Genetic Control of Environmental Variation of Two Quantitative Traits ofDrosophila melanogasterRevealed by Whole-Genome Sequencing

Abstract

Genetic studies usually focus on quantifying and understanding the existence of genetic control on expected phenotypic outcomes. However, there is compelling evidence suggesting the existence of genetic control at the level of environmental variability, with some genotypes exhibiting more stable and others more volatile performance. Understanding the mechanisms responsible for environmental variability not only informs medical questions but is relevant in evolution and in agricultural science. In this work fully sequenced inbred lines of Drosophila melanogaster were analyzed to study the nature of genetic control of environmental variance for two quantitative traits: starvation resistance (SR) and startle response (SL). The evidence for genetic control of environmental variance is compelling for both traits. Sequence information is incorporated in random regression models to study the underlying genetic signals, which are shown to be different in the two traits. Genomic variance in sexual dimorphism was found for SR but not for SL. Indeed, the proportion of variance captured by sequence information and the contribution to this variance from four chromosome segments differ between sexes in SR but not in SL. The number of studies of environmental variation, particularly in humans, is limited. The availability of full sequence information and modern computationally intensive statistical methods provides opportunities for rigorous analyses of environmental variability.KEYWORDS Bayesian inference; environmental sensitivity; genetic control of environmental variance; genomic models; random regression models E NVIRONMENTAL sensitivity can be defined either as mean phenotypic changes of a given genotype in different environments or as differences in the environmental variance of different genotypes in the same environment (Jinks and Pooni 1988). The first definition gives rise to genotype-byenvironment interaction at the level of the mean, a topic that has a long history due to its relevance in livestock and plant breeding as well as in medical genetics. Recent articles on specific areas are Huquet et al. (2012) in livestock, El-Soda et al. (2014) in plants, andHutter et al. (2013) in humans.The second definition implies that environmental variance is under genetic control and is the subject of the present work. Genetic control of environmental variation has implications in evolutionary biology, in animal and plant improvement, and in medicine. In evolutionary biology, a fundamental problem is to understand the forces that maintain phenotypic variation. Most of the models assume that environmental variance is constant and explain the observed levels of variation by invoking a balance between a gain of genetic variance by mutation and a loss by different forms of selection and drift. Zhang and Hill (2005) discuss models where environmental variance is partly under genetic control and study conditions for its maintenance under stabilizing selection. From a breeding point of view, if environmental variance is und...

Environmental variation partitioned into separate heritable components

“…; Sørensen et al. ). The finding that V WE is under genetic control suggests that this trait will be impacted by selection and genetic drift.…”

“…; Sørensen et al. ), and have recently been shown to respond to selection, without affecting trait mean (Blasco et al. ).…”

Genomic Prediction for Quantitative Traits Is Improved by Mapping Variants to Gene Ontology Categories inDrosophila melanogaster

“…In this study we used a GFBLUP model with two genomic effects (f and r in model M GFBLUP ), but in principle it is possible to include multiple genomic feature effects (Speed and Balding 2014;Sørensen et al 2015). However, as our simulations with only two genomic effects indicate, the complex correlation patterns that are likely to exist between different parts of the genome may lead to inaccurate estimates of the genomic variances and consequently decreased predictive ability.…”

“…The GFBLUP model can be implemented using a Bayesian mixed model (e.g., Sørensen et al 2015) or Bayesian mixture models such as BayesRC (MacLeod et al 2014). BayesRC is the same as BayesR except that, a priori, each SNP is identified as belonging to a specific genomic feature and it allows for differential shrinkage within each genomic feature.…”

Correlated Response to Selection for Litter Size Residual Variance in Rabbits

“…Nevertheless, there was a negative correlated response in early embryonic development and survival. In recent years, there has been an increasing interest in the genetic determination of the environmental variance Sørensen et al, 2015). In animal breeding, a decrease in environmental variance will increase the heritability, being particularly interesting for increasing the response to selection in low heritability traits, such as litter size Formoso-Rafferty et al, 2016).…”