Magic Traits in Magic Fish: Understanding Color Pattern Evolution Using Reef Fish

[en] Color patterns provide easy access to phenotypic diversity and allow the questioning of the adaptive value of traits or the constraints acting on phenotypic evolution. Reef fish offer a unique opportunity to address such questions because they are ecologically and phylogenetically diverse and have the largest variety of pigment cell types known in vertebrates. In addition to recent development of their genetic resources, reef fish also constitute experimental models that allow the discrimination of ecological, developmental, and evolutionary processes at work. Here, we emphasize how the study of color patterns in reef fish can be integrated in an Eco/Evo/Devo (ecological evolutionary developmental) perspective and we illustrate that such an approach can bring new insights on the evolution of complex phenotypes.

Research Center/Unit :

FOCUS - Freshwater and OCeanic science Unit of reSearch - ULiège
AFFISH-RC - Applied and Fundamental FISH Research Center - ULiège

Disciplines :

Zoology
Environmental sciences & ecology
Aquatic sciences & oceanology
Genetics & genetic processes

Author, co-author :

Salis, Pauline

Lorin, Thibault

Laudet, Vincent

Frederich, Bruno ; Université de Liège - ULiège > Département de Biologie, Ecologie et Evolution > Morphologie fonctionnelle et évolutive

Language :

English

Title :

Magic Traits in Magic Fish: Understanding Color Pattern Evolution Using Reef Fish

Publication date :

01 April 2019

Journal title :

Trends in Genetics

ISSN :

0168-9525

eISSN :

1362-4555

Publisher :

Elsevier Trends Journals, Cambridge, United Kingdom

Volume :

Issue :

Pages :

265-278

Peer reviewed :

Peer Reviewed verified by ORBi

Funders :

F.R.S.-FNRS - Fonds de la Recherche Scientifique

Available on ORBi :

since 26 February 2019

Statistics

Number of views

308 (5 by ULiège)

Number of downloads

401 (4 by ULiège)

