Genomics of Developmental Plasticity in Animals

Abstract

Developmental plasticity refers to the property by which the same genotype produces distinct phenotypes depending on the environmental conditions under which development takes place. By allowing organisms to produce phenotypes adjusted to the conditions that adults will experience, developmental plasticity can provide the means to cope with environmental heterogeneity. Developmental plasticity can be adaptive and its evolution can be shaped by natural selection. It has also been suggested that developmental plasticity can facilitate adaptation and promote diversification. Here, we summarize current knowledge on the evolution of plasticity and on the impact of plasticity on adaptive evolution, and we identify recent advances and important open questions about the genomics of developmental plasticity in animals. We give special attention to studies using transcriptomics to identify genes whose expression changes across developmental environments and studies using genetic mapping to identify loci that contribute to variation in plasticity and can fuel its evolution.

Keywords: developmental plasticity; environmentally responsive genes; genomics of plasticity; plasticity variation; reaction norms.

Figure 1

Environmental effects on phenotype expression. (A) Illustration of two emblematic examples of developmental plasticity: thermal plasticity in body size and pigmentation in D. melanogaster flies and B. anynana butterflies. (B–D) Illustration of reaction norms where phenotype is represented as a function of environmental conditions. Reaction norms can differ between traits (for the same genotype and in relation to the same cue), between environmental cues (for the same genotype and trait), and between genotypes (for the same cue and trait). (B) Reaction norms represent environmental effects on trait expression which can be of different general types: unresponsive phenotype robust to environmental variation (gray line), a continuous response (blue line), a switch-like relationship with discrete alternative phenotypes above and below some environmental threshold (red line). (C) Schematic representation of phenotypic values for two genetic backgrounds (G1 and G2) developing under two environmental conditions (E1 and E2). Total phenotypic variation in a population can be partitioned into genetic variation (difference between circles and squares), environmental variation (difference between filled and empty symbols) and GxE variation (difference between red and blue lines). There is also an intra-genotype, intra-environment component of variation, often assigned to “noise”, which is represented by the shadowing around the lines. (D) Genotypes can differ in distinct properties of reactions norms, such as intercept, slope, shape, and/or threshold at which the phenotype responds to environmental variation. In some cases it is possible to use genetic mapping approaches to identify the genes that contribute to such inter-genotype differences in reaction norms.

Figure 2

From the inductive environment to the production of alternative phenotypes. (A) For the external conditions to affect development environmental cues need to be perceived or sensed (via sensor mechanisms) and this information needs to be transmitted to the developing tissues by internal signals (via modulators, such as hormones). Upon receiving such signals, local changes in gene expression (effector genes) and/or function will modify development and give rise to alternative adult phenotypes. In cases of adaptive plasticity, alternative adult phenotypes are better suited to their respective environments. (B) Schematic representation of C. elegans life cycle and dauer formation showing examples of the molecular players involved in the plastic response (reviewed in Fielenbach and Antebi, 2008). Under favorable environments, C. elegans progresses rapidly through larval development until adulthood. When facing unfavorable conditions, such as high population density, starvation, and/or high temperature, C. elegans undergoes development to a specialized larval diapause stage called dauer, which can last several months. The process starts with the perception of the inductive environmental cues (e.g. ascaroside pheromones, nutrients, and/or temperature) via sensory organs, called amphid neurons. Amphid neurons then transduce external signals into endocrine signals (via G protein-coupled receptors). When hormonal signaling mechanisms (e.g. TGF-β, insulin, and steroids) are down regulated, they induce dauer diapause. Serotonergic signaling influences the production of TGF-β and insulin-like peptides (ILPs). Down-regulated ILP and TGF-β production results in nuclear translocation of different genes, including DAF genes and FOXO, that will then turn on genes for stress resistance, dauer formation, and longevity.

Figure 3

Genome-wide searches for the genetic basis of plasticity. Efforts to explore the genomics of plasticity include transcriptomics and mapping studies [e.g. genome-wide association studies (GWAS)] to identify genes whose expression changes across environments and loci contributing to variation in plasticity, respectively. These genes might or might not be the same, as illustrated by the colored loci in (A and B). (A) Volcano plot where the significance in gene expression differences (Y-axis) is displayed as a function of fold change expression across environments (X-axis). Two genes showing significant expression differences (above significance threshold represented by the horizontal line) are highlighted in blue and orange. One where expression is not statistically significantly difference is highlighted in red. (B) Manhattan plot where statistical significance in the association with inter-genotype differences in reaction norms (Y-axis) is displayed for each polymorphic site along the chromosomes (X-axis). The location of two polymorphisms showing statistically significant association with plasticity variation is highlighted in red and orange, respectively. One below the statistical significance threshold is highlighted in blue. Genes whose expression is plastic across environments may (gene in orange) or may not (gene in blue) harbor allelic variants contributing to variation in plasticity. Conversely, genes associated with variation in plasticity may (gene in orange) or may not (gene in red) differ in expression between environments.

Figure 4

Relationship between quantitative trait loci (QTL) effects on trait mean and trait plasticity. Schematic representation of the ways in which a bi-allelic polymorphic site, e.g. a single nucleotide polymorphism (SNP) with alternative alleles (A and B; squares and circles, respectively), can contribute to phenotypic variation within fixed environmental conditions (E1 or E2; filled and empty symbols, respectively) and/or to plasticity in relation to those environmental values (reaction norms; solid and dashed lines). The contribution of each polymorphic site to phenotypic variation within environments and/or to variation in plasticity is illustrated in the Venn diagram. The area of the Venn diagram with a striped pattern indicates the aspect(s) of phenotypic variance a polymorphic site would be significantly associated with (i.e. is a QTL for). (A) Genotypes with the A allele have higher trait values than those with the B allele, in both environments E1 and E2, but reaction norms are of the same slope (corresponding to no plasticity in the left and to plasticity in the right). Such SNP would be associated with inter-genotype variation in environments E1 and E2 but not to inter-genotype variation in plasticity. (B) Genotypes with the A allele have higher trait values than those with the B allele in environment E1 but not in environment E2. Genotypes with A and B alleles have reaction norms that can be flat or steep in any direction. Such SNP could be associated with inter-genotype trait variation in environment E1 but not trait variation in environment E2 or variation in plasticity. (C) Genotypes with A and B alleles have same mean trait values in both environments E1 and E2 but different reaction norm properties: flat (genotypes with the A allele) versus steep (B allele) reaction norms on the left and positive (A allele) versus negative (B allele) reaction norms on the right. Such SNPs would be associated with variation in plasticity but not variation within E1 or E2. (D) An example of an SNP affecting both trait variation in E1 (A alleles corresponding to higher trait values than B allele) and E2 (A alleles corresponding to lower trait values than B allele) as well as variation in plasticity (negative slope reaction norms for A allele versus positive for B allele).