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Coolidge Effect in Pond Snails: Male Motivation in a Simultaneous Hermaphrodite Jorismkoene*1 and Andries Ter Maat1,2

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Coolidge Effect in Pond Snails: Male Motivation in a Simultaneous Hermaphrodite Jorismkoene*1 and Andries Ter Maat1,2 BMC Evolutionary Biology BioMed Central Research article Open Access Coolidge effect in pond snails: male motivation in a simultaneous hermaphrodite JorisMKoene*1 and Andries Ter Maat1,2 Address: 1Department of Animal Ecology, Faculty of Earth & Life Sciences, Vrije Universiteit, De Boelelaan 1085, 1081 HV Amsterdam, The Netherlands and 2Max-Planck-Institut für Ornithologie, Postfach 1564, 82305 Starnberg, Germany Email: Joris M Koene* - [email protected]; Andries Ter Maat - [email protected] * Corresponding author Published: 6 November 2007 Received: 1 September 2006 Accepted: 6 November 2007 BMC Evolutionary Biology 2007, 7:212 doi:10.1186/1471-2148-7-212 This article is available from: http://www.biomedcentral.com/1471-2148/7/212 © 2007 Koene and Ter Maat; licensee BioMed Central Ltd. This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/2.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited. Abstract Background: The simultaneously hermaphroditic pond snail, Lymnaea stagnalis, can mate in the male and female role, but within one copulation only one sexual role is performed at a time. Previous work has shown that male motivation is determined by the availability of seminal fluid in the prostate gland, which is detected via a nervous connection by the brain area controlling male behaviour. Based on this knowledge, patterns of sexual role alternations within mating pairs can be explained. Results: The data presented here reveal that these snails can donate and receive sperm several times within 24 hours, and that they have increased mating rates in larger groups (i.e. more mating opportunities). For mating pairs we show, by introducing novel mating partners after copulation, that animals do inseminate new partners, while they are no longer motivated to inseminate their original partners. Conclusion: Our findings provide the first direct evidence for higher motivation in a hermaphrodite to copulate when a new partner is encountered. This Coolidge effect seems to be attenuated when mucus trails are excluded, which suggests that a chemical or textural cue may be responsible for mediating this response to sperm competition. Background non of preferentially inseminating a novel partner was Males of many species distribute their sperm over several first demonstrated experimentally in rats [6], and is gener- mates, and often do this in a way that is theoretically pre- ally assumed to be widespread among promiscuous verte- dicted to maximize their lifetime reproductive success brates [4,5,7]. The Coolidge effect is based on familiarity [e.g., [1,2]]. Since the seminal paper by Dewsbury [3], it is with a mating partner, and is often assumed to require the now generally accepted that sperm and seminal fluids are presence of an individual recognition mechanism. How- costly to produce and that males are selected to strategi- ever, individual recognition is not included in the defini- cally allocate their sperm [4]. One behavioural strategy to tion and has, to our knowledge, actually never been achieve the latter is via rekindled sexual motivation upon shown to lay at the basis of this phenomenon. Nonethe- encounter of a new partner, which has been dubbed the less, the Coolidge effect is usually thought to require cog- Coolidge effect by Whalen in 1959 (after an anecdote nitive brain areas involved in learning and memory that about President and Mrs. Coolidge) [5]. This phenome- can integrate the information from different neural sys- Page 1 of 6 (page number not for citation purposes) BMC Evolutionary Biology 2007, 7:212 http://www.biomedcentral.com/1471-2148/7/212 tems involved in individual discrimination, novelty detec- opening is accessible. This is followed by probing with the tion and memory maintenance, and motivation [e.g., everted preputium (penis carrying organ) and, once the [7,8]]. female gonopore is found, penis intromission and trans- fer of a copious amount of semen [24]. That the male Darwin [9] stated about molluscs, and other species reproductive investment of this simultaneous hermaphro- belonging to the "lower classes", that "it is almost certain dite equals the energetic costs of female reproduction was that these animals have too imperfect senses and much demonstrated by experimentally eliminating male behav- too low mental powers, to appreciate each other's beauty iour, which resulted in a doubling of egg production [27]. or other attractions, or to feel rivalry". However, it is now The above illustrates that these snails are expected to be clear that sexual selection and sperm competition are prudent with their expensive male reserves. It would be widespread among invertebrates [e.g., [10]]. Here, we prudent to use the sperm to inseminate different