Plasticity for colour adaptation in vertebrates explained by the evolution of the genes pomc, pmch and pmchl

Abstract

Different camouflages work best with some background matching colour. Our understanding of the evolution of skin colour is based mainly on the genetics of pigmentation (“background matching”), with little known about the evolution of the neuroendocrine systems that facilitate “background adaptation” through colour phenotypic plasticity. To address the latter, we studied the evolution in vertebrates of three genes, pomc, pmch and pmchl, that code for α‐MSH and two melanin‐concentrating hormones (MCH and MCHL). These hormones induce either dispersion/aggregation or the synthesis of pigments. We find that α‐MSH is highly conserved during evolution, as is its role in dispersing/synthesizing pigments. Also conserved is the three‐exon pmch gene that encodes MCH, which participates in feeding behaviours. In contrast, pmchl (known previously as pmch), is a teleost‐specific intron‐less gene. Our data indicate that in zebrafish, pmchl‐expressing neurons extend axons to the pituitary, supportive of an MCHL hormonal role, whereas zebrafish and Xenopus pmch+ neurons send axons dorsally in the brain. The evolution of these genes and acquisition of hormonal status for MCHL explain different mechanisms used by vertebrates to background‐adapt.

Decoding the Evolution of Melanin in Vertebrates

“…Key neuroendocrine and paracrine regulators of melanophore activity are α-MSH for melanin synthesis, melanophore proliferation and differentiation (as in mammals and birds), and α-MSH, MCH, noradrenaline, and melatonin for melanosome aggregation and dispersion [122]. In all vertebrates, α-MSH induces melanosome dispersion, while MCH may either be a dispersant in teleost fish or an aggregant similar to melatonin in other taxa, facilitating substrate matching (background adaptation) [89]. Long-term substrate matching may also induce melanophore apoptosis or proliferation [123].…”

“…In extant birds this is regulated, at least in part, by Sox10 [88], suggesting that α-MSH and/or MCH regulation of substrate matching [89] emerged early during vertebrate evolution.…”

“…Phylogenetic bracketing of genomic data from the literature[85,86,89,[93][94][95]123,[128][129][130][131][132] suggests that the emergence of certain regulatory genes can be linked tentatively to key nodes in the simplified phylogenetic tree. Dates (in millions of years, Ma) for key nodes in the phylogeny indicate when the capacity for certain functions may have emerged.…”

Melanin‐concentrating hormone like and somatolactin. A teleost‐specific hypothalamic‐hypophyseal axis system linking physiological and morphological pigmentation

“…These neurons are known to control appetite, food intake and energy balance in vertebrates. In contrast, the teleost MCHL is a peptide synthesized by hypothalamic neurons that project to the hypophysis; MCHL is stored in the pituitary neural lobe and released when organisms are suddenly exposed to a light‐colour background (Bertolesi et al., 2019; Diniz & Bittencourt, 2019; Kawauchi, 2006). Indeed, MCHL plasma levels increase in several teleost species reared on a white background, which causes pigment aggregation in skin chromatophores (Green, Baker, & Kawauchi, 1991; Kawauchi, 2006; Kishida, Baker, & Bird, 1988).…”

“…However, there was no clear recognition that the two genes that encoded peptides with different physiological roles were related evolutionarily. Moreover, antibodies generated against salmon MCHL and mammalian MCH cross react with the other peptide (Bertolesi et al., 2019). As such, immunohistochemical studies performed for 30 years after the identification of MCH and MCHL failed to distinguish between the two peptides, which are almost identical in amino acid sequence, and both contain a disulphide bridge that rings the molecule (Figure 1b).…”