Ronald Chase
Professor Emeritus
A.B. Stanford University
Ph.D. Massachusetts Institute of Technology
The Biology of Gastropod Molluscs: Nervous System, Behaviour, Reproduction

e-mail: ronald.chase {at} mcgill.ca

To learn more about snails, slugs and sex, visit my article in Scholarpedia.
http://www.scholarpedia.org/article/Gastropod_Reproductive_Behavior




Some people are surprised to learn that snails have brains, let alone that they have the world’s largest neurons. Others are intrigued by the fact that snails shoot each other with sharp ‘love’ darts before mating, or that they are hermaphrodites. All of these features make snails attractive to me. I like to do science at the intersection of neurobiology, behaviour and evolution.

Although I began my career working with mammals, I have used molluscan models for many years. Today, my experimental animal is the brown garden snail Cornu aspersum (formerly known as Helix aspersa). My research concerns the complicated sex life of this animal. Students working in my laboratory pursue either behavioural projects or neurobiological projects, or sometimes a combination of the two.

Photo (left): The land snail Cornu aspersum is a common inhabitant of gardens in Europe, California and South America. © C. Levesque


Studies of Dart Shooting

After discovering, years ago, a part of the snail’s brain that controls the shooting of the dart, I found myself obsessed with the question of why they even bother to shoot it. Eventually, we established that the dart functions after copulation to increase the reproductive fitness of the shooter. Snails are promiscuous, and they can store sperm from multiple donors for several years before they use it to fertilize eggs. Thus, sperm donors (‘males’) must compete to fertilize eggs. Dart receipt promotes the safe storage of the shooter's sperm, so there will be more sperm from successful shooters available for fertilization than from unsuccessful shooters. Since the female function chooses the sperm by a lottery-like mechanism, successful dart shooters sire more babies than unsuccessful dart shooters.

We recently tested whether the dart works by simply rupturing the skin or by injecting a bioactive agent (Chase and Blanchard, 2006). Just before the dart is ‘shot’, it is covered with mucus from a special gland located near the dart's launching site. We hypothesized that the dart works by injecting this mucus. Our test involved a competitive mating experiment, in which needle stabbings substituted for dart shooting. In one mating, saline was injected through the needle, in the other mating mucus was injected. We found that the matings that were associated with mucus injections were responsible for more than twice the number of offspring as were the matings associated with saline injections. Thus, mucus is the agent of the dart’s effect on reproduction.

Photo (right): Two snails in copula. During their courtship, the snail at the top shot a dart into the snail at the bottom. Can you see the dart? (Click on photo for enlarged version)

Photographs of the snail's dart, which is made of pure calcium carbonate. When ejected, it is covered with mucus from a special gland.


Neurobiological Studies of Sexual Behaviour

Because they are hermaphrodites, there is a lot of sex and reproduction going on in each snail. I am interested in how the key motor events are controlled by the nervous system. We think that the brain’s mesocerebral lobe plays an executive role in controlling male mating behaviours, including dart shooting. This part of the CNS is easy to work with because it contains many large neurons. The axons of mesocerebral neurons project to either the dart sac or the penis, or both.

Many types of stereotyped behaviours are controlled by neural circuits known as central pattern generators (CPGs). Some evidence points to the right mesocerebral lobe of the snail’s brain as a CPG for dart shooting. Electrophysiological records obtained from this region using a chronically implanted electrode demonstrated that neurons become active during courtship and dart shooting (Koene et al., 2000). Also, in vitro, direct electrical stimulation of either the entire lobe or, in some cases, individual neurons, causes contractions of the dart sac (Chase, 1986).

Photo (right): Immunohistochemical staining in the mesocerebrum. Green signifies the peptide FMRFamide; red signifies backfilling from the nerve that innervates the dart sac; yellow means the cell contains FMRFamide and it sends an axon to the dart sac.

 


The reciprocal nature of mating is evident when a copulating pair is gently pulled apart, as shown here in this hand-coloured drawing by Férussac, 1820.
Hermaphroditic Reciprocity

Whereas most hermaphroditic animals mate as one sex or the other on each occasion, in the case of our snail species, both members of a mating pair act simultaneously as male and female. Thus, sperm is nearly always transferred reciprocally between the two partners (136 of 138 matings). Related to this, is the remarkable fact that a pair is able to achieve nearly simultaneous intromissions despite having neither vision nor hearing. We have measured the mean interval between the first snail inserting its penis and the second animal inserting its penis at < 2 seconds. We are investigating the sensory mechanisms that are responsible for coordinating the copulatory acts.

