males that mated with die females on die first day of die ex- periment had spent 4 or 5 days (and one male 6 and anodier male 7 days) in die cold room before ...
Behavioral Ecology Vol. 9 No. 1: 20-25
Decoupling of reproductive rates and parental expenditure in a polyandrous butterfly Christer Wikhmd, Arja Kahala, and Nina Wedell Department of Zoology, University of Stockholm, S-106 91 Stockholm, Sweden
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t is arguable that some degree of competition for mates is common in both sexes, but in most anim^lf it is apparent that one sex clearly competes more than the other (Bateman, 1948; Darwin, 1871; Trivers, 1972). Although females may compete more intensely for mates than males in some species, the predominant pattern is that of males competing more intensely for mates than females. Differences in the relative intensity of mating competition in the two sexes are usually attributed to sex differences in parental investment (Krebs and Davies, 1987; Trivers, 1972;). The ways in which the members of one sex compete for that of another differ greatly between species, but ultimately the intensity in mating competition depends on the operational sex ratio (OSR; the ratio of males to females that are ready to mate; see Emlen and Oring, 1977). Parental investment theory has proved difficult to test empirically, partly because parental expenditures are often in different currencies such as time, energy, orrisk,which are rarely equivalent for males and females, making sexual comparisons of parental expenditure difficult (Knapton, 1984). Qutton-Brock and Vincent (1991) proposed using the potential reproductive rate (PRR) of males and females as an empirical measure to predict the direction of mating competition, claiming that PRR is more closely related to die OSR and more easily measured than parental investment They denned PRR as the ma-rimum rate at which an individual of a given sex can produce offspring, equaling the progeny produced divided by the time required to produce them. Time to produce progeny represents "time out" from mate searching (Qutton-Brock and Parker, 1992), where time out is the processing time for a given reproductive event, and "time in" is spent on mate acquisition. Recently, Simmons (1995) and Parker and Simmons (1996) have argued that determining the number of offspring produced is an unnecessary step for predicting The direction of mating competition- batausa the number of of&pring produced by males and females must, on avReceived 4 March 1996; revised 17 March 1997; accepted 6 May 1997. 1045-2249/98/$5.00 O 1998 International Society for Behavioral Ecology
erage, be equal and hence cancels out from the calculations. What is crucial, according to Parker and Simmons (1996), is the time cost associated with reproduction for males and females (coupled with adult sex ratio and "collateral investment," or the relative number of male and female times out per reproductive event). Parker and Simmons (1996) further argue that, by concentrating on the cost of reproduction, I/time out is actually a relevant measure of parental investment, as defined by Trivers (1972) in terms of its negative effect on the parent's ability to invest in additional of&pring. The most complete support for current theories on the control of sexual selection comes from recent work with bushcrickets (Simmons, 1995), in which both sexes invest in offspring through the provisioning of nutrients for egg production. The importance of male provisioning for female reproduction appears to depend on the availability of nutrients in the environment, and under condition* of nutrient limitation, females of one species, Kawanaphila nartee, compete for males and their nuptial gifts, but when nutrients availability increases, males aggregate and compete acoustically for females (Bailey and Simmons, 1991; Gwynne and Simmons, 1990, Simmons and Bailey, 1990, 199S). This role reversal is associated with a shift in the OSR, and Simmons (1992) has shown that underlying this diet-mediated shift in the OSR is a reversal in the relative energy expenditure on offspring by males and females. Recently, Simmons (1995) also showed the extent to which relative energy expenditure on of&pring production influences the PRR of males and females in K. nartee. Hence, for this bushcricket there are negative associations between relative parental expenditure and relative reproductive rate and between relative parental expenditure and the OSR. In butterflies males transfer an ejaculate containing both sperm and accessory substances to the female at mating. Radiotracer studies have shown that substances transferred by the auk to the female at mating ran later be retrieved both in die soma and in the reproductive tissue of the female, suggesting that part of the ejaculate of butterflies can be considered as a nuptial gift (Boggs and Gilbert, 1979; Wiklund et ah, 1993). Moreover, comparative studies have shown that relative ejaculate size increases with the degree of polyandry among butterflies, suggesting that butterfly mating systems
