Sexual dimorphism in shell coloration of Plectostoma (Caenogastropoda: Diplommatinidae) is caused by polyenes

Sexual dimorphism in shell coloration of Plectostoma (Caenogastropoda: Diplommatinidae) is caused... While many terrestrial gastropods are members of the Pulmonata and therefore hermaphroditic, a considerable fraction, especially in the humid tropics, belong to the Caenogastropoda and Neritimorpha, and have separate sexes. In marine and freshwater gastropods, sexual differences in shell size, shape and (occasionally) colour have been widely reported (e.g. Griffiths, 1961; reviews by Lamy, 1937 and Galindo Pérez, 2009). Nevertheless, sexual dimorphism of the shell is poorly studied in terrestrial gonochoristic gastropods (but see Raven, 1990; Reichenbach et al., 2012). Previously, we described a sexual colour dimorphism in the Plectostoma concinnum species complex (Schilthuizen et al., 2003). These diplommatinids with diverse and extravagant shell shapes (Vermeulen, 1994; Gittenberger, 1995; Schilthuizen, 2003; Clements et al., 2008) occur on isolated limestone outcrops along the Kinabatangan river in Sabah, Malaysian Borneo (Schilthuizen et al., 2006). Although we could not measure any sexual dimorphism in shell shape, there is a clear colour difference: the first three to four whorls of the shell are bright red in adult males, but white to pale yellow in adult females (Fig. 1). Juveniles of both sexes have entirely white shells, which means that the pigment is incorporated in the additional shell layers that snails deposit upon reaching sexual maturity (Schilthuizen, 1994). Schilthuizen et al. (2003) determined sex by microscopic examination of the gametes and confirmed that the colour dimorphism exists due to pigments in the shell itself, rather than in the soft body. Figure 1. View largeDownload slide Representative male (top) and female (bottom) Plectostoma concinnum from Gomantong Hill, Sabah, showing the difference in shell coloration. Figure 1. View largeDownload slide Representative male (top) and female (bottom) Plectostoma concinnum from Gomantong Hill, Sabah, showing the difference in shell coloration. Here, we used resonance Raman microspectrometry (RRMS) to assess the chemical background for the red shell coloration in male P. concinnum s. l. We used shells of five mature males and five mature females of P. concinnum s. l. from the entrance of Simud Hitam Cave in Gomantong Hill (5°31′50″N, 118°04′15″E) in Sabah, Malaysian Borneo. The specimens were collected alive on 18 November, 2003 as part of a different project and stored in pure ethanol since then. The top four shell whorls of these specimens were subjected nondestructively to in situ RRMS following the protocol of Hedegaard et al. (2006). The shells were analysed by Raman spectroscopy using a Thermo DXR Raman microscope with 532 nm laser excitation. Raman spectra were collected at room temperature in the confocal mode, which is necessary for analysis of individual layers of a sample on a micron scale (1–2 μm). A grating of 1,800 grooves/mm and a pinhole size of 25 μm were used which, combined with the optical path length, yielded a spectral resolution of 1.0 cm−1. Spectra were collected in the range of 100–1,800 cm−1. In the pale yellowish shell material of females, the Raman-shift spectra only contained peaks around 701, 705 and 1,085 cm−1, which conform with aragonite (Hedegaard et al., 2006; Wehrmeister et al., 2010). However, in the reddish shell material derived from males, we detected strong additional peaks around 1140 and 1,520 cm−1. These wavenumbers are consistent with polyene pigments with 10 carbon–carbon double bonds (Fig. 2; Supplementary Material). Polyenes are defined as polyunsaturated carbohydrates possessing three