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Recurrent modification of a conserved cis-regulatory element underlies fruit fly pigmentation diversity.

Rogers WA, Salomone JR, Tacy DJ, Camino EM, Davis KA, Rebeiz M, Williams TM - PLoS Genet. (2013)

Bottom Line: In Drosophila melanogaster fruit flies, the Bric-à-brac (Bab) transcription factors control the development of a suite of sexually dimorphic traits on the posterior abdomen.By reconstructing the sequence and regulatory activity of the ancestral Drosophila melanogaster dimorphic element, we demonstrate that a handful of mutations were sufficient to create independent CRE alleles with differing activities.Moreover, intraspecific and interspecific dimorphic element evolution proceeded with little to no alterations to the known body plan and sex-determination regulatory linkages.

View Article: PubMed Central - PubMed

Affiliation: Department of Biology, University of Dayton, Dayton, Ohio, United States of America.

ABSTRACT
The development of morphological traits occurs through the collective action of networks of genes connected at the level of gene expression. As any node in a network may be a target of evolutionary change, the recurrent targeting of the same node would indicate that the path of evolution is biased for the relevant trait and network. Although examples of parallel evolution have implicated recurrent modification of the same gene and cis-regulatory element (CRE), little is known about the mutational and molecular paths of parallel CRE evolution. In Drosophila melanogaster fruit flies, the Bric-à-brac (Bab) transcription factors control the development of a suite of sexually dimorphic traits on the posterior abdomen. Female-specific Bab expression is regulated by the dimorphic element, a CRE that possesses direct inputs from body plan (ABD-B) and sex-determination (DSX) transcription factors. Here, we find that the recurrent evolutionary modification of this CRE underlies both intraspecific and interspecific variation in female pigmentation in the melanogaster species group. By reconstructing the sequence and regulatory activity of the ancestral Drosophila melanogaster dimorphic element, we demonstrate that a handful of mutations were sufficient to create independent CRE alleles with differing activities. Moreover, intraspecific and interspecific dimorphic element evolution proceeded with little to no alterations to the known body plan and sex-determination regulatory linkages. Collectively, our findings represent an example where the paths of evolution appear biased to a specific CRE, and drastic changes in function were accompanied by deep conservation of key regulatory linkages.

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Pigmentation gene network model and the evolution of an ancestral CRE regulatory logic.(A–C) Schematic of the hierarchical structure of the D. melanogaster pigmentation gene network. Direct regulation is represented as solid connections and dashed connections represent connections where regulation has not been shown to be direct. Activation and repression are respectively indicated by the arrowhead and nail-head shapes. This network includes an (A) upper level of patterning genes, including Abd-B and dsx respectively of the body plan and sex-determination pathways, (B) a mid-level tier that integrates patterning inputs, (C) and a lower level that includes pigmentation genes whose encoded products function in pigment metabolism. Although Abd-B directly regulates the pigmentation gene yellow, sexually dimorphic expression of the yellow and tan genes results from the sexually dimorphic output of the bab locus that acts to repress tan and yellow expression in females. (D) A model for the evolution of diverse dimorphic element regulatory activities. The common ancestor of D. melanogaster populations and related species possessed a dimorphic element with both DSX and ABD-B regulatory linkages and that drove expression in the female A6–A8 segments. This ancestral regulatory logic was recurrently modified to increase the levels and expand the segmental domain of activity, or to decrease and contract activity. These changes occurred amidst the preservation of the core ABD-B and DSX regulatory linkages, perhaps though the loss (TF 3) and/or gain (TF 4) of other transcription factor linkages.
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pgen-1003740-g007: Pigmentation gene network model and the evolution of an ancestral CRE regulatory logic.(A–C) Schematic of the hierarchical structure of the D. melanogaster pigmentation gene network. Direct regulation is represented as solid connections and dashed connections represent connections where regulation has not been shown to be direct. Activation and repression are respectively indicated by the arrowhead and nail-head shapes. This network includes an (A) upper level of patterning genes, including Abd-B and dsx respectively of the body plan and sex-determination pathways, (B) a mid-level tier that integrates patterning inputs, (C) and a lower level that includes pigmentation genes whose encoded products function in pigment metabolism. Although Abd-B directly regulates the pigmentation gene yellow, sexually dimorphic expression of the yellow and tan genes results from the sexually dimorphic output of the bab locus that acts to repress tan and yellow expression in females. (D) A model for the evolution of diverse dimorphic element regulatory activities. The common ancestor of D. melanogaster populations and related species possessed a dimorphic element with both DSX and ABD-B regulatory linkages and that drove expression in the female A6–A8 segments. This ancestral regulatory logic was recurrently modified to increase the levels and expand the segmental domain of activity, or to decrease and contract activity. These changes occurred amidst the preservation of the core ABD-B and DSX regulatory linkages, perhaps though the loss (TF 3) and/or gain (TF 4) of other transcription factor linkages.

