Abstract

Morphological differentiation among closely related species provides opportunities to study mechanisms shaping natural phenotypic variation. Here, we address variation in the orientation of melanin-colored body stripes in three cichlid species of the tribe Haplochromini. Melanochromis auratus displays a common pattern of dark, straight horizontal body stripes, whereas in Aristochromis christyi and Buccochromis rhoadesii, oblique stripes extend from the anterior dorsal to the posterior mid-lateral trunk. We first validated a stably reference gene, and then, investigated the chromatophore distribution in the skin by assessing the expression levels of the iridophore and melanophore marker genes, ltk and slc24a5, respectively, as well as pmel, a melanophore pigmentation marker gene. We found anterior-posterior differences in the expression levels of the three genes in the oblique-striped species. The higher anterior expression of ltk, indicates increased iridophore density in the anterior region, i.e., uneven horizontal distribution of iridophores, which coincides with the anterior dorsalization of melanophore stripe in these species. The obliqueness of the horizontal body stripes might be a result of distinct migratory or patterning abilities of melanophores in anterior and posterior stripe regions which could be reflected by variation in the expression of genes involved in melanophore patterning. To address this, we investigated anterior-posterior expression levels of a primary set of candidate target genes with known functions in melanophore migration and stripe patterning in the adult zebrafish, and their related gene regulatory network. Among these genes, those with differences in anterior-posterior expression showed only species-specific differential expression, e.g., sdf1a, col14a1a, ifitm5, and agpat3, with the exception of fbxw4/hagoromo (differentially expressed in an oblique-and the straight-striped species). In summary, distinct anterior-posterior gradients in iridophore density found to be more similar characteristic between the two oblique-striped species. Furthermore, the species-specific differential expression of genes involved in stripe patterning might also implicate distinct molecular processes underlying the obliqueness of body stripe in two closely related cichlid species.

Highlights

  • Fish are renowned for their diverse color patterns

  • We focus on a particular modification of the horizontal stripe pattern, namely the display of oblique melanincolored stripes, which extend at an angle from an anterior dorsal position behind the head to a mid-lateral position at the end of the caudal peduncle, in Aristochromis christyi and Buccochromis rhoadesii from Lake Malawi, East Africa (Figs. 1A, 1B)

  • It has been shown that melanophores disperse throughout the skin in the absence of other chromatophores (Takahashi & Kondo, 2008), and a model of chromatophore interactions suggests that iridophores repel melanophores on a very short range but cause them to aggregate in their neighborhood, which contributes to the light-dark stripe pattern in the adult zebrafish (Frohnhöfer et al, 2013)

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Summary

Introduction

Fish are renowned for their diverse color patterns. These patterns include horizontal stripes, vertical bars, as well as clearly defined or gradually shading patches of color (Parichy, 2003; Kelsh, 2004). The molecular mechanisms contributing to color pattern morphogenesis have been studied extensively in the zebrafish, whose adult pattern consists of alternating dark and light stripes along the body and fins (Parichy, 2003; Singh & Nüsslein-Volhard, 2015). Short distance inhibitory interactions with iridophores do not allow melanophores to settle within the light regions of zebrafish skin, but iridophores promote melanophore aggregation nearby through long distance attraction (Patterson & Parichy, 2013; Frohnhöfer et al, 2013). A number of genes involved in adult stripe formation and/or maintenance have already been identified in the zebrafish (Singh & Nüsslein-Volhard, 2015) and can readily be tested as candidates contributing to the natural variation of color patterns across different groups of fishes (Ahi & Sefc, 2017)

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