partners show that the Coolidge effect is also not restricted to ver- rather than the same partner several times, which we set tebrates, because we find that this motivational strategy is out to test here. used by a hermaphroditic invertebrate. Results There is now abundant evidence that insects are prudent The mean number of inseminations per individual with their expensive sperm and seminal fluids, despite observed during 24 hour observations of Pairs, Quartets, their relatively high mating rates. Gage [11,12] was the and Octets are shown in Figure 1. The overall difference first to show that for the medfly, Ceratitis capitata, the pres- between the groups was significant (Nested ANOVA: F2,18 ence of sperm competition results in the transfer of more = 3.88, p = 0.027). Post-hoc testing showed that Octets sperm per ejaculate. Subsequent studies further focused had a higher insemination frequency than Pairs (Tukey on sperm numbers as a response to the risk or intensity of HSD, p < 0.05), while the Quartets' frequency was in sperm competition [e.g., [13-18]]. Interestingly, we have between but different from neither. only been able to find one insect study, on Tribolium cas- taneum, that specifically looked at whether males prefer to In pairs of snails we subsequently tested experimentally inseminate novel females over familiar females, which whether the observed increase in insemination frequency they had already inseminated [19]. Although that study in larger groups was due to the presence of new partners. provided evidence for a Coolidge effect this connection We used a mixed model (nominal logistic REML proce- was somehow not made at the time, possibly because of dure) to test for the fixed effects of treatment (New/Same the lack of knowledge about the underlying motivational partner) and test (Dirty/Clean aquarium) and the random mechanism. Another study, on Gryllus bimaculatus, effect of replicates (nested in treatment) on whether showed that females preferred to mate with a novel male, insemination occurred. Prior to the treatment, i.e. during indicating that the Coolidge effect is not limited to males the first 6 hours of the experiment, on average 39.25 (± [20]. The great pond snail, L. stagnalis, is a simultaneous her- maphrodite that can mate in the male and female role, 3 but within a single copulation one sexual role is per- b formed (and roles can be swapped afterwards) [21]. These ab snails seem usually prepared to receive sperm [21], they 2 a can receive sperm multiple times within a breeding season [22], and they can store and use the received sperm from different partners [23]. However, they will only donate per individual 1 sperm after several days of sexual isolation [24]. Previous studies have demonstrated that this male motivation is Mean no. of inseminations determined by the amount of seminal fluid in the prostate 0 Pairs Quartets Octets gland [25]. The gland's volume increase is detected, via a nervous connection, by an evolutionarily conserved brain 24andFigure hour 8 snails 1observations of copulation activity in groups of 2, 4 region controlling male behaviour in gastropod molluscs 24 hour observations of copulation activity in groups of 2, 4 [26]. and 8 snails. The mean number of inseminations per individ- ual are shown, the error bars represent standard errors of L. stagnalis' male behaviour comprises a fixed sequence of the mean of the replicates. For clarity the replicates are events. These events include shell mounting and circular pooled. Groups with different letters (a or b) differ signifi- locomotion over the partner's shell to eventually find the cantly from each other. position on the edge of the shell from where the female Page 2 of 6 (page number not for citation purposes) BMC Evolutionary Biology 2007, 7:212 http://www.biomedcentral.com/1471-2148/7/212 1.71 S.D., N = 4 replicates) of the 48 animals inseminated A: Dirty their partner. For this observation period no differences 50 were found in the number of inseminations (treatment: 2 2 χ < 0.00, df = 1, p = 1.00; test: χ = 0.31, df = 1, p = 0.57; 40 interaction: χ2 = 0.07, df = 2, p = 0.96). In all cases where insemination took place after the treatment, i.e. during 30 the second 6 hours, animals inseminated their partners only once. Significantly more new partners were insemi- nated than familiar partners (χ2 = 6.14, df = 1, p = 0.013). inseminations 20 In a clean aquarium more copulations were observed than nd 2 10 in an uncleaned aquarium (χ = 3.88, df = 1, p = 0.049), % 2 indicating that the presence of mucus is important for this 0 effect. The interaction between the two factors was also 0 significant (χ2 = 6.84, df = 2, p = 0.033), suggesting that the Same partner New partner effect of a new partner depended on the factor Clean/ Dirty. The percentage of animals performing an insemina- tion during the second 6 hours is shown separately for the two replicates in the Dirty (Figure 2A) and the two repli- B: Clean cates in the Clean aquaria (Figure 2B).
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