More statistics

Scopus citations^®

Scopus citations^®
without self-citations

OpenCitations

OpenAlex citations

Bibliography

Cuthill, I.C., et al. The biology of color. Science, 357, 2017, eaan0221.
Harris, M.P., et al. Molecular evidence for an activator-inhibitor mechanism in development of embryonic feather branching. Proc. Natl. Acad. Sci. U. S. A. 102 (2005), 11734–11739.
Hoekstra, H.E., Genetics, development and evolution of adaptive pigmentation in vertebrates. Heredity 97 (2006), 222–234.
Parichy, D.M., Spiewak, J.E., Origins of adult pigmentation: diversity in pigment stem cell lineages and implications for pattern evolution. Pigment Cell Melanoma Res. 28 (2015), 31–50.
Santos, M.E., et al. Comparative transcriptomics of anal fin pigmentation patterns in cichlid fishes. BMC Genomics, 17, 2016, 712.
Santos, M.E., et al. The evolution of cichlid fish egg-spots is linked with a cis-regulatory change. Nat. Commun., 5, 2014, 5149.
Kottler, V.A., et al. Adenylate cyclase 5 is required for melanophore and male pattern development in the guppy (Poecilia reticulata). Pigment Cell Melanoma Res. 28 (2015), 545–558.
Schartl, M., et al. What is a vertebrate pigment cell?. Pigment Cell Melanoma Res. 29 (2016), 8–14.
Lorin, T., et al. Teleost fish-specific preferential retention of pigmentation gene-containing families after whole genome duplications in vertebrates. G3 (Bethesda) 8 (2018), 1795–1806.
Justin Marshall, N., Communication and camouflage with the same “bright” colours in reef fishes. Philos. Trans. R. Soc. B Biol. Sci. 355 (2000), 1243–1248.
Cortesi, F., et al. From crypsis to mimicry: changes in colour and the configuration of the visual system during ontogenetic habitat transitions in a coral reef fish. J. Exp. Biol. 219 (2016), 2545–2558.
Cortesi, F., et al. Phenotypic plasticity confers multiple fitness benefits to a mimic. Curr. Biol. 25 (2015), 949–954.
Frédérich, B., et al. Iterative ecological radiation and convergence during the evolutionary history of damselfishes (Pomacentridae). Am. Nat. 181 (2013), 94–113.
Frédérich, B., Santini, F., Macroevolutionary analysis of the tempo of diversification in snappers and fusiliers (Percomorpha: Lutjanidae). Belg. J. Zool. 147 (2017), 17–35.
McRobert, S.P., Bradner, J., The influence of body coloration on shoaling preferences in fish. Anim. Behav. 56 (1998), 611–615.
McFarland, W.N., et al. The influence of light on the twilight migrations of grunts. Environ. Biol. Fishes 4 (1979), 9–22.
Kelley, J.L., et al. Spots and stripes: ecology and colour pattern evolution in butterflyfishes. Proc. Biol. Sci., 280, 2013, 20122730.
Barlow, G.W., The attitude of fish eye-lines in relation to body shape and to stripes and bars. Copeia, 1972, 1972, 4.
Stevens, M., The role of eyespots as anti-predator mechanisms, principally demonstrated in the Lepidoptera. Biol. Rev. 80 (2005), 573–588.
Gagliano, M., On the spot: the absence of predators reveals eyespot plasticity in a marine fish. Behav. Ecol. 19 (2008), 733–739.
Gagliano, M., Depczynski, M., Spot the difference: mimicry in a coral reef fish. PLoS One, 8, 2013, e55938.
Price, S.A., et al. Phylogenetic insights into the history and diversification of fishes on reefs. Coral Reefs 34 (2015), 997–1009.
Van Belleghem, S.M., et al. Patternize: an R package for quantifying colour pattern variation. Methods Ecol. Evol. 9 (2018), 390–398.
Klingenberg, C.P., Morphological integration and developmental modularity. Annu. Rev. Ecol. Evol. Syst. 39 (2008), 115–132.
Hirata, M., et al. Pigment cell organization in the hypodermis of zebrafish. Dev. Dyn. 227 (2003), 497–503.
Patterson, L.B., Parichy, D.M., Interactions with iridophores and the tissue environment required for patterning melanophores and xanthophores during zebrafish adult pigment stripe formation. PLoS Genet., 9, 2013, e1003561.
Singh, A.P., et al. Proliferation, dispersal and patterned aggregation of iridophores in the skin prefigure striped colouration of zebrafish. Nat. Cell Biol. 16 (2014), 604–611.
van Eeden, F.J., et al. Genetic analysis of fin formation in the zebrafish, Danio rerio. Development 123 (1996), 255–262.
Mahalwar, P., et al. Local reorganization of xanthophores fine-tunes and colors the striped pattern of zebrafish. Science 345 (2014), 1362–1364.
Johnson, S.L., et al. Mitfa is required at multiple stages of melanocyte differentiation but not to establish the melanocyte stem cell. Dev. Biol. 350 (2011), 405–413.
Laudet, V., The origins and evolution of vertebrate metamorphosis. Curr. Biol. 21 (2011), R726–R737.
McMenamin, S.K., et al. Thyroid hormone-dependent adult pigment cell lineage and pattern in zebrafish. Science 345 (2014), 1358–1361.
Frohnhöfer, H.G., et al. Iridophores and their interactions with other chromatophores are required for stripe formation in zebrafish. Development 140 (2013), 2997–3007.
Nakamasu, A., et al. Interactions between zebrafish pigment cells responsible for the generation of Turing patterns. Proc. Natl. Acad. Sci. U. S. A. 106 (2009), 8429–8434.
Eom, D.S., Parichy, D.M., A macrophage relay for long-distance signaling during postembryonic tissue remodeling. Science 355 (2017), 1317–1320.
Yamaguchi, M., et al. Pattern regulation in the stripe of zebrafish suggests an underlying dynamic and autonomous mechanism. Proc. Natl. Acad. Sci. U.S.A. 104 (2007), 4790–4793.
Svetic, V., et al. Sdf1a patterns zebrafish melanophores and links the somite and melanophore pattern defects in choker mutants. Development 134 (2007), 1011–1022.
Patterson, L.B., et al. Pigment cell interactions and differential xanthophore recruitment underlying zebrafish stripe reiteration and Danio pattern evolution. Nat. Commun., 5, 2014, 5299.
Spiewak, J.E., et al. Evolution of endothelin signaling and diversification of adult pigment pattern in Danio fishes. PLoS Genet., 14, 2018, e1007538.