or more alternating double and single carbon–carbon bonds (Basheer and Umesh, 2016). A well known class of polyenes are carotenoids, which possess four methyl groups attached to the polyenic chain (Karampelas et al., 2009). Polyenes have been detected before as shell pigments in several species of marine Caenogastropoda (Hedegaard et al., 2006; Shimizu et al., 2011; Williams et al., 2016; Williams, 2017), bivalves (Stemmer and Nehrke, 2014) and chitons (Peebles et al., 2017). Figure 2. View largeDownload slide Representative Raman spectra (corrected for background fluorescence) for top whorls of male (top) and female (bottom) Plectostoma concinnum. Figure 2. View largeDownload slide Representative Raman spectra (corrected for background fluorescence) for top whorls of male (top) and female (bottom) Plectostoma concinnum. As far as we know, this is the only reported case of discrete sexual shell colour dimorphism in land snails, although Reichenbach et al. (2012) reported that the last whorl of females is, on average, slightly less strongly pigmented in Cochlostoma septemspirale. We note that several other terrestrial Cyclophoroidea, for example the cyclophorid genus Chamalycaeus, as well as many other species of Plectostoma, similarly display a white/red polymorphism in protoconch coloration. To our knowledge, it has not yet been investigated whether this signifies sexual dimorphism as well. The evolution of sexual colour dimorphism, if it is adaptive, is most commonly driven by intraspecific sexual selection, which would imply that these snails have good vision, perhaps even colour vision—something that is considered rare or nonexistent in Gastropoda (Chase, 2001; Williams, 2017). If this should indeed prove to be the case, then these gonochoristic snails could conceivably join a larger group of animals in which polyenes, and particularly carotenoids, play a role in sexual honest signalling of genetic quality, given the immunomodulatory action of these and similar pigments (McGraw, 2005). Alternatively, the colour difference could be unrelated to sexual selection, but rather a byproduct of a sexually differentiated metabolic or catabolic process. SUPPLEMENTARY MATERIAL Supplementary material is available at Journal of Molluscan Studies online. ACKNOWLEDGEMENTS The Sabah Wildlife Department, the Sabah Forestry Department and the Village Heads of Sukau gave permission to conduct the fieldwork; the specimens were collected by A. van Til. We thank B. Páll-Gergely and A. Correoso for help in finding literature, and Associate Editor S.T. Williams and an anonymous reviewer for suggestions that improved the paper. REFERENCES Basheer, T. & Umesh, M. 2016. Polyketides. In: Secondary metabolites  ( P. Kathirvel, ed.), pp. 131– 144. Darshan Publishers, Tamil Nadu, India. Clements, R.G., Liew, T.S., Vermeulen, J.J. & Schilthuizen, M. 2008. Further twists in gastropod shell evolution. Biology Letters , 4: 179– 182. Google Scholar CrossRef Search ADS PubMed  Chase, R. 2001. Sensory organs and the nervous system. In: The biology of terrestrial molluscs  ( G.M. Barker, ed.), pp. 179– 211. CABI, Wallingford, UK. Google Scholar CrossRef Search ADS   Galindo Pérez, L.A. 2009. Estudio morfométrico del dimorfismo sexual de las conchas de especies de gastrópodos marinos comunes (Mollusca: Gastropoda) en Venezuela. MSc thesis, Universidad de Oriente. Gittenberger, E. 1995. On the one hand…. Nature , 373: 19. Google Scholar CrossRef Search ADS PubMed  Griffiths, R.J. 1961. Sexual dimorphism in Cypraeidae. Proceedings of the Malacological Society of London , 34: 203– 206. Hedegaard, C., Bardeau, J.F. & Chateigner, D. 2006. Molluscan shell pigments: an in situ resonance Raman study. Journal of Molluscan Studies , 72: 157– 162. Google