Trends in Genetics
Volume 35, Issue 4, April 2019, Pages 265-278
Journal home page for Trends in Genetics

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

https://doi.org/10.1016/j.tig.2019.01.006Get rights and content

Highlights

Organisms live in continuously changing environments. Eco/Evo/Devo aims to uncover the rules that underlie the interactions between the environment, genes, and development of an organism.

Color patterns have a clear ecological and behavioral significance, with a wide range of functions in animals and in teleosts in particular.

Study of model species such as zebrafish allows the understanding of the developmental mechanisms underlying phenotypic evolution.

Changes in expression of key molecular factors coupled with changes in cell–cell interactions can lead to color pattern diversification during evolution.

Recent studies about color patterns in reef fishes emphasize the need to address such questions in this group in an Eco/Evo/devo perspective, integrating proximate causation and ultimate causation.

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.

Section snippets

Why Study Reef Fish and Their Color Patterns?

Questions regarding the diversity, evolution, and ecological significance of color patterns (see Glossary) have caught scientists’ attention for centuries [1]. Pigmentation has been studied using a wide variety of animal models from hexapods to vertebrates 1, 2. Fruit flies and mice are still important models to study pigmentation genes [3] but, over the last few years, teleost fish have also became efficient systems for addressing questions related to color patterns. Zebrafish and medaka are

Diversity and Function of Color Patterns in Reef Fish

Reef fish harbor a myriad of colors and associated patterns. Some display uniform body color such as the blue–green damselfish Chromis viridis (Figure 2A), whereas others show complex patterns as seen in the clown triggerfish Balistoides conspicillum (Figure 2B). The latter combines a series of large ventral white spots, with a dorsal yellow shield punctuated with small brown spots. Strikingly, some reef fish species share ornamental similarities, whereas others have the exact same color

Understanding the Ontogeny of Color Patterns Using Fish Models

Developmental studies are needed to provide additional information on proximate mechanisms, allowing the emergence of various color patterns during development and evolution. Up to now, cellular and molecular studies have mainly been carried out using zebrafish (Danio rerio), a widely used model. Thanks to the genetic and live imaging tools developed in this species, it has been possible to investigate the mechanisms underlying color pattern formation and evolution.

Integrating Ecology with Evo/Devo to Understand the Color Patterns of Reef Fish

Integrating ecology with evolution and development allows us to address how developmental mechanisms modified during evolutionary changes are selected. If zebrafish with its unique toolkit is an excellent model to understand the development of reiterated striped pattern, its ecological diversity is limited, and thus how the developmental mechanisms at the origin of variation in the pigmentation patterns have been selected remains unknown. This is why reef fish, with their diversity of pigment

Concluding Remarks and Future Perspectives

Color patterns in reef fish, with their extreme divergence and plasticity, can indeed be considered as a ‘magic trait’ that may easily lead to speciation [53]. Thanks to work on the zebrafish model, we have more knowledge about the developmental mechanisms generating color patterns. The combination of ecological analysis with genomic and/or developmental analysis using magic reef fish as model systems (in addition to other valuable models such as cichlids and guppies) will help to provide an

Acknowledgments

Work from our laboratories is funded by the CNRS (France), the Sorbonne Université (France), ENS Lyon (France), and the FNRS (Belgium). We thank Fabio Cortesi, Nico Michiels, Shigeru Kondo, Matthias Wucherer, Makoto Goda, Hans Georg Frohnhöfer, Yuko Wakamatsu, Germain Boussarie, Philippe Bourjon, Joe De Vroe, Mark Rosenstein, Derek Ramsey, Franck Merlier, Anders Poulsen, Alan Sutton, Guido Poppe, and Philippe Poppe for the pictures used in the Figures. We also thank Natacha Roux, Laurence

Glossary

Color pattern
distribution of color across the body.
Color polymorphism
consequence of developmental plasticity, in which the trajectories of developing organisms diverge under the influence of ultimate cues.
Eco/Evo/Devo
the interactions between the environment, genes, and development of an organism, and their consequences in evolution.
Eyespots (or ocelli)
concentric markings that contrast with the surrounding area.
Eye stripes
a dark bar that runs through the eye, matching the eye color and therefore

References (79)

  • D.M. Parichy et al.

