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The Coolidge Effect, Individual Recognition and Selection For ARTICLE IN PRESS Proc. R. Soc. B 1 doi:10.1098/rspb.2008.0375 65 2 66 3 67 4 68 5 The Coolidge effect, individual recognition 69 6 70 7 and selection for distinctive cuticular signatures 71 8 72 9 in a burying beetle 73 10 1,* 1,† 1,2 ¨ 1 74 11 Sandra Steiger , Ragna Franz , Anne-Katrin Eggert and Josef K. Muller 75 12 1Department of Evolutionary Biology and Ecology, Faculty of Biology, University of Freiburg, 76 13 Hauptstrasse 1, 79104 Freiburg, Germany 77 14 2Behavior, Ecology, Evolution, and Systematics (BEES) Section, Department of Biological Sciences, 78 15 Illinois State University, Normal, IL 61790-4120, USA 79 16 80 The ability to recognize individuals is an important aspect of social interactions, but it can also be useful to 17 81 avoid repeated matings with the same individual. The Coolidge effect is the progressive decline in a male’s 18 82 propensity to mate with the same female combined with a heightened sexual interest in new females. 19 83 Although males that recognize previous partners and show a preference for novel females should have a 20 84 selective advantage as they can distribute sperm evenly among the females they encounter, there are few 21 85 invertebrate examples of the Coolidge effect. Here we present evidence for this effect in the burying beetle 22 86 Nicrophorus vespilloides and examine the mechanism underlying the discrimination between familiar and 23 87 novel mates. Burying beetles feed and reproduce on vertebrate carcasses, where they regularly encounter 24 88 conspecifics. Males showed greater sexual interest in novel females (virgin or mated) than in females they 25 89 had inseminated before. The application of identical cuticular extracts allowed us to experimentally create 26 90 females with similar odours, and male responses to such females demonstrated that they use female 27 91 cuticular patterns for discrimination. The chemical analysis of the cuticular profile revealed greater inter- 28 92 individual variation in female than in male cuticular patterns, which might be due to greater selection on 29 93 females to signal their individual identity. 30 94 31 Keywords: burying beetles; Nicrophorus; Coolidge effect; individual recognition; cuticular lipids; 95 32 identity signals 96 33 97 34 98 35 99 1. INTRODUCTION (bees: Barrows 1975; amphibians: Donovan & Verrell 36 100 Although the cost of mating to males has long been 1991; reptiles: Tokarz 1992; flies: Wcislo 1992, O¨ deen & 37 101 regarded as negligible, recent evidence shows that mating Moray 2008; beetles: Arnaud & Haubruge 1999; fishes: 38 102 and sperm production may generate non-trivial costs Kelley et al. 1999) have been shown to avoid mating or 39 103 (Dewsbury 1982; Van Voorhies 1992; Olsson et al. 1997; re-mating with familiar individuals. 40 104 41 Preston et al. 2001), promoting the evolution of prudent The Coolidge effect per se has received no attention in 105 42 ejaculate allocation or even male reluctance to mate invertebrates with the exception of one recent study on 106 43 (Wedell et al. 2002). If the value of a female to a male snails (Koene & Ter Maat 2007). Given the number of 107 44 decreases with his increasing mating investment to that studies that have examined mate choice in insects, it is 108 45 individual female, males are expected to avoid re-mating surprising that there have been no investigations of the 109 46 with the female in favour of other reproductive opportu- Coolidge effect per se in this group. Researchers may 110 47 nities (Wedell et al. 2002; Pizzari et al. 2003). The frequently have assumed that the Coolidge effect requires 111 48 ‘Coolidge effect’, defined as a decline in the propensity of a more complex neural processing than invertebrates are 112 49 male to copulate repeatedly with the same female capable of Koene & Ter Maat (2007). However, some 113 50 combined with a heightened sexual interest in novel social insects have proved capable of individual recog- 114 51 females (Wilson et al. 1963; Dewsbury 1981), can be a nition (Tibbetts 2002, 2004; D’Ettorre & Heinze 2005), 115 52 mechanism to distribute sperm more evenly. The Cool- and avoiding matings with one’s previous mate may not 116 53 idge effect was first observed in rats (Beach & Jordan necessarily require individual recognition. Female crickets 117 54 1956) and has since been demonstrated in a number of Gryllus sigillatus use self-referencing (marking males with 118 55 other mammals (see Dewsbury 1981) and birds (Pizzari their individual specific chemical signature) to avoid 119 56 et al. 2003). Similarly, animals of many different groups re-mating with previous mates (Ivy et al. 2005). Numer- 120 57 ous insects have evolved other mechanisms of discrimi- 121 58 nation against previously mated individuals that have 122 59 * Author for correspondence ([email protected]). 