Repeated morphological evolution through cis-regulatory changes in a pleiotropic gene

Nature
Benjamin Prud'hommeS B Carroll

Abstract

The independent evolution of morphological similarities is widespread. For simple traits, such as overall body colour, repeated transitions by means of mutations in the same gene may be common. However, for more complex traits, the possible genetic paths may be more numerous; the molecular mechanisms underlying their independent origins and the extent to which they are constrained to follow certain genetic paths are largely unknown. Here we show that a male wing pigmentation pattern involved in courtship display has been gained and lost multiple times in a Drosophila clade. Each of the cases we have analysed (two gains and two losses) involved regulatory changes at the pleiotropic pigmentation gene yellow. Losses involved the parallel inactivation of the same cis-regulatory element (CRE), with changes at a few nucleotides sufficient to account for the functional divergence of one element between two sibling species. Surprisingly, two independent gains of wing spots resulted from the co-option of distinct ancestral CREs. These results demonstrate how the functional diversification of the modular CREs of pleiotropic genes contributes to evolutionary novelty and the independent evolution of morphological similarities.

References

Jun 10, 1977·Science·F Jacob
Apr 26, 2000·Proceedings of the National Academy of Sciences of the United States of America·E Sucena, D L Stern
Jul 6, 2000·Science·J P HuelsenbeckJ P Masly
Mar 30, 2001·Molecular Phylogenetics and Evolution·S G Goto, M T Kimura
Aug 29, 2001·Bioinformatics·J P Huelsenbeck, F Ronquist
Oct 10, 2002·Current Biology : CB·Patricia J WittkoppSean B Carroll
Apr 22, 2003·Proceedings of the National Academy of Sciences of the United States of America·Michael W NachmanSusan L D'Agostino
Oct 8, 2003·Systematic Biology·Stéphane Guindon, Olivier Gascuel
Nov 17, 2004·Systematic Biology·Mark PagelDaniel Barker
Jul 28, 2005·Proceedings of the National Academy of Sciences of the United States of America·Bevil R Conway, Margaret S Livingstone
Dec 13, 2005·Nature Genetics·Meredith E ProtasClifford J Tabin
May 17, 2006·Trends in Ecology & Evolution·Fredrik Ronquist

❮ Previous
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Citations

Dec 6, 2011·Development Genes and Evolution·Laura C FergusonChris D Jiggins
Aug 21, 2009·Journal of Plant Research·Takahiro Yamaguchi, Hirokazu Tsukaya
Aug 27, 2013·Trends in Ecology & Evolution·Christopher W Wheat, Niklas Wahlberg
May 4, 2010·Genetics Research·Kim van der LindeScott J Steppan
May 16, 2013·Nature Communications·Junichi YamaguchiHaruhiko Fujiwara
Aug 19, 2007·Nature Reviews. Genetics·Antony M Dean, Joseph W Thornton
Aug 10, 2007·Heredity·C R LandryJ M Ranz
Sep 13, 2007·Heredity·M Anisimova, D A Liberles
Jan 24, 2008·Proceedings of the National Academy of Sciences of the United States of America·Alexander G OphirSteven M Phelps
Mar 4, 2009·Proceedings of the National Academy of Sciences of the United States of America·Kohtaro TanakaArtyom Kopp
Feb 24, 2009·Proceedings of the National Academy of Sciences of the United States of America·Suzanne E OsborneBrian K Coombes
Feb 6, 2010·Proceedings of the National Academy of Sciences of the United States of America·Hunter B FraserEric E Schadt
Jan 5, 2011·Proceedings of the National Academy of Sciences of the United States of America·Ekaterina ShevtsovaJostein Kjærandsen
May 20, 2011·Proceedings of the National Academy of Sciences of the United States of America·Mark RebeizSean B Carroll
Dec 1, 2012·Proceedings of the National Academy of Sciences of the United States of America·Nicolás FrankelDavid L Stern
Mar 19, 2013·Genome Biology and Evolution·Lino OmettoOmar Rota-Stabelli
Aug 21, 2013·Integrative and Comparative Biology·Antje H L FischerJoel Smith
Sep 19, 2008·Molecular Biology and Evolution·Sean Michael CarrollJoseph W Thornton
Oct 4, 2008·Molecular Biology and Evolution·Cynthia C SteinerHopi E Hoekstra
Jul 6, 2010·Molecular Biology and Evolution·Kelly E O'QuinKaren L Carleton
Jul 14, 2010·Molecular Biology and Evolution·Arnaud Martin, Robert D Reed
Jul 27, 2010·Molecular Biology and Evolution·Laura C FergusonChris D Jiggins
Jan 8, 2011·Molecular Biology and Evolution·Hong-Song YuZe Zhang
Nov 22, 2011·Molecular Biology and Evolution·Sarah S Saminadin-PeterJohn Parsch
Oct 9, 2012·Nucleic Acids Research·Michael HillerGill Bejerano
Jun 12, 2009·Proceedings. Biological Sciences·Matthew H DickShunsuke F Mawatari
May 8, 2013·Philosophical Transactions of the Royal Society of London. Series B, Biological Sciences·Orsolya Symmons, François Spitz
Nov 13, 2013·Philosophical Transactions of the Royal Society of London. Series B, Biological Sciences·Marcelo Rubinstein, Flávio S J de Souza
Jan 17, 2008·Genes & Development·Chris J CretekosRichard R Behringer
Sep 6, 2007·Genome Research·Richard R CopleyIrina A Udalova
Nov 9, 2007·Genome Research·Pouya KheradpourManolis Kellis
May 15, 2012·Pigment Cell & Melanoma Research·Marcus R KronforstHopi E Hoekstra

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Next ❯

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