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<title xml:lang="en">The
<italic>pdm3</italic>
locus is a hotspot for recurrent evolution of female-limited color dimorphism in
<italic>Drosophila</italic>
</title>
<author>
<name sortKey="Yassin, Amir" sort="Yassin, Amir" uniqKey="Yassin A" first="Amir" last="Yassin">Amir Yassin</name>
<affiliation>
<nlm:aff id="A1">Laboratory of Genetics, University of Wisconsin-Madison, 425-G Henry Mall, Madison, WI, 53705, USA</nlm:aff>
</affiliation>
</author>
<author>
<name sortKey="Delaney, Emily K" sort="Delaney, Emily K" uniqKey="Delaney E" first="Emily K." last="Delaney">Emily K. Delaney</name>
<affiliation>
<nlm:aff id="A2">Department of Evolution and Ecology, University of California-Davis, One Shields Avenue, Davis, CA, 95616, USA</nlm:aff>
</affiliation>
</author>
<author>
<name sortKey="Reddiex, Adam J" sort="Reddiex, Adam J" uniqKey="Reddiex A" first="Adam J." last="Reddiex">Adam J. Reddiex</name>
<affiliation>
<nlm:aff id="A3">School of Biological Sciences, The University of Queensland, St. Lucia, Brisbane 4072, Australia</nlm:aff>
</affiliation>
</author>
<author>
<name sortKey="Seher, Thaddeus D" sort="Seher, Thaddeus D" uniqKey="Seher T" first="Thaddeus D." last="Seher">Thaddeus D. Seher</name>
<affiliation>
<nlm:aff id="A2">Department of Evolution and Ecology, University of California-Davis, One Shields Avenue, Davis, CA, 95616, USA</nlm:aff>
</affiliation>
<affiliation>
<nlm:aff id="A4">Department of Quantitative and Systems Biology, University of California-Merced, 5200 North Lake Rd, Merced, CA, 95343, USA</nlm:aff>
</affiliation>
</author>
<author>
<name sortKey="Bastide, Heloise" sort="Bastide, Heloise" uniqKey="Bastide H" first="Héloïse" last="Bastide">Héloïse Bastide</name>
<affiliation>
<nlm:aff id="A1">Laboratory of Genetics, University of Wisconsin-Madison, 425-G Henry Mall, Madison, WI, 53705, USA</nlm:aff>
</affiliation>
</author>
<author>
<name sortKey="Appleton, Nicholas C" sort="Appleton, Nicholas C" uniqKey="Appleton N" first="Nicholas C." last="Appleton">Nicholas C. Appleton</name>
<affiliation>
<nlm:aff id="A3">School of Biological Sciences, The University of Queensland, St. Lucia, Brisbane 4072, Australia</nlm:aff>
</affiliation>
</author>
<author>
<name sortKey="Lack, Justin B" sort="Lack, Justin B" uniqKey="Lack J" first="Justin B." last="Lack">Justin B. Lack</name>
<affiliation>
<nlm:aff id="A1">Laboratory of Genetics, University of Wisconsin-Madison, 425-G Henry Mall, Madison, WI, 53705, USA</nlm:aff>
</affiliation>
</author>
<author>
<name sortKey="David, Jean R" sort="David, Jean R" uniqKey="David J" first="Jean R." last="David">Jean R. David</name>
<affiliation>
<nlm:aff id="A5">Laboratoire Evolution, Génomes, Comportement, Ecologie (EGCE), CNRS, IRD, Université Paris Sud, Université Paris-Saclay, Gif-sur-Yvette, France</nlm:aff>
</affiliation>
</author>
<author>
<name sortKey="Chenoweth, Stephen F" sort="Chenoweth, Stephen F" uniqKey="Chenoweth S" first="Stephen F." last="Chenoweth">Stephen F. Chenoweth</name>
<affiliation>
<nlm:aff id="A3">School of Biological Sciences, The University of Queensland, St. Lucia, Brisbane 4072, Australia</nlm:aff>
</affiliation>
</author>
<author>
<name sortKey="Pool, John E" sort="Pool, John E" uniqKey="Pool J" first="John E." last="Pool">John E. Pool</name>
<affiliation>
<nlm:aff id="A1">Laboratory of Genetics, University of Wisconsin-Madison, 425-G Henry Mall, Madison, WI, 53705, USA</nlm:aff>