Scholar CrossRef Search ADS   Karampelas, S., Fritsch, E., Rondeau, B., Andouche, A. & Métivier, B. 2009. Identification of the endangered pink-to-red Stylaster corals by Raman spectroscopy. Gems & Gemology , 45: 48– 52. Google Scholar CrossRef Search ADS   Lamy, E. 1937. Sur le dimorphisme sexuel des coquilles. Journal of Conchology , 81: 283– 301. Mcgraw, K.J. 2005. The antioxidant function of many animal pigments: are there consistent health benefits of sexually selected colourants? Animal Behaviour , 69: 757– 764. Google Scholar CrossRef Search ADS   Peebles, B.A., Gordon, K.C., Smith, A.M. & Smith, G.P.S. 2017. First record of carotenoid pigments and indications of unusual shell structure in chiton valves. Journal of Molluscan Studies . https://doi.org/10.1093/mollus/eyx033. Raven, J.G.M. 1990. A revision of Obscurella Clessin, 1889 (Gastropoda Prosobranchia: Cyclophoridae). Basteria , 54: 17– 62. Reichenbach, F., Baur, H. & Neubert, E. 2012. Sexual dimorphism in shells of Cochlostoma septemspirale (Caenogastropoda, Cyclophoroidea, Diplommatinidae, Cochlostomatinae). ZooKeys , 208: 1– 16. Google Scholar CrossRef Search ADS   Schilthuizen, M. 1994. Differentiation and hybridisation in a polytypic snail. PhD thesis, Leiden University. Schilthuizen, M. 2003. Sexual selection on land snail shell ornamentation: a hypothesis that may explain shell diversity. BMC Evolutionary Biology , 3: e1. Google Scholar CrossRef Search ADS   Schilthuizen, M., Rosli, R.B., Ali, A.M.B.M., Salverda, M., van Oosten, H., Bernard, H., Ancrenaz, M. & Lackman-Ancrenaz, I. 2003. The ecology and demography of Opisthostoma (Plectostoma) concinnum s. l. (Gastropoda: Diplommatinidae) on limestone outcrops along the Kinabatangan River. In: Kinabatangan Scientific expedition  ( M. Mohamed, B. Goossens, M. Ancrenaz & M. Andau, eds), pp. 55– 71. UMS, Kota Kinabalu, Malaysia. Schilthuizen, M., Van Til, A., Salverda, M., Liew, T.-S., James, S.S., Elahan, B. & Vermeulen, J.J. 2006. Microgeographic evolution of snail shell shape and predator behavior. Evolution , 60: 1851– 1858. Google Scholar CrossRef Search ADS PubMed  Shimizu, K., Sarashina, I., Kagi, H. & Endo, K. 2011. Possible functions of Dpp in gastropod shell formation and shell coiling. Development, Genes and Evolution , 221: 59– 68. Google Scholar CrossRef Search ADS   Stemmer, K. & Nehrke, G. 2014. The distribution of polyenes in the shell of Arctica Islandica from North Atlantic localities: a confocal Raman microscopy study. Journal of Molluscan Studies , 80: 365– 370. Google Scholar CrossRef Search ADS   Vermeulen, J.J. 1994. Notes on the non-marine molluscs of the island of Borneo. 6. The genus Opisthostoma (Gastropoda Prosobranchia: Diplommatinidae). Basteria , 58: 75– 191. Wehrmeister, U., Soldati, A.L., Jacob, D.E., Häger, T. & Hofmeister, W. 2010. Raman spectroscopy of synthetic, geological and biological vaterite: a Raman spectroscopic study. Journal of Raman Spectroscopy , 41: 193– 201. Williams, S.T. 2017. Molluscan shell colour. Biological Reviews , 92: 1039– 1058. Google Scholar CrossRef Search ADS PubMed  Williams, S.T., Ito, S., Wakamatsu, K., Goral, T., Edwards, N.P., Wogelius, R.A., Henkel, T., de Oliveira, L.F.C., Maia, L.F., Strekopytov, S., Jeffries, T., Speiser, D.I. & Marsden, J.T. 2016. Identification of shell colour pigments in marine snails Clanculus pharaonius and C. margaritarius (Trochoidea; Gastropoda). PLoS One , 11: e0156664. Google Scholar CrossRef Search ADS PubMed  © The Author 2017. Published by Oxford University Press on behalf of The Malacological Society of London, all rights reserved. For Permissions, please email: journals.permissions@oup.com http://www.deepdyve.com/assets/images/DeepDyve-Logo-lg.png Journal of Molluscan Studies Oxford University Press

