Sexual roles and gender conflict in pond snails

I caught these pond snails mating in my indoor tank today. The bluish, tongue-like structure between both snails is the penis of the snail on the background, entering the other snail's mantle cavity. So, that snails is acting as a male, (the one with a walrus-like head resting on its partner's shell) and the other as a female. Pond snails are simultaneous hermaphrodites, all individuals have functional ovaries and testis. The snails can self-fertilise, but if sperm from other individual is present, they prefer to use it. Although reciprocal sperm exchange might appear as a logical reproductive strategy, each individual snail might benefit more from acting as a male or as a female in a particular encounter with a potential partner. For example, large snails are able to invest in energetically demanding eggs, and might prefer to act as a female. Individuals acting as females are limited in the frequency at which they produce eggs, so they might prefer not to mate as often. Male reproductive efficiency might depend more on how many sexual encounters he has had, so snails preferring to be males might want to mate more often.

Sexual encounters of pond snails can result in just one of them acting as a male and the other like a female, or in subsequent reciprocation.  But, the snails could disagree, what if both mating partner insist on providing, but not receive sperm? This is called gender conflict, and the resolution depends on one of the individuals compromising and adopting its less preferred role, at least initially.

Petra Hermann and collaborators studied the effect of age on sex role preferences in the great pond snails, Limnaea stagnalis, disentangling it from the effect of size.  They reared three batches of snails that had known ages at the time of the experiments (young, Y, middle age M, and senior, S) and matched them by size.

First, they looked at the effect of age on mating interactions in age-matched couples. The chances of copulation decreased strongly with age, with young snails copulating with much higher frequency (80%) than senior snails (30%). Encounters between young snails normally ended in a reciprocal intromission (the individual acting as a female initially, then acting as a male), middle aged and senior snails, in contrast, had mostly unilateral sperm exchanges.

 Then they set encounters between snails of different ages. When pairing young and middle aged snails, also size-matched, about 25% ended in no copulation, and unilateral encounters were more common than reciprocal. The primary role in the copulation (the snail acting as a male first) was adopted by the young snail in about 80% of the encounters, indicating that the male role is the coveted one for the young snail, and that the fact that reciprocation is rare indicates that the middle ages snail is content acting as a female in unilateral encounters. There is an age related shift in sexual role preferences from male to female.

Fig. 6. Sexual interactions between young and middle-aged Lymnaea.

(A) Most couples of a young and a middle-aged snail (YM) performed a

copulation. The majority of these interactions were unilateral, i.e. the snails

do not reverse roles after finishing the first copulation. Note that in the

cases in which the middle-aged animals acted as primary male all young

partners reciprocated. By contrast, role reversal occurred in only a small

minority (18%) in the couples in which the middle-aged animals acted as

female. (B) Younger snails act significantly more often as primary male than

their middle-aged partner. (modified from Hermann et al 2009)

They concluded:

Animals in the early phase of the species’ life cycle tend to assure that they act as male (either primary or secondary), independent of the age of their partner (Fig. 7A). Senior animals, by contrast, tend to act preferentially as females. The sexual behaviour of middle-aged animals depends on the age of their partner. Combined with similarly aged partners they either act as male or female. Combined with a younger partner they tend to act as female only. Combined with an older partner, they tend to execute both gender roles and will act as males with a similar probability as younger animals

Interestingly, the snails resolved conflict by engaging in reciprocation. When both agreed on a role the encounters tend to be unidirectional. Note that as these snails store sperm and the partners were not virgins, the lack of interest in copulation of the older snails might stem from the fact that they might have accumulated enough sperm to fertilise their eggs. So although the authors removed the confounding effect of age from their experiments, they failed to account for the effect of sperm storage.

 The snails' efforts are resulting on these lovely egg masses appearing attached on the walls of the tank.

More information

Hermann PM, Genereux B, & Wildering WC (2009). Evidence for age-dependent mating strategies in the simultaneous hermaphrodite snail, Lymnaea stagnalis (L.). The Journal of experimental biology, 212 (19), 3164-73 PMID: 19749110