Body coloration and mechanisms of colour production in Archelosauria: the case of deirocheline turtles

Abstract

Animal body coloration is a complex trait resulting from the interplay of multiple mechanisms. While many studies address the functions of animal coloration, the mechanisms of colour production still remain unknown in most taxa. Here we compare reflectance spectra, cellular, ultra- and nano-structure of colour-producing elements, and pigment types in two freshwater turtles with contrasting courtship behaviour, Trachemys scripta and Pseudemys concinna . The two species differ in the distribution of pigment cell-types and in pigment diversity. We found xanthophores, melanocytes, abundant iridophores and dermal collagen fibres in stripes of both species. The yellow chin and forelimb stripes of both P. concinna and T. scripta contain xanthophores and iridophores, but the post-orbital regions of the two species differ in cell-type distribution. The yellow post-orbital region of P. concinna contains both xanthophores and iridophores, while T. scripta has only xanthophores in the yellow-red postorbital/zygomatic regions. Moreover, in both species, the xanthophores colouring the yellow-red skin contain carotenoids, pterins and riboflavin, but T. scripta has a higher diversity of pigments than P. concinna . Trachemys s. elegans is sexually dichromatic. Differences in the distribution of pigment cell types across body regions in the two species may be related to visual signalling but do not match predictions based on courtship position. Our results demonstrate that archelosaurs share some colour production mechanisms with amphibians and lepidosaurs (i.e. vertical layering/stacking of different pigment cell types and interplay of carotenoids and pterins), but also employ novel mechanisms (i.e. nano-organization of dermal collagen) shared with mammals.

Estimating the distribution of carotenoid coloration in skin and integumentary structures of birds and extinct dinosaurs

“…We are confident that our scorings accurately represent colorations that are consistent with those produced by carotenoids, but recognize that perceived coloration may not reflect the presence or absence of carotenoids themselves (hence our use of "carotenoid-consistent" when referring to colors from unverified pigment sources, following Thomas et al 2014a). However, given that previous work has not identified other similarly colored pigments in the skins or keratinous tissues of living archosaur groups (i.e., pterins ;Hill & Mc-Graw, 2006;Iverson & Karubian, 2017;Brejcha et al, 2019), the hypothesis that these colors in birds are due to carotenoids is a reasonable one until evidence suggests otherwise. Within birds, noncarotenoid pigments of similar colors to carotenoids are thought to be exclusive to plumage (penguins, turacos, and parrots;Krukenberg 1882;Dyck 1992;McGraw & Nogare, 2005;Hill & McGraw, 2006;Thomas et al, 2013); however, it is possible that they are simply yet to be detected in other integument structures.…”

Pterin-based pigmentation in animals

“…All dermal cell types originate from the neural crest cell population, and thus share a similar developmental path [63]. In xanthophores, pterins are concentrated in intra-cytoplasmic organelles termed pterinosomes, formed by a three-layered outer membrane and a variable internal arrangement of pterincontaining membranes, depending on the developmental stage [64][65][66][67][68][69]. Developmentally, pterinosomes are homologous to melanin-containing melanosomes, and seem to share a similar dual origin from the Golgi and endoplasmic reticulum, as lysosome-related organelles [70,71].…”

“…Signalling in a reproductive context has been another of the primary functions ascribed to pterins. Examples of these pigments creating sexually dichromatic signals can be found in insects [35,60,94,95], fish [96,97], reptiles [69,98,99] and amphibians [100]. Sexual dichromatism in a visual trait may not necessarily mean that the trait is implicated in sexual selection; for example, it could be associated with differential susceptibility of males and females to predators leading to enhanced aposematic displays in one of the sexes.…”

Genetic and correlative light and electron microscopy evidence for the unique differentiation pathway of erythrophores in brown trout skin

“…the transformation of one type into another) 8 , 38 . Furthermore, mosaic pigment cells containing more than one type of organelle, and mosaic organelles containing more than one type of pigment can be found in vertebrate skin 8 , 39 . For instance, in frogs, a mosaic of chromatophores containing melanosomes, erythrosomes, xanthosomes, and refractosomes was observed 40 , 41 .…”