Sexual dimorphism in shell coloration of Plectostoma (Caenogastropoda: Diplommatinidae) is caused by polyenes

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Abstract

While many terrestrial gastropods are members of the Pulmonata and therefore hermaphroditic, a considerable fraction, especially in the humid tropics, belong to the Caenogastropoda and Neritimorpha, and have separate sexes. In marine and freshwater gastropods, sexual differences in shell size, shape and (occasionally) colour have been widely reported (e.g. Griffiths, 1961; reviews by Lamy, 1937 and Galindo Pérez, 2009). Nevertheless, sexual dimorphism of the shell is poorly studied in terrestrial gonochoristic gastropods (but see Raven, 1990; Reichenbach et al., 2012). Previously, we described a sexual colour dimorphism in the Plectostoma concinnum species complex (Schilthuizen et al., 2003). These diplommatinids with diverse and extravagant shell shapes (Vermeulen, 1994; Gittenberger, 1995; Schilthuizen, 2003; Clements et al., 2008) occur on isolated limestone outcrops along the Kinabatangan river in Sabah, Malaysian Borneo (Schilthuizen et al., 2006). Although we could not measure any sexual dimorphism in shell shape, there is a clear colour difference: the first three to four whorls of the shell are bright red in adult males, but white to pale yellow in adult females (Fig. 1). Juveniles of both sexes have entirely white shells, which means that the pigment is incorporated in the additional shell layers that snails deposit upon reaching sexual maturity (Schilthuizen, 1994). Schilthuizen et al. (2003) determined sex by microscopic examination of the gametes and confirmed that the colour dimorphism exists due to pigments in the shell itself, rather than in the soft body. Figure 1. View largeDownload slide Representative male (top) and female (bottom) Plectostoma concinnum from Gomantong Hill, Sabah, showing the difference in shell coloration. Figure 1. View largeDownload slide Representative male (top) and female (bottom) Plectostoma concinnum from Gomantong Hill, Sabah, showing the difference in shell coloration. Here, we used resonance Raman microspectrometry (RRMS) to assess the chemical background for the red shell coloration in male P. concinnum s. l. We used shells of five mature males and five mature females of P. concinnum s. l. from the entrance of Simud Hitam Cave in Gomantong Hill (5°31′50″N, 118°04′15″E) in Sabah, Malaysian Borneo. The specimens were collected alive on 18 November, 2003 as part of a different project and stored in pure ethanol since then. The top four shell whorls of these specimens were subjected nondestructively to in situ RRMS following the protocol of Hedegaard et al. (2006). The shells were analysed by Raman spectroscopy using a Thermo DXR Raman microscope with 532 nm laser excitation. Raman spectra were collected at room temperature in the confocal mode, which is necessary for analysis of individual layers of a sample on a micron scale (1–2 μm). A grating of 1,800 grooves/mm and a pinhole size of 25 μm were used which, combined with the optical path length, yielded a spectral resolution of 1.0 cm−1. Spectra were collected in the range of 100–1,800 cm−1. In the pale yellowish shell material of females, the Raman-shift spectra only contained peaks around 701, 705 and 1,085 cm−1, which conform with aragonite (Hedegaard et al., 2006; Wehrmeister et al., 2010). However, in the reddish shell material derived from males, we detected strong additional peaks around 1140 and 1,520 cm−1. These wavenumbers are consistent with polyene pigments with 10 carbon–carbon double bonds (Fig. 2; Supplementary Material). Polyenes are defined as polyunsaturated carbohydrates possessing three or more alternating double and