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Evolutionary developmental genetics of ?phenotypic novelties and convergences

English title Evolutionary developmental genetics of ?phenotypic novelties and convergences
Applicant Milinkovitch Michel
Number 140785
Funding scheme Project funding (Div. I-III)
Research institution Département de Génétique et Evolution Faculté des Sciences Université de Genève
Institution of higher education University of Geneva - GE
Main discipline Zoology
Start/End 01.06.2012 - 31.05.2015
Approved amount 564'000.00
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Keywords (7)

Evolutionary convergences; Reptilian scales; Mammalian spines; Evo-Devo; New model organisms; Evolutionary novelties; Comparative transcriptomics

Lay Summary (French)

Lead
Lay summary

Génétique évolutive du développement des nouveautés phénotypiques et des convergences.

La génétique évolutive du développement (EvoDevo) étudie les mécanismes par lesquels la physiologie et la morphologie des organismes sont modifiées au cours de l’évolution de nouvelles formes et fonctions. De récentes technologies permettent d’étudier de nombreux phénotypes spectaculaires chez de nouvelles espèces. Nous proposons d’exploiter et d’étendre nos résultats précédents afin de déchiffrer les mécanismes moléculaires expliquant le développement spectaculaire de l’organe voméro-nasal (VNO) chez les reptiles (particulièrement les serpents). Nos analyses porteront notamment sur le séquençage du transcriptome (partie exprimée du génome) chez le crocodile, le lézard, le serpent, et la tortue. Ces analyses nous permettront de comprendre comment les reptiles ont modifié leur répertoire sensoriel lors de leur adaptation à divers habitats. Ces données permettront aussi de résoudre les relations évolutives entre ces grands groupes de reptiles et de générer de nombreux marqueurs moléculaires utiles pour la génétique de la conservation et la génétique quantitative. 

Nous étudierons également l’origine des appendices cutanés tels que les épines chez les mammifères (par exemple les hérissons et les tenrecs) et les écailles chez les reptiles. En ce qui concerne l’évolution des épines, nous identifierons les gènes impliqués dans la transformation des follicules pileux en organes producteurs d’épines. Pour les écailles de reptiles, nos modèles seront les crocodiles, les serpents, et les lézards. Ces analyses intègreront des approches histologiques, génomiques, protéomiques et mathématiques.  


