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Molecular and cellular bases of color pattern evolution in cichlid fishes

Molecular and cellular bases of color pattern evolution in cichlid fishes

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LIANG, Yipeng, 2020. Molecular and cellular bases of color pattern evolution in cichlid fishes [Dissertation]. Konstanz: University of Konstanz

@phdthesis{Liang2020Molec-50490, title={Molecular and cellular bases of color pattern evolution in cichlid fishes}, year={2020}, author={Liang, Yipeng}, address={Konstanz}, school={Universität Konstanz} }

eng terms-of-use Animal coloration and pigmentation vary within and between species and play important roles in natural selection and sexual selection. The diversity and visibility of animal color patterns provide unique opportunities for exploring the processes of divergent and repeated evolution. Whether similar color patterns share common genetic and developmental mechanisms and how gene regulatory complexities translate into diverse color phenotypes are among the long-standing questions in the evolutionary developmental biology of animal color patterns. Considerable efforts have been made in a few model organisms, yet these questions are still just beginning to answer as the general insights into the molecular processes of phenotypic diversity require a wide taxonomic range. Taking advantages of their intrafamilial diversity in color patterns, experimental and genetical tractability and manipulability, the chapters of this thesis use cichlid fishes as an amenable system to integrative investigate the mechanistic basis of color pattern formation.<br />Chapter I investigates the genetic basis underlying the convergent evolution of stripe patterns in cichlid radiations. The melanic horizontal stripes are a notable example of phenotypic convergence and have evolved many times across the cichlid adaptive radiations of Lake Victoria, Malawi, and Tanganyika. Genetic mapping and gene expression analyses suggest that regulatory changes of agouti-related peptide (agrp2), a teleost-specific agouti gene, account for this evolutionarily labile trait: high expression of agrp2 blocks formation of stripe, while low expression permits stripe presence. Experimental manipulation of agrp2 in nonstriped cichlid by CRISPR-Cas9 knockout results in stripes reconstitution further supports the link between this gene and stripe patterns. Yet, cis-regulatory mutations are only predictive of stripes in Lake Victoria, while additional genetic modifiers may exist in species from other lakes, suggesting independent regulatory mechanisms underlying a shared genomic basis (regulatory changes of agrp2) of stripes across East African cichlid adaptive radiations.<br />Chapter II comprehensively characterizes mutational and structural changes at the agrp2 locus and illustrates how these genomic features may promote the functional divergence of agrp2. Using combination of comparative genomic approaches, 5’ and 3’RACE, RNA-sequencing, TaqMan probe assays and molecular evolutionary analyses, several unknown isoform, duplications, insertions and deletions in agpr2 were uncovered. In particular, a tandem duplication of the last exon of agrp2 is described and can date the age to 8-12 million years that likely predates the East African cichlid radiations. Variation in presence/absence patterns and copy numbers between and even within species are observed in this duplication among all African cichlid radiations, suggesting this tandem duplication may facilitate neofunctionalization or even functional degeneration of agrp2, thus serve as a source of incipient diversification in color patterns of cichlid fishes.<br />Striped patterns and dorsa-ventral countershading in cichlids are similar to those seen in the radiation of teleost fishes. In vertebrates, members of the agouti gene family, including agrp2 and agouti-signaling protein 1 (asip1), have been repeatedly linked to the evolution of these two color patterns. Chapter III specifically investigates the functional conservation and diversity of agpr2 and asip1 in color patterns presence-absence and formation across teleost fishes. Comparative gene expression in striped–nonstriped species pairs, together with results from Chapter I, support that regulatory changes of agrp2 act as global molecular switches controlling the presence-absence of stripe patterns across the teleost fish radiation. Spatial expression differences of agrp2 and asip1 across dorsa-ventral axis suggest that the paralogs may have complementary functions in stripe-interstripe patterning. In addition, the asip1 expression patterns are strikingly constrained and conserved across vertebrate and associated with countershading and stripe patterns, suggesting a functional convergence of this gene. Finally, this study gives insights into the functional conservation and sub- and neofunctionalization that occurred during the evolution of agouti gene family and highlight the evolutionary consequence in teleost color patterns.<br />Another remarkable feature of some species is that they change their coloration during ontogeny or even as adults. Color changes are dramatic in some cichlid species, e.g. the Malawi golden cichlid (Melanochromis auratus) which has a prominent sexual dimorphism in coloration. While females and subordinate males are bright yellow with two dark horizontal stripes (yellow morph), dominant males undergo a drastic morphological change in coloration and become dark with two light blue horizontal stripes (dark morph). Chapter IV describes the cellular basis and transcriptional differences between the two morphs. Using light microscope and transmission electron microscope imaging, pronounced changes in cellular and ultrastructural levels are detected, which include changes in chromatophore distribution, pigment dispersal, and organelle properties. The transcriptomic analysis uncovers beside differentially regulated pigmentation genes, also several neural genes that are highly expressed in the skin of the dark morph. These results are further supported by immunohistochemistry staining as the density of neuronal fibers increases in the dark morph compared with the yellow morph. Therefore, this chapter gives novel insights into the cellular, physiological and genetic basis of color change in cichlid fishes.<br />Although progress has been made to identify the genetic basis underlying the diversification of cichlid color patterns, the developmental aspects of color phenotypes in cichlid fishes have been understudied. Chapter V investigates the development and cellular and transcriptional correlates of vertical bar patterns of Lake Victoria cichlid Haplochromis latifasciatus. By tracking the pattern formation, the macroscopic appearance of vertical bars is caused by increased differentiation of melanoblasts and accumulation of melanin within bar regions during the first three weeks. In adults, melanic bars are characterized by a higher density of melanophores, which is associated with increased expression of melanin synthesis genes. The marker genes of xanthophore and iridophore are not differentially expressed showing rather homogenous distribution of iridophores and xanthophores across the trunk. Such complement results suggest that the vertical bars of H. latifasciatus are formed through dynamic control of melanophore characteristics and therefore provide a baseline for studying the molecular and cellular properties that contribute to the development of color patterns of cichlid fishes.<br />In summary, this thesis demonstrates how genes generate environments that repress/permit and shape the color pattern formation across the cichlid and teleost radiations, while independent regulatory and structural mutations of the same genes may serve as a source of diversification in color patterns. The detailed morphological description of cichlid color pattern from this thesis, on the other hand, provides a conceptual illustration of how pigment organelles and chromatophores in certain environments acting as paints on a palette to color the body of the fishes. Overall, the integrative analyses within this thesis provide both deeper and broader insights into the developmental and genetic mechanisms underlying color pattern evolution in cichlid fishes. Liang, Yipeng 2020-08-12T06:57:59Z Liang, Yipeng 2020-08-12T06:57:59Z Molecular and cellular bases of color pattern evolution in cichlid fishes 2020

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