    Origins of adult pigmentation: diversity in pigment stem cell lineages and implications for pattern evolution

    Pigment Cell Melanoma Res.

    (2015)
  • M.E. Santos

    Comparative transcriptomics of anal fin pigmentation patterns in cichlid fishes

    BMC Genomics

    (2016)
  • M.E. Santos

    The evolution of cichlid fish egg-spots is linked with a cis-regulatory change

    Nat. Commun.

    (2014)
  • V.A. Kottler

    Adenylate cyclase 5 is required for melanophore and male pattern development in the guppy (Poecilia reticulata)

    Pigment Cell Melanoma Res.

    (2015)
  • M. Schartl

    What is a vertebrate pigment cell?

    Pigment Cell Melanoma Res.

    (2016)
  • T. Lorin

    Teleost fish-specific preferential retention of pigmentation gene-containing families after whole genome duplications in vertebrates

    G3 (Bethesda)

    (2018)
  • N. Justin Marshall

    Communication and camouflage with the same “bright” colours in reef fishes

    Philos. Trans. R. Soc. B Biol. Sci.

    (2000)
  • F. Cortesi

    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.

    (2016)
  • B. Frédérich

    Iterative ecological radiation and convergence during the evolutionary history of damselfishes (Pomacentridae)

    Am. Nat.

    (2013)
  • B. Frédérich et al.

    Macroevolutionary analysis of the tempo of diversification in snappers and fusiliers (Percomorpha: Lutjanidae)

    Belg. J. Zool.

    (2017)
  • W.N. McFarland

    The influence of light on the twilight migrations of grunts

    Environ. Biol. Fishes

    (1979)
  • J.L. Kelley

    Spots and stripes: ecology and colour pattern evolution in butterflyfishes

    Proc. Biol. Sci.

    (2013)
  • G.W. Barlow

    The attitude of fish eye-lines in relation to body shape and to stripes and bars

    Copeia

    (1972)
  • M. Stevens

    The role of eyespots as anti-predator mechanisms, principally demonstrated in the Lepidoptera

    Biol. Rev.

    (2005)
  • M. Gagliano

    On the spot: the absence of predators reveals eyespot plasticity in a marine fish

    Behav. Ecol.

    (2008)
  • M. Gagliano et al.

    Spot the difference: mimicry in a coral reef fish

    PLoS One

    (2013)
  • S.A. Price

    Phylogenetic insights into the history and diversification of fishes on reefs

    Coral Reefs

    (2015)
  • S.M. Van Belleghem

    Patternize: an R package for quantifying colour pattern variation

    Methods Ecol. Evol.

    (2018)
  • C.P. Klingenberg

    Morphological integration and developmental modularity

    Annu. Rev. Ecol. Evol. Syst.

    (2008)
  • M. Hirata

    Pigment cell organization in the hypodermis of zebrafish

    Dev. Dyn.

    (2003)
  • L.B. Patterson et al.

    Interactions with iridophores and the tissue environment required for patterning melanophores and xanthophores during zebrafish adult pigment stripe formation

    PLoS Genet.

    (2013)
  • A.P. Singh

    Proliferation, dispersal and patterned aggregation of iridophores in the skin prefigure striped colouration of zebrafish

    Nat. Cell Biol.

    (2014)
  • F.J. van Eeden

    Genetic analysis of fin formation in the zebrafish, Danio rerio

    Development

    (1996)
  • P. Mahalwar

    Local reorganization of xanthophores fine-tunes and colors the striped pattern of zebrafish

    Science

    (2014)
  • S.K. McMenamin

    Thyroid hormone-dependent adult pigment cell lineage and pattern in zebrafish

    Science

    (2014)
  • H.G. Frohnhöfer

    Iridophores and their interactions with other chromatophores are required for stripe formation in zebrafish

    Development

    (2013)
  • A. Nakamasu

    Interactions between zebrafish pigment cells responsible for the generation of Turing patterns

    Proc. Natl. Acad. Sci. U. S. A.

    (2009)
  • D.S. Eom et al.

    A macrophage relay for long-distance signaling during postembryonic tissue remodeling

    Science

    (2017)
  • M. Yamaguchi

    Pattern regulation in the stripe of zebrafish suggests an underlying dynamic and autonomous mechanism

    Proc. Natl. Acad. Sci. U.S.A.

    (2007)
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