title: Emergence of tissue sensitivity to Hox protein levels underlies the evolution of an adaptive morphological trait.
abstract: Growth control scales morphological attributes and, therefore, provides a critical contribution to the evolution of adaptive traits. Yet, the genetic mechanisms underlying growth in the context of specific ecological adaptations are poorly understood. In water striders, adaptation to locomotion on the water surface is associated with allometric and functional changes in thoracic appendages, such that T2-legs, used as propelling oars, are longer than T3-legs, used as steering rudders. The Hox gene Ubx establishes this derived morphology by elongating T2-legs but shortening T3-legs. Using gene expression assays, RNAi knockdown, and comparative transcriptomics, we demonstrate that the evolution of water surface rowing as a novel means of locomotion is associated with the evolution of a dose-dependent promoting-repressing effect of Ubx on leg growth. In the water strider Limnoporus dissortis, T3-legs express six to seven times higher levels of Ubx compared to T2-legs. Ubx RNAi shortens T2-legs and the severity of this phenotype increases with increased depletion of Ubx protein. Conversely, Ubx RNAi lengthens T3-legs but this phenotype is partially rescued when Ubx protein is further depleted. This dose-dependent effect of Ubx on leg growth is absent in non-rowing relatives that retain the ancestral relative leg length. We also show that the spatial patterns of expression of dpp, wg, hh, egfr, dll, exd, hth, and dac are unchanged in Ubx RNAi treatments. This indicates that the dose-dependent opposite effect of Ubx on T2- and T3-legs operates without any apparent effect on the spatial expression of major leg patterning genes. Our data suggest that scaling of adaptive allometries can evolve through changes in the levels of expression of Hox proteins early during ontogeny, and in the sensitivity of the tissues that express them, without any major effects on pattern formation.
authors.affiliation: Institut de Génomique Fonctionnelle de Lyon, CNRS-UMR5242, Ecole Normale Supérieure de Lyon, 46 Allée d׳Italie, 69364 Lyon Cedex 07, France; Université Claude Bernard Lyon 1, 43 Boulevard du 11 Novembre 1918, 69622 Villeurbanne Cedex, France.
authors.forename: Peter Nagui
authors.initials: PN
authors.lastname: Refki
authors.affiliation: Institut de Génomique Fonctionnelle de Lyon, CNRS-UMR5242, Ecole Normale Supérieure de Lyon, 46 Allée d׳Italie, 69364 Lyon Cedex 07, France.
authors.forename: David
authors.initials: D
authors.lastname: Armisén
authors.affiliation: Institut de Génomique Fonctionnelle de Lyon, CNRS-UMR5242, Ecole Normale Supérieure de Lyon, 46 Allée d׳Italie, 69364 Lyon Cedex 07, France; Université Claude Bernard Lyon 1, 43 Boulevard du 11 Novembre 1918, 69622 Villeurbanne Cedex, France.
authors.forename: Antonin Jean Johan
authors.initials: AJ
authors.lastname: Crumière
authors.affiliation: Institut de Génomique Fonctionnelle de Lyon, CNRS-UMR5242, Ecole Normale Supérieure de Lyon, 46 Allée d׳Italie, 69364 Lyon Cedex 07, France.
authors.forename: Séverine
authors.initials: S
authors.lastname: Viala
authors.affiliation: Institut de Génomique Fonctionnelle de Lyon, CNRS-UMR5242, Ecole Normale Supérieure de Lyon, 46 Allée d׳Italie, 69364 Lyon Cedex 07, France. Electronic address: abderrahman.khila@ens-lyon.fr.
authors.forename: Abderrahman
authors.initials: A
authors.lastname: Khila
mesh_terms: D000220:Adaptation, Biological / Q000502:physiology*; D000704:Analysis of Variance; D000818:Animals; D005075:Biological Evolution; D005121:Extremities / Q000254:growth & development*; D020869:Gene Expression Profiling; D005786:Gene Expression Regulation / Q000235:genetics / Q000502:physiology*; D020062:Heteroptera / Q000235:genetics / Q000254:growth & development*; D018398:Homeodomain Proteins / Q000378:metabolism*; D017403:In Situ Hybridization; D034622:RNA Interference; D014157:Transcription Factors / Q000378:metabolism*
chemical_list: D018398:Homeodomain Proteins; D014157:Transcription Factors
keywords: Adaptation; Allometry; Hox genes; Morphological evolution; RNA interference