Direct link to Lay Summary Last update: 21.02.2013

Responsible applicant and co-applicants

Employees

Publications

Publication
Photonic crystals cause active colour change in chameleons
Teyssier Jérémie, Saenko Suzanne V., Van Der Marel Dirk, Milinkovitch Michel C. (2015), Photonic crystals cause active colour change in chameleons, in Nature Communications, 6, 6368.
R2OBBIE-3D, a fast robotic high-resolution system for quantitative phenotyping of surface geometry and colour-texture
Martins António F., Martins António F., Bessant Michel, Manukyan Liana, Manukyan Liana, Milinkovitch Michel C Milinkovitch, Milinkovitch Michel C Milinkovitch (2015), R2OBBIE-3D, a fast robotic high-resolution system for quantitative phenotyping of surface geometry and colour-texture, in PLoS ONE, 10(6), e0126740.
Phylogeography and support vector machine classification of colour variation in panther chameleons
Grbic Djordje, Grbic Djordje, Saenko Suzanne V., Randriamoria Toky M., Randriamoria Toky M., Debry Adrien, Raselimanana Achille P., Raselimanana Achille P., Milinkovitch Michel C., Milinkovitch Michel C. (2014), Phylogeography and support vector machine classification of colour variation in panther chameleons, in Molecular Ecology, 24(13), 3455-3466.
The genome sequence of the corn snake (Pantherophis guttatus), a valuable resource for EvoDevo studies in squamates
Ullate-Agote Asier, Ullate-Agote Asier, Ullate-Agote Asier, Milinkovitch Michel C., Milinkovitch Michel C., Milinkovitch Michel C., Tzika Athanasia C., Tzika Athanasia C., Tzika Athanasia C. (2014), The genome sequence of the corn snake (Pantherophis guttatus), a valuable resource for EvoDevo studies in squamates, in International Journal of Developmental Biology, 58(10-12), 881-888.
Two waves of anisotropic growth generate enlarged follicles in the spiny mouse
Montandon Sophie A., Tzika Athanasia C., Martins António F., Chopard Bastien, Milinkovitch Michel C. (2014), Two waves of anisotropic growth generate enlarged follicles in the spiny mouse, in EvoDevo, 5(1), 33.
Contrasted evolution of the vomeronasal receptor repertoires in mammals and squamate reptiles.
Brykczynska Urszula, Tzika Athanasia C, Rodriguez Ivan, Milinkovitch Michel C (2013), Contrasted evolution of the vomeronasal receptor repertoires in mammals and squamate reptiles., in Genome biology and evolution, 5(2), 389-401.
Crocodile head scales are not developmental units but emerge from physical cracking.
Milinkovitch Michel C, Manukyan Liana, Debry Adrien, Di-Poï Nicolas, Martin Samuel, Singh Daljit, Lambert Dominique, Zwicker Matthias (2013), Crocodile head scales are not developmental units but emerge from physical cracking., in Science (New York, N.Y.), 339(6115), 78-81.
Crocodylians evolved scattered multi-sensory micro-organs.
Di-Poï Nicolas, Milinkovitch Michel C (2013), Crocodylians evolved scattered multi-sensory micro-organs., in EvoDevo, 4(1), 19-19.
Development and embryonic staging in non-model organisms: the case of an afrotherian mammal.
Werneburg Ingmar, Tzika Athanasia C, Hautier Lionel, Asher Robert J, Milinkovitch Michel C, Sánchez-Villagra Marcelo R (2013), Development and embryonic staging in non-model organisms: the case of an afrotherian mammal., in Journal of anatomy, 222(1), 2-18.
Interactive diffraction from biological nanostructures
Dhillon D. S., Teyssier J., Single M., Gaponenko I., Milinkovitch M. C., Zwicker M. (2013), Interactive diffraction from biological nanostructures, in Computer Graphics Forum, 33(8), 177-188.
Multiple enhancers regulate Hoxd genes and the Hotdog LncRNA during cecum budding.
Delpretti Saskia, Montavon Thomas, Leleu Marion, Joye Elisabeth, Tzika Athanasia, Milinkovitch Michel, Duboule Denis (2013), Multiple enhancers regulate Hoxd genes and the Hotdog LncRNA during cecum budding., in Cell reports, 5(1), 137-50.
Patterns of ossification in southern versus northern placental mammals.
Hautier Lionel, Bennett Nigel C, Viljoen Hermien, Howard Lauren, Milinkovitch Michel C, Tzika Athanasia C, Goswami Anjali, Asher Robert J (2013), Patterns of ossification in southern versus northern placental mammals., in Evolution; international journal of organic evolution, 67(7), 1994-2010.
Precise colocalization of interacting structural and pigmentary elements generates extensive color pattern variation in Phelsuma lizards.
Saenko Suzanne V, Teyssier Jérémie, van der Marel Dirk, Milinkovitch Michel C (2013), Precise colocalization of interacting structural and pigmentary elements generates extensive color pattern variation in Phelsuma lizards., in BMC biology, 11, 105-105.
Recovery of a nearly extinct Galápagos tortoise despite minimal genetic variation.
Milinkovitch Michel C, Kanitz Ricardo, Tiedemann Ralph, Tapia Washington, Llerena Fausto, Caccone Adalgisa, Gibbs James P, Powell Jeffrey R (2013), Recovery of a nearly extinct Galápagos tortoise despite minimal genetic variation., in Evolutionary applications, 6(2), 377-83.

Collaboration

Group / person Country
Types of collaboration
Ivan Rodriguez, Dept of Genetics & Evolution Biology, University of Geneva Switzerland (Europe)
- Publication
Toni Gabaldon, Comparative Genomics group, Centre for Genomic Regulation, Barcelona Spain (Europe)
- in-depth/constructive exchanges on approaches, methods or results
Clive D’Santos, Proteomics Core Facility, Cancer Research UK, Cambridge Great Britain and Northern Ireland (Europe)
- in-depth/constructive exchanges on approaches, methods or results
Denis Headon, The Roslin Institute, UK Great Britain and Northern Ireland (Europe)
- in-depth/constructive exchanges on approaches, methods or results

