Prolonged copulation in Alloporus uncinatus is a form of mate guarding against sperm competition. Here we show, using a simple experiment, that males control the duration of copulation, an often overlooked assumption regarding the adaptive significance of prolonged copulation. The sex-specific evolutionary benefits of prolonged copulation are discussed in relation to the role played by sperm competition in the evolution of the mating system of A. uncinatus

Dangerfield, J.M.

Telford, S.R.

English

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266 Australia with North and South ArneTie:!. F-uJlogy 66: 1859-1866. NEL. 1.AJ. 1992. Fluctuations in small mammal populalions in the Kalahari. Zoological Society of Southern Africa Sympo-sium, Kimberley, South Africa. NELSON, LF. & CHEW, R.M. 1977. Factors affccLin~ seed reserves in the soil of a Mojave dcscn ecosystem, Rock Valley, Nyc Country, Nevada. Am. Mid!. Nal. 97: 300-320. PARMENTER, R.R., MACMAHON, l.A. & VAN DER WALT, S.R. 1984. The measurement of granivory by desert rodents, birds and ants: a comparison of an energetics approach and a seed dish technique. 1. Arid Enll. 7: 75-92. PRICE, M.V. & JENKINS, S.H. 1986. Rodenl, as seed comumers and dispersers. In: Seed dispersal. (cd.) D.R. Murray. Academic Press, AUSlTalia. SKINNER, J.D. & SMITHERS, R.H.N. 1990. The ~bmlllaisof the Southern African Subregion. University of Pr<.'lori~, Pretoria. SOHOL T, L.F. 1973. Consumption of primary production by a population of kangaroo raL~ (Dipodomys merriaml) in the Mojave Desert. Er:ol. Mono. 43: 357-376. SWANEPOEL, C.M. 1980. Some factors influencing thc brced-ing season of Praomys nalalensis. S. Afr. 1. Zool. 15: YS-YH. TA YLOR, K.D. & GREEN, M.D. 1976. The influence of rainfall in diet and reproduction in four African rodent species. J wal. Land 180: 3(i7-3~9. WATSON, C.R.B. 1987. The comparative ecology of two small mammal communities in the Kruger National Park. Unrub. M.Sc. thesis, University of Pretoria. S.-Afr. Tydskr. Dierk. 1994,29(4) Males control the duration of copulation in the tropical millipede Alloporus uncinatus (Diplopoda: Julida) S.R. Telford' Zoology Department, University of Pretoria, Pretoria, 0002 Republic of South Africa J,M, Dangerfield Department of Biology, University of Botswana, Private Bag 0022, Gaborone, Botswana Prolonged copulation in Affoporus uncinatus is a form of mate guarding against sperm competition. Here we show, using a simple experiment, that males control the duration of copUlation, an often overlooked assumption regarding the adaptive significance of prolonged copulation. The sex-spe-cific evolutionary benefits of prolonged copulation are dis-cussed in relation to the role played by sperm competition in the evolution of the mating system of A. uncinatus. Lang paringstye by Alloporus uncmatus beskerm paarge-note teen spermkompetisie. Ons dui hier met behulp van 'n eenvoudige eksperiment aan dat mannetjies die duur van paring beheer. Dit het betrekking op 'n aanname wat dik-wels oorgesien word ten opsigte van die aanpassingsbelang van lang paringstye. Die geslagspesifieke evolutionere voordele van lang paringstye word bespreek met betrekking tot die rol wat spermkompetise in die ontwikkeling van die paringstelsel van A uncinatus speeL A controversy exists over whether or not prolonged copula-tion has evolved through more than one suite of -"elective pressurcs (Thornhill 1984) and benefits males (e.g. Parkcr 1970; Sillcn TUllberg 1981; Dickinson 1986), females (e.g. Wilcox 1984) or hoth scxes (sec Walkcr 1980). Clark (1988) tested two alternative hypotheses to explain the adaptive significance of prolonged copulation in the water strider Gerris remigis. The data refuted a female foraging hypothesis where females prolong mating to avoid interfer-ence from other males, thereby improving their foraging effi-ciency; but supported a male mate-guarding hypothesis in which the mating periud but not genital joining is prolonged. However, implicit in both potential explanations are assump-tions concerning the roles of males and females in controlling mating time. These experiments could not determine which sex control-led copulation duration (Clark 1988). This knowledgc may have relevance in determining the sex-specific benefits of pro-longed copulation. For example. if it is advantageous to males to guard females, physical control of female movement would be an efficient mechanism particularly if achieved with minimal energetic cost to the male. There may also be bene-tits for the female though more likely there wi]] be an associ-ated cost which could lead tu a sexual conflict of interest with selection favouring discrimination and avoidance