single carbon–carbon bonds (Basheer and Umesh, 2016). A well known class of polyenes are carotenoids, which possess four methyl groups attached to the polyenic chain (Karampelas et al., 2009). Polyenes have been detected before as shell pigments in several species of marine Caenogastropoda (Hedegaard et al., 2006; Shimizu et al., 2011; Williams et al., 2016; Williams, 2017), bivalves (Stemmer and Nehrke, 2014) and chitons (Peebles et al., 2017). Figure 2. View largeDownload slide Representative Raman spectra (corrected for background fluorescence) for top whorls of male (top) and female (bottom) Plectostoma concinnum. Figure 2. View largeDownload slide Representative Raman spectra (corrected for background fluorescence) for top whorls of male (top) and female (bottom) Plectostoma concinnum. As far as we know, this is the only reported case of discrete sexual shell colour dimorphism in land snails, although Reichenbach et al. (2012) reported that the last whorl of females is, on average, slightly less strongly pigmented in Cochlostoma septemspirale. We note that several other terrestrial Cyclophoroidea, for example the cyclophorid genus Chamalycaeus, as well as many other species of Plectostoma, similarly display a white/red polymorphism in protoconch coloration. To our knowledge, it has not yet been investigated whether this signifies sexual dimorphism as well. The evolution of sexual colour dimorphism, if it is adaptive, is most commonly driven by intraspecific sexual selection, which would imply that these snails have good vision, perhaps even colour vision—something that is considered rare or nonexistent in Gastropoda (Chase, 2001; Williams, 2017). If this should indeed prove to be the case, then these gonochoristic snails could conceivably join a larger group of animals in which polyenes, and particularly carotenoids, play a role in sexual honest signalling of genetic quality, given the immunomodulatory action of these and similar pigments (McGraw, 2005). Alternatively, the colour difference could be unrelated to sexual selection, but rather a byproduct of a sexually differentiated metabolic or catabolic process. SUPPLEMENTARY MATERIAL Supplementary material is available at Journal of Molluscan Studies online. ACKNOWLEDGEMENTS The Sabah Wildlife Department, the Sabah Forestry Department and the Village Heads of Sukau gave permission to conduct the fieldwork; the specimens were collected by A. van Til. We thank B. Páll-Gergely and A. Correoso for help in finding literature, and Associate Editor S.T. Williams and an anonymous reviewer for suggestions that improved the paper. REFERENCES Basheer, T. & Umesh, M. 2016. Polyketides. In: Secondary metabolites  ( P. Kathirvel, ed.), pp. 131– 144. Darshan Publishers, Tamil Nadu, India. Clements, R.G., Liew, T.S., Vermeulen, J.J. & Schilthuizen, M. 2008. Further twists in gastropod shell evolution. Biology Letters , 4: 179– 182. Google Scholar CrossRef Search ADS PubMed  Chase, R. 2001. Sensory organs and the nervous system. In: The biology of terrestrial molluscs  ( G.M. Barker, ed.), pp. 179– 211. CABI, Wallingford, UK. Google Scholar CrossRef Search ADS   Galindo Pérez, L.A. 2009. Estudio morfométrico del dimorfismo sexual de las conchas de especies de gastrópodos marinos comunes (Mollusca: Gastropoda) en Venezuela. MSc thesis, Universidad de Oriente. Gittenberger, E. 1995. On the one hand…. Nature , 373: 19. Google Scholar CrossRef Search ADS PubMed  Griffiths, R.J. 1961. Sexual dimorphism in Cypraeidae. Proceedings of the Malacological Society of London , 34: 203– 206. Hedegaard, C., Bardeau, J.F. & Chateigner, D. 2006. Molluscan shell pigments: an in situ resonance Raman study. Journal of Molluscan Studies , 72: 157– 162. Google Scholar CrossRef Search ADS   