Understanding colour and chemical diversity in marine molluscs

A project undertaken at the School of Biological Sciences, The University of Queensland, and supervised by Karen Cheney

Summary

Animals frequently use dazzling colour patterns to find food, attract mates and avoid predation. Aposematic signals are used to warn predators that a species contains chemical or other defence mechanisms. Nudibranchs (marine shell-less molluscs) store secondary metabolites from dietary sources for their own chemical defences, and also exhibit a variety of colour patterns, ranging from those that are highly camouflaged against their background to those that display highly conspicuous colour patterns. Using a multidisciplinary approach, we aim to investigate the evolution of visual signals in this intriguing model system by evaluating the conspicousness of colour patterns, identify and determine the relative strength of chemical compounds used to deter predators in a range of nudibranch species.

Background

Theoretical and experimental models predict that warning signals in animals evolve from defended inconspicuous (cryptic) species that mutate to produce conspicuous morphs  (Leimar et al., 1986). Secondary defences deter predators during an attack, and once a predator has associated bright colouration with unprofitability of prey, they avoid similarly-coloured prey in future encounters. However, in evolutionary terms, it is unclear whether visual signals in aposematic species are ‘quantitatively honest’, in the sense that conspicuousness correlates positively with levels of toxicity and thus conveys reliable information. Or whether signals reach a threshold over which predators avoid all signals, irrespective of how conspicuous a signal is (Speed et al., 2010).

One intriguing, understudied model system to study how aposematic signals have evolved are nudibranchs, which appear strikingly exposed to predation, yet they are avoided by most predators. The majority of nudibranchs have evolved to sequester secondary metabolites from dietary sources, or produce chemicals de novo, which they then use as chemical deterrents. Many nudibranchs also use cryptic color patterns or camouflage to blend into their surroundings, opting to avoid detection altogether rather than promote predator recognition (Marin et al., 1997; Cheney et al., 2014). This variation in predator avoidance strategies makes nudibranchs an ideal model system to test theories about the evolution of visual signaling and chemical defences.

However, we know little about the identity and relative strength of chemical defenses in most nudibranch species. Indeed, the identity and level of chemical defense is known for less than <1% of all mollusc species even though marine molluscs, are an important source of diverse natural products, and investigations into their biological and chemical properties have lead to the discovery of many biologically potent chemicals with FDA approval due to their analgesic, anti-inflammatory, antiviral and anticancer activity (Gerwick and Moore, 2012). Indeed, the antitumour depsipeptide Kahalalide F was also isolated from the opisthobranch mollusc Elysia rufescens, which is used by both the mollusc and its dietary alga Bryopsis spp. (the true source of Kahalalide F) as a chemical defense from predation. Kahalalide F is currently in clinical trials for the treatment of advanced cancerous tumors, including those related to melanoma (Salazar et al 2013).

Aims

Using our combined expertise in marine and visual ecology (Karen Cheney), natural product chemistry (Prof. Mary Garson), and animal vision and signlling (Prof. Justin Marshall) we aim to:

  1. conduct a systematic chemical survey of secondary metabolites from 40-50 nudibranch species;
  2. examine the relative strength of these chemical defences to potential predators by conducting unpalatability and toxicity assays with shrimp and fish;
  3. test key evolutionary hypotheses on the relationship between the conspicuousness of visual signals (i.e. how bright and colourful the signal is) and level of chemical defences; and
  4. highlight the significance of this intriguing, emerging model system to the fields of evolution, ecology and sensory neurobiology.
References

Cheney, K.L., Cortesi, F., How, M.J., Wilson, N.G., Blomberg, S.P., Winters, A.E., et al. 2014. Conspicuous visual signals do not coevolve with increased body size in marine sea slugs. J. Evol. Biol. 27 (4): 676-687.

Cortesi, F. & Cheney, K.L. 2010. Conspicuousness is correlated with toxicity in marine opisthobranchs. J. Evol. Biol. 23: 1509-1518.

Gerwick WH, Moore BS, 2012. Lessons from the past and charting the future of marine natural products drug discovery and chemical biology. Chem. Biol. 19:85-98. doi: 10.1016/J.Chembiol.2011.12.014.

Leimar, O., Enquist, M. & Sillentullberg, B. 1986. Evolutionary stability of aposematic coloration and prey unprofitability - a theoretical-analysis. Am. Nat. 128: 469-490.

Marin, A., Belluga, M.D.L., Scognamiglio, G. & Cimino, G. 1997. Morphological and chemical camouflage of the Mediterranean nudibranch Discodoris indecora on the sponges Ircinia variabilis and Ircinia fasciculata. J. Mollus. Stud. 63: 431-439.

Marshall, N. J. and Cheney, K. L. (2013). Vision and body colouration in marine invertebrates. In: The New Visual Neurosciences, Eds - Werner, J. and Chalupa, L., MIT Press (pp. 1165-1178).

Mudianta, I. W., Challinor, V. L., Winters, A. E., Cheney, K. L., De Voss, J. J., Garson, M. J. 2013. Synthesis and determination of absolute configuration of (–)-(5R,6Z)-dendrolasin-5-acetate from the nudibranch Hypselodoris jacksoni. Beilstein Journal of Organic Chemistry 9 (1): 2925-2933.

Salazar R, et al. 2013. Phase I study of weekly kahalalide F as prolonged infusion in patients with advanced solid tumors. Cancer Chemo. Pharm. 72 (1): 75-83

Speed, M.P., Ruxton, G.D., Blount, J.D. & Stephens, P.A. 2010. Diversification of honest signals in a predator-prey system. Ecol. Lett. 13: 744-753.

Figure 1. Conspicuous colour patterns exhibited by nudibranch molluscs: Chromodoris kuiteri (top left); Phyllidia picta (top right); Mexichromis festiva (bottom left); Goniobranchus splendida (bottom right) (Photos Karen Cheney/Anne Winters)

Figure 2. Secondary metabolites from nudibranchs that provide chemical defense from predators (Mary Garson, unpublished data).

Figure 3. Glossodoris atromarginata searching for dietary sponges in the field (Photo by Karen Cheney)

Figure 4. Ceratsoma amoenum display yellow spots and bright purple gills to warn predators of their toxic defences (Photo by Karen Cheney)