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

Hoffman EA, Goodisman MA - BMC Biol. (2007)

Bottom Line: 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.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.Finally, overall differences between social insect taxa suggest that the independent evolution of caste arose via distinct developmental trajectories.

View Article: PubMed Central - HTML - PubMed

Affiliation: Department of Biology, University of Central Florida, Orlando, FL 32816, USA. eahoffma@mail.ucf.edu

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.

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Distribution of GenBank Blast matches (expectation (e) values < 10-5) within each V. squamosa cDNA library. Q, queen; W, worker; M, male; E, egg; LE, early larval instars; LL, late larval instars; P, pupa; A, adult.
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Figure 4: Distribution of GenBank Blast matches (expectation (e) values < 10-5) within each V. squamosa cDNA library. Q, queen; W, worker; M, male; E, egg; LE, early larval instars; LL, late larval instars; P, pupa; A, adult.

Mentions: Our analysis of sequenced ESTs uncovered another interesting pattern regarding sex in V. squamosa. We found that the proportion of ESTs matching known sequences in GenBank varied significantly among libraries (G10 = 102.60; p < 0.0001). Specifically, the differences in the proportion of genes displaying homology in the adult male and adult female libraries is striking (Figure 4), with adult females exhibiting significantly higher (G1 = 25.51, p < 0.001) numbers of homologs (adult workers 69%, adult queens 53%) compared with adult males (26%). One possible explanation for these differences is that genes expressed in adult males evolve particularly rapidly relative to those expressed in females and at other developmental stages. This result is consistent with studies in other taxa that have shown that male-specific genes evolve rapidly [24-26]. Indeed, Singh and Kulathinal [27] deduced from comparative analyses of genome evolution that much de novo gene evolution occurs among male-biased genes. Our data indicate that similar processes may operate in social insects. Whether such putatively rapidly evolving genes are exclusively or primarily expressed in sex-specific tissues, as has been found to be the case in other taxa [24], represents an area of future research. Regardless, our suggestion that genes expressed in males may evolve differently from those expressed in females is notable because it points to the importance of males in the evolution of social-insect populations, a subject that until recently has been largely ignored [28].


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

Hoffman EA, Goodisman MA - BMC Biol. (2007)

Distribution of GenBank Blast matches (expectation (e) values < 10-5) within each V. squamosa cDNA library. Q, queen; W, worker; M, male; E, egg; LE, early larval instars; LL, late larval instars; P, pupa; A, adult.
© Copyright Policy - open-access
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC1884141&req=5

Figure 4: Distribution of GenBank Blast matches (expectation (e) values < 10-5) within each V. squamosa cDNA library. Q, queen; W, worker; M, male; E, egg; LE, early larval instars; LL, late larval instars; P, pupa; A, adult.
Mentions: Our analysis of sequenced ESTs uncovered another interesting pattern regarding sex in V. squamosa. We found that the proportion of ESTs matching known sequences in GenBank varied significantly among libraries (G10 = 102.60; p < 0.0001). Specifically, the differences in the proportion of genes displaying homology in the adult male and adult female libraries is striking (Figure 4), with adult females exhibiting significantly higher (G1 = 25.51, p < 0.001) numbers of homologs (adult workers 69%, adult queens 53%) compared with adult males (26%). One possible explanation for these differences is that genes expressed in adult males evolve particularly rapidly relative to those expressed in females and at other developmental stages. This result is consistent with studies in other taxa that have shown that male-specific genes evolve rapidly [24-26]. Indeed, Singh and Kulathinal [27] deduced from comparative analyses of genome evolution that much de novo gene evolution occurs among male-biased genes. Our data indicate that similar processes may operate in social insects. Whether such putatively rapidly evolving genes are exclusively or primarily expressed in sex-specific tissues, as has been found to be the case in other taxa [24], represents an area of future research. Regardless, our suggestion that genes expressed in males may evolve differently from those expressed in females is notable because it points to the importance of males in the evolution of social-insect populations, a subject that until recently has been largely ignored [28].

Bottom Line: 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.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.Finally, overall differences between social insect taxa suggest that the independent evolution of caste arose via distinct developmental trajectories.

View Article: PubMed Central - HTML - PubMed

Affiliation: Department of Biology, University of Central Florida, Orlando, FL 32816, USA. eahoffma@mail.ucf.edu

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.

Show MeSH
Related in: MedlinePlus