Abstract

The East African adaptive radiations of cichlid fishes are renowned for their diversity in coloration. Yet, the developmental basis of pigment pattern formation remains largely unknown. One of the most common melanic patterns in cichlid fishes are vertical bar patterns. Here we describe the ontogeny of this conspicuous pattern in the Lake Kyoga species Haplochromis latifasciatus. Beginning with the larval stages we tracked the formation of this stereotypic color pattern and discovered that its macroscopic appearance is largely explained by an increase in melanophore density and accumulation of melanin during the first 3 weeks post-fertilization. The embryonal analysis is complemented with cytological quantifications of pigment cells in adult scales and the dermis beneath the scales. In adults, melanic bars are characterized by a two to threefold higher density of melanophores than in the intervening yellow interbars. We found no strong support for differences in other pigment cell types such as xanthophores. Quantitative PCRs for twelve known pigmentation genes showed that expression of melanin synthesis genes tyr and tyrp1a is increased five to sixfold in melanic bars, while xanthophore and iridophore marker genes are not differentially expressed. In summary, we provide novel insights on how vertical bars, one of the most widespread vertebrate color patterns, are formed through dynamic control of melanophore density, melanin synthesis and melanosome dispersal.

Highlights

  • Pigment patterns play important roles in many aspects of animal biology

  • To investigate the formation of vertical bars (Figure 1E), we described the development of H. latifasciatus larvae between 7 and 21 days post-fertilization

  • Our study shows that vertical bar number remains constant over the course of development in H. latifasciatus (Figures 1F–R, 2D–M and Supplementary Figure S1), which contrasts with a recent study on the Lake Malawi cichlid Copadichromis azureus, a species with unfixed bar number and thinner bars (Hendrick et al, 2019)

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Summary

Introduction

Pigment patterns play important roles in many aspects of animal biology. Yet, until now, only in a few “model” organisms we do have insights into the molecular and developmental underpinnings of color pattern formation and evolutionary diversification. Progress has been made identifying target genes and loci that drive evolutionary diversification in cichlids (Roberts et al, 2009; Kratochwil et al, 2018) and play key roles in adaptation and speciation (Seehausen et al, 1999; Elmer et al, 2009; Maan and Sefc, 2013), the developmental and cellular mechanisms of pigmentation phenotypes have been barely studied. Pigment patterns are caused by spatial variation in pigmentary and/or structural tissue properties Those can be generated by different distribution, density and aggregation state of pigment cells (chromatophores) and their multi-layered arrangement, as well as variation in the synthesis and arrangement of light-absorbing pigments or molecules causing structural coloration (Irion and NüssleinVolhard, 2019; Patterson and Parichy, 2019). Melanophores (containing the brown to black pigment melanin), xanthophores/erythrophores (containing yellow to red pigments) and iridophores (containing reflective guanine platelets causing structural coloration) have been found in cichlids (Maan and Sefc, 2013)

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