The reliability of simultaneous, reciprocal mating raises the question of why there is no cheating. Because pulmonate snails have high resource investments in male reproduction, a snail might benefit by receiving sperm but not delivering sperm. However, if cheating were to become common, the system of reciprocal mating would break down and disappear. We are testing the hypothesis that sensory-motor mechanisms prevent a snail from receiving sperm unless it simultaneously delivers sperm.

 

Garden snails lay clutches of about 100 eggs. They first excavate a nest in moist soil, then deposit the eggs. The mother snail must mobilize large amounts of calcium to endow each egg with a calcified shell, which the newly hatched snail then uses to produce its own shell. Time is indicated here as hours:minutes.




Dr. Ron Chase in his lab with students


SELECTED PUBLICATIONS

Chase, R., Darbyson, E., Horn, K.E. and Samarova, E. (2010). A mechanism aiding simultaneously reciprocal mating in snails. Canadian Journal of Zoology 88, 99-107. (Supplementary data)

Chase, R. (2007) Gastropod Reproductive Behavior. Scholarpedia 2(9): 4125.

Chase, R. and Blanchard, K.C. (2006) The snail's love-dart delivers mucus to increase paternity. Proceedings of the Royal Society B 273, 1471-1475.

Geoffroy, E., Hutcheson, R. and Chase, R. (2005) Nervous control of ovulation and ejaculation in Helix aspersa. Journal of Molluscan Studies 71, 393-399.

Antkowiak, T. and Chase, R. (2003) Sensory innervation of the ovotestis in the snail Helix aspersa. Journal of Experimental Biology 206, 3913-3921.

Chase, R. (2002) Behavior and its Neural Control in Gastropod Molluscs. Oxford University Press , New York, 336 pp. [Click here for excerpts from published reviews]

Rogers, D.W. and Chase, R. (2002). Determinants of paternity in the garden snail Helix aspersa. Behavioral Ecology and Sociobiology 52, 289-295.

Rogers, D.W. and Chase, R. (2001). Dart receipt promotes sperm storage in the garden snail Helix aspersa. Behavioral Ecology and Sociobiology 50, 122-127.

Prescott, S. A. and Chase, R. (1999).  Sites of plasticity in the neural circuit mediating tentacle withdrawal in the snail Helix aspersa: implications for behavioral change and learning kinetics. Learning and Memory 6, 363-380.

Koene, J.M. and Chase, R. (1998). Changes in the reproductive system of the snail Helix aspersa caused by mucus from the love dart.  Journal of Experimental Biology 201, 2313-2319.

Li, G. and Chase, R. (1995). Correlation of axon projections and peptide immunoreactivity in mesocerebral neurons of the snail Helix aspersa. Journal of Comparative Neurology 353, 9-17.
COMPREHENSIVE LIST OF PUBLICATIONS

Chase, R., Darbyson, E., Horn, K.E. and Samarova, E. (2010). A mechanism aiding simultaneously reciprocal mating in snails. Canadian Journal of Zoology 88, 99-107. (Supplementary data)

Chase, R. and Darbyson, E. (2008). Differential survival of allosperm by location within the female storage organ of the snail Cornu aspersum (Müller, 1774). Canadian Journal of Zoology 86, 1244-1251.

Chase, R. (2008). Schizophrenia is a disease, so electrons aren’t at risk (Correspondence). Nature 451,127.
 
Chase, R. (2007). The function of dart shooting in helicid snails. American Malacological Bulletin 23, 183-189.

Chase, R. (2007) Gastropod Reproductive Behavior. Scholarpedia 2(9): 4125.

Chase, R. and Blanchard, K.C. (2006) The snail's love-dart delivers mucus to increase paternity. Proceedings of the Royal Society B 273, 1471-1475.
 
Chase, R. and Vaga, K. (2006) Independence, not conflict, characterizes dart-shooting and sperm exchange in a hermaphroditic snail. Behavioral Ecology and Sociobiology 59, 732-739.

Geoffroy, E., Hutcheson, R. and Chase, R. (2005) Nervous control of ovulation and ejaculation in Helix aspersa. Journal of Molluscan Studies 71, 393-399.

Weatherill, D. and Chase, R. (2005) Modulation of heart activity during withdrawal reflexes in the snail Helix aspersa. Journal of Comparative Physiology A 191, 355-362.

Chase, R., Antkowiak, T., Geoffroy, E. and Weatherill, D. (2004) Why the ovotestis of Helix aspersa is innervated. Acta Biologica Hungarica 55, 239-249.

Antkowiak, T. and Chase, R. (2003) Sensory innervation of the ovotestis in the snail Helix aspersa. Journal of Experimental Biology 206, 3913-3921.