123 † typically been interpreted as adaptations to sperm 60 Present address: Division of Zoo Animals, Exotic Pets and Wildlife, 124 Vetsuisse Faculty, University of Zurich, Winterthurerstaße 260, 8057 competition. The so-called ‘antiaphrodisiacs’ are male- 61 Zu¨rich, Switzerland. produced chemicals that are transferred to females 125 62 126 Electronic supplementary material is available at http://dx.doi.org/10. during mating and discourage further matings by these 63 1098/rspb.2008.0375 or via http://journals.royalsociety.org. females (e.g. Happ 1969; Kukuk 1985; Peschke 1987; 127 64 128 Received 18 March 2008 1 This journal is q 2008 The Royal Society Accepted 23 April 2008 RSPB 20080375—30/4/2008—12:51—CHANDRAN—299268—XML – pp. 1–9 ARTICLE IN PRESS 2 S. Steiger et al. Coolidge effect in burying beetle 129 Carlson & Schlein 1991; Andersson et al. 2003) which (b) General procedures of behavioural experiments 193 130 may also help the original male to avoid re-mating with Experiments that involved observation of copulatory 194 131 the same female. behaviour were conducted during the last 2 hours before 195 132 This study investigated the occurrence and underlying the end of the light phase. Males emit pheromones and mate 196 133 mechanism of the Coolidge effect in the burying beetle with attracted females during this period both in our own 197 134 Nicrophorus vespilloides. Males of this species show clear Q2 (unpublished data) and a northern German population near 198 135 evidence of sperm depletion after several days spent with Bielefeld (Mu¨ller & Eggert 1987; Eggert & Mu¨ller 1989). 199 136 multiple females (Eggert 1990). To a male of this species, Matings were observed in small plastic containers (8!5! 200 137 re-mating with a female may thus entail a twofold cost: 6 cm) with a moistened plaster bottom. To minimize 201 138 time that could have been spent seeking out other females disturbance immediately prior to an observation, males 202 139 and sperm that could have been more efficiently used to were transferred to observation chambers 3 hours before 203 140 inseminate another female. Burying beetles reproduce on the onset of an experiment. Over the course of an experiment, 204 141 vertebrate carcasses, frequently in groups with several males remained in the same chamber while females were 205 142 females (Pukowski 1933;Mu¨ller et al. 1990, 2007). When introduced and removed. In each trial, a male was presented 206 143 females leave the carcass early, or males have only limited with a female and either mated with her or did not mate 207 144 time on a carcass, males may benefit from distributing (see below), then the female was removed and the male 208 145 sperm evenly among the available females. Even without remained alone for 5 min before the next female (either the 209 146 reproductive resources, males mate more frequently when same one or a different one) was introduced into the chamber. 210 147 held with multiple females than with a single one (Eggert For each encounter, we recorded the time to mating defined 211 148 1990). This effect could arise if males respond more as the time from the beetles’ first physical contact to the actual 212 149 readily to females other than their last mate. coupling of genitalia. Females were removed from the 213 150 In burying beetles, cuticular contact pheromones chamber as soon as the first mating ended. If the pair did 214 151 contain information about breeding and nutritional status, not mate within 5 min (300 s), we removed the female, 215 152 sex and species (Whitlow 2003; Steiger et al. 2007), and scoring a time to mating of 300 s. 216 153 could play an important role in recognition processes like Our study was designed to determine the readiness 217 154 nestmate recognition (Mu¨ller et al. 2003). To date, there is of males to mate, and we interpret a long time to mating 218 155 no information about the role of cuticular substances in as low male sexual interest, since matings are initiated by 219 156 interactions between the sexes. We tried to address males, who approach and mount females prior to mating. In 220 157 whether males are capable of discriminating between order to avoid the potentially confounding effects of the 221 158 222 their last mate and other females on the basis of cuticular females’ response to male attempts, we excluded trials in 159 223 substances. Following the experimental protocol of Ivy which females clearly tried to avoid copulations by struggling 160 224 et al. (2005), we tested whether males transfer their own and attempting to leave during male mating attempts (17 out 161 225 chemical substances to females or learn cues from the of 198 trials). 162 chemical profile of their females to recognize previous 226 163 mates.
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