Red carotenoids and associated gene expression explain colour variation in frillneck lizards

Abstract

A long-standing hypothesis in evolutionary ecology is that red–orange ornamental colours reliably signal individual quality owing to limited dietary availability of carotenoids and metabolic costs associated with their production, such as the bioconversion of dietary yellow carotenoids to red ketocarotenoids. However, in ectothermic vertebrates, these colours can also be produced by self-synthesized pteridine pigments. As a consequence, the relative ratio of pigment types and their biochemical and genetic basis have implications for the costs and information content of colour signals; yet they remain poorly known in most taxonomic groups. We tested whether red- and yellow-frilled populations of the frillneck lizard, Chlamydosaurus kingii, differ in the ratio of different biochemical classes of carotenoid and pteridine pigments, and examined associated differences in gene expression. We found that, unlike other squamate reptiles, red hues derive from a higher proportion of ketocarotenoids relative to both dietary yellow carotenoids and to pteridines. Whereas red frill skin showed higher expression of several genes associated with carotenoid metabolism, yellow frill skin showed higher expression of genes associated with steroid hormones. Based on the different mechanisms underlying red and yellow signals, we hypothesize that frill colour conveys different information in the two populations. More generally, the data expand our knowledge of the genetic and biochemical basis of colour signals in vertebrates.

Pteridine pigments compensate for environmental availability of carotenoids

“…Yellow, orange and red hues can all be produced exclusively by carotenoids (Fitze et al 2009) or pteridines (snakes; Kikuchi & Pfennig 2012;Kikuchi et al2014). Furthermore, red hues can be produced by a higher proportion of red ketocarotenoids relative to both dietary yellow carotenoids and to pteridines (McLean et al 2019), or exclusively by drosopterin (Merkling et al 2018). In the majority of lizards, however, both carotenoids and pteridines contribute to colour variation within and between species, with yellow produced by relatively higher concentrations of dietary carotenoids and orange-red produced by a high relative proportion of red pteridines (usually drosopterin;Ortizet al 1963;Ortiz & Maldonado 1966;Macedonia et al2000;Steffen & McGraw 2009;Weiss et al 2012;Haisten et al 2015;McLean et al 2017;Andrade et al 2019).…”

“…structural; Twomey et al 2020b). Furthermore, skin tissue commonly contains high concentrations of colourless pteridines such as isoxanthopterin, pterin and biopterin (Bagnara & Matsumoto 2006;McLeanet al 2017;McLean et al 2019;Twomey et al2020b). We found an association between the concentration of colourless pteridines and skin colour saturation and luminance.…”

“…We quantified concentrations of 5 carotenoids (lutein/zeaxanthin, 3'-dehydrolutein, β-carotene, astaxanthin, canthaxanthin) and 6 pteridines (drosopterin, xanthopterin, pterin, 6-biopterin, isoxanthopterin, pterine-6-carboxylic acid) in two separate liquid chromatography-mass spectrometry analyses on an Agilent 6490 triple quadrupole MS system with a Jet Stream electrospray ionization source coupled to an Agilent 1290 series LC system (Agilent Technologies Inc, Santa Clara, CA). The yellow carotenoid β-cryptoxanthin and very low levels of the yellow pteridine sepiapterin have also been identified in skin tissue of agamid lizards (McLean et al 2017;McLean et al 2019); however runs for these pigments were inconsistent, so they were not analyzed further.…”

Convergence and divergence in lizard colour polymorphisms

“…Differences in the biochemical basis of polymorphism has implications for the cost and information content of colour signals. Specifically, costs associated with synthesis of coloured pteridines, acquisition and metabolism of carotenoids, and trade‐offs in allocation to colour signals versus other physiological functions, all clearly differ for different types of pigments (McLean et al ., 2019). Consequently, the extent to which colour signals individual condition may differ for different morphs within species, or for similar morphs among species.…”

Untangling the structural and molecular mechanisms underlying colour and rapid colour change in a lizard, Agama atra

“…Regardless, both pigments absorb short‐wavelength light and are responsible for yellow to reddish hues. Nonetheless, carotenoids are the primary mechanism for yellow and/or red hues in birds, while in reptiles these hues are mostly generated by pteridines (Mclean et al, 2019). The fourth type, iridophores, contains stacks of guanine crystals that, through differences in refraction and reflection, and often in conjunction with the basal melanophore layer, can produce (typically) blue colours (Saenko et al, 2013; Teyssier et al, 2015).…”