Rogers, D.W. and Chase, R. (2002). Determinants of paternity in the garden snail Helix aspersa. Behavioral Ecology and Sociobiology 52, 289-295.

Chase, R. (2002) Behavior and its Neural Control in Gastropod Molluscs. Oxford University Press, New York, 336 pp.

Landolfa, M.A., Green, D.M. and Chase, R. (2001). Dart shooting influences paternal reproductive success in the snail Helix aspersa (Pulmonata, Stylommatophora). Behavioral Ecology 12, 773-777.

Chase, R. (2001). Sense organs and the nervous system. In The Biology of Terrestrial Molluscs, ed. G. M. Barker, CAB International, U.K., pp 179-211.

Chase, R. and Robinson, D. (2001). The uncertain history of land snails on Barbados: Implications for conservation.  Malacologia 43, 33-57.

Rogers, D.W. and Chase, R. (2001). Dart receipt promotes sperm storage in the garden snail Helix aspersa. Behavioral Ecology and Sociobiology 50, 122-127.

Ratté, S. and Chase, R. (2000). Synapse distribution of olfactory interneurons in the procerebrum of the snail Helix aspersa.  Journal of Comparative Neurology 417, 366-384.

Koene, J.M., Jansen, R.F., ter Maat, A. and Chase, R. (2000). A conserved location for the CNS control of mating behaviour in gastropod molluscs: Evidence from a terrestrial snail.  Journal of Experimental Biology 203,1071-1080.

Chase, R. (2000). Structure and function in the cerebral ganglion. (Invited paper for special issue).  Microscopy Research and Technique 49, 511-520.

Prescott, S. A. and Chase, R. (1999).  Sites of plasticity in the neural circuit mediating tentacle withdrawal in the snail Helix aspersa: implications for behavioral change and learning kinetics. Learning and Memory 6, 363-380.

Koene, J.M., Jansen, R.F., ter Maat, A. and Chase, R. (1999). An in vivo electro-physiological study of mating behaviour in the snail Helix aspersa.  Invertebrate Reproduction and Development 36, 123-127.

Lemaire, M. and Chase, R. (1998). Twitching and quivering of the tentacles during snail olfactory orientation.  Journal of Comparative Physiology 182, 81-87.

Koene, J.M. and Chase, R. (1998). The love dart of Helix aspersa is not a gift of calcium.  Journal of Molluscan Studies 64, 75-80.

Koene, J.M. and Chase, R. (1998). Changes in the reproductive system of the snail Helix aspersa caused by mucus from the love dart.  Journal of Experimental Biology 201, 2313-2319.

Ratté, S. and Chase, R. (1997).  Morphology of interneurons in the procerebrum of the snail Helix aspersa.  Journal of Comparative Neurology 384, 359-372.

Prescott, S., Gill, N. and Chase, R. (1997).  The neural circuit mediating tentacle withdrawal in Helix aspersa, with specific reference to the motoneuron C3.  Journal of Neurophysiology 78, 2951-2965.

Adamo, S. and Chase, R. (1996). Dart shooting in helicid snails: an ‘honest’ signal or an instrument of manipulation?  Journal of Theoretical Biology 180, 77-80.

Matsubara, J.A., Chase, R., and Thejomayen, M. (1996). Comparative morphology of three types of projection-identified pyramidal neurons in the superficial layers of cat visual cortex.  Journal of Comparative Neurology 366, 93-108.

Prescott, S. and Chase, R. (1996). Two types of plasticity in the tentacle withdrawal reflex of Helix aspersa are dissociated by tissue location and response measure.  Journal of Comparative Physiology 179, 407-414.

Chase, R. and Hall, B. (1996).  Nociceptive inputs to C3, a motoneuron of the tentacle withdrawal reflex in Helix aspersa. Journal of Comparative Physiology   179, 809-818.

Chase, R. (1996). Protrusible eyes; retractable noses (Scientific Correspondence).  Nature 383, 29-30.

Li, G. and Chase, R. (1995).  Correlation of axon projections and peptide immunoreactivity in mesocerebral neurons of the snail Helix aspersa.  Journal of Comparative Neurology 353, 9-17. (Cover illustration)

Chase, R. and Li, G. (1994).  Mesocerebral neurons and their role in the control of mating behaviour.  Netherlands Journal of Zoology 44, 212-222.

Chase, R. and Tolloczko, B. (1993). Tracing neural pathways in snail olfaction:  From the tip of the tentacle to the brain and beyond. Microscopy Research and Technique, 24, 214-230.

Chase, R. and Tolloczko, B. (1992).  Synaptic innervation of the giant cerebral neuron in sated and hungry snails. Journal of Comparative Neurology 318, 93-102.