behaviour hy females especially if alrcady mated. Experiments that determine male and female effects on mating time may be difficult to design. and for many species observations alone are insufficient to make the distinction (but see Eberhard 1985). Consequently, mosl attempts 10 address this prohlem have been indirect, with a tendency to Reproduced by Sabinet Gateway under licence granted by the Publisher (dated 2009).S. Afr. J. Zool. 1994,29(4) focus more on the predictions of the adaptive hypotheses for prolonged mating rather than the assumptions implicit in them (e.g. Clark 1988). Previously we have shown that for the tropical millipede Allopoyus uflcinatus, copulation duration varies between pop-ulations (Telford & Dangerfield 199Ia). This population dif-ference allowed us to design a simple experiment to test the assumption that in A. uncinatus males control the duration or copulation. We predicted that if males control copulation then mating times for between population pairings should not differ significantly from mating times for the population from which the males originate. To test this prediction, we con-ducted experiments with pairings of males and females from the same populations as controls and between-population reciprocal crosses as treatments in a contingency design. Samples of surface active animals were collected hy hand from two widely separated geographic locations in Zimba-bwe; riparian forest near Mazowe (IT 30' S, 30" 57' E) and Bllrkea scrub in Hwange National Park (18" 44' S, 26" 55' E). Collections were made and experiments conducted during I'ebruary and Mareh 1989. Individual males and females were placed together in plastic pots (12 em diameter x 15 cm deep) containing a thin layer of moist soil. Courtship ensued followed rapidly by copulation. Copulation duration (min-utes) was measured from the moment the pair assumed the characteristic copula position (see HMord & Dangerfield 1991 h) to the time when the male and female separated. The copulation durations generated from these mating combinations are summarized in Table I. Within-population copulation durations showed that animals from Hwange mate for a significantly longer time than animals from Mal.owe (Mann-Whitney U test, U =757,5; P < 0.001; Table I). The results of he tween population reciprocal crosses generated copulation durations consistent with durations characteristic of the population from whieh males originated (Table I). Although females accepted males from both populations. the results of reciprocal crosses suggest that, in copula pairs of A. uncinatus males control the duration of copulation. These results lend support to the hypothesis that prolonged mating in A. utlcinatus is a form of mate guarding against sperm competition. In an earlier experiment we showed that mating time for A. wlcinatHs increases with increase in male bias in the opera-tional sex: ratio (OSR); a situation that mimics variation in the Table 1 Mean duration of copulation (minutes ± S.D.) in all combinations of matings. Sample sizes are given in brackets, Mann-Whitney U test pairwise comparisons are given at the ends of rows and columns MALES Mnzowe Hwange Mazowe J 22,7±49,4 J:>U.J±65,[ 756*** (35) (2."> FE~ALES Hwange IU4.4iJJ.7 205,8±60,H 1167*'"'" (23) (2S) J (nil' 676",' *"'*p < 0,00[; '" nul significant 267 intensity of competition between males for access to females (Telford & Dangerfield 1991 a) and we interpret this as a phe-notypic response to local changes in the intensity of intrasex-ual competition. These results, the results of the present study, and behavioural observations suggest that sperm competition is the process responsible for selection favouring the evolu-tion of this form of mate guarding. In A. uncinatus the exact nature of sperm competition is not known but the prerequi-sites exist: multiple mating. internal fertilization and sperm storage (Blower 1985; Telford & Dangerfield 1991a, b). Fur-thennore, during copulation male gonopods not only playa role in sperm transfer but also function in the displacement of sperm from previous matings (Barnett, Telford & de Villiers 1991, in press). Males achieve the copula position by coiling around the body of the female in a tight 'emhrace' (see figure I in Tel-ford & Dangerfield 1991b) and females rarely attempt to escape from a male once in copula. It is probably the unique nature of copulation in these animals which allows the male to exert some control over mating time. The reason why mat-ing pairs from the two populations differ in copulation dura-tion (in the ahsence of intrasexual competition) remains an interesting unanswered question. The Mazowe population breeds over a three-month