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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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Population level differences in Bab paralog expression.(A–C) The expression of Bab1 in the dorsal abdomens of female pupae at 85 hAPF. (A) Light 1 females display uniform Bab1 expression throughout segments A2-A6, whereas expression is reduced in the A5 and A6 segments of (B) Dark 1 and (C) Dark 2 females. (D and E) Expression of Bab1 in the female genitalia (g) and analia (a) at 29 hAPF. (F–H) Bab2 expression in the dorsal abdomen of female pupae is at 85 hAPF. Bab2 expression is (F) uniform throughout the A2–A6 segments of Light 1 females, (G) reduced in the A5 and A6 segments of Dark 1 females, and (H) uniform throughout the A2–A6 of Dark 2 females. (I and J) Expression of Bab2 in the female genitalia (g) and analia (a) is at 29 hAPF. Red arrowheads indicate segments where expression is reduced compared to more anterior segments, whereas yellow arrowheads indicate the segments where Bab2 is expressed at a higher level than that observed for Bab1 for Dark 2 females.
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pgen-1003740-g003: Population level differences in Bab paralog expression.(A–C) The expression of Bab1 in the dorsal abdomens of female pupae at 85 hAPF. (A) Light 1 females display uniform Bab1 expression throughout segments A2-A6, whereas expression is reduced in the A5 and A6 segments of (B) Dark 1 and (C) Dark 2 females. (D and E) Expression of Bab1 in the female genitalia (g) and analia (a) at 29 hAPF. (F–H) Bab2 expression in the dorsal abdomen of female pupae is at 85 hAPF. Bab2 expression is (F) uniform throughout the A2–A6 segments of Light 1 females, (G) reduced in the A5 and A6 segments of Dark 1 females, and (H) uniform throughout the A2–A6 of Dark 2 females. (I and J) Expression of Bab2 in the female genitalia (g) and analia (a) is at 29 hAPF. Red arrowheads indicate segments where expression is reduced compared to more anterior segments, whereas yellow arrowheads indicate the segments where Bab2 is expressed at a higher level than that observed for Bab1 for Dark 2 females.

Mentions: Considering that the phenotypic effects of these naturally occurring dimorphic element alleles and pigmentation phenotypes were restricted to the A6 and to a lesser extent the A5 abdominal segment (Figure 1), we suspected that mutations in the dimorphic element could cause the observed differences in pigmentation. This hypothesis would be supported by differing levels and/or patterns of Bab expression in the pupal abdominal epidermis for females that develop different pigmentation phenotypes. Thus, we characterized the pattern of Bab expression in the abdominal epidermis at the end of pupal development when tergite pigmentation is being specified. If the regulatory activity for the dimorphic element alleles identified in reporter transgene assays (Figure 1) were indicative of the endogenous Bab expression, then Bab1 and Bab2 expression should be elevated in females with Light tergite pigmentation compared to those with Dark pigmentation. Consistent with this expectation, Bab1 and Bab2 were expressed robustly throughout the A2–A7 abdominal segments of Light 1 females (Figure 3A and 3F), while Bab1 and Bab2 expression were reduced in the A5 and A6 abdominal segments of Dark 1 female pupae (Figure 3B and 3G, red arrowheads). This reduction corresponds with the reduced regulatory activity of this strain's dimorphic element allele (Figure 1G′) and where the pigmentation develops on adult females (Figure 1G). Compared to Dark 1 females that possess expanded pigmentation on the A5 and A6 tergites, expanded pigmentation is limited to the A6 tergite of Dark 2 females (Figure 1H). Consistent with the Dark 2 phenotype, the expression of Bab1, but not Bab2, was reduced in the A6 segment and to a lesser extent the A5 segment (Figure 3C and 3H). These patterns of expression are consistent with the finding that the bab1 pigmentation phenotype is limited to the female A6 tergite, whereas a bab2 phenotype affects both the A6 and A5 tergite [41]. We also characterized Bab expression in the developing female genitalia and analia that respectively develop from the A8 and A9/A10 segments. In contrast to the reduced expression seen in the A5 and A6 segments epidermis of Dark 1 females, expression in these more posterior structures was comparable to that observed for Light 1 females (compare Figure 3D and 3I to 3E and 3J).