Associated projects

Number Title Start Funding scheme
132430 UNITED LIVING COLOURS “dot CH”: Integrating Evolutionary Developmental Genetics, 3D Computer Graphics, and Natural Photonics for deciphering variation & complexity in reptilian colour traits 01.01.2011 Sinergia
150817 High-throughput sequencing for research on evolution and ecology of microeukaryotes 01.12.2013 R'EQUIP
125060 From patterns to processes: bottom-up and top-down approaches for investigating the emergence of phenotypic novelties and convergences in evolution 01.04.2009 Project funding (Div. I-III)
159675 Evolutionary developmental genetics of phenotypic novelties and convergences 01.06.2015 Project funding (Div. I-III)

Abstract

Evolutionary Developmental Biology (EvoDevo) addresses the generative mechanisms by which morphology and physiology are altered to produce new forms serving novel functions. Recent technological / analytical advances make possible the analysis of numerous spectacular phenotypes in new model species. In the last 2.5 years, we successfully (i) established new mammalian and reptilian model species in our laboratory; (ii) investigated the evolution of genome content in chordates; (iii) analysed transcriptomes of 5 divergent reptilian lineages; and (iv) studied the corn-snake vomeronasal organ (VNO) transcriptome. This research led to the publication of 6 articles in peer-reviewed international journals, 1 book chapter, and 1 manuscript soon to be submitted for publication. In addition, we (v) accumulated very significant results on the genetic basis of the convergent development of spines in spiny mice, hedgehogs, and tenrecs and (vi) started the analysis of the genetic determinism of scales in reptiles. The two latter studies (on spines and scales) are very related conceptually (they both involve reaction-diffusion mechanisms of skin appendage patterning) and in terms of required laboratory techniques (deep sequencing, microarray analyses, in situ hybridisation, immuno-histochemistry, ex-vivo skin cultures). Here, we propose to exploit the results of the last 2.5 years for (a) developing the version 2 of the ‘Reptilian Transcriptome’ by performing RNA sequencing with much improved coverage, depth, and assembly; (b) extending our evolutionary analyses of reptile VNO receptors repertoires to turtles as well as aquatic, arboreal, and burrowing snakes; and (c) extending our understanding of the evolutionary developmental mechanisms generating skin appendage novelties in amniotes, namely spines in mammals, and scales in reptiles. More specifically, we propose to generate much additional transcriptome sequence data in (i) the Nile crocodile, (ii) the Corn snake, (iii) the Bearded dragon, and (iv) the red-eared turtle for building true Phylomes. We will generate multiple alignments and phylogenetic trees among all protein sequences within each gene family, and integrate all gene trees (including ENSEMBL genes from other amniote species) into MANTiS, a software which will then allow easy investigation of genome content evolution and associated molecular functions across amniotes in general and among reptiles in particular. Very large numbers of SSR loci and SNPs will be identified for future quantitative and population genetic analyses. Finally, a massive dataset of several million aa for each species will be analysed under Grid and Cloud versions of MetaPIGA for generating what could become one of the best supported phylogeny of vertebrates. Second, we suggest performing extended VNO transcriptome sequencing and analysis in 2 turtles, 1 monitor lizard, and 3 snake species to identify whether changes in VNO repertoires have evolved by adaptations to different habitats and life styles, and shifts in the significance of sensory inputs, or through the development of tongue flicking. Finally, we will complete our analyses of the molecular mechanisms responsible for the development of morphological novelties associated with the skin epidermis, namely spines in mammals and scales in reptiles. In the spine project, we will build up on our significantly advanced results. More specifically, we will (i) confirm the molecular mechanisms involved in the evolutionary transformation of hairs into spines by validating our microarray analyses with Nanostring technology, ex-vivo skin cultures, as well as in-vivo perturbation of the corresponding signalling pathways in the developing embryo, (ii) model mathematically the induction dynamics of spine development in each of the three species on reconstructed 3D geometry and high-resolution texture, (iii) perform quantitative proteomic analyses (with iTRAQ labelling) for the fine characterisation of hair and spine protein content, and (iv) evaluate the possibility to extend our analyses to other spiny mammals (porcupines and echidnas). In the scale project, we will use wild-type and spectacular scaleless mutants in the bearded dragon, the corn snake, and the Texas rat snake for analysing (i) the morphogenesis of the integumentary system in developing squamate reptiles using histology/immuno-histochemistry methods and mathematical simulations, and (ii) the molecular mechanisms of reptile-specific scale development using in situ hybridisation, deep sequencing, Nanostring technology, and ex-vivo skin cultures.
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