Sense and sensitivity : a quantitative genetic analysis of gene-environment interactions in life history traits in the nematode Caenorhabditis elegans (2004)

In studying the relationship between DNA (orthe genotype) and phenotypic characteristics (or the phenotype) scientists often use single genes coding for single traits. Fundamentally this choice makes sense, as it makes research easier. However, most traits are determined by more than one gene. They furthermore often depend on environmental factors as well, of which temperature is a good example. For instance, the sex of most reptile species is determined by the temperature at which the eggs develop. Next, for most ectotherms size at reproduction is also temperature-dependent, with decreasing temperatures usually leading to increased sizes at maturity.In general, these interactions are referred to as phenotypic plasticity. The ability of a single genotype (for example, clones) to produce different phenotypes in response to different environments is widespread in nature. Since long, scientists have been intrigued by what mechanism could cause the plastic response. Although it is generally accepted that there is ageneticregulation of the response, perspectives on the underlying mechanism frequently disagreed. Two models have been proposed in literature: allelic sensitivity and regulatory loci . Here, the model of allelic sensitivity assumes that the environment directly affects the expression of the genes underlying the trait and in that way causes the plastic response. The model of regulatory loci, on the other hand, assumes that there are separate genes for the response to the environment and for the trait itself. These separate genes are the regulatory loci, and 'cause' the plastic response by mediating the expression of the genes underlying the trait. The difference in perspectives, therefore, lies within the effect of the environment on the expression of the genes underlying the trait: either directly, as for the model of allelic sensitivity, or indirectly, as for the model of regulatory loci. However, although theoretically frequently discussed in literature, little empirical data is available on which mechanism occurs in nature.The research described in this thesis aims to finding an answer to this question using the model organism Caenorhabditis elegans , a 1 to 1.5 mm long nematode. To do so two wildtype populations, originating from Bristol (UK) and Hawaii (USA), were crossed in the laboratory to obtain a set of genetically divergent (recombinant inbred) strains. A subset of these strains was subsequently genetically analyzed using single nucleotide polymorphisms as genetic markers, to determine which section of DNA was inherited by all strains from which parent. Lines were furthermore phenotypically analyzed at two different temperatures for several life history traits, such as age and size at maturity, growth rate, and fecundity. Finally, a quantitative trait loci (QTL) analysis was performed on both the phenotypic characteristics at each temperature as well as on the phenotypically plastic response, in order to identify QTL correlating with the trait(s) in question.A detailed analysis of the genotypes of all strains (chapter 2) showed that during the crossing and inbreeding of the recombinant inbred strains selection had occurred for heritable traits of one of the two parents. We could not determine exactly which traits were selected for, although in one case (a biased segregation of a genetic marker on chromosome I) it appeared that selection had occurred for a gene (or several genes) involved in reproduction.For most traits, the quantitative genetic analysis (chapters 3, 4, and 5) resulted in the identification of several QTL for most of the traits analyzed. Here, chapter 3 elaborates on the QTL for traits if measured in different environments, of which many show significant QTL x Environment interaction. Therefore (or because of that), the detection of QTL is dependent on the conditions in which the experiments are performed. This appears to be obvious but is largely neglected in most QTL studies.Chapter 4 focuses on the correlations between traits. Apart from being under environmental control most life history traits are known to be connected to each other by means of trade-offs (in both positive as negative sense). For C. elegans several of the studied life history traits indeed show such correlations, although the magnitude as well as (in some cases) the direction of this correlation appears to depend on environmental conditions as well.Chapter 5, finally, describes the quantitative genetic analysis of phenotypic plasticity in the studied life history traits. For four out of six traits plasticity QTL are detected.Theseplasticity QTL were compared with the QTL found for the traits in one of the two environments (chapter 3) and were in more detail analyzed for the effects on the trait itself in one of the two environments. The results of these analyses suggest that in C. elegans phenotypic plasticity in response to temperature is caused by temperature-dependent gene expression of the genes underlying the trait itself, or in other words the model of allelic sensitivity. With regulatory loci being explained as a potential mechanism for anticipating to environmental change C. elegans in that respect lives too short to develop or need such a mechanism, and therefore uses allelic sensitivity to optimize fitness to environmental conditions.Despite the fact that much is already known on the genetics of C. elegans we could not identify individual genes within the QTL found. However, with QTL encompassing several hundreds to thousands of candidate genes for the gene underlying the plastic response this was also an (almost) impossible task. However, we expect that the use of a combination of different techniques, for example mutant analysis or mRNA expression profiling combined with QTL analyses or the data presented here, will succeed to do so in the foreseeable future.