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Joris M. Koene

Dr. J. (Joris) M. Koene, Research associate - Endless forms


Email: joris.koene@vu.nl
Phone: +31 (0)20 59 87 095
Room number: not applicable

See also www.joriskoene.com

(within the Department of Ecological Science of VU University Amsterdam)


2002-present - Lecturer & PI - VU University, Amsterdam (NL)

2000-2002- Post-doc - Westfälische Wilhelms-Universität, Münster (DE)

1995-2000 - PhD - McGill University, Montreal (CA)

1990-1995 - MSc + Bsc - Vrije Universiteit, Amsterdam (NL)


Research interest

Sex and conflict in simultaneous hermaphrodites

In animal species that mate promiscuously, store sperm and fertilise internally, the sperm from two or more donors usually compete for access to eggs. Such sperm competition often leads to sexual conflict, because traits that are advantageous to the sperm donor can be harmful to the recipient. There are many studies investigating how an individual can manipulate its mating partner to its own benefit, but most of these are restricted to species with separate sexes.

One famous example from hermaphroditic animals is the bizarre act of dart shooting in land snails. In many species, a so-called "love dart" is forcefully stabbed through the skin of the mating partner. In Cornu aspersum (previously Helix aspersa) this results in the injection of an allohormone that increases sperm storage and paternity, probably via a decrease in sperm digestion. This project aims at investigating the darts shape, function and use within as well as between species of different families of land snails. Within species nothing is currently known about, for example, the diversity in dart shapes between individuals from different populations. Between species there is a large diversity in dart shapes and numbers and on top of that these darts are stabbed in very different ways. In addition, in none of these species has it been established whether the dart has a similar effect on the recipient as the demonstrated effect in C. aspersum. All this information about darts and dart shooting within and between species is essential for a full understanding of the evolution of this odd reproductive act.

Cross-sections of love darts from different species of land snails. Source: BioMed Central, Koene & Schulenburg 2005, BMC Evol. Biol. 5:25


allohormone, love dart, sexual selection, sexual conflict, sperm competition, reproduction, hermaphrodite, seminal fluid

Current research topics

Research projects and internships are available. See www.joriskoene.com for details (click "research")

Prospective PhDs and post-docs can contact me directly via e-mail (joris.koene@vu.nl).






MSc internships are available, see http://www.joriskoene.com.

BSc internships are available, see http://www.joriskoene.com)

Available student projects


Nakadera, Y., Swart, E.M., Maas, J.P.A., Montagne-Wajer, K. Ter Maat, A. & Koene, J.M. Effects of age, size and mating history on sex role decision of a simultaneous hermaphrodite. Behavioral Ecology, in press.

Zimmer, E.I., Ducrot, V., Jager, T., Koene, J.M., Lagadic, L. & Kooijman S.A.L.M. 2014. Metabolic acceleration in the pond snail Lymnaea stagnalis? Journal of Sea Research, in press.
(preprint PDF, 616Kb)

Lewis, S.M., Vahed, K., Koene, J.M., Engqvist, L., Bussiere, L.F., Perry, J.C., Gwynne, D. & Lehmann, G.U.C. 2014. Emerging issues in the evolution of animal nuptial gifts. Biology Letters 10: 20140336.
(PDF, 208Kb)

Nakadera, Y., Swart, E.M., Hoffer, J.N.A., Den Boon, O., Ellers, J. & Koene, J.M. 2014.
Receipt of seminal fluid proteins causes reduction of male investment in a simultaneous hermaphrodite. Current Biology 24: 1-4
(PDF, 221Kb)
(Supporting information Supplemental information 1, PDF, 147Kb)

Zizzari, Z.V., Smolders, I. & Koene, J.M. 2014. Alternative delivery of male accessory gland products. Frontiers in Zoology 11: 32
(PDF, 378Kb)

Kimura, K., Chiba, S. & Koene, J. M. 2014. Common effect of the mucus transferred during mating in two dart-shooting snail species from different families. Journal of Experimental Biology 217: 1150-1153
(PDF, 1.3Mb)

Van Iersel, S., Swart, E.M., Nakadera, Y., Van Straalen, N.M. & Koene, J.M. 2014.
Effect of male accessory gland products on egg laying in gastropod molluscs. Journal of Visualized Experiments 88: e51698
(Video link: http://www.jove.com/video/51698)
(PDF, 167Kb)
(Supplement: PDF, 57Kb)

Nakadera, Y., Blom, C. & Koene, J.M. 2014. Duration of sperm storage in the simultaneous hermaphrodite Lymnaea stagnalis. Journal of Molluscan Studies 80: 1-7
(PDF, 335Kb)

