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

Handle URI:
http://hdl.handle.net/10754/626681
Title:
Colorful seashells: Identification of haem pathway genes associated with the synthesis of porphyrin shell color in marine snails
Authors:
Williams, Suzanne T. ( 0000-0003-2995-5823 ) ; Lockyer, Anne E.; Dyal, Patricia; Nakano, Tomoyuki; Churchill, Celia K. C.; Speiser, Daniel I.
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.
Publisher:
Wiley-Blackwell
Journal:
Ecology and Evolution
KAUST Grant Number:
CRG-1-2012-BER-002; 59130357
Issue Date:
30-Oct-2017
DOI:
10.1002/ece3.3552
Type:
Article
ISSN:
2045-7758
Sponsors:
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).
Appears in Collections:
Publications Acknowledging KAUST Support

Full metadata record

DC FieldValue Language
dc.contributor.authorWilliams, Suzanne T.en
dc.contributor.authorLockyer, Anne E.en
dc.contributor.authorDyal, Patriciaen
dc.contributor.authorNakano, Tomoyukien
dc.contributor.authorChurchill, Celia K. C.en
dc.contributor.authorSpeiser, Daniel I.en
dc.date.accessioned2018-01-04T07:51:38Z-
dc.date.available2018-01-04T07:51:38Z-
dc.date.issued2017-10-30en
dc.identifier.citationWilliams 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.en
dc.identifier.issn2045-7758en
dc.identifier.doi10.1002/ece3.3552en
dc.identifier.urihttp://hdl.handle.net/10754/626681-
dc.description.abstractVery 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.en
dc.description.sponsorshipWe 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).en
dc.publisherWiley-Blackwellen
dc.titleColorful seashells: Identification of haem pathway genes associated with the synthesis of porphyrin shell color in marine snailsen
dc.typeArticleen
dc.identifier.journalEcology and Evolutionen
dc.contributor.institutionDepartment of Life Sciences; Natural History Museum; London UKen
dc.contributor.institutionInstitute of Environment, Health and Societies; Brunel University London; Uxbridge UKen
dc.contributor.institutionCore Research Laboratories; Natural History Museum; London UKen
dc.contributor.institutionSeto Marine Biological Laboratory; Kyoto University; Nishimuro Wakayama Prefecture Japanen
dc.contributor.institutionMarine Science Institute; University of California; Santa Barbara CA USAen
dc.contributor.institutionDepartment of Biological Sciences; University of South Carolina; Columbia SC USAen
kaust.grant.numberCRG-1-2012-BER-002en
kaust.grant.number59130357en
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