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(3) SS 3XEOLVKHGE\The University of Chicago PressIRUThe American Society of Naturalists 6WDEOH85/http://www.jstor.org/stable/20491518 . $FFHVVHG Your use of the JSTOR archive indicates your acceptance of the Terms & Conditions of Use, available at . http://www.jstor.org/page/info/about/policies/terms.jsp JSTOR is a not-for-profit service that helps scholars, researchers, and students discover, use, and build upon a wide range of content in a trusted digital archive. We use information technology and tools to increase productivity and facilitate new forms of scholarship. For more information about JSTOR, please contact support@jstor.org.. The University of Chicago Press and The American Society of Naturalists are collaborating with JSTOR to digitize, preserve and extend access to The American Naturalist.. http://www.jstor.org.

(4) VOL.. 173, NO.. 3. THE AMERICAN. NATURALIST. MARCH. 2009. Testosterone Levels in Dominant. Sociable Males Are Lower. than in Solitary Roamers: Physiological Differences between Three Male Reproductive Tactics in a Sociably Flexible Mammal Carsten Schradin,l,2 Michael. Scantlebury,3 4 Neville Pillay,2 and Barbara Konig'. 1. Institute of Zoology, University of Zurich,Winterthurerstr. 190, 8057 Zurich, Switzerland; 2. School of Animal, Plant, and Environmental Sciences, University of theWitwatersrand, Private Bag 3,Wits 2050, Johannesburg, South Africa; 3. Quercus, School of Biological Sciences, Queen's University Belfast, Belfast BT9 7BL,Northern Ireland; 4. Mammal Research Institute, Department of Zoology and Entomology, University of Pretoria, Pretoria 0002, South Africa SubmittedMay 17, 2008; Accepted September 30, 2008; Electronicallypublished January 29, 2009. ABSTRACT: The relativeplasticity hypothesis predicts that alternative tactics are associated with changes in steroid hormone levels. In species with alternative male reproductive tactics, the highest an drogen levels have usually been reported in dominant males. How ever, in sociable species, dominant males show amicable behaviors to gain access to females,which might conflict with high testosterone levels.We compared testosterone, corticosterone, and restingmet abolic rate in male striped mice (Rhabdomyspumilio) following a conditional strategywith three different reproductive tactics: (i) phil opatric group-living males, (ii) solitary-living roamers, (iii) dominant but sociable group-living territorial breeders. Philopatrics had the lowest testosterone but highest corticosterone levels, suggesting that theymake the best of a bad job. Dominant territorialbreeders had lower testosterone levels than roamers, which have a lower com petitive status. Roamers had the highest testosterone levels,which might promote risky behavior, such as invading territories defended by territorialmales. Roamers also had lower restingmetabolic rates than either type of group-living males. Our results suggest that dom inantmales' testosterone levels reflect a trade-off between low tes tosterone amicable behavior and high testosterone dominance be havior.. fitness. (Shuster and Wade. low competitive. 1991) or on individuals with. status making. the "best of a bad. job". (based on status-dependent selection; Thornhill 1981; Gross. 1996; Koprowski. 2008; Taborsky et al. 2008). Within. social vertebrates, tacticsemployedmight includebeing a dominant territorialbreeder, satellite, roamer, or helper (e.g., Reyer et al. 1986; Young al. 2008; Taborsky. et al. 2008). et al. 2007; Scantlebury and depend. et. on the indi. vidual's assessment of the relative inclusive fitness gains given itscurrentenvironmental,social,physical,and phys iological status (Clutton-Brock 1989). While. some attention. has been given. to the ultimate. (evolutionary)significanceof alternativereproductivetac tics (e.g., Sinervo. et al. 2000; Tomkins. and Brown. 2004),. less is known about the proximate (e.g., physiological) factors underlying. these tactics (Gross 1996; Oliveira. et al.. 2008). Differences in display or fightingbehaviormay re quire substantialdifferences in energy investmentbetween individualsfollowing alternativetactics (e.g.,Kenagy et al.. 1989; Boonstra et al. 2001). In several bird species, the Keywords: Rhabdomys, corticosterone, RMR, helper, group living, most dominant or sexually active individuals generally in flexibility. cur the greatest energy costs (reflected in elevated resting metabolic. rates [RMRs]; Hogstad. 1987; Buchanan. et al.. 2001) and thehighest circulatingtestosteronelevels (Evans Introduction. et al. 2000).. Alternativemale reproductivetacticshave been described in a number of vertebrate. taxa. Such an intraspecific poly. morphism can be based either on frequency-dependent selection *. resulting. Corresponding. in alternative. 0003-0147/2009/17303-50465$15.00. 10.1086/596535. (C2009 by The University All. rights reserved.. relationships. are presumed. to occur. "agonistic interactions with high overall activity levels that act to increase energy expenditures and the need for food" (Vezina and Thomas 2000, p. 231). In mammals, there is convincing. evidence. that physiology. and energetics. play a. dominant role in alternativetactics (Koprowski2008). For. author; e-mail: carsten.schradin@zool.uzh.ch.. Am. Nat. 2009. Vol. 173, pp. 376-388. DOI:. tactics that yield the same. These. because reproductivesuperioritymay necessitate increased. of Chicago.. example, Damaraland mole rats pursue either infrequent or frequent worker tactics as determined by their. worker. level of energy expenditure. (Scantlebury. et al. 2006a)..

