Mating Systems and Sexual Dimorphism in Mass in Microtines

MATING SYSTEMS AND SEXUAL DIMORPHISMIN MASS IN MICROTINES

R. BOONSTRA, B. S. GILBERT, AND C. J. KREBS Division of Life Sciences, ScarboroughCampus, Universityof Toronto, 1265 Military Trail, Scarborough,Ontario, Canada M1C 1A4 (RB) Kluane Lake ResearchStation, Mile 1054 Alaska Highway, Yukon,Canada Y1A 3 V4 (BSG) Departmentof Zoology,The Universityof BritishColumbia, 6270 UniversityBoulevard, Vancouver, B.C., Canada V6T 2A9 (CJK)

Sexual dimorphismin body size is expected to vary as a function of mating system. Heske and Ostfeld (1990, J. Mammal.71:510-519) foundno differencein body-lengthdimorphism between the majorityof promiscuousand monogamousmicrotines. In five species we used body mass and in three species, length of body to test the robustnessof these findings. We found no significantdimorphism in length of body in any species, but significantdimorphism in body mass in all species, independentof mating system. We proposethat 1) mass rather than length is the measure needed to assess dimorphismin microtines,and 2) the bias in favor of large males should rank as follows with respect to mating system: facultative monogamy= polygyny > promiscuity> obligate monogamy.

Key words: Microtus, sexual dimorphism,mating systems, body mass

Sexual dimorphism is expected to occur rank as follows with respect to mating sys- when one sex competes for access to the tem: polygynous > promiscuous > monog- other (Darwin, 1871). In mammals, where amous. In contrast, in a comparative study the dominant mating system is polygyny on microtine species of the generaMicrotus (Kleiman, 1977) and where males do the and Clethrionomys, Heske and Ostfeld competing, they may obtain an advantage (1990) found the following rankingwith re- by being large (Reiss, 1989). Emlen and Or- spect to sexual dimorphism:polygynous > ing (1977) predictedthat the greaterthe po- promiscuous= monogamous.None of their tential for multiple-mate monopolization, monogamous species and only one of 12 the more intenseintrasexual selection should promiscuous species showed male-biased be and hence the greater the tendency for sexual dimorphism. Two of the promiscu- polygyny. Thus, knowledge of the mating ous species showed female-biasedsexual di- system should allow one to predict the de- morphism. These results are counter-intu- gree of sexual dimorphism: in polygynous itive and we believe they are incorrect mating systems, where one male has exclu- becauselength of body ratherthan mass was sive access to multiple females, selection used as a measure of sexual dimorphism. should cause dimorphism to be greatest;in a promiscuousmating system, whereno one METHODS male exclusive access to a may gain female, evidence to examine sex- should be and in We used two lines of dimorphism less; finally, ual in microtines.To avoid a where each dimorphism drawing monogamous mating system, conclusionsfrom comparisons in whichdifferent male has exclusive access to only one fe- aged cohortswere included,both our tests in- male, dimorphism should be minimal. volved examiningonly animalsthat had over- Therefore,the expectation is that sexual di- wintered.First, a populationof Microtuspenn- morphism (male/female body size) would sylvanicuswas intensivelylive-trapped at the

J. Mamm., 74(1):224-229, 1993 224 February1993 BOONSTRAET AL.-SEXUAL DIMORPHISM IN MICROTINES 225 onset of breedingand the mass of males and pennsylvanicus,is known to have a mating femalesdetermined. The majordisadvantage of system with female territorialityand male usingmass from live-trapped animals to assess promiscuity (Boonstra and Rodd, 1983; is thatthe of dimorphism earlystages pregnancy Madison, 1980; Ostfeld et al., 1988; Web- cannotbe detectedand hencemay makemales ster and Heske and Ost- and femalesmore similarthan are. Brooks, 1981), yet they really feld's results indicate that this However,if dimorphismwere to be found in (1990) spe- spiteof thisbias, it wouldonly serve to strength- cies is monomorphic with respect to length. en the conclusionthat the sexes weredifferent Fig. 1 shows the distributionof body masses withrespect to mass.From March to May 1983, of field-capturedvoles on 30 March 1983, a dense population of M. p. pennsylvanicuswas excludingobviously pregnantfemales. Males live-trappedweekly for 2 days/weekat a sitenear (X = 47.9 g, SD 6.09, n = 105) were sig- Toronto,Ontario, and females were removed near nificantlyheavier than females (X = 39.9 g, theend of pregnancyto allowparturition to occur SD 4.91, n = 86)(t = 9.86, d.f = 189, P < in the laboratory.Thus, we knewthe pregnancy 0.0001). The male:femaleratio is thus 1.20:1 statusof most femalesand hencewere able to compared with that of between 0.99:1 and minimizethe effectof pregnancyon bodymass. 1.04:1 for the three subspecies obtained by Breedinghad not occurredthe previouswinter and sincealmost no animalssurvived to breed Heske and Ostfeld (1990). Our study thus in 2 differentyears (Cockburn, 1988), the voles indicated a pronouncedsexual dimorphism presentin Marchmust have been born in the in this promiscuous species. Second, signif- previoussummer and autumnand thus were icant sexual dimorphism in mass, but not similarin age. Whentrapping started in March length, occurred in all species examined only 10%of themales were in breedingcondition throughautopsy (Table 1). Thus, males were and none of the females were pregnant. By 30 significantlyheavier than females in all spe- March, 96% of the males were in breedingcon- cies independent of mating system. These ditionand 6%of the femaleswere pregnant.No results are similar to those found by Dews- other females had a litter before 14 April. bury et al. (1980) in a laboratory study of Second,we collectedsamples of four species animals in three species of Mi- of voles and performedautopsies, thus allowing equal-aged crotus. us to subtractthe contribution of pregnancyto body mass in females. In the southern Yukon, Therefore,we believe that Heske and Ost- we obtainedsnap-trap samples ofM. oeconomus, feld (1990) used the wrong index to assess M. pennsylvanicus,and C. rutilus from 1974- sexual dimorphism in microtines. All stud- 1977(see Krebsand Wingate, 1985 for details). ies that we know of in microtines indicate Only overwinteredanimals collected in spring mass is the crucial measure and the consis- (April-June)were included in the analysisand tent result is that heavier males are domi- springsamples were pooled. In southernBritish nant or have greaterbreeding success than we obtaineda of over- Columbia, largesample lighter males (Kawata, 1988; Sheridanand winteredM. townsendiifrom 6 Marchto 29 April Turnerand 1974 1976for de- Tamarin, 1988; Iverson, 1973). usinglive-traps (see Boonstra, none of these studies mea- tails).In bothstudies, plusuterine mass Unfortunately, embryo sured of so weretaken in pregnantfemales and this was sub- length body, a similar assess- tractedfrom total mass to obtain body mass ment is not possible. Other species of mam- comparableto thatof males.In theformer study, mals show the same advantage of being lengthof body(excluding length of tail)and body heavier (e.g., Mus musculus-Franks and masswere recorded; in thelatter study only body Lenington, 1986; Cervuselaphus-Clutton- masswas recorded. Brock et al., 1982; Sciurus vulgaris-Wau- ters and Dhondt, 1989). It is likely that the RESULTS AND DISCUSSION differences in the relationship between length Our two methods to assess sexual di- and body mass in males and females do morphism were consistent and showed the not occur until puberty, but thereafter an- same result. First, the meadow vole, drogenic and estrogenic hormones act to dif- M.. 226 JOURNALOF MAMMALOGY Vol74, No. 1 MICROTUS 16 PENNSYLVANICUS