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)

Population level differences in Bab paralog expression.(A–C) The expression of Bab1 in the dorsal abdomens of female pupae at 85 hAPF. (A) Light 1 females display uniform Bab1 expression throughout segments A2-A6, whereas expression is reduced in the A5 and A6 segments of (B) Dark 1 and (C) Dark 2 females. (D and E) Expression of Bab1 in the female genitalia (g) and analia (a) at 29 hAPF. (F–H) Bab2 expression in the dorsal abdomen of female pupae is at 85 hAPF. Bab2 expression is (F) uniform throughout the A2–A6 segments of Light 1 females, (G) reduced in the A5 and A6 segments of Dark 1 females, and (H) uniform throughout the A2–A6 of Dark 2 females. (I and J) Expression of Bab2 in the female genitalia (g) and analia (a) is at 29 hAPF. Red arrowheads indicate segments where expression is reduced compared to more anterior segments, whereas yellow arrowheads indicate the segments where Bab2 is expressed at a higher level than that observed for Bab1 for Dark 2 females.
© Copyright Policy
Related In: Results  -  Collection

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

pgen-1003740-g003: Population level differences in Bab paralog expression.(A–C) The expression of Bab1 in the dorsal abdomens of female pupae at 85 hAPF. (A) Light 1 females display uniform Bab1 expression throughout segments A2-A6, whereas expression is reduced in the A5 and A6 segments of (B) Dark 1 and (C) Dark 2 females. (D and E) Expression of Bab1 in the female genitalia (g) and analia (a) at 29 hAPF. (F–H) Bab2 expression in the dorsal abdomen of female pupae is at 85 hAPF. Bab2 expression is (F) uniform throughout the A2–A6 segments of Light 1 females, (G) reduced in the A5 and A6 segments of Dark 1 females, and (H) uniform throughout the A2–A6 of Dark 2 females. (I and J) Expression of Bab2 in the female genitalia (g) and analia (a) is at 29 hAPF. Red arrowheads indicate segments where expression is reduced compared to more anterior segments, whereas yellow arrowheads indicate the segments where Bab2 is expressed at a higher level than that observed for Bab1 for Dark 2 females.
Mentions: Considering that the phenotypic effects of these naturally occurring dimorphic element alleles and pigmentation phenotypes were restricted to the A6 and to a lesser extent the A5 abdominal segment (Figure 1), we suspected that mutations in the dimorphic element could cause the observed differences in pigmentation. This hypothesis would be supported by differing levels and/or patterns of Bab expression in the pupal abdominal epidermis for females that develop different pigmentation phenotypes. Thus, we characterized the pattern of Bab expression in the abdominal epidermis at the end of pupal development when tergite pigmentation is being specified. If the regulatory activity for the dimorphic element alleles identified in reporter transgene assays (Figure 1) were indicative of the endogenous Bab expression, then Bab1 and Bab2 expression should be elevated in females with Light tergite pigmentation compared to those with Dark pigmentation. Consistent with this expectation, Bab1 and Bab2 were expressed robustly throughout the A2–A7 abdominal segments of Light 1 females (Figure 3A and 3F), while Bab1 and Bab2 expression were reduced in the A5 and A6 abdominal segments of Dark 1 female pupae (Figure 3B and 3G, red arrowheads). This reduction corresponds with the reduced regulatory activity of this strain's dimorphic element allele (Figure 1G′) and where the pigmentation develops on adult females (Figure 1G). Compared to Dark 1 females that possess expanded pigmentation on the A5 and A6 tergites, expanded pigmentation is limited to the A6 tergite of Dark 2 females (Figure 1H). Consistent with the Dark 2 phenotype, the expression of Bab1, but not Bab2, was reduced in the A6 segment and to a lesser extent the A5 segment (Figure 3C and 3H). These patterns of expression are consistent with the finding that the bab1 pigmentation phenotype is limited to the female A6 tergite, whereas a bab2 phenotype affects both the A6 and A5 tergite [41]. We also characterized Bab expression in the developing female genitalia and analia that respectively develop from the A8 and A9/A10 segments. In contrast to the reduced expression seen in the A5 and A6 segments epidermis of Dark 1 females, expression in these more posterior structures was comparable to that observed for Light 1 females (compare Figure 3D and 3I to 3E and 3J).

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