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Current theory postulates that the operational sex ratio (OSR) determines the relative degree of mating competition in the two sexes and is in turn influenced by a sexual difference in the potential reproductive rate (PRR) denned as I/time out, where time out is the time an individual must spend recovering from a bout of mating activity and/or caring for offspring. In bushcricket mating systems where males provide females with a nuptial gift, relative energy expenditure in of&pring influences the PRR of males and females and underlies a diet-mediated shift in the OSR. Here we investigated if there is a similar positive relationship between relative parental nutrient expenditure in of&pring and PRR in the polyandrous butterfly Pieris napi, where female fecundity is strongly dependent on male nuptial gifts at mating. By varying the amount of nutrients females receive at mating and relating this to number of of&pring produced, we show that male P. napi have, on average, a nutrient expenditure in of&pring equaling that of females. In spite of this, the male reproductive rate is 8-13 times higher than that of females. Hence the relative degree of parental expenditure in of&pring is largely decoupled from the degree of mating competition in P. napi. Two alternative explanations are advanced to account for the difference between the butterfly and the bushcricket mating systems. Key words: butterflies, nuptial gifts, parental investment, Pieris napi, polyandry, reproductive rate, sexual selection. [Behav Ecol 9:20-25 (1998)]
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Wiklund et al. * Butterfly reproductive rates and parental expenditure
MATERIALS AND METHODS The butterflies used in diis study were die offspring from female P. napi collected in die wild in die vicinity of Stockholm, Sweden. After being caught, we allowed die females to lay eggs on die natural host plant AlUaria petiolata in egg-laying cages in die laboratory, after which larvae hatching from die eggs were reared individually in 0.5-1 plastic jars on A. petiolata until pupation. On die day of eclosion each individual was sexed, marked with a Staedler lumocolor pen, weighed on an automatic electrobalance, and put in a room maintained at 8°C, until die start of die experiment Twenty of die virgin males that mated with die females on die first day of die experiment had spent 4 or 5 days (and one male 6 and anodier male 7 days) in die cold room before die start of die experiment (i.e., die day when they successfully mated with a female). These males were given die opportunity to mate a second time within die first 2 days of die experiment, and 10 males remated on die first day, anodier 6 mated on die following day, and die remaining 4 males did not remate during die first 2 days. The females we used in die experiment had spent between 2 and 7 days in die cold room before die start of die experiment, and die mean times spent in die cold room by (1) females mated once with a nonvirgin male, (2) females mated once with a virgin male, (3) females mated first
widi a nonvirgin male and then with a virgin male, and (4) females mated twice with virgin males were 4.0 days, 2.9 days, 45 days, and 4.1 days, respectively. We used S3 females in die experiment aimed at assessing die influence of ejaculate mass on female fecundity. After termination of mating, we put die females individually in cages measuring 0.7 X 0.7 X 0.5 m in a greenhouse on die roof of die zoology building. These cages were provided widi flowers of Ctrmtm arvenst, to which drops of a 25% sucrose solution were added three to four times daily, as well as a botde widi leaves of die host plant A. petiolata. The leaves of A petiolata were changed every day and die number of eggs laid counted. Females that were allowed to mate only once were alone in dieir cages diroughout their lives, whereas females that were allowed to mate a second time widi a virgin male were accompanied by an unmated male up to die time of remating. Females that were allowed to mate a second time widi a nonvirgin male were accompanied by a nonvirgin male that had eidier mated diat same day, or die day previously, up to die time of remating (hence a given nonvirgin male could be used for a maximum of 2 days, after which he was replaced by anodier recendy mated male). We observed die egg-laying cages every 15 min, and females were dissected after death to assess that die number of spermatophores in die bursa copulatrix corresponded widi die number of observed matings; in diis experiment diis was invariably die case. We calculated die amount of ejaculate transferred by a male to a female at mating using die empirical relationship established by Wiklund and Kaitala (1995), according to which log ejaculate mass m 0.63 X log male mass — 0.21 for virgin males, and log ejaculate mass - 2.92 log male mass - 4.65 for recendy mated nonvirgin males. The experiment during which die mating rate of males was measured was performed in four 0.8 X 0.8 X 05 m cages, in which 10 males and 10 females were allowed to fly freely. These cages were provided widi flowers of C arvenst, which were supplied widi extra drops of sucrose solution for butterflies to feed on, and were lit between 0830 and 1730 h. We observed die cages continuously during die 2 days of die experiment, and as soon as a mating couple was observed, they were put gendy in a 05-1 plastic cup and transferred to anodier cage. The mating couple was confined to die plastic cup by putting a gauze top on die jar, and die time of copula initiation and termination were noted. After copula termination we immediately released die male in anodier cage, provided widi a surplus of virgin females, so all of die 20 males used in diis experiment had die opportunity to mate diroughout their first 2 days of life. We measured female mating rate under die same conditions, except that die females, after mating a first time, were transferred individually to single cages where they were accompanied by one virgin male until they mated a second time. RESULTS On die basis of die earlier established relationship between male weight and ejaculate weight, there was a threefold variation in die amount of ejaculate mass that females received (Table 1, Figure 1). There was a significant effect of male ejaculate mass on female lifetime fecundity (F => 3.004, df = 3; p