Mentions: Here, we have shown that the D. melanogaster dimorphic element, a CRE that regulates a suite of sexually dimorphic traits, has alleles of strikingly different regulatory activities that impact just one of these traits, female abdomen pigmentation. By reconstructing the ancestral dimorphic element sequence for these alleles and determining its regulatory activity, we were able to identify the derived mutations responsible for the divergent activities of various alleles. These functionally-relevant mutations were few in number, each responsible for measureable effects on regulatory activity, and all but one modify a property other than the known ABD-B and DSX regulatory linkages identified previously [20]. Furthermore, we discovered that species related to D. melanogaster harbored evolutionarily relevant mutations in this same CRE, altering its regulatory activity in magnitudes and patterns comparable to the D. melanogaster alleles. These CRE modifications likely contribute to the divergent patterns of abdomen pigmentation for females of these species. These interspecific differences in dimorphic element activity occurred in the absence of noteworthy alterations to the known ancestrally encoded body plan and sex-determination pathway regulatory linkages. As a result, this CRE's regulatory activity in the terminal body segments (A7 and genitalia) has been conserved, while activity in more anterior segments has diverged. Collectively, this study can be interpreted to support a model where recurrent evolution can be biased to target certain genes and CREs (Figure 7A–7C), while preserving certain ancestral linkages (Figure 7D).


Recurrent modification of a conserved cis-regulatory element underlies fruit fly pigmentation diversity.

Rogers WA, Salomone JR, Tacy DJ, Camino EM, Davis KA, Rebeiz M, Williams TM - PLoS Genet. (2013)

Pigmentation gene network model and the evolution of an ancestral CRE regulatory logic.(A–C) Schematic of the hierarchical structure of the D. melanogaster pigmentation gene network. Direct regulation is represented as solid connections and dashed connections represent connections where regulation has not been shown to be direct. Activation and repression are respectively indicated by the arrowhead and nail-head shapes. This network includes an (A) upper level of patterning genes, including Abd-B and dsx respectively of the body plan and sex-determination pathways, (B) a mid-level tier that integrates patterning inputs, (C) and a lower level that includes pigmentation genes whose encoded products function in pigment metabolism. Although Abd-B directly regulates the pigmentation gene yellow, sexually dimorphic expression of the yellow and tan genes results from the sexually dimorphic output of the bab locus that acts to repress tan and yellow expression in females. (D) A model for the evolution of diverse dimorphic element regulatory activities. The common ancestor of D. melanogaster populations and related species possessed a dimorphic element with both DSX and ABD-B regulatory linkages and that drove expression in the female A6–A8 segments. This ancestral regulatory logic was recurrently modified to increase the levels and expand the segmental domain of activity, or to decrease and contract activity. These changes occurred amidst the preservation of the core ABD-B and DSX regulatory linkages, perhaps though the loss (TF 3) and/or gain (TF 4) of other transcription factor linkages.
© Copyright Policy
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC3757066&req=5