</affiliation>
</author>
<author>
<name sortKey="Kopp, Artyom" sort="Kopp, Artyom" uniqKey="Kopp A" first="Artyom" last="Kopp">Artyom Kopp</name>
<affiliation>
<nlm:aff id="A2">Department of Evolution and Ecology, University of California-Davis, One Shields Avenue, Davis, CA, 95616, USA</nlm:aff>
</affiliation>
</author>
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<idno type="pmid">27546577</idno>
<idno type="pmc">5450831</idno>
<idno type="url">http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5450831</idno>
<idno type="RBID">PMC:5450831</idno>
<idno type="doi">10.1016/j.cub.2016.07.016</idno>
<date when="2016">2016</date>
<idno type="wicri:Area/Pmc/Corpus">002078</idno>
<idno type="wicri:explorRef" wicri:stream="Pmc" wicri:step="Corpus" wicri:corpus="PMC">002078</idno>
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<title xml:lang="en" level="a" type="main">The
<italic>pdm3</italic>
locus is a hotspot for recurrent evolution of female-limited color dimorphism in
<italic>Drosophila</italic>
</title>
<author>
<name sortKey="Yassin, Amir" sort="Yassin, Amir" uniqKey="Yassin A" first="Amir" last="Yassin">Amir Yassin</name>
<affiliation>
<nlm:aff id="A1">Laboratory of Genetics, University of Wisconsin-Madison, 425-G Henry Mall, Madison, WI, 53705, USA</nlm:aff>
</affiliation>
</author>
<author>
<name sortKey="Delaney, Emily K" sort="Delaney, Emily K" uniqKey="Delaney E" first="Emily K." last="Delaney">Emily K. Delaney</name>
<affiliation>
<nlm:aff id="A2">Department of Evolution and Ecology, University of California-Davis, One Shields Avenue, Davis, CA, 95616, USA</nlm:aff>
</affiliation>
</author>
<author>
<name sortKey="Reddiex, Adam J" sort="Reddiex, Adam J" uniqKey="Reddiex A" first="Adam J." last="Reddiex">Adam J. Reddiex</name>
<affiliation>
<nlm:aff id="A3">School of Biological Sciences, The University of Queensland, St. Lucia, Brisbane 4072, Australia</nlm:aff>
</affiliation>
</author>
<author>
<name sortKey="Seher, Thaddeus D" sort="Seher, Thaddeus D" uniqKey="Seher T" first="Thaddeus D." last="Seher">Thaddeus D. Seher</name>
<affiliation>
<nlm:aff id="A2">Department of Evolution and Ecology, University of California-Davis, One Shields Avenue, Davis, CA, 95616, USA</nlm:aff>
</affiliation>
<affiliation>
<nlm:aff id="A4">Department of Quantitative and Systems Biology, University of California-Merced, 5200 North Lake Rd, Merced, CA, 95343, USA</nlm:aff>
</affiliation>
</author>
<author>
<name sortKey="Bastide, Heloise" sort="Bastide, Heloise" uniqKey="Bastide H" first="Héloïse" last="Bastide">Héloïse Bastide</name>
<affiliation>
<nlm:aff id="A1">Laboratory of Genetics, University of Wisconsin-Madison, 425-G Henry Mall, Madison, WI, 53705, USA</nlm:aff>
</affiliation>
</author>
<author>
<name sortKey="Appleton, Nicholas C" sort="Appleton, Nicholas C" uniqKey="Appleton N" first="Nicholas C." last="Appleton">Nicholas C. Appleton</name>
<affiliation>
<nlm:aff id="A3">School of Biological Sciences, The University of Queensland, St. Lucia, Brisbane 4072, Australia</nlm:aff>
</affiliation>
</author>
<author>
<name sortKey="Lack, Justin B" sort="Lack, Justin B" uniqKey="Lack J" first="Justin B." last="Lack">Justin B. Lack</name>
<affiliation>
<nlm:aff id="A1">Laboratory of Genetics, University of Wisconsin-Madison, 425-G Henry Mall, Madison, WI, 53705, USA</nlm:aff>