(5) Testosterone. ulation of alternative male ture of both. to contribute. are expected. Steroid hormones. reproductive. tactics as the na. breeding. avian and mammalian. to the reg is. systems. proximately regulatedby temporalpatterns of androgen secretion (Wingfieldet al. 1990).Androgensmay increase male. aggression, mate. mate. searching. attraction,. and copulation. and. the frequency. but negatively. of. affect pa. rental care (Wingfield et al. 1990). Dominant breeders typicallyhave higher testosterone levels than sneakersor satellites (Moore 1991; Moore et al. 1998; Sinervo et al. 2000; Wikelski et al. 2004; Oliveira et al. 2005; Knapp and. Neff 2007).Most studies show a synchronous increaseof energy expenditureand testosterone level (e.g.,Buchanan et al. 2001), suggestingthat increasedreproductiveactivity is energeticallycostly (GittlemanandThompson 1988). In comparison, glucocorticoids influence reproductivebe havior by regulating. the availability. of energy by influ. encing glucogenesis and fat and protein metabolism (ReederandKramer 2005). Thesemetabolic processesare reliableindicatorsof energeticallydemanding, stressfulsit uations. (Romero. 2002; Reeder. and Kramer. 2005),. but. in Dominant. Sociable Males. 377. with aggressivehigh-testosterone behaviors, suggesting a trade-offbetween aggressionand amicability in dominant group-livingmales. Concerning corticosterone,Moore et that stress might play an important one tactic is inferior to another but not when. al. (1998) predicted role when. different tactics yield identical fitness payoffs. Conse quently, corticosterone levelswill be increasedin individ uals that follow a best of a bad job tactic (Koprowski 2008).. In the Succulent Karoo, African stripedmice (Rhab domyspumilio) typicallyformextended familygroupswith one breeding male,. up to four breeding females, and sev and females that do not breed. eral adult philopatric males. in the group (Schradin and Pillay 2004b). Groups can contain up to 30 adult individuals of both sexes (Schradin and Pillay 2004b). Striped mouse males follow one of three. tactics: (i) group-living philopatricsor (ii) solitary-living roamers that are thought to sneak copulations. from females. groups that are defended by (iii) group-living amicable territorial breeders (Schradin and Pillay 2003, 2004b, 2005b; Schradin 2004). Males of all three tactics. of communal. are thought. to seek copulations. with. females,. and pre. their influenceon alternativereproductivebehaviors and. liminary resultsof genetic paternity analysis support that. RMR remain unresolved (Buttemer et al. 1991). One sug gestion is that in group-living animals, dominant individ. expectation, with the majority of offspring sired by ter unpub ritorial males (C. Schradin and A. Lindholm,. uals suppressthe reproductionof subordinatesby inducing chronic stress, resulting in sustained high levels of glu cocorticoids in the subordinates:the "physiologicalcas. lished data).. and Sa tration" hypothesis (Reyer et al. 1986; Wingfield polsky 2003). However, it is not always the lower-ranking individuals that have the highest gluco or subordinate corticoid levels since the secretion of these hormones de. showing a cor philopatrics of care alloparental (Schradin and Pillay responding degree in any parental care 2004b), and roamers not engaging. pends on whether high stress levels are a consequence of (Creel 2001; subordinate rank or a cost of dominance. more. Romero 2002). Moore (1991)proposed the relativeplasticityhypothesis. or sitting in body contact (Schradin and allogrooming Pillay 2004b). In contrast, roamers live solitarily and do. to explain. the proximate. regulation. of alternative male. reproductivetactics.According to this hypothesis, orga (nonreversible) hormonal effects are expected to occur during early development when different tactics are fixed and yield the same average fitness. In contrast, activational (reversible) effects may occur in adults when. nizational. different tacticsyield different fitnesspayoffs, indicatinga conditional strategy (Moore et al. 1998). In all fish and reptile species studied to date, dominant males show the highest level of aggression and the highest androgen levels (Moore 1991; Moore et al. 1998; Sinervo et al. 2000; Wi kelski et al. 2004; Oliveira et al. 2005; Knapp and Neff however, domi 2007). In some group-living mammals, nant males engage in amicable behaviors in which they court females by grooming them, sitting in body contact, or providing them with food (Stopka and Graciasova 2001; 2003; Kutsakake and Clutton Schradin and Anzenberger Brock 2006). This strategy might potentially be in conflict. The three male territorial breeders (Schradin. tactics differ in caregiving behavior, with showing a high degree of paternal care. and Pillay 2003),. (Schradinand Pillay 2005b). Territorialbreeders initiate amicable behaviors. than other group members,. and. philopatricsoften engage in amicable interactions,such as. not participate in amicable relationships.Therefore the to examine offers a useful opportunity striped mouse whether amicable dominant males (the territorial breed ers) have lower testosterone levels than males of a sub dominant, nonsocial, solitary-living tactic. If too high tes. tosterone hinders amicability, territorialbreederswould have intermediate levels, even if it is the most competitive, dominant tactic. Group-living philopatrics would have the lowest and solitary roamers the highest testosterone levels. In this study, we explored the following question and and in a species exhibiting two group-living predictions tactic: (i) Is the observed behavioral solitary-living in male striped mice based on status polymorphism dependent selection (Gross 1996)? To answer this question tactics of individual we documented the reproductive one. over the course of several breeding seasons. Thus, and how often males aimed to quantify whether. males we. switched between. tactics and whether. switching was cor.

