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Gene expression and the evolution of phenotypic diversity in social wasps.

ABSTRACT: BACKGROUND: Organisms are capable of developing different phenotypes by altering the genes they express. This phenotypic plasticity provides a means for species to respond effectively to environmental conditions. One of the most dramatic examples of phenotypic plasticity occurs in the highly social hymenopteran insects (ants, social bees, and social wasps), where distinct castes and sexes all arise from the same genes. To elucidate how variation in patterns of gene expression affects phenotypic variation, we conducted a study to simultaneously address the influence of developmental stage, sex, and caste on patterns of gene expression in Vespula wasps. Furthermore, we compared the patterns found in this species to those found in other taxa in order to investigate how variation in gene expression leads to phenotypic evolution. RESULTS: We constructed 11 different cDNA libraries derived from various developmental stages and castes of Vespula squamosa. Comparisons of overall expression patterns indicated that gene-expression differences distinguishing developmental stages were greater than expression differences differentiating sex or caste. Furthermore, we determined that certain sets of genes showed similar patterns of expression in the same phenotypic forms of different species. Specifically, larvae upregulated genes related to metabolism and genes possessing structural activity. Surprisingly, our data indicated that at least a few specific gene functions and at least one specific gene family are important components of caste differentiation across social insect taxa. CONCLUSION: Despite research on various aspects of development originating from model systems, growth in understanding how development is related to phenotypic diversity relies on a growing literature of contrasting studies in non-model systems. In this study, we found that comparisons of patterns of gene expression with model systems highlighted areas of conserved and convergent developmental evolution across diverse taxa. Indeed, conserved biological functions across species implicated key functions related to how phenotypes are built. Finally, overall differences between social insect taxa suggest that the independent evolution of caste arose via distinct developmental trajectories.

SUBMITTER: Hoffman EA

PROVIDER: S-EPMC1884141 | biostudies-literature | 2007

REPOSITORIES: biostudies-literature

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Gene expression and the evolution of phenotypic diversity in social wasps.

Hoffman Eric A EA Goodisman Michael A D MA

BMC biology 20070515

<h4>Background</h4>Organisms are capable of developing different phenotypes by altering the genes they express. This phenotypic plasticity provides a means for species to respond effectively to environmental conditions. One of the most dramatic examples of phenotypic plasticity occurs in the highly social hymenopteran insects (ants, social bees, and social wasps), where distinct castes and sexes all arise from the same genes. To elucidate how variation in patterns of gene expression affects phen ...[more]

PMID: 17504526

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Project description:BackgroundMendelian inheritance is a fundamental law of genetics. When we consider two genomes in a diploid cell, a heterozygote's phenotype is dominated by a particular homozygote according to the law of dominance. Classical Mendelian dominance is concerned with which proteins are dominant, and is usually based on simple genotype-phenotype relationship in which one gene regulates one phenotype. However, in reality, some interactions between genes can exist, resulting in deviations from Mendelian dominance. Whether and how Mendelian dominance is generalized to the phenotypes of gene expression determined by gene regulatory networks (GRNs) remains elusive.ResultsHere, by using the numerical evolution of diploid GRNs, we discuss whether the dominance of phenotype evolves beyond the classical Mendelian case of one-to-one genotype-phenotype relationship. We examine whether complex genotype-phenotype relationship can achieve Mendelian dominance at the expression level by a pair of haplotypes through the evolution of the GRN with interacting genes. This dominance is defined via a pair of haplotypes that differ from each other but have a common phenotype given by the expression of target genes. We numerically evolve the GRN model for a diploid case, in which two GRN matrices are added to give gene expression dynamics and simulate evolution with meiosis and recombination. Our results reveal that group Mendelian dominance evolves even under complex genotype-phenotype relationship. Calculating the degree of dominance shows that it increases through the evolution, correlating closely with the decrease in phenotypic fluctuations and the increase in robustness to initial noise. We also demonstrate that the dominance of gene expression patterns evolves concurrently. This evolution of group Mendelian dominance and pattern dominance is associated with phenotypic robustness against meiosis-induced genome mixing, whereas sexual recombination arising from the mixing of genomes from the parents further enhances dominance and robustness. Due to this dominance, the robustness to genetic differences increases, while optimal fitness is sustained to a significant difference between the two genomes.ConclusionGroup Mendelian dominance and gene-expression pattern dominance are achieved associated with the increase in phenotypic robustness to noise.

Dataset Information

Gene expression and the evolution of phenotypic diversity in social wasps.

Publications

Gene expression and the evolution of phenotypic diversity in social wasps.

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