Lehmann, R., et al. Finding Nemo's genes: a chromosome-scale reference assembly of the genome of the orange clownfish Amphiprion percula. Mol. Ecol. Resour. 00 (2018), 1–16.
Marcionetti, A., et al. First draft genome of an iconic clownfish species (Amphiprion frenatus). Mol. Ecol. Resour. 18 (2018), 1092–1101.
Kondo, S., Asai, R., A reaction diffusion wave on the skin of the marine angelfish Pomacanthus. Nature 376 (1995), 765–768.
Messmer, V., et al. Genetic and ecological characterisation of colour dimorphism in a coral reef fish. Environ. Biol. Fishes 74 (2005), 175–183.
Puebla, O., et al. Colour pattern as a single trait driving speciation in Hypoplectrus coral reef fishes?. Proc. R. Soc. B Biol. Sci. 274 (2007), 1265–1271.
Robertson, D.R., Who resembles whom? Mimetic and coincidental look-alikes among tropical reef fishes. PLoS One, 8, 2013, e544939.
Holt, B.G., et al. Searching for speciation genes: molecular evidence for selection associated with colour morphotypes in the caribbean reef fish genus hypoplectrus. PLoS One, 6, 2011, e20194.
Puebla, O., et al. Genomic atolls of differentiation in coral reef fishes (Hypoplectrus spp., Serranidae). Mol. Ecol. 23 (2014), 5291–5303.
Picq, S., et al. Population genomics of local adaptation versus speciation in coral reef fishes (Hypoplectrus spp., Serranidae). Ecol. Evol. 6 (2016), 2109–2124.
Jeong, S., et al. Regulation of body pigmentation by the abdominal-B Hox protein and its gain and loss in Drosophila evolution. Cell 125 (2006), 1387–1399.
Salis, P., et al. Ontogenetic and phylogenetic simplification during white stripe evolution in clownfishes. BMC Biol., 16, 2018, 90.
Salis, P. et al. Developmental and comparative transcriptomic identification of iridophore contribution to white barring in clownfish, Pigment Cell Melanoma Res. (in press).
Merilaita, S., Kelley, J.L., Scary clowns: adaptive function of anemonefish coloration. J. Evol. Biol. 10 (2018), 1558–1571.
Servedio, M.R., et al. Magic traits in speciation: “magic” but not rare?. Trends Ecol. Evol. 26 (2011), 389–397.
Laland, K.N., et al. Cause and effect in biology revisited: is Mayr's proximate-ultimate dichotomy still useful?. Science 334 (2011), 1512–1516.
Bennett, D.C., Lamoreux, M.L., The color loci of mice – a genetic century. Pigment Cell Melanoma Res. 16 (2003), 333–344.
Nüsslein-Volhard, C., Singh, A.P., How fish color their skin: a paradigm for development and evolution of adult patterns. Bioessays, 39, 2017, 1600231.
Cal, L., et al. BAC recombineering of the agouti loci from spotted gar and zebrafish reveals the evolutionary ancestry of dorsal–ventral pigment asymmetry in fish. J. Exp. Zool. B Mol. Dev. Evol. 328 (2017), 697–708.
Fadeev, A., et al. Zebrafish leucocyte tyrosine kinase controls iridophore establishment, proliferation and survival. Pigment Cell Melanoma Res. 29 (2016), 284–296.
Nagao, Y., et al. Sox5 functions as a fate switch in medaka pigment cell development. PLoS Genet., 10, 2014, e1004246.
Nagao, Y., et al. Distinct interactions of Sox5 and Sox10 in fate specification of pigment cells in medaka and zebrafish. PLoS Genet., 14, 2018, e1007260.
McGrath, C.L., et al. Differential retention and divergent resolution of duplicate genes following whole-genome duplication. Genome Res. 24 (2014), 1665–1675.
Braasch, I., et al. Pigmentation pathway evolution after whole-genome duplication in fish. Genome Biol. Evol. 1 (2009), 479–493.
Kimura, T., et al. Leucophores are similar to xanthophores in their specification and differentiation processes in medaka. Proc. Natl. Acad. Sci. U. S. A. 111 (2014), 7343–7348.
Goda, M., Fujii, R., Blue chromatophores in two species of Callionymid fish. Zool. Sci. 12 (1995), 811–813.
Stieb, S.M., et al. Why UV vision and red vision are important for damselfish (Pomacentridae): structural and expression variation in opsin genes. Mol. Ecol. 26 (2017), 1323–1342.
Goda, M., et al. Integumental reddish-violet coloration owing to novel dichromatic chromatophores in the teleost fish, Pseudochromis diadema. Pigment Cell Melanoma Res. 24 (2011), 614–617.
Goda, M., et al. Novel dichromatic chromatophores in the integument of the mandarin fish Synchiropus splendidus. Biol. Bull. 224 (2013), 14–17.
Goda, M., Rapid integumental color changes due to novel iridophores in the chameleon sand tilefish Hoplolatilus chlupatyi. Pigment Cell Melanoma Res. 30 (2017), 368–371.
Wakamatsu, Y., et al. The see-through medaka: a fish model that is transparent throughout life. Proc. Natl. Acad. Sci. U. S. A. 98 (2001), 10046–10050.
Michiels, N.K., et al. Red fluorescence in reef fish: a novel signalling mechanism?. BMC Ecol., 8, 2008, 16.
Wucherer, M.F., Michiels, N.K., A fluorescent chromatophore changes the level of fluorescence in a reef fish. PLoS One, 7, 2012, e37913.
Ban, E., et al. The signaling pathway in photoresponses that may be mediated by visual pigments in erythrophores of Nile tilapia. Pigment Cell Melanoma Res. 18 (2005), 360–369.
Turing, A.M., The chemical basis of morphogenesis. Philos. Trans. R. Soc. B Biol. Sci. 237 (1952), 37–72.
Hiscock, T.W., Megason, S.G., Mathematically guided approaches to distinguish models of periodic patterning. Development 142 (2015), 409–419.
Painter, K.J., et al. Stripe formation in juvenile Pomacanthus explained by a generalized Turing mechanism with chemotaxis. Proc. Natl. Acad. Sci. U. S. A. 96 (1999), 5549–5554.
Kondo, S., Miura, T., Reaction-diffusion model as a framework for understanding biological pattern formation. Science 329 (2010), 1616–1620.
Sick, S., et al. WNT and DKK determine hair follicle spacing through a reaction-diffusion mechanism. Science 314 (2006), 1447–1450.
Miura, T., Shiota, K., Depletion of FGF acts as a lateral inhibitory factor in lung branching morphogenesis in vitro. Mech. Dev. 116 (2002), 29–38.
Haupaix, N., et al. The periodic coloration in birds forms through a prepattern of somite origin. Science, 361, 2018 eaar4777.