Abstract

Fish color patterns are among the most diverse phenotypic traits found in the animal kingdom. Understanding the molecular and cellular mechanisms that control in chromatophore distribution and pigmentation underlying this diversity is a major goal in developmental and evolutionary biology, which has predominantly been pursued in the zebrafish model system. Here, we apply results from zebrafish work to study a naturally occurring color pattern phenotype in the fins of an African cichlid species from Lake Tanganyika. The cichlid fish Neolamprologus meeli displays a distinct dorsal color pattern, with black and white stripes along the edges of the dorsal fin and of the dorsal half of the caudal fin, corresponding with differences in melanophore density. To elucidate the molecular mechanisms controlling the differences in dorsal and ventral color patterning in the fins, we quantitatively assessed the expression of 15 candidate target genes involved in adult zebrafish pigmentation and stripe formation. For reference gene validation, we screened the expression stability of seven widely expressed genes across the investigated tissue samples and identified tbp as appropriate reference. Relative expression levels of the candidate target genes were compared between the dorsal, striped fin regions and the corresponding uniform, grey-colored regions in the anal and ventral caudal fin. Dorso-ventral expression differences, with elevated levels in both white and black stripes, were observed in two genes, the melanosome protein coding gene pmel and in igsf11, which affects melanophore adhesion, migration and survival. Next, we predicted potential shared upstream regulators of pmel and igsf11. Testing the expression patterns of six predicted transcriptions factors revealed dorso-ventral expression difference of irf1 and significant, negative expression correlation of irf1 with both pmel and igsf11. Based on these results, we propose pmel, igsf11 and irf1 as likely components of the genetic mechanism controlling distinct dorso-ventral color patterns in N. meeli fins.

Highlights

  • The mechanisms underlying the formation and diversification of integumental colour patterns in vertebrates have always been a fascinating subject of biological research

  • Comparisons of melanophore density and gene expression patterns were conducted between anatomically comparable regions of the dorsal, caudal and anal fins; i.e., either among the total areas cut from each fin (e.g. D-1 + D-2 + D-3 for the dorsal fin), or separately within each of the corresponding fin region classes; the distal fin regions (D-1, Cd-1, Cv-1 and A-1); the middle fin regions (D-2, Cd-2, Cv-2 and A-2); and the proximal fin regions (D-3, Cd-3, Cv-3 and A-3)

  • Expression comparisons between different classes of fin regions were avoided because given the different histological properties of distinct anatomical fin regions along proximal-distal axis, gene expression differences between non-analogous regions could arise for various reasons not associated with colour patterning

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Summary

Introduction

The mechanisms underlying the formation and diversification of integumental colour patterns in vertebrates have always been a fascinating subject of biological research. The extensive diversity of vertebrate integumental colour patterns arises from variation in migration, organization and differentiation of pigment cells, which themselves originate from neural crest-derived precursor cells during embryonic development (Kelsh et al, 2009; Bronner & LeDouarin, 2012). Genetic studies in fish and tetrapod models, using zebrafish, mouse and chicken mutants, have revealed conservation in some patterning mechanisms such as genes involved in migration and formation of melanophores (Lister, Close & Raible, 2001; Kelsh, 2004; Hoekstra, 2006; Mills & Patterson, 2009; Kelsh et al, 2009)

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