</affiliation>
</author>
<author>
<name sortKey="David, Jean R" sort="David, Jean R" uniqKey="David J" first="Jean R." last="David">Jean R. David</name>
<affiliation>
<nlm:aff id="A5">Laboratoire Evolution, Génomes, Comportement, Ecologie (EGCE), CNRS, IRD, Université Paris Sud, Université Paris-Saclay, Gif-sur-Yvette, France</nlm:aff>
</affiliation>
</author>
<author>
<name sortKey="Chenoweth, Stephen F" sort="Chenoweth, Stephen F" uniqKey="Chenoweth S" first="Stephen F." last="Chenoweth">Stephen F. Chenoweth</name>
<affiliation>
<nlm:aff id="A3">School of Biological Sciences, The University of Queensland, St. Lucia, Brisbane 4072, Australia</nlm:aff>
</affiliation>
</author>
<author>
<name sortKey="Pool, John E" sort="Pool, John E" uniqKey="Pool J" first="John E." last="Pool">John E. Pool</name>
<affiliation>
<nlm:aff id="A1">Laboratory of Genetics, University of Wisconsin-Madison, 425-G Henry Mall, Madison, WI, 53705, USA</nlm:aff>
</affiliation>
</author>
<author>
<name sortKey="Kopp, Artyom" sort="Kopp, Artyom" uniqKey="Kopp A" first="Artyom" last="Kopp">Artyom Kopp</name>
<affiliation>
<nlm:aff id="A2">Department of Evolution and Ecology, University of California-Davis, One Shields Avenue, Davis, CA, 95616, USA</nlm:aff>
</affiliation>
</author>
</analytic>
<series>
<title level="j">Current biology : CB</title>
<idno type="ISSN">0960-9822</idno>
<idno type="eISSN">1879-0445</idno>
<imprint>
<date when="2016">2016</date>
</imprint>
</series>
</biblStruct>
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<textClass></textClass>
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<front>
<div type="abstract" xml:lang="en">
<title>Summary</title>
<p id="P1">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
<italic>Drosophila montium</italic>
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
<italic>montium</italic>
subgroup supports multiple origins of FLCD. Despite this, we mapped FLCD to the same locus in four distantly related species – the transcription factor
<italic>POU domain motif 3</italic>
(
<italic>pdm3</italic>
), which acts as a repressor of abdominal pigmentation in
<italic>D. melanogaster</italic>
. In
<italic>D. serrata,</italic>
FLCD maps to a structural variant in the first intron of
<italic>pdm3</italic>
; however, this variant is not found in the three other species –
<italic>D. kikkawai</italic>
,
<italic>D. leontia,</italic>
and
<italic>D. burlai</italic>
– and sequence analysis strongly suggests the
<italic>pdm3</italic>
alleles responsible for FLCD originated independently at least three times. We propose that
<italic>cis</italic>
-regulatory changes in
<italic>pdm3</italic>
form sexually dimorphic and monomorphic alleles that segregate within species and are preserved, at least in one species, by structural variation. Surprisingly,
<italic>pdm3</italic>
has not been implicated in the evolution of sex-specific pigmentation outside the
<italic>montium</italic>
subgroup, suggesting that the genetic paths to sexual dimorphism may be constrained within a clade, but variable across clades.</p>
</div>
</front>
</TEI>
<pmc article-type="research-article">
<pmc-comment>The publisher of this article does not allow downloading of the full text in XML form.</pmc-comment>
<pmc-dir>properties manuscript</pmc-dir>
<front>
<journal-meta>
<journal-id journal-id-type="nlm-journal-id">9107782</journal-id>
