The pdm3 locus is a hotspot for recurrent evolution of female-limited color dimorphism in Drosophila

Yassin, Amir, Delaney, Emily K., Reddiex, Adam J., Seher, Thaddeus D., Bastide, Heloise, Appleton, Nicholas C., Lack, Justin B., David, Jean R., Chenoweth, Stephen F., Pool, John E. and Kopp, Artyom (2016) The pdm3 locus is a hotspot for recurrent evolution of female-limited color dimorphism in Drosophila. Current Biology, 26 18: 2412-2422. doi:10.1016/j.cub.2016.07.016


Author Yassin, Amir
Delaney, Emily K.
Reddiex, Adam J.
Seher, Thaddeus D.
Bastide, Heloise
Appleton, Nicholas C.
Lack, Justin B.
David, Jean R.
Chenoweth, Stephen F.
Pool, John E.
Kopp, Artyom
Title The pdm3 locus is a hotspot for recurrent evolution of female-limited color dimorphism in Drosophila
Formatted title
The pdm3 locus is a hotspot for recurrent evolution of female-limited color dimorphism in Drosophila
Journal name Current Biology   Check publisher's open access policy
ISSN 0960-9822
1879-0445
Publication date 2016-09-26
Year available 2016
Sub-type Article (original research)
DOI 10.1016/j.cub.2016.07.016
Open Access Status Not yet assessed
Volume 26
Issue 18
Start page 2412
End page 2422
Total pages 11
Place of publication Cambridge, MA United States
Publisher Cell Press
Language eng
Subject 1300 Biochemistry, Genetics and Molecular Biology
1100 Agricultural and Biological Sciences
Abstract Sex-limited polymorphisms are an intriguing form of sexual dimorphism that offer unique opportunities to reconstruct the evolutionary changes that decouple male and female traits encoded by a shared genome. We investigated the genetic basis of a Mendelian female-limited color dimorphism (FLCD) that segregates in natural populations of more than 20 species of the Drosophila montium subgroup. In these species, females have alternative abdominal color morphs, light and dark, whereas males have only one color morph in each species. A comprehensive molecular phylogeny of the montium subgroup supports multiple origins of FLCD. Despite this, we mapped FLCD to the same locus in four distantly related species—the transcription factor POU domain motif 3 (pdm3), which acts as a repressor of abdominal pigmentation in D. melanogaster. In D. serrata, FLCD maps to a structural variant in the first intron of pdm3; however, this variant is not found in the three other species—D. kikkawai, D. leontia, and D. burlai—and sequence analysis strongly suggests the pdm3 alleles responsible for FLCD originated independently at least three times. We propose that cis-regulatory changes in pdm3 form sexually dimorphic and monomorphic alleles that segregate within species and are preserved, at least in one species, by structural variation. Surprisingly, pdm3 has not been implicated in the evolution of sex-specific pigmentation outside the montium subgroup, suggesting that the genetic paths to sexual dimorphism may be constrained within a clade but variable across clades.
Formatted abstract
Sex-limited polymorphisms are an intriguing form of sexual dimorphism that offer unique opportunities to reconstruct the evolutionary changes that decouple male and female traits encoded by a shared genome. We investigated the genetic basis of a Mendelian female-limited color dimorphism (FLCD) that segregates in natural populations of more than 20 species of the Drosophila montium subgroup. In these species, females have alternative abdominal color morphs, light and dark, whereas males have only one color morph in each species. A comprehensive molecular phylogeny of the montium subgroup supports multiple origins of FLCD. Despite this, we mapped FLCD to the same locus in four distantly related species—the transcription factor POU domain motif 3 (pdm3), which acts as a repressor of abdominal pigmentation in D. melanogaster. In D. serrata, FLCD maps to a structural variant in the first intron of pdm3; however, this variant is not found in the three other species—D. kikkawai, D. leontia, and D. burlai—and sequence analysis strongly suggests the pdm3 alleles responsible for FLCD originated independently at least three times. We propose that cis-regulatory changes in pdm3 form sexually dimorphic and monomorphic alleles that segregate within species and are preserved, at least in one species, by structural variation. Surprisingly, pdm3 has not been implicated in the evolution of sex-specific pigmentation outside the montium subgroup, suggesting that the genetic paths to sexual dimorphism may be constrained within a clade but variable across clades.
Keyword Sex-limited polymorphism
Sexual dimorphism
Abdominal pigmentation
Parallel evolution
pdm3
Q-Index Code C1
Q-Index Status Provisional Code
Grant ID R01 GM084947
R01 GM111797
Institutional Status UQ

Document type: Journal Article
Sub-type: Article (original research)
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