pgen-1003740-g007: Pigmentation gene network model and the evolution of an ancestral CRE regulatory logic.(A–C) Schematic of the hierarchical structure of the D. melanogaster pigmentation gene network. Direct regulation is represented as solid connections and dashed connections represent connections where regulation has not been shown to be direct. Activation and repression are respectively indicated by the arrowhead and nail-head shapes. This network includes an (A) upper level of patterning genes, including Abd-B and dsx respectively of the body plan and sex-determination pathways, (B) a mid-level tier that integrates patterning inputs, (C) and a lower level that includes pigmentation genes whose encoded products function in pigment metabolism. Although Abd-B directly regulates the pigmentation gene yellow, sexually dimorphic expression of the yellow and tan genes results from the sexually dimorphic output of the bab locus that acts to repress tan and yellow expression in females. (D) A model for the evolution of diverse dimorphic element regulatory activities. The common ancestor of D. melanogaster populations and related species possessed a dimorphic element with both DSX and ABD-B regulatory linkages and that drove expression in the female A6–A8 segments. This ancestral regulatory logic was recurrently modified to increase the levels and expand the segmental domain of activity, or to decrease and contract activity. These changes occurred amidst the preservation of the core ABD-B and DSX regulatory linkages, perhaps though the loss (TF 3) and/or gain (TF 4) of other transcription factor linkages.
Mentions: Here, we have shown that the D. melanogaster dimorphic element, a CRE that regulates a suite of sexually dimorphic traits, has alleles of strikingly different regulatory activities that impact just one of these traits, female abdomen pigmentation. By reconstructing the ancestral dimorphic element sequence for these alleles and determining its regulatory activity, we were able to identify the derived mutations responsible for the divergent activities of various alleles. These functionally-relevant mutations were few in number, each responsible for measureable effects on regulatory activity, and all but one modify a property other than the known ABD-B and DSX regulatory linkages identified previously [20]. Furthermore, we discovered that species related to D. melanogaster harbored evolutionarily relevant mutations in this same CRE, altering its regulatory activity in magnitudes and patterns comparable to the D. melanogaster alleles. These CRE modifications likely contribute to the divergent patterns of abdomen pigmentation for females of these species. These interspecific differences in dimorphic element activity occurred in the absence of noteworthy alterations to the known ancestrally encoded body plan and sex-determination pathway regulatory linkages. As a result, this CRE's regulatory activity in the terminal body segments (A7 and genitalia) has been conserved, while activity in more anterior segments has diverged. Collectively, this study can be interpreted to support a model where recurrent evolution can be biased to target certain genes and CREs (Figure 7A–7C), while preserving certain ancestral linkages (Figure 7D).

Bottom Line: In Drosophila melanogaster fruit flies, the Bric-à-brac (Bab) transcription factors control the development of a suite of sexually dimorphic traits on the posterior abdomen.By reconstructing the sequence and regulatory activity of the ancestral Drosophila melanogaster dimorphic element, we demonstrate that a handful of mutations were sufficient to create independent CRE alleles with differing activities.Moreover, intraspecific and interspecific dimorphic element evolution proceeded with little to no alterations to the known body plan and sex-determination regulatory linkages.

View Article: PubMed Central - PubMed

Affiliation: Department of Biology, University of Dayton, Dayton, Ohio, United States of America.

ABSTRACT
The development of morphological traits occurs through the collective action of networks of genes connected at the level of gene expression. As any node in a network may be a target of evolutionary change, the recurrent targeting of the same node would indicate that the path of evolution is biased for the relevant trait and network. Although examples of parallel evolution have implicated recurrent modification of the same gene and cis-regulatory element (CRE), little is known about the mutational and molecular paths of parallel CRE evolution. In Drosophila melanogaster fruit flies, the Bric-à-brac (Bab) transcription factors control the development of a suite of sexually dimorphic traits on the posterior abdomen. Female-specific Bab expression is regulated by the dimorphic element, a CRE that possesses direct inputs from body plan (ABD-B) and sex-determination (DSX) transcription factors. Here, we find that the recurrent evolutionary modification of this CRE underlies both intraspecific and interspecific variation in female pigmentation in the melanogaster species group. By reconstructing the sequence and regulatory activity of the ancestral Drosophila melanogaster dimorphic element, we demonstrate that a handful of mutations were sufficient to create independent CRE alleles with differing activities. Moreover, intraspecific and interspecific dimorphic element evolution proceeded with little to no alterations to the known body plan and sex-determination regulatory linkages. Collectively, our findings represent an example where the paths of evolution appear biased to a specific CRE, and drastic changes in function were accompanied by deep conservation of key regulatory linkages.

Show MeSH
Related in: MedlinePlus