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Volume 49

Research Grant Report


Mating behaviour of Deroceras
Heike Reise,
State Museum of Natural History, Görlitz, Germany

Our grant application concerned the recording of mating behaviour in a number of Deroceras slug species; particularly we proposed to address two separate questions.

Question 1: Is extreme morphology associated with extreme behaviour in Deroceras gorgonium?

Figure 1: Morphology of distal male genitalia of Deroceras gorgonium. A. The whole penis. B. Component part of the penial gland (position shown boxed in A). C. The sarcobelum revealed by cutting open the main part of the penis sack. Scale bars = 1 mm.
One striking aspect of mating in many Deroceras species is the eversion of the appending penial gland over the partner to transfer a secretion. The timing of the transfer in some species, just after sperm exchange, rules out a function such as synchronising the copulation; instead, it suggests a role in sperm competition. The secretion may act as an anti-aphrodisiac to hinder re-mating, or as an allohormone that manipulates the partner into using the sperm just received, thus being comparable to the function of the helicid love dart (Chase and Blanchard, 2006)
We examined the mating behaviour of Deroceras gorgonium, the species with the largest and most branched penial gland (Fig. 1) amongst the several (more than 100) species of this genus. We collected specimens from a small area of endemism from Crete, and we video recorded 22 matings in our laboratory in Germany (Reise et al., in press). Additionally, we collected specimens of six other Deroceras species, of which we also studied the mating behaviour in the laboratory; however, this data have yet to be analysed.

Our results show that in Deroceras gorgonium the penial gland is everted either at or just after the very rapid (< 1s) sperm exchange. The eversion looked like time-lapse recordings of growing roots; often, the branches of the penial gland seemed to be clumsily misdirected, initially sticking up in the air and consequently not always covering the partner before being retracted. Often, the glands were also everted under the partner's body; such function was not recorded in the mating behaviour of other species we studied. We suggest that this is the function for which the unusual size and shape of the penial gland of Deroceras gorgonium are adapted.

The mating behaviour of Deroceras gorgonium turned out to be unusual in other respects as well. First, the courtship process was at least 6, and sometimes over 9, hours longer compared to other Deroceras species. Secondly, it always consisted of many short bouts of different behaviour, including periods of apparent inactivity. Thirdly, much of the courtship consisted of stereotyped waving of sarcobela, reminiscent of two circling swordsmen afraid to strike (Fig. 2).
In other Deroceras the finger- or hand-like sarcobelum is stroked along the side of the partner's body. However, in Deroceras gorgonium the sarcobelum is unusually long and pointed and during the first hours of courtship it is merely waved in front of the partner's face; when it does touch the partner it takes hours before it does so with more than its tip.

Figure 2: Courtship of Deroceras gorgonium. A and B. Distant waving and circling during early courtship. C and D. Closer waving and circling with body contact characteristic of later courtship. E. Close contact between sarcobela. F. Close yin-yang, shortly before sperm exchange.

This waving is regularly coordinated with the circular moves of the partners that eventually lead to swapping positions (Fig. 2). It is possible that these circular moves and action of the sarcobela serve in assessing partner's size or sensing components of the partner's mucus in order to receive information about its physiological state. During our recordings we observed the transfer of drops of secretion, thus confirming for the first time in Deroceras, such a function for the sarcobelum.

Currently, we are conducting further experiments, regarding a more accessible species, Deroceras panormitanum, to investigate further the function of the appending penial gland.

Question 2: Assessing whether mating behaviour functions as an isolation mechanism between sibling Deroceras species.

Although Deroceras is the most speciose genus of terrestrial slugs there is very little variation in the external morphology of different species. This could be the result of (i) sexual selection that drives divergence of reproductive anatomy and mating behaviour between allopatric populations, and (ii) selection against hybridisation in the event the populations meet.
Previously, we have identified extremely narrow zones of contact between pairs of sibling Deroceras species: between Deroceras praecox and Deroceras rodnae in the Babia Gora mountains of Poland, and between Deroceras praecox and Deroceras fatrense in the Mala Fatra mountains of Slovakia. These pairs of species are morphologically distinguishable only by differences in the shape of their penis, and specifically the sarcobelum. Subtle differences in the mating behaviour of the allopatric populations, e.g. the way in which the sarcobelum strokes and the timing of the different stages of mating, were recorded previously (Reise, 1995).
In the present study we examined the mating behaviour of pairs of sibling species across these narrow contact zones. Our objective was to assess whether mating behaviour gradually intergrades due to introgression, or whether it is more distinct in the contact zone as a result of selection against hybridisation.

In each geographical area we collected both sibling pecies from populations whose habitats were well away from the zone of contact, and we compared interspecific and intraspecific mating behaviour. We then repeated this for populations whose habitats were only a few hundred metres on either side of the zone of contact. Finally, we studied the mating behaviour between individuals of both sibling species collected within the zone of contact, in habitats where individuals of both species are found together with the occasional apparent intermediate. All recordings took place in our laboratory using specimens collected from the wild within the previous few weeks.
So far, we have recorded 211 mating events. The analysis, though, is still incomplete and we wish to remain blind to the pattern of results until we have finished scoring. So far, we observed that interspecific crosses, lead to mating behaviour, even when individuals come from distant populations; however, many of these mating events fail to lead to successful sperm exchange.

In the future, we plan to follow up these comparisons on anatomy and mating behaviour with a genetic analysis of gene flow across Deroceras sibling species inhabiting the contact zones.

The Malacological Society of London provided the funds to improve our digital video system for analysing the mating behaviour of Deroceras slugs, and we are extremely grateful for this financial assistance.

Literature cited

Chase, R. and K.C. Blanchard, 2006. The snail's love-dart delivers mucus to increase paternity.Proc. R. Soc. Lond. B., 273, 1471-1475.
Reise, H., 1995. Mating behaviour of Deroceras rodnae Grossu et Lupu, 1965 and D. praecox Wiktor, 1966 (Pulmonata: Agriolimacidae). Journal of Molluscan Studies 61, 325-330.
Reise, H., S. Visser, and J.M.C. Hutchinson. In press. Mating behaviour in the terrestrial slug Deroceras gorgonium: is extreme morphology associated with extreme behaviour? Animal Biology

[Figs. 1 and 2 are reproduced from Animal Biology 57(2) with permission.]