<journal-id journal-id-type="pubmed-jr-id">8548</journal-id>
<journal-id journal-id-type="nlm-ta">Curr Biol</journal-id>
<journal-id journal-id-type="iso-abbrev">Curr. Biol.</journal-id>
<journal-title-group>
<journal-title>Current biology : CB</journal-title>
</journal-title-group>
<issn pub-type="ppub">0960-9822</issn>
<issn pub-type="epub">1879-0445</issn>
</journal-meta>
<article-meta>
<article-id pub-id-type="pmid">27546577</article-id>
<article-id pub-id-type="pmc">5450831</article-id>
<article-id pub-id-type="doi">10.1016/j.cub.2016.07.016</article-id>
<article-id pub-id-type="manuscript">NIHMS860083</article-id>
<article-categories>
<subj-group subj-group-type="heading">
<subject>Article</subject>
</subj-group>
</article-categories>
<title-group>
<article-title>The
<italic>pdm3</italic>
locus is a hotspot for recurrent evolution of female-limited color dimorphism in
<italic>Drosophila</italic>
</article-title>
</title-group>
<contrib-group>
<contrib contrib-type="author">
<name>
<surname>Yassin</surname>
<given-names>Amir</given-names>
</name>
<xref ref-type="aff" rid="A1">a</xref>
<xref rid="FN2" ref-type="author-notes">*</xref>
</contrib>
<contrib contrib-type="author">
<name>
<surname>Delaney</surname>
<given-names>Emily K.</given-names>
</name>
<xref ref-type="aff" rid="A2">b</xref>
<xref rid="FN2" ref-type="author-notes">*</xref>
</contrib>
<contrib contrib-type="author">
<name>
<surname>Reddiex</surname>
<given-names>Adam J.</given-names>
</name>
<xref ref-type="aff" rid="A3">c</xref>
</contrib>
<contrib contrib-type="author">
<name>
<surname>Seher</surname>
<given-names>Thaddeus D.</given-names>
</name>
<xref ref-type="aff" rid="A2">b</xref>
<xref ref-type="aff" rid="A4">d</xref>
</contrib>
<contrib contrib-type="author">
<name>
<surname>Bastide</surname>
<given-names>Héloïse</given-names>
</name>
<xref ref-type="aff" rid="A1">a</xref>
</contrib>
<contrib contrib-type="author">
<name>
<surname>Appleton</surname>
<given-names>Nicholas C.</given-names>
</name>
<xref ref-type="aff" rid="A3">c</xref>
</contrib>
<contrib contrib-type="author">
<name>
<surname>Lack</surname>
<given-names>Justin B.</given-names>
</name>
<xref ref-type="aff" rid="A1">a</xref>
</contrib>
<contrib contrib-type="author">
<name>
<surname>David</surname>
<given-names>Jean R.</given-names>
</name>
<xref ref-type="aff" rid="A5">e</xref>
</contrib>
<contrib contrib-type="author">
<name>
<surname>Chenoweth</surname>
<given-names>Stephen F.</given-names>
</name>
<xref ref-type="aff" rid="A3">c</xref>
</contrib>
<contrib contrib-type="author">
<name>
<surname>Pool</surname>
<given-names>John E.</given-names>
</name>
<xref ref-type="aff" rid="A1">a</xref>
<xref rid="FN1" ref-type="author-notes">+</xref>
</contrib>
<contrib contrib-type="author">
<name>
<surname>Kopp</surname>
<given-names>Artyom</given-names>
</name>
<xref ref-type="aff" rid="A2">b</xref>
<xref rid="FN1" ref-type="author-notes">+</xref>
</contrib>
</contrib-group>
<aff id="A1">
<label>a</label>
Laboratory of Genetics, University of Wisconsin-Madison, 425-G Henry Mall, Madison, WI, 53705, USA</aff>
<aff id="A2">
<label>b</label>
Department of Evolution and Ecology, University of California-Davis, One Shields Avenue, Davis, CA, 95616, USA</aff>
<aff id="A3">
<label>c</label>
School of Biological Sciences, The University of Queensland, St. Lucia, Brisbane 4072, Australia</aff>
<aff id="A4">
<label>d</label>