Koene, J.M., Liew, T.-S., Montagne-Wajer, K. & Schilthuizen, M. 2013. A syringe-like love dart injects male accessory gland products in a tropical hermaphrodite. PLoS ONE 8: e69968
(PDF, 400Kb)

Nakadera, Y. & Koene, J.M. 2013.
Reproductive strategies in hermaphroditic gastropods: conceptual and empirical approaches. Canadian Journal of Zoology 91: 367–381
(PDF, 365Kb)

Liu, T., Koene, J.M., Dong, X. & Fu, R. 2013. Sensitivity of isolated eggs of pond snails: a new method for toxicity assays and risk assessment Environmental Monitoring and Assessment 185: 4183–4190
(PDF, 170Kb)

Koene, J.M. 2012. Editorial: Zoology is dead, long live zoology! Animal Biology 62: 379–380
(PDF, 112Kb)

Koene, J.M. & Cosijn, J. 2012. Twisted sex in a hermaphrodite: Mirror-image mating behaviour is not learned. Journal of Molluscan Studies 78: 308-311
(PDF, 180Kb)

Hoffer, J.N.A., Schwegler, D., Ellers, J. & Koene, J.M. 2012. Mating rate influences female reproductive investment in a simultaneous hermaphrodite, Lymnaea stagnalis. Animal Behaviour 84: 523-529
(PDF, 501Kb)

Ter Maat, A, Pieneman, A.W. & Koene, J.M. 2012. The effect of light on induced egg laying in the simultaneous hermaphrodite Lymnaea stagnalis. Journal of Molluscan Studies 78: 262-267
(PDF, 195Kb)

Koene, J.M. 2012. Sexual conflict in nonhuman animals. In: The Oxford Handbook of Sexual Conflict in Humans (eds. A.T. Goetz & T. Schackelford), pp. 15-30, Oxford University Press
Please contact me if you want a reprint: joris.koene-at-vu.nl
See book content at OUP

Escobar, J.S., Auld, J.R., Correa, A.C., Alonso, J.M., Bony, Y.K., Coutellec, M.-A., Koene, J.M., Pointier, J.-P., Jarne, P. & David, P. 2011. Patterns of mating-system evolution in hermaphroditic animals: Correlations among selfing rate, inbreeding depression and the timing of reproduction. Evolution 65: 1233-1253
(PDF, 353Kb)
(Supporting information Supplementary Table 1, DOC, 35Kb)

Hoffer, J.N.A., Ellers, J. & Koene, J.M. 2010. Costs of receipt and donation of ejaculates in a simultaneous hermaphrodite. BMC Evolutionary Biology 10: 393
(PDF, 350Kb)

Koene, J.M. 2010. Neuro-endocrine control of reproduction in hermaphroditic freshwater snails: mechanisms and evolution. Frontiers in Behavioral Neuroscience 4: 167
(PDF, 2.6Mb)
See complete special issue on Neuroethology

Anthes, N., David, P., Auld, J.R., Hoffer, J.N.A., Jarne, P., Koene, J.M., Kokko, H., Lorenzi, M.C., Pélissié, B., Sprenger, D., Staikou, A., Schärer, L. 2010. Bateman gradients in hermaphrodites: An extended approach to quantify sexual selection. American Naturalist 176: 249-263
(PDF, 2Mb)
(Online Enhancements Appendix A, PDF, 32Kb; Appendix B, PDF, 23Kb)

Jarne, P., David, P., Pointier, J.-P. & Koene, J.M. 2010. Basommatophoran Gastropods. In: The Evolution of Primary Sexual Characters in Animals (eds. A. Córdoba-Aguilar & J.L. Leonard), pp. 173-196, Oxford University Press
Please contact me if you want a reprint: joris.koene-at-falw.vu.nl
See book content at OUP

Koene, J.M., Sloot, W., Montagne-Wajer, K., Cummins, S.F., Degnan, B.M., Smith, J.S., Nagle, G.T. & Ter Maat, A. 2010. Male accessory gland protein reduces egg laying in a simultaneous hermaphrodite. PLoS ONE 5: e10117
(PDF, 303Kb)
(Supporting information Table S1, DOC, 30Kb; Table S2, DOC, 79Kb)

Benke, M., Reise, H., Montagne-Wajer, K. & Koene, J.M. 2010. Cutaneous application of an accessory-gland secretion after sperm exchange in a terrestrial slug (Mollusca: Pulmonata). Zoology 113: 118-124
(PDF, 634Kb)

De Boer, P.A.C.M., Jansen, R.F., Ter Maat, A., Van Straalen, N.M. & Koene, J.M. 2010.
The distinction between retractor and protractor muscles of the freshwater snail's male organ has no physiological basis. Journal of Experimental Biology 213: 40-44
(PDF, 159Kb)