(6) 378. The American Naturalist. town, South Africa) for individualrecognitionduring be havioral observations (described in detail in Schradin and (Schradin2004). (ii)Circulating testosteroneshould differ between the alternativetactics,with lowest levelsobserved Pillay 2004b). an indicator of competitive. related with body mass,. If dominance. in philopatrics.. status mainly. ability. depends. on. testosterone, territorialbreederswill have the highest lev els. If, however, high testosteroneconflictswith amicable roamers are expected. behavior,. to have the highest. levels.. (iii) Corticosterone levelswill be highest in philopatric follow a best of a bad job tactic. They are stress as a conse physiological. males, which. to experience. expected. of being. quence dispersal. forcing. subdominant. containing. to high costs of. (Schradin 2005). rate will be highest in territorial. (iv) Resting metabolic breeders, which. and due. them to remain natal. a territory. are sexually active and defend. a group of communally. breeding. females.. Home. range sizes of 10 philopatric males,. breeding males,. ing the six breeding seasons for 2002-2007 during Sep tember toNovember.All radio-trackedmales were scrotal. Individualswere equippedwithMD-2C radio transmitters (Holohil, Ontario,. Canada). as 95% minimum. convex polygons. 6 for best comparison. and Methods. The study was conducted from 2005 to 2007 in Goegap in the Northern Cape Nature Reserve near Springbok. Province, South Africa (41.56?S,1.60?E).Additional data for home. ranges are included for 2002-2004. The area is an average rainfall of 160 mm per annum. The. vegetation type is classified et al. 1999).. as Succulent. in the program Ranges. with previous. studies (Schradin and. as philopatric. if they had previously. Pillay 2004b, 2005b). We classified males. (<30 g) and were observed. dur. ing the study as adults at the same group. Roaming males were classified as adult males that did not share nesting sites with any other mice. Territorial-breeding males were. Study Area and Period. arid, with. and radio tracked as described. elsewhere (Schradinand Pillay 2005b) to determinehome ranges and sleeping sites.Home rangeswere determined. been trapped as juveniles Material. 39 territorial. and 31 roaming males were collected dur. Karoo. adult males. that lived in groups. groups.. The. last were. groups,. and each communal. always. other. than their natal. the heaviest males. of the. group had only one. terri. torial-breedingmale (see "Results").. (Cowling. Blood Collection Study Species Blood Striped mice are diurnal, inhabit an open habitat, and are readily habituated to the presence of observers, which al. samples. for this study were. collected. during. the. 2005-2007 breeding seasonsduringAugust toNovember. Mice. were. trapped. at their nests. during. the morning. lows direct behavioralobservations in the field (Schradin shortly after they became active, controlling for possible 2006). The breeding season of 3-4 months occurs in spring (two to three litters per female; Schradin and Pillay 2005a) and depends on rainfall. In our study, breeding took place from August to October in 2006 and from September to December during 2005 and 2007.. Determination. of Male. Tactics. striped mice may become sexually mature at 4-6 weeks of age, with a body mass of 20-30 g (Brooks 1982). In our study, only males with a body mass above 30 g and that were older than 6 weeks were considered. Male strat. Male. egies were determined havioral observations, done. around. nesting in Schradin. by a combination of trapping, be and radio tracking. Trapping was as sites at least 3 days per month. and Pillay (2004b). Trapped mice were weighed and sexed; males were recorded as scrotal (testes descended) or not (testes inside the body); and all mice were permanently marked with ear tags (National Band and Tag, Newport, KY) and hair dye (Rapido, Pine described. circadian rhythms of hormone release. Traps were watched from a distance of 10 m. As soon as amale entered a trap, he was removed and anesthetized with diethyl ether (val idated in Schradin 2008b), a blood sample was taken from the retro-orbital sinus (without any damage to the eye; Schradin and Pillay 2004a), and the body mass, identifi cation (ID), and whether the male was scrotal were noted. Using this protocol, samples could be collected within 1.5 3min after amouse entered a trap, which did not influence basal corticosterone. levels (see "Results"). Additional traps set at a second nest and striped mice were sampled 45 min later, which meant that individuals would have. were. spent up to 45 min in the traps before being sampled. This was done to obtain further samples for testosterone testosterone val (but not corticosterone) measurements; ues are not influenced by this trapping procedure (Schra din 2008b and "Results"). Blood samples were left at room temperature for 1.5 h (indoor temperatures below 20?C) to clot and then centrifuged for 10 min to obtain serum for analysis..

(7) Testosterone. HormoneAssays All. samples were. analyzed. in the EIA. (Enzyme. Immu. noassy) laboratoryof the Zoological Institute,University of Zurich. Commercial. kits from IBL (Immuno Biological. Laboratories)Hamburg were used for corticosteroneand testosterone. We followed theprocedures listed in theman uals of the kits, but due to very high corticosterone levels, samples were diluted 1: 50 or 1: 100. In some cases, the. available sample volume for testosteronemeasurements was too small and had to be diluted 1: 1 with the zero standard. Inter- and intra-assay variability was measured with pools from striped mouse serum left over from sam ples used for this study. Three pools were used to deter. mine interassayvariabilityfor testosterone(pool 1: 12.8%, N =. 7; pool 2: 19.1%, N =. 4; pool 3: 7.3%, N = 4), and. two of them were also used for intra-assay variability (pool 1: 9.9%, N = 8; pool 2: 6.9%, N = 8). Two pools were. used to determine interassayvariabilityfor corticosterone (pool 1: 15.8%, N = 12; pool 2:14.4%, N = 12), and one of these pools was used to determine intra-assay variability (pool 1: 8.0%, N = 8).. InOctober 2006,we determinedRMR of sevenphilopatric males, 10 roaming males, and 10 territorial-breeding males. No blood samples were taken from these males on the were taken to avoid an days when RMR measurements influence of stress on RMR; RMR was determined. as the. minimal oxygen consumption (mLO2/h), as described in In brief, we used an system with a 1,610-cm3 met abolic chamber set at 31.0? ? 0.5?C, which is within the zone of this species (Scantlebury et al. thermoneutral 2006b). Dried air was pumped into the chamber at a rate of 500 mL/min, and depressions in oxygen concentration were 0.25%-0.4%. Readings were taken every 30 s for 20 min after an initial hour, when animals were accustomed to the chamber (Bennett et al. 1992). The mean of the detail by Scantlebury. et al. (2006b).. open circuit respirometry. lowest 10 readingsof oxygen consumption (mLO2/h)was taken as RMR when. animals were. Data Analysis. seen to be at rest.. Sociable Males. 