LaBerge, S. and Chase, R. (1992).  The development of mesocerebral neurons in the snail Helix aspersa maxima.  Canadian Journal of Zoology 70, 2034-2041.

Chase, R., Adamo, S., and Li, G. (1992)  Eros in mollusca: the love dart of Helix aspersa.  Third International Congress of Neuroethology, Montreal. (2 pp.)

Adamo, S. and Chase, R. (1991).  The interactions of courtship, feeding and locomotion in the behavioural hierarchy of the snail Helix aspersa.  Behavioral and Neural Biology, 55, 1-18.

Adamo, S. and Chase, R. (1991).  ‘Central arousal’ and sexual responsiveness in the snail, Helix aspersa.  Behavioral and Neural Biology 55, 194-213.

Chase, R. and Tidd, C. (1991).  Stability of dendritic mass during aestivation.  Journal of Comparative Neurology 303, 150-158.

Chase, R., Tolloczko, B. and Tidd, C. (1991).  The dendritic structure of the giant cerebral neuron in sated and hungry snails.  In:  Molluscan Neurobiology, North-Holland, Amsterdam, eds. K.S. Kits, H.H. Boer and J. Joosse, pp. 43-48.

Balaban, P.M. and Chase, R. (1990).  Stimulation of mesocerebrum in Helix aspersa inhibits the neural network underlying avoidance behavior.  Journal of Comparative Physiology 166, 421-427.

Balaban, P.M. and Chase, R. (1990).  Relations of emotionally positive and negative brain areas in the snail Helix aspersa.  Journal of Higher Nervous Activity 40, 125-134 (in Russian).  Translation published in Neuroscience and Behavioral Physiology 21, 172-180.

Adamo, S. and Chase, R. (1990).  The ‘love dart’ of the snail, Helix aspersa , injects a pheromone that decreases courtship duration.  Journal of Experimental Zoology 255, 80-87.

Adamo, S. and Chase, R. (1990).  Dissociation of sexual arousal and sexual proclivity in the garden snail, Helix aspersa.  Behavioral and Neural Biology 54, 115-130.

Chase, R. and Tolloczko, B. (1989).  Interganglionic dendrites constitute an output pathway from the procerebrum of the snail.  Journal of Comparative Neurology 283, 143-152.

Balaban, P.M. and Chase, R. (1989).  Self-stimulation in snails. Neuroscience Research Communications 4, 139-147.

Chase, R. (1988).  A mutant strain of terrestrial snails, Achatina fulica, exhibiting a supernumerary penis.  Canadian Journal of Zoology 66, 1491-1493.

Adamo, S. and Chase, R. (1988).  Courtship and copulation in the terrestrial snail, Helix aspersa .  Canadian Journal of Zoology 66, 1446-1453.

Pawson, P. and Chase, R. (1988).  The development of transmission at an identified molluscan synapse.  II.  A quantal analysis of transmission.  Journal of Neurophysiology 60, 2211-2222.

Pawson, P. and Chase, R. (1988).  The development of transmission at an identified molluscan synapse.  I.  The emergence of synaptic plasticities.  Journal of Neurophysiology 60, 2196-2210.

Chase, R. and Tolloczko, B. (1987).  Evidence for differential DNA endoreplication during the development of a molluscan brain. Journal of Neurobiology 18, 395-406.

Chase, R. (1986). Brain cells that command sexual behavior in the snail Helix aspersa . Journal of Neurobiology 17, 669-679.

Chase, R. and Rieling, J. (1986).  Autoradiographic evidence for receptor cell renewal in the olfactory epithelium of a snail. Brain Research 384, 232-239.

Chase, R. and Tolloczko, B. (1986).  Synaptic glomeruli in the olfactory system of a snail. Cell and Tissue Research 246, 567-573.

Chase, R. (1986).  Lessons from snail tentacles.  Chemical Senses 11, 411-426.

Chase, R. and Wells, M.J. (1986).  Chemotaxic behaviour in Octopus. Journal of Comparative Physiology 158, 375-381.

McCarragher, G. and Chase, R. (1985).  Quantification of ultrastructural symmetry at molluscan chemical synapses. Journal of Neurobiology 16, 69-74.

Chase, R. and Tolloczko, B. (1985).  Secretory glands of the snail tentacle and their relation to the olfactory organ.  Zoomorphology 105, 60-67.

Chase, R. (1985).  Responses to odors mapped in snail tentacle and brain by 14C-2-deoxyglucose autoradiography.  Journal of Neuroscience 5, 2930-2939.

Pawson, P.A. and Chase, R. (1985).  Developmental changes in the passive membrane properties of an identified molluscan neuron. Developmental Brain Research 17,296-300.