Department of Quantitative and Systems Biology, University of California-Merced, 5200 North Lake Rd, Merced, CA, 95343, USA</aff>
<aff id="A5">
<label>e</label>
Laboratoire Evolution, Génomes, Comportement, Ecologie (EGCE), CNRS, IRD, Université Paris Sud, Université Paris-Saclay, Gif-sur-Yvette, France</aff>
<author-notes>
<corresp id="FN1">
<label>+</label>
Correspondence: John E. Pool, 425-G Henry Mall, Madison, WI, 53705, USA, +1-608-265-1036,
<email>jpool@wisc.edu</email>
, Artyom Kopp, One Shields Avenue, Davis, CA, 95616, USA, +1-530-752-8657,
<email>akopp@ucdavis.edu</email>
</corresp>
<fn id="FN2" fn-type="equal">
<label>*</label>
<p>Equal contributions.</p>
</fn>
</author-notes>
<pub-date pub-type="nihms-submitted">
<day>5</day>
<month>4</month>
<year>2017</year>
</pub-date>
<pub-date pub-type="epub">
<day>18</day>
<month>8</month>
<year>2016</year>
</pub-date>
<pub-date pub-type="ppub">
<day>26</day>
<month>9</month>
<year>2016</year>
</pub-date>
<pub-date pub-type="pmc-release">
<day>31</day>
<month>5</month>
<year>2017</year>
</pub-date>
<volume>26</volume>
<issue>18</issue>
<fpage>2412</fpage>
<lpage>2422</lpage>
<pmc-comment>elocation-id from pubmed: 10.1016/j.cub.2016.07.016</pmc-comment>
<abstract id="abs1">
<title>Summary</title>
<p id="P1">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
<italic>Drosophila montium</italic>
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
<italic>montium</italic>
subgroup supports multiple origins of FLCD. Despite this, we mapped FLCD to the same locus in four distantly related species – the transcription factor
<italic>POU domain motif 3</italic>
(
<italic>pdm3</italic>
), which acts as a repressor of abdominal pigmentation in
<italic>D. melanogaster</italic>
. In
<italic>D. serrata,</italic>
FLCD maps to a structural variant in the first intron of
<italic>pdm3</italic>
; however, this variant is not found in the three other species –
<italic>D. kikkawai</italic>
,
<italic>D. leontia,</italic>
and
<italic>D. burlai</italic>
– and sequence analysis strongly suggests the
<italic>pdm3</italic>
alleles responsible for FLCD originated independently at least three times. We propose that
<italic>cis</italic>
-regulatory changes in
<italic>pdm3</italic>
form sexually dimorphic and monomorphic alleles that segregate within species and are preserved, at least in one species, by structural variation. Surprisingly,
<italic>pdm3</italic>
has not been implicated in the evolution of sex-specific pigmentation outside the
<italic>montium</italic>
subgroup, suggesting that the genetic paths to sexual dimorphism may be constrained within a clade, but variable across clades.</p>
</abstract>
<abstract abstract-type="graphical" id="Abs2">
<title>Graphical abstract</title>
<p id="P2">Yassin et al. show that a female-limited polymorphism has evolved multiple times in the
<italic>Drosophila montium</italic>
species subgroup through independent changes in the same gene,
<italic>pdm3</italic>
. This strong genetic bias suggests that the evolution of sex-specific traits may follow relatively predictable paths constrained by genetic architecture.</p>
</abstract>
<kwd-group>
<kwd>sex-limited polymorphism</kwd>
<kwd>sexual dimorphism</kwd>
<kwd>abdominal pigmentation</kwd>
<kwd>parallel evolution</kwd>
<kwd>
<italic>pdm3</italic>
</kwd>
</kwd-group>
</article-meta>
</front>
</pmc>
</record>

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