Abstract
Very little is known about the evolution of molluskan shell pigments, although Mollusca is a highly diverse, species rich, and ecologically important group of animals comprised of many brightly colored taxa. The marine snail genus Clanculus was chosen as an exceptional model for studying the evolution of shell color, first, because in Clanculus margaritarius and Clanculus pharaonius both shell and foot share similar colors and patterns; and second, because recent studies have identified the pigments, trochopuniceus (pink‐red), and trochoxouthos (yellow‐brown), both comprised of uroporphyrin I and uroporphyrin III, in both shell and colored foot tissue of these species. These unusual characteristics provide a rare opportunity to identify the genes involved in color production because, as the same pigments occur in the shell and colored foot tissue, the same color‐related genes may be simultaneously expressed in both mantle (which produces the shell) and foot tissue. In this study, the transcriptomes of these two Clanculus species along with a third species, Calliostoma zizyphinum, were sequenced to identify genes associated with the synthesis of porphyrins. Calliostoma zizyphinum was selected as a negative control as trochopuniceus and trochoxouthos were not found to occur in this species. As expected, genes necessary for the production of uroporphyrin I and III were found in all three species, but gene expression levels were consistent with synthesis of uroporphyrins in mantle and colored foot tissue only in Clanculus. These results are relevant not only to understanding the evolution of shell pigmentation in Clanculus but also to understanding the evolution of color in other species with uroporphyrin pigmentation, including (mainly marine) mollusks soft tissues and shells, annelid and platyhelminth worms, and some bird feathers.
Highlights
Color and pattern are important features of morphological adaptive variation and are often associated with crypsis, aposematism, and mating displays (Ruxton, Sherratt, & Speed, 2004)
We investigated the biosynthesis of two dominant shell porphyrin pigments that have recently been found to contribute to shell color in the marine snails Clanculus pharaonius and C. margaritarius
We identify genes associated with the production of porphyrin pigments in colored foot tissue and mantle tissue in two species known to have porphyrin pigmentation and one that does not
Summary
Color and pattern are important features of morphological adaptive variation and are often associated with crypsis, aposematism, and mating displays (Ruxton, Sherratt, & Speed, 2004). Uroporphyrin I and uroporphyrin III are produced in several forms of porphyria, a metabolic disorder affecting humans, and their synthesis has been well studied (Layer, Reichelt, Jahn, & Heinz, 2010) They are synthesized as side products of the evolutionarily ancient heme pathway, which is conserved among metazoans and has been well characterized in humans, Mus and Drosophila (Ajioka, Phillips, & Kushner, 2006; Heinemann, Jahn, & Jahn, 2008; Figure 2). We used qPCR to compare expression levels within all three species between three tissue types: mantle tissue, which is responsible for shell construction and potentially pigment production, colored foot tissue (in Clanculus only), and unpigmented columellar muscle tissue. We did not expect to necessarily observe the same pattern in Ca. zizyphinum, which has unknown shell pigments
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