Pawson, P.A. and Chase, R. (1984). The life-cycle and reproductive activity of Achatina fulica (Bowdich) in laboratory culture. Journal of Molluscan Studies, 50, 85-91.

Chase, R. and Kamil, R. (1983b).  Morphology and odor sensitivity of regenerated snail tentacles.  Journal of Neurobiology 14, 43-50.

Chase, R. and Kamil, R. (1983a).  Neuronal elements in snail tentacles as revealed by HRP backfilling.  Journal of Neurobiology l4, 29-42.

Munoz, D.P., Pawson, P.A. and Chase, R. (1983).  Symmetrical giant neurons in asymmetrical ganglia: Implications for evolution of the nervous system in pulmonate molluscs.  Journal of Experimental Biology 107, 147-161.

Chase, R. (1982).  The olfactory sensitivity of snails, Achatina fulica. Journal of Comparative Physiology 148, 225-235.

Chase, R. and Piotte, M. (1981).  A cephalic dimple in the terrestrial snail Achatina achatina.  Veliger 23, 241-244.

Chase, R. and Croll, R.  (1981).  Tentacular function in snail olfactory orientation.  Journal of Comparative Physiology  143, 357-362.

Chase, R. (1981).  Electrical responses of snail tentacle ganglion to stimulation of the epithelium with wind and odors.  Comp. Biochem. Physiol. 70A, 149-155.

Croll, R. and Chase, R. (1980).  Plasticity of olfactory orientation to foods in the snail Achatina fulica.  Journal of Comparative Physiology 136, 267-277.

Chase, R, Croll, R. and Zeichner, L. (1980).  Aggregation in snails, Achatina fulica.  Behavioral and Neural Biology 30, 218-230.

Chase, R. (1979).  Photic sensitivity of the rhinophore in Aplysia.  Canadian Journal of Zoology 57, 698-701.

Chase, R. (1979).  An electrophysiological search for pheromones of Aplysia californica.  Canadian Journal of Zoology 57, 781-784.

Chase, R. (1979).  The mentalist hypothesis and invertebrate neurobiology.  Perspectives in Biology and Medicine 23, 103-117.

Chase, R., Pryer, K., Baker, R. and Madison, D. (1978).  Responses to conspecific chemical stimuli in the terrestrial snail Achatina fulica.  Behavioral Biology 22, 302-315.

Chase, R. and Boulanger, C. (1978).  Attraction of the snail Achatina fulica to extracts of conspecific pedal glands.  Behavioral Biology 23, 107-112.

Chase, R. and Goodman, H. (1977).  Homologous neurosecretory cell groups in the land snail Achatina fulica and the sea slug Aplysia californica.  Cell and Tissue Research 176,109-120.

Croll, R. and Chase, R. (1977).  A long-term memory for food odors in the land snail Achatina fulica.  Behavioral Biology 19, 261-268.

Acosta-Urquidi, J. and Chase, R. (1975).  The effects of delta-9-tetrahydrocannabinol on action potentials in the mollusc, Aplysia. Canadian Journal of Physiology and Pharmacology 53, 793-798.

Chase, R. (1975).  The suppression of excitatory synaptic responses by ethyl alcohol in the nudibranch mollusc, Tritonia diomedia.  Comparative Biochemistry and Physiology 50C, 37-40.

Chase, R. (1975).  The electrophysiology of transduction, retinal interaction and axonal conduction in invertebrate photoreceptors. Comparative Biochemistry and Physiology 52A, 571-576.

Chase, R. (1974).  The electrophysiology of photoreceptors in the nudibranch mollusc, Tritonia diomedia.  Journal of Experimental Biology 60, 707-719.

Chase, R. (1974).  The initiation and conduction of action potentials in the optic nerve of Tritonia.  Journal of Experimental Biology 60, 721-734.

Chase, R. and Kalil, R.E. (1972).  Suppression of visual evoked responses to flashes and pattern shifts during voluntary saccades.  Vision Research 12, 215-220.

Fernald, R.D. and Chase, R. (1971).  An improved method for plotting retinal landmarks and focusing the eyes.  Vision Research 11, 95-96.

Kalil, R.E. and Chase, R. (1970).  Corticofugal influence on activity of lateral geniculate neurons in the cat.  Journal of Neurophysiology 33, 459-474. (Authors contributed equally.)

Chorover, S.L. and Chase, R. (1968).  Persistence of visual pattern discrimination in binocularly-occluded albino rats. Journal of Comparative and Physiological Psychology 68, 238-245.
(Last update: Feb. 5, 2010)
 
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