Pigment patterns in adult fish result from superimposition of two largely independent pigmentation mechanisms

Abstract

Dorso-ventral pigment pattern differences are the most widespread pigmentary adaptations in vertebrates. In mammals, this pattern is controlled by regulating melanin chemistry in melanocytes using a protein, agouti-signalling peptide (ASIP). In fish, studies of pigment patterning have focused on stripe formation, identifying a core striping mechanism dependent upon interactions between different pigment cell types. In contrast, mechanisms driving the dorso-ventral countershading pattern have been overlooked. Here, we demonstrate that, in fact, zebrafish utilize two distinct adult pigment patterning mechanisms - an ancient dorso-ventral patterning mechanism, and a more recent striping mechanism based on cell-cell interactions; remarkably, the dorso-ventral patterning mechanism also utilizes ASIP. These two mechanisms function largely independently, with resultant patterns superimposed to give the full pattern.

Developmental and Cellular Basis of Vertical Bar Color Patterns in the East African Cichlid Fish Haplochromis latifasciatus

“…Two proteins of the Agouti family, Asip1 and Agrp2, likely act as the antagonists for the melanocortin receptors Mc1r and/or Mc5r in teleost skin (Cal et al, 2017). As previous studies suggest, asip1 is a key regulator of dorso-ventral countershading, presumably by regulating melanophore number (Ceinos et al, 2015;Cal et al, 2017Cal et al, , 2019. Interestingly we also found significant variation along the anterior-posterior axis (ANOVA: P < 0.01) with asip1 being expressed significantly higher in some pair-wise post hoc comparisons between bars and interbars (Tukey HSD: P = 0.0016-0.8222; Figure 5I and Supplementary Table S2).…”

Pigment Cell Progenitors in Zebrafish Remain Multipotent through Metamorphosis

“…The environment, in turn, might be defined by the ligands for pigment cell-specific signaling systems such as Kita for melanophores, Ltk and Ednrb for iridophores, and Csf1ra for xanthophores (Dooley et al, 2013a;Fadeev et al, 2016;Frohnhö fer et al, 2013;Lopes et al, 2008;Parichy et al, 1999Parichy et al, , 2000aParichy et al, , 2000b. Consistent with a role for the tissue environment, other genes have been identified that affect pigment cell fate non-cell autonomously, and in a body region-specific manner (Ceinos et al, 2015;Krauss et al, 2014a;Lang et al, 2009). Expression of the ligands may lead to a specific pigment cell fate by interactions between specific ligand-receptor systems, although it is also possible that there are other mechanisms that prime the progenitors toward specific cell fates.…”

“…The cell numbers required to generate the adult stripe pattern are not identical along the anterior-posterior body axis; in the anterior region of the trunk there are four to five dark stripes and four light stripes, and only three dark and two light stripes extend to the posterior regions. Similarly, along the dorsoventral axis, pigment cell numbers and composition varies in body, viscera, and scales (Ceinos et al, 2015;Fadeev et al, 2016). Given that the pigment cells share a lineage along the dorsoventral axis, it might be advantageous to have progenitors that are not fate restricted: this will allow an efficient local regulation of specific cell fates during development and regeneration.…”

Agouti-related peptide 2 facilitates convergent evolution of stripe patterns across cichlid fish radiations

“…The teleost-specific agrp2 ( fig. S3) is a strong candidate gene for stripes because its paralogs have been previously associated with pigmentation phenotypes (18)(19)(20). To test for agrp2 expression differences between nonstriped (Pnye) and striped (Hsau) Lake Victoria cichlids, we performed quantitative polymerase chain reaction (qPCR; Fig.…”