379. Satterthwaitemethod. Effectswere tested using Type III (simultaneous)modeling; that is, inmultiple effectsmod els, parameters for each independentvariablewere cor rected for all other fixed effects in themodel. Differences between the least squaresmeans (function LSMEANS in SAS) of multiple categories were compared post hoc using t-tests, and all P-values stated are given after a Tukey. Kramer adjustment formultiple comparisons. For each male. trapped at the beginning. of a breeding. season (October 2005, N = 67; September 2006, N = 27; and September2007,N = 16),we determined its cur rent, previous,. and next. tactic. This could not be deter. mined for every male, as many philopatrics disappeared (either due to mortality or dispersal; table 1), and several. males immigrated into roaming and territorial-breeding the study area from elsewhere, so that we did not know their previous tactic. For each male, its month of birth was estimated from body mass at the first trapping event, using a population-specific growth curve available from 7. years of field studies (C. Schradin,unpublished data). For comparison using. between. body mass. and age of males. tactics, we used data collected of the breeding season. Body mass. the three different the first month. during RMR Measurements. in Dominant. and age were compared between the three tactics at the start of the 2005-2007 breeding seasons using two GLMMs with year as a random effect. Age data were log trans formed to meet. the criterion of a normal distribution.. tactic for each male was determined male. switched. with. its original. every month.. The If a. from the tactic it had followed at the start of the breeding season to another tactic, we compared its age and body mass in the month when it changed tactics age and body mass. at the beginning. of. the breeding season. Home. range data were analyzed using a GLMM in the observed tactic (philopatric, roamer, or terri torial breeder) was a fixed effect and year a random effect. Home range data were log transformed before analysis to meet the criterion of normality. which. To explain corticosterone and testosterone levels, GLMMs were fitted to the data set. Tactic, whether males were scrotal, whether males carried a transmitter, and whether traps were watched (and checked immediately) or checked 45 min after they were set (only for testoster one) were entered as fixed categorical effects into the model. The time it took to take the blood sample (in. and Statistics. The software packages Instat 3.05 and SAS 9.1.3 were used. Data are presented asmean ? SD. Correlations were done using Spearman correlations coefficient r,.General linear. seconds), body mass (in grams), and age (in months) were entered as covariates into the model. Year was included as. distributedwhen Shapiro-Wilk statisticsyielded P> .05.. random factor. Hormone data were log transformed before analysis. The current data include samples used for another study (Schradin 2008b) and additional data collected over 2007, as well as data for roaming males. For basal corti costerone, we had 62 blood samples from 54 individuals.. Error degrees of freedom. For testosterone, we had 134 blood. mixed models. (GLMM) were. fitted to normal data using. restrictedmaximum likelihood (SAS,procedureMIXED). In all GLMMs,. residuals were accepted (df) were. as being normally. calculated. using. the. samples from 100 in.

(8) The American Naturalist. 380. Table 1:Number of male striped mice that switched reproductive tactics at any time during the breeding season To. 2005. Juvenile Juvenile Juvenile. Territorial breeder Roamer Philopatric. 0 0 47. Total juveniles Philopatric Philopatric Philopatric. Roamer Territorial breeder Disappeared. Total philopatricsb Roamer Roamer Roamer. Territorial breeder Philopatric Disappeared. Total roamersb Territorial breeder Territorial breeder Territorial breeder. Philopatric Roamer Disappeared. From. 2006. 2007. Total. 0 0 5. 0 0 0. 0 oa 52. 7 9 37. 7 9 4. 5 6 0. 52 19 24 41. 3 0 9. 6 0 5. 3 0 6. 84 12 0 20. 0 0 10. 0 0 12. 0 0 7. 32 0 0 29. Total territorial breedersb for adult males. Note: Data the previous. at the start of the 2005-2007. tactic used by philopatrics,. aJuvenile males 1980; Schradin. becoming that switched. seasons. Data for juvenile males were obtained. breeding. reaching adulthood. are regularly observed. and Pillay 2005b) but were not observed from philopatric. to roamer before disappearing. to territorial breeder and then disappeared to territorial breeder and then disappeared. total number. of individuals. sampled.. are included are included. for both philopatrics for both. If an individual was. per individual (nine individualsfor testosteroneand four In all other cases, we only for corticosterone). the last measurement per individual and discarded. individuals. all others (14 individuals for testosteroneand four indi for corticosterone).. We used the last instead of the. first samplebecause individualswere oftenmeasured first as philopatric, the class for which we already had more samples than for roamers and territorial breeders. If we had chosen to use the first sample only, to discard all data or to use all sam from males with several measurements, ID as a random factor, statistical have been the same, which means our results robust with respect to data point selection.. ples and use individual results would were. and roamers; 16 males. Results in Home Range Size, Body Mass,. between Males. Following. and Age. the Three Tactics. of the three tactics differed significantly in their measured home range size (F = 12.65, df = 2, 73.9, P < .0001; fig. 1). Philopatric males had significantly smaller home ranges than roaming males (t = -4.64, df = 74.7,. Males. that switched. and territorial breeders; six males. (Perrin. switched from. from philopatric. that switched from roamer. P < .0001), and there was a nonsignificant that home. ranges were (t =. breeding males. smaller. trend indicating. than those of territorial. -2.26, df =. 72.6, P =. .068). Roam. ers had significantly largerhome ranges than territorial breeders At. (t =. -4.09,. df =. 74.9, P =. the start of the breeding. .0003).. season, philopatrics. were. than either roamers or ter likely to be nonscrotal ritorial breeders (15 of 52 philopatric males were non. more. scrotal, while. all 29 roamers and all 29 territorial breeders scrotal; P = .0007, Fisher's Exact Test,. we handled were. for both comparisons). Scrotal philopatricswere signifi cantly heavier. than nonscrotal. N = 37 vs. 32.7 ?. philopatrics. 1.9 g, N =. (40.1 ? 6.9 g,. 15; t = 4.02,. df =. 50,. P = .0002). Males mass. of the three tactics differed significantly. at the beginning. df = 2,107, P<. Differences. of striped mice. roamers and territorial breeders.. repeatedly within the same variable (social tactic, scrotality, carrying a transmitter or not), we used the mean. viduals. in grassland populations. in our study.. for both philopatrics. sampled. used. post hoc by examining. season.. to roamer to territorial breeder are included for all three tactics; 10 males. and are included. The sample size in this study was based on the. dividuals.. at the start of the breeding. roamers, and territorial breeders. roamers when. 2005; Schradin. bSeven males philopatric. 29. of the breeding. season (F =. .0001; fig. 2A). Philopatric males. in body 75.16, (38.0 +. 6.8 g) were significantly lighter than both territorial-breed df = 106, P< ing males (60.7 ? 6.8 g; t = -12.19, .0001) and roaming males (52.2 ? 7.1 g; t = -7.30, df = 106, P<.0001), and roaming males were signifi males (t = 4.85, cantly lighter than territorial-breeding df = 105, P< .0001). Males of the three tactics differed significantly in age at the beginning of the breeding season (F = 27.30, df =. 2,106, P< .0001). Philopatricmales (3.9 ? 1.9months).

