Formation and Evolution of Color Patterns
Principal Investigator: Marie MANCEAU, CR1 Cnrs
PSL / ERC
Our laboratory is interested in the developmental processes governing the evolution of adaptive traits in Vertebrates. As a model, we study color patterning (i.e., distribution of color across the body) in populations of songbirds and rodents. Using in ovo manipulation, genetics, and imaging, we test the function of pigmentation genes in color pattern formation and study how changes in these genes contribute to variation in this trait.
Color patterns (i.e., distribution of color across the body) are crucial for survival and reproductive success and vary tremendously among animals. Despite their ecological importance, the genetic and developmental mechanisms responsible for the formation and variation of naturally-occurring color patterns have remained a black box. To address this question, our laboratory takes advantage of (1) the typical color pattern of the zebra finch (genus Taeniopygia; Figure1), an Australian song bird which has the technical advantages of both an avian model (i.e., amenability to experimental embryology through in ovo manipulation) and a genetic model (i.e., sequenced genome, availability of molecular tools, transgenic strategies), and (2) the extensive natural variation in the periodic patterns of various species of rodents.
We previously showed in rodents that the formation of the simple dorso-ventral color pattern (present in most Vertebrates) relies on the establishment of an embryonic "pre-pattern" (i.e., the spatial restriction of pigmentation genes) causing regional differences in pigment cell behavior (Figure 2). What developmental pathways act upstream of pigmentation genes to create a pre-pattern? To answer this question, we use classical embryological manipulations, gene expression analyses and gain- and loss-of-function experiments in zebra finch embryos to (1) investigate the role of cell lineage and instructing neighboring organs on the formation of the pre-pattern and (2) study the molecular pathways controlling this process. Color pre-pattern formation is a great model to understand how developmental pathways establish discrete domains in the skin, and more generally, govern positional signaling in the embryo.
Figure 2: The spatial restriction of pigmentation gene expression in the rodent embryo forms a pre-pattern resulting in regional differences in pigment cell behavior and thus, in color distribution. Left panel: Agouti expression, in purple. Right panel: confocal and optical views of pigment cells in the embryonic skin, in green.
Color Pattern Variation
Small changes in the pre-pattern can provoke large changes in the adult color pattern that impact fitness in the wild. What type of genes and developmental mechanisms constrain (or promote) color pattern evolution in Vertebrates? In finches, we use existing natural variation in the extent and position of colored body domains characterizing closely-related species. In these birds, we integrate a quantitative genetic approach and developmental biology to pinpoint the genetic changes and the subsequent developmental modifications responsible for variation in color patterns in birds.
Complex Color Patterning
Many animals display complex and periodic patterns (from zebra stripes to leopard spots) superimposed to the typical colored domains observed in most Vertebrates. How do periodic patterns form? Using a combination of gene expression analyses and mathematical modeling in field-caught and museum specimens of rodents, we work to identify the molecular factors establishing periodic patterns in the skin. We test whether these pattern-forming mechanisms (1) rely on the formation of embryonic pre-patterns and (2) act through theoretical mechanismspredicted to produce naturally-occurring complex patterns. We also investigate how developmental and phylogenetic constraints shape the evolution of periodic patterns in the skin.
- Bailleul, R., Curantz, C., Desmarquet-Trin Dinh, C., Hidalgo, M., Touboul, J., and Manceau, M. (2019). Symmetry breaking in the embryonic skin triggers directional and sequential plumage patterning. PLoS Biol. 17, e3000448.
- Haupaix, N., and Manceau, M. (2019). The embryonic origin of periodic color patterns. Dev. Biol.
- Haupaix, N., Curantz, C., Bailleul, R., Beck, S., Robic, A., and Manceau, M. (2018). The periodic coloration in birds forms through a prepattern of somite origin. Science 361.
- Friocourt, F., Lafont, A.-G., Kress, C., Pain, B., Manceau, M., Dufour, S. & Chédotal, A., (2017), Recurrent DCC gene losses during bird evolution. Sci Rep 7, 37569.
- Mallarino, R., Henegar, C., Mirasierra, M., Manceau, M., Schradin, C., Vallejo, M., Beronja, S., Barsh, G. S., Hoekstra, H. E. (2016), Developmental mechanisms of stripe patterns in rodents. Nature 539, 518–523.
- Mallarino, R., Hoekstra, H. E. & Manceau, M. (2016), Developmental genetics in emerging rodent models: case studies and perspectives. Current Opinion in Genetics & Development, Developmental mechanisms, patterning and evolution 39, 182–186.
- Metz H. C., Manceau M. & Hoekstra H. E. ( 2011), Turing patterns: how the fish got its spots. Pigment Cell and Melanoma Research, 24(1):12-4.
- Manceau M., Domingues V., Mallarino R. & Hoekstra H. E. (2011), The developmental role of Agouti in the evolution of color pattern. Science, 331:1062-5.
- Manceau M., Domingues V., Linnen C. R., Rosenblum E. B. & Hoekstra H. E. (2010), Convergence in pigmentation at multiple levels: mutations, genes and function. Philosophical Transactions of the Royal Society B, 365:2439-50.
- Kingsley E. P., Manceau M., Wiley C. D. & Hoekstra H. E. (2009), Melanism in Peromyscusis caused by independent mutations in Agouti. PLoS One, 4:e6435.
- Lagha M., Kormish J. D., Rocancourt D., Manceau M., Epstein J. A., Zaret K. S., Relaix F. & Buckingham M. E. (2008), Pax3 regulation of FGF signaling affects the progression of embryonic progenitor cells into the myogenic program. Genes & Development, 22(13):1828-37.
- Manceau M., Gros J., Savage K., Thomé V., McPherron A., Paterson B. & Marcelle C. (2008), Myostatin promotes the terminal differentiation of embryonic muscle progenitors. Genes & Development, 22(5):668-81.
- Gros J., Manceau M., Thomé V. & Marcelle C. (2005), A common somitic origin for embryonic muscle progenitors and satellite cells. Nature, 435(7044):954-8.
- Manceau M., Marcelle C. & Gros J. (2005), A common somitic origin for embryonic muscle progenitors. Med. Sciences, 21(11):915-7.
Manceau Marie, CRCN CNRS
Postdoctoral fellows & PhD Students:
Hidalgo-le-Norcy Magdalena, Postdoctoral fellow
Haupaix Nicolas, Postdoctoral fellow
Bailleul Richard, PhD student
Curantz Camille, PhD student
Desmarquet Carole, IEHC INSERM