Koene, J.M., Brouwer, A. & Hoffer, J.N.A. 2009. Reduced egg laying caused by a male accessory gland product opens the possibility for sexual conflict in a simultaneous hermaphrodite. Animal Biology 59: 435-448
(PDF, 685Kb)
See complete special issue of Animal Biology

Koene, J.M. 2009. Preface: Broadening sexual conflict. Animal Biology 59: 387-389
(PDF, 569Kb)
See complete special issue of Animal Biology

Bedhomme, S., Bernasconi, G., Koene, J.M., Lankinen, Å., Arathi, S., Michiels, N.K. & Anthes, N. 2009. How does breeding system variation modulate sexual antagonism? Biology Letters 5: 717-720
(PDF, 216Kb)
See complete special issue of Biology Letters

Koene, J.M., Montagne-Wajer, K., Roelofs, D. & Ter Maat, A. 2009. The fate of received sperm in the reproductive tract of a hermaphroditic snail and its implications for fertilisation. Evolutionary Ecology 23: 533-543
(PDF, 277Kb)

Van Straalen, N.M., Koene, J.M. & Ellers, J. 2008. Foreword. Animal Biology 58: 337-339
(PDF, 981Kb)
See complete special issue of Animal Biology

Koene, J.M., Loose, M.J. & Wolters, L. 2008. Mate choice is not affected by mating history in the simultaneously hermaphroditic snail, Lymnaea stagnalis. Journal of Molluscan Studies 74: 331-335
(PDF, 133Kb)

De Schamphelaere, K.A.C., Koene, J.M., Heijerick, D.G. & Janssen, C.R. 2008.
Reduction of growth and haemolymph Ca levels in the freshwater snail Lymnaea stagnalis chronically exposed to cobalt. Ecotoxicology and Environmental Safety 71: 65-70
(PDF, 175Kb)

Loose, M.J. & Koene, J.M. 2008. Sperm transfer is affected by mating history in the simultaneously hermaphroditic snail Lymnaea stagnalis. Invertebrate Biology 127: 162-167
(PDF, 119Kb)

Koene, J.M. & Ter Maat, A. 2007.
Coolidge effect in pond snails: Male motivation in a simultaneous hermaphrodite. BMC Evolutionary Biology 7: 212
(PDF, 249b)

Ter Maat, A., Zonneveld, C., De Visser, J.A.G.M., Jansen, R.F., Montagne-Wajer, K. & Koene, J.M. 2007.
Food intake, growth, and reproduction as affected by day length and food availability in the pond snail Lymnaea stagnalis. American Malacological Bulletin 23: 113-120
(PDF, 150b)

Koene, J.M., Montagne-Wajer, K. & Ter Maat, A. 2007. Aspects of body size and mate choice in the simultaneously hermaphroditic pond snail Lymnaea stagnalis. Animal Biology 57: 247-259
(PDF, 572Kb)
See complete special issue of Animal Biology

Reyes-Tur, B. & Koene, J.M. 2007. Use of the dart apparatus by the hermaphroditic land snail Polymita muscarum (Lea, 1834). Animal Biology 57: 261-266
(PDF, 432Kb)

Koene J.M. 2007. Preface: Animal behaviour, an integrative discipline. Animal Biology 57: 117-120
(PDF, 39Kb)
See complete special issue of Animal Biology

Koene, J.M. & Chiba S. 2006. The way of the samurai snail. American Naturalist 168: 553-555
(PDF, 841Kb)
(Online Enhancement Movie on Am. Nat. server: AVI, 1.7 Mb)
or (AVI, 1.7 Mb)

Michiels, N.K. & Koene, J.M. 2006. Sexual selection favors harmful mating in hermaphrodites more than in gonochorists. Integrative & Comparative Biology 46: 473-480
(PDF, 204Kb)
See complete special issue of Integrative & Comparative Biology

Koene, J.M. 2006. Tales of two snails: Sexual selection and sexual conflict in Lymnaea stagnalis and Helix aspersa. Integrative & Comparative Biology 46: 419-429
(PDF, 134Kb)
See complete special issue of Integrative & Comparative Biology

Koene, J.M. 2006. Slakken schieten met scherp. Natura 2006/3: 73-75
(PDF, 447Kb)

Koene, J.M., Montagne-Wajer, K. & Ter Maat, A. 2006.
Effects of frequent mating on sex allocation in the simultaneously hermaphroditic great pond snail. Behavioral Ecology & Sociobiology 60: 332-338
(PDF, 185Kb)