(9) Testosterone. in Dominant. Sociable Males. 381. p=0068 3.0 -. 31. 2.5. *. 2.0. U) 0)1.5. 3. E E1.0 zT. 0. ~~ 0.5-10. ~~~1. _. ,. 0.0 ,. Roamer. Philopatric. Figure. 1: Home. range sizes of philopatric,. roaming,. Territorial breeder. striped mouse. and territorial-breeding. males. Mean. ?. SD;. sample. sizes are provided. above. bars. Four asterisks,P < .0001.. were significantly younger than both roaming males t = -5.14, df = 107, P< .0001) and (8.4 ? 2.9 months; t = -7.20, territorial-breeding males (10.4 ? 2.7 months; df = 107, P<.0001). Roaming males did not differ sig. nificantly from territorial-breeding males (t = 2.04, df =. t=. -5.88,. df = 66, P<.0001).. However,. philopatric. males that became territorialbreeders did not differ in body mass from roaming males that became territorial breeders (59.5 ? 6.6 g vs. 60.9 ? 5.2 g; t = -0.61, df = 66, P = .82).. Males differed significantlyin agewhen switching from. 105, P = .11). A GLMM with. tactic as the response variable could not determine whether age or body mass was more important. one tactic to another, depending on their previous and tactics (F = 19.45, df = 2,63, P<.0001). subsequent. in predicting the tactic, as both were significant (body Philopatricmales thatbecame roamerswere significantly younger than philopatricmales that became territorial. mass: F = 21.24, df = 1, 105, P< .0001; age: F = 15.70, df = 1, 59.3, P = .0002), as was their interaction (F = 11.77, df = 1, 100, P = .0009).. t= breeders (7.4 ? 2.6 months vs. 10.1 ? 1.7 months; 4.34, df = 63, P<.0002). Philopatric males that became. roamerswere significantlyyounger than roamingmales that became territorial breeders (7.4 ? 2.6 months vs. 11.8 ? 2.4 months; t = -5.67, df = 63, P< .0001). How. TacticSwitching We never observed juvenilesbecoming roamersor terri torial breederswithout first becoming adult philopatrics (table 1). Philopatric males either disappeared (49%; pre sumably due to predation or by emigrating into areas out side the study area) or became roamers (23%) or territorial. breeders (28%;table1).Roamers eitherdisappeared(63%) or became. territorial breeders. (37%; table 1). All territorial. ever,philopatricmales thatbecame territorialbreedersdid not differ from roaming males that became territorial breeders (10.1 ? 1.7 months vs. 11.8 ? 2.4 months; t= -1.99, df = 63, P = .12).. Hormonal. Differences. between Male. Tactics. breeders (100%) disappearedwithout being observed to Nonscrotal philopatrics (N = 38) did not differ signifi change. their tactics. (table. 1), although. two territorial. breeders changed groups before disappearing. Males switching from philopatric nificantly lighter than males changing territorial breeder (48.1 ? 7.7 g vs. 5.99, df = 66, P<.001). Philopatric. to roamer were sig from philopatric to 59.5 ? 6.6 g; t = males that became. roamerswere significantlylighterthan roamingmales that became. territorial breeders. (48.1 ? 7.7 g vs. 60.9 ? 5.2 g;. cantly in testosterone levels (0.46 ? 0.3 ng/mL) from scro tal philopatrics (0.40 ? 0.3 ng/mL, N = 23; t = 0.68, df = 59, P = .50). Thus, we pooled scrotal and nonscrotal males for all following analyses, including scrotality as a. covariate.Serum testosteronelevelswere not significantly influenced by body mass (F = 0.55, df = 1,48.9, P = .46), age of individual (F = 0.18, df = 1,46.5, P = .67), method of sampling (whether traps were emptied imme.