period during summer under high population density conditions. Hwange animals breed over a shorter time and at a much lower population density. In the Mazowe population the OSR undergoes dynamic change (female biased to male biased, Telford & Dangerfield, in press) over the hreeding season. OSR conditions for the Hwange population remain unknown. If selection had favoured an increase in mating time in response to population density. then on average, Mazowe animals should mate for longer than Hwange animals. Our results show the opposite. However, considering the degree of female hias in the OSR of the Mazowe population over most of the breeding season. then the benefits of prolonged mating may he outweighed hy the costs in terms of lost additional mates encountered (Alcock, pers. comm.). This selection to reduce mating time may he responsihle for the shorter duration matings in the high density Mazowe population, compared to the low den-sity Hwange population. This study does not attempt to test the hypothesis that pro-longed mating in A. ullcinatus has evolved to reduce sperm competition. It docs, however, test the assumption implicit in this hypothesis that males may control copulation duration. Selection may favour this ability because of the evolutionary benefits a male derives from prolonged mating under condi-tions of intense intrasexual competition. However, mates andl or females can benefit from extended mating. Consequently, to fully understand the adaptive significance of prolonged copulation necessitates investigation of which sex controls its duration. Acknowledgements Tarombera Mwabvu, Busani Ndlcla and Charity Mckiyi helped with the collection of animals and execution of experi-ments. Financial support was provided by the University of Zimhabwe and logistical support by the Tropical Soil Biology and Fertility programme. John Alcock and Peter Adler pro-vided useful comments on an earlier version of the manu-SCflPt. Reproduced by Sabinet Gateway under licence granted by the Publisher (dated 2009).268 References BARNETf. M .. TELFORD. S.R. & DE VILLIERS. CJ. 1991. Ganopod morphology or the millipede Orthopoms {J)'rhocephallJs a possihle mechanism of sperm displacement. Proc. ELectron Micros. Soc. SA. 21: 179-180. BARNEIT.M .. TELFORD. S.R. & DE VILLIERS. C.l. In press Morphological evidence for sperm displacement in the millipede OrrhoponJs [lyrhoceplw/!J.s. 1. Zool. Lond. BLOWER, J.G. 1985. Millipedes. In: Synopses orthe British fauna. (eds) D.M. Kcrmack & R.S.K. Barnt:s, EJ. Brill. London, 242 pp. CLARK. SJ. 1988. The effects of operational sex ratio and food deprivation on copulation duration in the water strider (Cerri.I' remigis S<lY). Bchav. E'eo/. Sociohio!. 23: 317-322. DICKENSOl\", lL. \986. Prolonged mating in the milk-weed leaf heetle Labidomera divicollil" (Coleoptera: Chrysomelidae): a test of the 'sperm-loading' hypothesis. Behav. Ecol S(winhiol. 18 331-338. EBERHARD, W.G. 1985. Sexual Selection and Animal Genitalia. Harvard University Press, Massachusetts. PARKER, G.A. 1970. Sperm competition and its evolutionary consequences in the insects. BioI. Rev. 45: 525-567. S.-Mr. Tydskr. Dlerk. 1994.29(4) SILLEl\"-TULLBERG, B. 1981. Prolonged copulation: a male 'postcopulatory' stratcgy in a promiscuous species, Lyg(lel~.\ ('(JlU!.I·lri.\ (Hetcroptera: Lygaedae). Rehav. Eco!. Sociohio!. 9: 283-289. TELFORD. S.R. & DANGERFIELD. J.M. 1991a. Manipulalinn of the sex ratio and duration of copulation in the tropical millipede Allopoms ullcinalus: a test of the copulatory guarding hypothesis. Arlim. Behav. 40: 984-986. TELFORD. S.R. & DANGERFIELD. JM. 199 I h. Sex in millipedes: lahoratory ~tudies on sexual selection. 1. Rio!. Ed. 199 233-238. TELFORD. S.H.. & DAl'.""GERFIELO, J.M. In press. Mating tactics in a tropical population of the millipede Alloporus uncina/lH. Behaviour. THORNHILL, R. 1984. Alternative hypotheses for traits belin'cd to have evolved by sperm competition. In: Sperm Competition and the Evolution of Animal Mating Systems. (ed.) R.L. Smith. Academic Press, Orlando, pp. IS 1-17X. WALKER, W.F. 1980. Sperm utilization strategies in non-social insects. Am. Nat. 115: 780-799. WILCOX. R.S. 1984. Male copulatory guarding enhances female foraginginawaterstrider. Behav. Ecoi. Sociohio!. 15: 171-174. Reproduced by Sabinet Gateway under licence granted by the Publisher (dated 2009).

Males control the duration of copulation in the tropical millipede Alloporus uncinatus (Diplopoda: Julida)

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Males control the duration of copulation in the tropical millipede Alloporus uncinatus (Diplopoda: Julida)

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