Karampelas, S., Fritsch, E., Rondeau, B., Andouche, A. & Métivier, B. 2009. Identification of the endangered pink-to-red Stylaster corals by Raman spectroscopy. Gems & Gemology , 45: 48– 52. Google Scholar CrossRef Search ADS   Lamy, E. 1937. Sur le dimorphisme sexuel des coquilles. Journal of Conchology , 81: 283– 301. Mcgraw, K.J. 2005. The antioxidant function of many animal pigments: are there consistent health benefits of sexually selected colourants? Animal Behaviour , 69: 757– 764. Google Scholar CrossRef Search ADS   Peebles, B.A., Gordon, K.C., Smith, A.M. & Smith, G.P.S. 2017. First record of carotenoid pigments and indications of unusual shell structure in chiton valves. Journal of Molluscan Studies . https://doi.org/10.1093/mollus/eyx033. Raven, J.G.M. 1990. A revision of Obscurella Clessin, 1889 (Gastropoda Prosobranchia: Cyclophoridae). Basteria , 54: 17– 62. Reichenbach, F., Baur, H. & Neubert, E. 2012. Sexual dimorphism in shells of Cochlostoma septemspirale (Caenogastropoda, Cyclophoroidea, Diplommatinidae, Cochlostomatinae). ZooKeys , 208: 1– 16. Google Scholar CrossRef Search ADS   Schilthuizen, M. 1994. Differentiation and hybridisation in a polytypic snail. PhD thesis, Leiden University. Schilthuizen, M. 2003. Sexual selection on land snail shell ornamentation: a hypothesis that may explain shell diversity. BMC Evolutionary Biology , 3: e1. Google Scholar CrossRef Search ADS   Schilthuizen, M., Rosli, R.B., Ali, A.M.B.M., Salverda, M., van Oosten, H., Bernard, H., Ancrenaz, M. & Lackman-Ancrenaz, I. 2003. The ecology and demography of Opisthostoma (Plectostoma) concinnum s. l. (Gastropoda: Diplommatinidae) on limestone outcrops along the Kinabatangan River. In: Kinabatangan Scientific expedition  ( M. Mohamed, B. Goossens, M. Ancrenaz & M. Andau, eds), pp. 55– 71. UMS, Kota Kinabalu, Malaysia. Schilthuizen, M., Van Til, A., Salverda, M., Liew, T.-S., James, S.S., Elahan, B. & Vermeulen, J.J. 2006. Microgeographic evolution of snail shell shape and predator behavior. Evolution , 60: 1851– 1858. Google Scholar CrossRef Search ADS PubMed  Shimizu, K., Sarashina, I., Kagi, H. & Endo, K. 2011. Possible functions of Dpp in gastropod shell formation and shell coiling. Development, Genes and Evolution , 221: 59– 68. Google Scholar CrossRef Search ADS   Stemmer, K. & Nehrke, G. 2014. The distribution of polyenes in the shell of Arctica Islandica from North Atlantic localities: a confocal Raman microscopy study. Journal of Molluscan Studies , 80: 365– 370. Google Scholar CrossRef Search ADS   Vermeulen, J.J. 1994. Notes on the non-marine molluscs of the island of Borneo. 6. The genus Opisthostoma (Gastropoda Prosobranchia: Diplommatinidae). Basteria , 58: 75– 191. Wehrmeister, U., Soldati, A.L., Jacob, D.E., Häger, T. & Hofmeister, W. 2010. Raman spectroscopy of synthetic, geological and biological vaterite: a Raman spectroscopic study. Journal of Raman Spectroscopy , 41: 193– 201. Williams, S.T. 2017. Molluscan shell colour. Biological Reviews , 92: 1039– 1058. Google Scholar CrossRef Search ADS PubMed  Williams, S.T., Ito, S., Wakamatsu, K., Goral, T., Edwards, N.P., Wogelius, R.A., Henkel, T., de Oliveira, L.F.C., Maia, L.F., Strekopytov, S., Jeffries, T., Speiser, D.I. & Marsden, J.T. 2016. Identification of shell colour pigments in marine snails Clanculus pharaonius and C. margaritarius (Trochoidea; Gastropoda). PLoS One , 11: e0156664. Google Scholar CrossRef Search ADS PubMed  © The Author 2017. Published by Oxford University Press on behalf of The Malacological Society of London, all rights reserved. For Permissions, please email: journals.permissions@oup.com

Journal

Journal of Molluscan StudiesOxford University Press

Published: Feb 1, 2018

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