(10) 382. The American Naturalist. A. 80 29 70. 29. 60 50. >. 0) 40 T E 20~~~~5. E _ _ _. 10 B so -. _. _. _. _. _. _. _. _. _. _. _. _. _. _. _. Territorial. Roamer. Philopatric. _. breeder. 231. 70. 31. 60 50. ~20 10 0 Philopatric. to roamer. Philopatric to territorial breeder. Roamer to territorial breeder. season and (B) when males switched males at the start of the breeding roamer, and territorial-breeding Figure 2: Body mass of (A) philopatric, three asterisks, P < .00 1; four tactic at any time during the breeding season. Mean ? SD; sample sizes are provided above bars. n. s., not significant; asterisks, P< .0001.. diately after capture or checked after 45 min; F = 0.22, df = 1, 43.9, P = .63), time needed to take the blood sam ple (F = 0.36, df = 1, 48.3, P = .55), whether males were scrotal (F = 0.02, df = 1, 48.5, P = .8), and whether mice were carrying a transmitter (F = 0.63, df = 1,47.1, P = .43). The only significant factor was tactic (F = 25.49,. df = 2,47.7, P<.0001). Stepwise exclusionof nonsignifi cant effectsconfirmedthese findings,with tacticremaining as the only. significant. factor (F = 41.29,. df = 2,55.0,. (F = 1.55, df = 1, 35.1, P = .22), and whether mice were carrying a transmitter (F = 2.20, df = 1,35.9, P = .15).. The only two significantfactorsinfluencingcorticosterone were body mass (F = 5.26, df = tic (F = 3.31, df = 2,35.6, P =. 1, 37.0, P = .03) and tac .048). Stepwise exclusion. of nonsignificanteffectsconfirmedthesefindings,with body mass (F = 8.46, df = 1, 40.9, P = .006) and tactic being significant (F = 10.79, df = 2,40.8, P = .0002). Heavier levels (rs = -0.73, N = males had lower corticosterone. P < .0001).Philopatricmales had lower testosteronelevels 54, P<.0001). Philopatricshad highermass-independent thanboth roamers(t =-8.74, df = 55.0, P< .0001)and corticosterone levels than both roamers (t = 4.64, df = territorialbreeders(t =-2.67, df = 55.0, P = .02),while 41, P< .0001) and territorial breeders (t = 3.33, df = 41, roamershad significantlyhigher testosteronelevelsthanter P = .005), while roamers and territorial breeders did not ritorial breeders (t =. -6.16, df = 55.0, P < .0001; fig. 3A).. differ significantly. (t =. 1.17, df = 40.3, P =. Basal corticosterone levelswere not significantlyinflu enced by age of the individual (F = 0.09, df = 1,36.9, P = .76), time needed to take the blood sample (F = 0.72, df = 1, 36.2, P = .40), whether males were scrotal. Resting Metabolic. .48; fig. 3B).. Rate. roamers, absolute values of RMR for philopatrics, and territorial breeders were 45.7 ? 8.8 kJ/day, 49.5 ?. Mean.

(11) Testosterone. in Dominant. 383. Sociable Males. A *. 6. E. 5. -*. .-. 44. -. 3. -. 0. 36**. 37. 1:. 61 0. Roamer. Philopatric. Territorial breeder. B. 3000-. _ E. 18. *. , 2500. **. 2000 2-. 0. 0. 1500. -. 11. ~~~. ~ _.U)1000. ns ~~~~~~22. I. ~E500 Roamer. Philopatric. Territorial breeder. 3: Comparisons of steroid hormone levels between philopatric, males. A, Testosterone roamer, and territorial-breeding levels; B, basal Figure corticosterone levels. Mean ? SD; sample sizes are provided above bars. n.s., not significant; one asterisk, P < .05; two asterisks, P < .01; three asterisks, P< .001.. 8.6 kJ/day, and 75.5 ?. 15.0 kJ/day. There were significant. differences inRMR betweenmales followingdifferent tac tics (ANCOVA; F =. 10.26, df = 2,23,. P =. (ANCOVA; F = 0.14, df = 2,21, P = .87), suggesting that the relationship between RMR and body mass was similar for all males. Post hoc tests revealed that there was. no significantdifferenceinRMRbetween territorialbreed ers and philopatric males but that roamers had signifi cantly lower RMR than both territorial breeders (P < .01) and philopatric males (P < .05; fig. 4). The least squares fitted regressions for RMR against body mass were as fol lows: territorial breeders (r2 = 0.43; F = 6.03, df = 1, 8, P = .04), (kJ/day) =. 1.9 + 1.22 x body mass. RMR. (kJ/day) =. -0.25. 0.43; F =. 3.76, df =. 1,5, P=. .11),. (g);. (1). (kJ/day) =. RMR. (g);. (g).. (3). philopatrics).Therewas no significantpositive correlation between RMR and corticosterone (rs = -0.67, N = 8, P = .08) or between RMR and testosterone (ri = 0.17, N = 9, P = .68).. Discussion Male striped mice in the Succulent Karoo begin adult life as philopatrics and can later switch to being roamers or. territorialbreeders.Tactic change depends on theirbody in turn correlates with. their success. in ter. ritorialencounters (Schradin2004). Different tactics are associatedwith differences in steroidhormone levels (fig.. 1,8, P<.001),. + 0.96 x body mass. 5.3 + 1.06 x body mass. rates and hormonal data were avail Resting metabolic able for five territorial breeders and four roamers (but no. mass, which roamers (r2 = 0.84; F = 42.41, df =. (r2 =. .001). How. ever, therewas no significant interactionbetween body mass and tactic (breeder/roamer/philopatric)on RMR. RMR. and philopatrics. (2). 5), which. is in accordance with. the relative plasticity hy.

