Colorful seashells: Identification of haem pathway genes associated with the synthesis of porphyrin shell color in marine snails

Williams, Suzanne T.; Lockyer, Anne E.; Dyal, Patricia; Nakano, Tomoyuki; Churchill, Celia K. C.; Speiser, Daniel I.

Colorful seashells: Identification of haem pathway genes associated with the synthesis of porphyrin shell color in marine snails

Type

Article

Authors

Williams, Suzanne T.

Lockyer, Anne E.
Dyal, Patricia
Nakano, Tomoyuki
Churchill, Celia K. C.
Speiser, Daniel I.

KAUST Grant Number

CRG-1-2012-BER-002
59130357

Online Publication Date

2017-10-30

Print Publication Date

2017-12

Date

2017-10-30

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.

Citation

Williams ST, Lockyer AE, Dyal P, Nakano T, Churchill CKC, et al. (2017) Colorful seashells: Identification of haem pathway genes associated with the synthesis of porphyrin shell color in marine snails. Ecology and Evolution 7: 10379–10397. Available: http://dx.doi.org/10.1002/ece3.3552.

Acknowledgements

We are very grateful to Piotr Kuklinski for collecting and preserving Calliostoma zizyphinum and for the photograph of the living animal; Gustav Paulay for collecting Clanculus pharaonius in Saudi Arabia while at KAUST and Michael Berumen and Joey DiBattista for the invitation to STW to visit KAUST. We also thank Lisa Smith and Kevin Hopkins for expert help in the laboratory and Harry Taylor for photographs of specimens. We thank Chiho Ikebe for discussions about qPCR and Menno Schilthuizen, Tim Littlewood, Ana Riesgo, Andrew Parker, David Reid, John Taylor, and Alfried Vogler for comments on text that predated this manuscript and three anonymous reviewers for helpful comments. Finally, we gratefully acknowledge funding from the Life Sciences Department at the Natural History Museum, London, and support from Todd Oakley and the Oakley Laboratory at the University of California Santa Barbara, as well as UCSB's Center for Scientific Computing at the CNSI and MRL. UCSB's Center for Scientific Computing at the CNSI and MRL was a recipient of NSF MRSEC DMR-1121053 and NSF CNS-0960316. DIS was supported by NSF EAGER-10457 and NSF DEB-1355230. STW's visit to KAUST was funded by KAUST awards CRG-1-2012-BER-002 and 59130357 (to M.L. Berumen).