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

Abstract

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. 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 helpful models for combining genetic manipulations with live imaging, and their study has provided new insights on the cellular and molecular mechanisms that drive the development of color patterns [4]. Other fish such as cichlids and guppies have also provided valuable insight into genes and molecular mechanisms underlying specific traits (egg spots and stripes) and various color ornaments [5][6][7].While mammals only possess melanocytes, the teleost lineage harbors the highest number of pigment cell typesalso called chromatophores (e.g., melanophores, xanthophores, and iridophores) [8]. This diversity can explain the diversity of color and their patterns and implies the involvement of many pigmentation genes. The list of identified genes has increased in recent years (Box 1) and the whole genome duplication that occurred at the basis of the teleost lineage has been identified as a major contributor to this diversity [9].To be able to fully understand the evolution of traits such as those displayed in color patterns and the genetic mechanisms underlying the responses of organisms to their natural environment, it is important to perform Eco/Evo/Devo approaches. However, ecological and behavioral roles of color patterns have not been studied in the model organisms cited above, leading to a black box concerning how proximate factors shape color patterns and their diversity over evolution. Reef fish offer promising models to address such questions because they do express much of the amazing diversity of color patterns as well as associated behavioral and ecological variation. Their original color patterns include dark or conspicuous colors, and can be made of a diverse combin...

Unique and non-redundant function of csf1r paralogues in regulation and evolution of post-embryonic development of the zebrafish

“…In addition, in teleost fishes, csf1ra has been found to be expressed in neural crest progenitors and to act to regulate pigmentation cell differentiation and pattern (Parichy et al, 2000), a trait not related with Csf1 signaling in other vertebrates. It has been argued that selection on pigmentation phenotypes in fishes have contributed to their diversification (Irion et al, 2016;Salis et al, 2019). However, the additional role of csf1r function in regulating skeletal development may constrain the phenotypic spectrum of morphological variation in evolution.…”

Fine-scale species delimitation: speciation in process and periodic patterns in nudibranch diversity

“…Finer analysis shows that such complexes are possible to distinguish morphologically, by using a combination of various methods including the periodic approach suggested here. Several further studies on different groups, such as rodents (Johnson et al 2018) and fishes (Gante 2018;Salis et al 2019), confirmed the existence of periodic patterns during the development of morphological characters, yet without direct construction of periodic-like tables, which can be a next step. Thus, these complex periodic-like genetic-epigenetic interactions within an ontogenetic framework can work as a theoretical foundation and confirmation of the practical validity of a periodic approach in taxonomy and phylogeny.…”

Anemonefish, a model for Eco-Evo-Devo

“…The juveniles of some species have supplementary bars that later disappear in a caudo-rostral sequence. The reduction of bar number during the ontogeny matches the sequence of bar loss across evolution [46,47]. In zebrafish, color pattern composed of periodic stripes forms through a reaction-diffusion system (Turing model), whereby stripe numbers depend on the size of the fish (review in [45]).…”

“…Whereas most previous investigations of teleost pigment pattern formation focused on the horizontal stripe patterns of the zebrafish (Danio rerio), anemonefish offer an alternative case study in which different mechanisms controlling vertical bar patterns are at play and can be deciphered [45,46]. The 30 anemonefish species display a simple color pattern made of 0 to 3 white bars, containing iridophores, visible on a darker body background (red, orange or black) ( Fig.…”

“…In zebrafish, color pattern composed of periodic stripes forms through a reaction-diffusion system (Turing model), whereby stripe numbers depend on the size of the fish (review in [45]). In anemonefish, the developmental mechanism at the origin of the formation of the white bars differs, as the number of bars does not depend on the size of the fish [46,47]. Moreover, in anemonefish, new bars do not form when the distance between two existing ones increases but are added following an ordered anterior-to-posterior pattern.…”