(12) 384. The American Naturalist. 120. * breeder A roamer. 100. o philopatn'R *. >.. 80. Xe. 60. *. ,,. -o. -t.*. 40. 0~~~~ 20. 30.0. 40.0. 50.0. 60.0. body mass. (g). 70.0. 80.0. males Figure 4: Relationship between restingmetabolic rate (RMR;kJ/day) and body mass (g) of philopatric, roaming, and territorial-breeding (open circles,triangles,and filled circles,respectively).. pothesis proposed byMoore (1991).However, in contrast the breeding season (and not during the dry nonbreeding to previous studies on fish and reptiles (e.g.,Wikelski et season)predictswhether they remainphilopatric,switch to al. 2004; Oliveira et al. 2005), it is not the large dominant roaming,or switch to becoming territorialbreeders. males. but solitary. roaming males. that have. the highest. testosterone levels, suggesting that testosterone levelsde pend not entirely on status but also on the social tactic. employed.. to revert to roaming once status, although on two oc. casions breeders switched their groups. Theoretically, it may. A ConditionalStrategywith ThreeTactics Male striped mice follow a conditional strategy, which means that adults can change their tactic depending on. their status (Gross 1996). Status depends on body mass, which to some extent correlates positively with age during the breeding season but also decreases with age in the dry season (Schradin and Pillay 2005a). The competitive and social status is likely to be maintained by aggressive in teractions as heavier individuals are more likely to attack. lighter individualsthanvice versa (Schradin2004).Young males. Mice were never observed attaining a territorial-breeding. of low body mass. remain philopatric. in their natal. pay to revert to roaming if the fitness payoffs were greater (e.g., if the number of breeding females in a group decreases by predation). A short breeding season (2-3 months) and low mortality (Schradin and Pillay 2005a) might make such a scenario unlikely. When male striped mice in grassland populations reach adulthood, they be. come roamerswithout firstbeing adult philopatrics, and territorialbreedersdo not occur in thispopulation (Perrin 1980; Schradin 2005; Schradin and Pillay 2005b; fig. 5). In grasslands, striped mice live solitarily, and solitary breeding females are visited by roaming males (Schradin 2005). Thus, the philopatric tactic is not obligate for male. stripedmice. Territorial-breedingmales defend their harems from. group.With increasingbody mass, they change to either. other males, while. roamers or territorial breeders, with the switch to terri torial breeders occurring at a higher body mass than that to roamers. Roamers occur only during the breeding sea son, not during the nonbreeding season, when they either disappear or become group living by associating with a. Philopatricmales might also gain mating opportunities,. single breeding. female and her philopatric offspring (C. data). During the nonbreeding sea become solitary roamers but ben (Schradin 2005; Scantlebury et al. mass of philopatrics at the start of. Schradin, unpublished son, philopatrics never efit from group living 2006b). Thus, the body. roamers seem to follow a sneaker tactic.. as described for other species with subdominant male helpers (Double and Cockburn 2003; Young et al. 2007). Home ranges of philopatric male striped mice overlap with those of females from neighboring groups (Schradin and Pillay 2004b), and breeding females meet philopatric males from other groups during foraging (Schradin 2006). Our results predict that territorial breeders have the highest and philopatrics the lowest fitness, with roamers occupying an intermediate position (preliminary support exists for.

(13) Testosterone. PRL T p h i ,, p a t Roamer Territorial. PRL. ;_i. breeder. in Dominant. Sociable Males. 385. Succulent Karoo. RMR t. Juvenile. Succulent Karoo ?. \. ~~~~TS -. ~~~RMR. RMR. Grasslands Figure 5:Alternativemale reproductivetactics in stripedmice and correlatedphysiologicalchanges.Lightgray = philopatrics;darkgray= roamers; black =. territorial breeders; arrow =. upward. increase;. PRL = horizontal. prolactin;. T =. testosterone;. double arrow =. Cort =. RMR =. corticosterone;. stays the same; question mark. =. resting metabolic. predicted. change. When. rate; downward reaching. arrow = decrease;. adulthood,. male. striped. mice in the SucculentKaroo remainphilopatric in theirnatalnest (topandmiddle arrows).Philopatricscan become roamersfirst (toparrow),which is associatedwith an increase in testosteroneand a decrease in corticosteroneand RMR, before becoming territorialbreedersand experiencingan increase in prolactin (Schradin2008a) and RMR and a decrease in testosterone.Philopatricscan also directlybecome territorialbreeders (middle arrow),which is associatedwith a decrease in corticosteroneand an increasein testosteroneand prolactin (Schradin2008a). The situation in the grassland. striped mouse. population. is provided. for comparison. (bottom. arrow; Schradin. and Pillay. 2005b): males. become. and remain. roamers,. which is predicted to be associatedwith an increasein testosteroneand a decrease in corticosteroneand RMR.. this prediction. for 1 year; C. Schradin. and A. Lindholm,. unpublished data).. Differences. in Hormone. Levels and the Relative. Plasticity Hypothesis Our results are in agreement with the relative plasticity hypothesis (see fig. 5), which states that changes in be. havioral phenotypes during adulthood are regulatedby hormones. (Moore et al. 1998). It is known. that in species. with alternativemale reproductivetactics, the dominant males are most aggressive and have the highest androgen levels (Moore et al. 1998; Wikelski et al. 2004; Oliveira et al. 2005, 2008; Knapp and Neff 2007). However, in sociable. living roamers reflect a trade-offbetween aggressiveand amicablebehaviors. Why do roamershave the highest testosterone levels? Roamersmight benefit from the anxiolytic (fear-reducing) effect of high testosterone levels (Aikey et al. 2002; Ver meersch et al. 2008). Roamers have 10 times larger home ranges than philopatrics and more than three times larger. home ranges than territorialbreeders, overlapping the home. ranges of several groups. Roamer males. invade the. home ranges of several female groups defended by heavier breeding males and even by smaller philopatric males (Schradin 2004). If roamers engage more often in aggres. sivemale-male interactions,theirhigh testosterone levels could also be explained by the challenge hypothesis, which predicts that testosterone levels increase as a result of ag. species,high testosterone levelsmight not be compatible with high levels of amicable behavior (Wingfieldet al. gressiveinteractionsbetweenmales (Wingfieldet al. 1990). 1990). Thus, a trade-off between amicable and dominance behavior, both part of the tactic of the territorial breeders,. However,. this is unlikely. in our case, as males were trapped. shortly after they left their nests and thus probably before interactions with other mice had oc. during. the morning. was predicted to be representedby intermediatetestos terone levels.Territorialbreederswith the highest com curred.Therefore,differences in testosteronelevelsmight petitive status have three times higher testosterone levels be explained by differences in the social tactic, differences in caregivingbehavior, reproductivesuppression in phil than philopatrics with the lowest status. However, terri torial breeders have testosterone levels only half as high as those of roamers, which have a lower status than ter. ritorialbreeders.This supports our hypothesis that tes tosterone. levels of territorial breeders but not of solitary. opatrics, and risk-prone behavior. in roamers.. Corticosterone levels,however, are seven times higher inphilopatricsthan in territorialbreedersor roamers.This suggeststhatphilopatricmales arephysiologicallystressed,.