Koene, J.M. 2005. Allohormones and sensory traps: A fundamental difference between hermaphrodites and gonochorists? Invertebrate Reproduction & Development 48: 101-107
(PDF, 140Kb)

Koene J.M. 2005. Book review: "Sexual Conflict" by Göran Arnqvist & Locke Rowe. Animal Behaviour 70: 1439-1440
(PDF, 71Kb)

Koene, J.M., Pförtner, T. & Michiels, N.K. 2005. Piercing the partner's skin influences sperm uptake in the earthworm Lumbricus terrestris. Behavioral Ecology & Sociobiology 59: 243-249
(PDF, 297Kb)

Koene, J.M. & Schulenburg, H. 2005. Shooting darts: co-evolution and counter-adaptation in hermaphroditic snails. BMC Evolutionary Biology 5: 25
(PDF, 939Kb)
(Additional Files: PDF, 289Kb)

De Jong-Brink, M. & Koene, J.M. 2005. Parasitic manipulation: going beyond behaviour. Behavioural Processes 68: 229-233
(PDF, 71Kb)

Koene, J.M. & Ter Maat, A. 2005. Sex role alternation in the simultaneously hermaphroditic pond snail Lymnaea stagnalis is determined by the availability of seminal fluid. Animal Behaviour 69: 845-850
(PDF, 202Kb)

Koene, J.M. 2005. Love darts of land snails. Invertebrate Biology 124: 1
(PDF, 1537Kb)

Koene, J.M. 2004. Immunomodulation, allohormones and fertility. Medical Hypotheses 63: 1084-1085
(PDF, 34Kb)

Koene, J.M. & Muratov, I.V. 2004. Revision of the reproductive morphology of three Leptaxis species (Gastropoda, Pulmonata, Hygromiidae) and its implication on dart evolution. Malacologia 46: 73-78
(PDF, 1531Kb)

Koene, J.M. & Ter Maat, A. 2004. Energy budgets in the simultaneously hermaphroditic pond snail, Lymnaea stagnalis: A trade-off between growth and reproduction during development. Belgian Journal of Zoology 134: 41-45
(PDF, 57Kb)

Koene J.M. 2002. Book review: "Behavior and its Neural Control in Gastropod Molluscs" by Ronald Chase. Animal Behaviour 64: 969-970
(PDF, 54Kb)

Koene, J.M., Sundermann, G. & Michiels, N.K. 2002. On the function of body piercing during copulation in earthworms. Invertebrate Reproduction & Development 41: 35-40
(PDF, 471Kb)

Koene, J.M. & Ter Maat, A., 2002.The distinction between pheromones and allohormones. Journal of Comparative Physiology A 188: 163-164
(PDF, 51Kb)

Koene, J.M. & Ter Maat, A., 2001. "Allohormones": A class of bioactive substances favoured by sexual selection. Journal of Comparative Physiology A 187: 323-326
(PDF, 74Kb)

Koene, J.M., 2000. Het Proefschrift: Behavioural and neurobiological aspects of dart shooting in the garden snail Helix aspersa. NVG-Nieuwsbrief 9(1): 7-10
(PDF, 720Kb)

Koene, J.M., Jansen, R.F., Ter Maat, A. & Chase, R. 2000.
A conserved location for the central nervous system control of mating behaviour in gastropod molluscs: Evidence from a terrestrial snail. Journal of Experimental Biology 203: 1071-1080
(PDF, 463Kb)

Koene, J.M. 1999. Behavioural and neurobiological aspects of dart shooting in the garden snail Helix aspersa. Ph.D. thesis, McGill University, Montréal, Canada
(PDF of abstract, 13Kb)
Link to Thesis
Link to scanned thesis at the National Library of Canada (PDF, 8.7Mb)

Koene, J.M., Jansen, R.F., Ter Maat, A. & Chase, R. 1999. An in vivo electrophysiological study of mating behaviour in the snail Helix aspersa. Invertebrate Reproduction & Development 36: 123-127
(PDF, 802Kb)

Koene, J.M. & Chase, R. 1998. Changes in the reproductive system of the snail Helix aspersa caused by the mucus covering the love dart. Journal of Experimental Biology 201: 2313-2319
(PDF, 222Kb)

Koene, J.M. & Chase, R. 1998. The love dart of Helix aspersa Muller is not a gift of calcium. Journal of Molluscan Studies 64: 75-80
(PDF, 953Kb)

Boer, P.A.C.M. de, Jansen, R.F., Koene, J.M. & Ter Maat, A. 1997.Nervous control of male sexual drive in the hermaphroditic snail Lymnaea stagnalis. Journal of Experimental Biology 200: 941-951
(PDF, 321Kb)