudia Mühlhäuser

AbstractIn the common dung or black scavenger fly Sepsis cynipsea (Diptera: Sepsidae) several morphological and behavioural male and female traits interact during mating. Previous studies show that males attempt to mount females without courtship, females use vigorous shaking behaviour in response to male mounting, the duration of shaking is an indicator of both direct and indirect female choice and sexual conflict, and larger males enjoy a mating advantage. We conducted a quantitative genetic paternal half sib study to investigate the genetic underpinnings of these traits, notably body size (the preferred trait) and the associated female preference, and to assess the relative importance of various models generally proposed to account for the evolution of sexually selected traits. Several morphological traits and female shaking duration were heritable, thus meeting a key requirement of all sexual selection models. In contrast, two traits indicative of male persistence in mating were not. Male longevity was also heritable and negatively correlated with his mating effort, suggesting a mating cost. However, the crucial genetic correlation between male body size and female shaking duration, predicted to be negative by both 'good genes' and Fisherian models and positive by the sexual conflict (or chase-away) model, was zero. This could be because of low power, or because of constraints imposed by the genetic correlation structure. Based on our rsults we conclude that discriminating sexual selection models by sole means of quantitative genetics is difficult, if not impossible.


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