(14) 386. The American Naturalist. which could be one reason for their low testosteronelevels was greater in individualsfrom smallergroups, probably (Creel 2001; Young et al. 2006; Scantlebury et al. 2008). due to thermoregulatorybenefits of huddling in larger Chronically increasedglucocorticoid levels indicate allo groups (Scantlebury et al. 2006b). The implications of static load, that is, physiological. costs due to an overac. these results are that solitary roamers are expected. to have. tivation of the neuroendocrine stress response (McEwen larger thermoregulatorycosts at night than group-living 1999). Strategies to cope with this would be to down reg philopatrics or territorialbreeders. If roamersdo expend ulate glucocorticoid receptorsor to behaviorallyavoid the more energy at night, they might then need to reduce situation leading to chronically increasedglucocorticoid energy expenditure in other aspects of their energy bud levels.This supports our interpretationthatbeing a phil get-such as RMR. Evidence of such energy compensation the best of a bad job (Moore et opatric male is making al. 1998). As a consequence, philopatric males should leave their natal groups as soon as another tactic becomes more. has been shown. appropriate. for them, that is, when costs of dispersing to roamers or territorial breeders are lower than costs of remaining philopatrics. It is likely that philopatric males. Hence, energyconservationdue to huddlingmight enable. become. both. would become territorialbreeders if free territorieswere available (Schradin 2005). Importantly, about 75% of phil at the start of the breeding season were. opatric males. scrotal and thus probably physiologically able to breed, levels. In captivity, adult despite their low testosterone males kept in their family groups have low testosterone levels but when paired with an unfamiliar female can breed immediately. and have viable sperm, although much. in zebra finches Taeniopygia guttata and starlings Sturnus vulgaris (Deerenberg et al. 1998) as well as in laboratory mice (e.g., Hambly and Speakman 2005).. territorial breeders and philopatrics to sustain a higher RMR, allowing them to achieve a higher maximal rate of energy expenditure and Diamond (Hammond 1997; Speakman et al. 2004), which is potentially advan tageous in dealing with predator encounters and territorial. disputes with conspecifics. Roamers might not be able to increase their RMR and thus obtain the associated benefits because of their extra energy expenditure due to solitary. sleeping.. less. than breeders (C. Schradin,unpublished data).. Conclusions. Male stripedmice following different reproductivetactics in a conditional strategydiffer in steroid hormone levels In support of our prediction, territorialbreedershave the (this study) and in peptide hormone levels (Schradin Differences inRMR. highest absolute RMR values, but this was only because they are the largest individuals. When body mass is taken into account, breeders have similar RMR values to those of philopatric males, whereas roamers have lower values than those of either breeders or philopatric males. Inter. estingly, the relationshipbetweenRMR and corticosterone level marginally failed to reach significance (P = .08), with low RMR values tending to be associated with higher cor. ticosterone levels.This is inconsistentwith the prediction that high stress hormone levels cause high RMR. Whether this relationship is biologically relevant is unclear as the current sample size is low. By comparison, no relationship is evident. Thus, RMR between RMR and testosterone values obtained in these mice are complex and more likely depend on a variety of factors. Elevated RMR values are often associated with a higher reproductive and social status (Buchanan et al. 2001), possibly as a consequence. in contrast to the results of previous However, studies with other species, we found that dominant males have lower testosterone levels than males of a lower status 2008a).. (roamers).This suggestsa possible trade-offbetween am icable and aggressive behaviors. Corticosterone levels are almost an order of magnitude higher in philopatric males than in roamers or territorial breeders. This suggests that philopatrics are making the best of a bad job, being forced to remain philopatric due to high population density, and that they would disperse when given the opportunity (Schradin 2005). Surprisingly, RMR values are similar for territorial breeders and philopatric males but lower in roamers. It is unclear why this is the case, but some form of an energetic compensatory mechanism might be oc curring because thermoregulatory. of mate. searching and acquisition, as well as mating (Git tleman and Thompson 1988). In our study, roamers have. lower values than both territorialbreeders and philopa trics. This is consistent with our prediction that high RMR values should occur in territorial-breeding males but raises the question of why values were similarly high in philo In patrics. One possibility is a compensatory mechanism. a recent study on the same population, energy expenditure. roamers are expected costs at night.. to have the highest. Acknowledgments We are thankful for the support by the Department of Tour ism, Environment, and Conservation of the Northern Cape and the support by Goegap Nature Reserve. This study was. supported by the Holcim Foundation (Switzerland),the Vontobel Foundation (Switzerland),theSwissNational Sci ence Foundation. (3100A0-120194),. the Claude Leon Foun.

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