U MALES FEMALES 12. [

c u 30 35 4 I45 50 55 60 65

BODY WEIGHTS - g FIG.1.--Distribution of body mass of a populationof M. pennsylvanicusfrom southern Ontario on 30 March1985. ferentiate between the sexes (Glucksmann, found by Heske and Ostfeld (1990), but also 1974; Widdowson, 1976; Wilson and Fos- contraryto our prediction that polygynous ter, 1985). Androgens working in conjunc- species should have the largestmales. Why? tion with growthhormone are known to have The generalityof our conclusions could be an additional anabolic effecton protein syn- strengthenedby includingmore specieswith thesis, causing increasedprotein deposition various mating systems. However, we pro- to all partsof the body, especiallyto skeletal pose that for microtines, a largersample of muscle and cartilage. Our results indicate species will show the followingtrend in sex- that in adult breeding microtines, length of ual dimorphism with respect to mating sys- body is similar in both sexes, but males are tem: facultative monogamy = polygyny > more robust. promiscuity > obligate monogamy. A mo- The most pronounced sexual dimor- nogamous and a polygynousmating system phism in mass occurred in M. townsendii, are closely related if the males can switch a species that primarily is monogamous between either tactic and thus selection (Lambin and Krebs, 1991). The least-pro- should operate to give largermales a com- nounced sexual dimorphism in mass oc- petitive advantage if polygyny is a possi- curredin C rutilus,a promiscuous species, bility. Monogamyis known to occurin three which Heske and Ostfeld (1990) found to Microtusspecies, but in at least two of them exhibit female-biased sexual dimorphism. it is facultative. Lambin and Krebs (1991) Thus, our rankingof sexual dimorphism in found that althoughmonogamy was the pre- mass relative to mating system was as fol- dominant mating system in M. townsendii lows: monogamous > polygynous > pro- in spring,polygyny increased in summer. In miscuous.These resultsare contrary to those M. ochrogastermonogamy is the main type TABLE1.- The between and sexual in and mass -t SD) in three Microtus C relationship mating system dimorphism length of body (X species of C and one species of Clethrionomys. z rJ, Lengthof body (mm) Female Body weight (g) Mating Female til Species n Females n Males ratio Female Male ratio system References H M. p. alcorni 40 106.9 ? 7.7 43 109.9 ? 6.6 1.03 25.8 ? 5.9 28.7 ? 5.7* 1.11 promiscuous Madison, 1980; r Boonstraand Rodd, 1983; Ost- feldetal., 1988; Websterand Brooks, 1981 M. oeconomus 18 111.3 + 9.2 24 111.7 ? 5.9 1.00 24.4 ? 5.4 29.0 ? 5.5** 1.19 polygynous Lambin et al., 1992; macfarlani Tast, 1966 C M. t. townsendii 70 - 58 - 40.9 + 6.8 53.9 ? 7.9*** 1.32 monogamous Lambin and Krebs, 1991 rJ, C rutilus 169 102.6 ? 7.1 220 101.6 ? 4.5 0.99 23.4 ? 5.0 24.4 ? 3.2* 1.04 promiscuous Bums, 1981 dawsoni * P < 0.05, ** < 0.01, *** < 0.001. C) 0 H

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