locomotor capacity and dominance in male lizards lacerta monticola: a trade-off between survival and...

Biological Journal of the Linnean Society

, 2002,

77

, 201–209. With 2 figures

© 2002 The Linnean Society of London,

Biological Journal of the Linnean Society,

2002,

77

, 201–209

201

Blackwell Science, LtdOxford, UKBIJBiological Journal of the Linnean Society0024-4066The Linnean Society of London, 200277

Original Article

PILAR LÓPEZ and JOSÉ. MARTÍNLOCOMOTION and SOCIAL DOMINANCE IN LIZARDS

*Correspondence. E-mail: [email protected]

Locomotor capacity and dominance in male lizards

Lacerta monticola

: a trade-off between survival and reproductive success?

PILAR LÓPEZ

*

and JOSÉ MARTÍN

Departamento de Ecología Evolutiva, Museo Nacional de Ciencias Naturales, CSIC, José Gutiérrez Abascal 2, 28006 Madrid, Spain

Received 29 October 2001; accepted for publication 26 June 2002

Trade-offs between reproduction and survival are important determinants of life-history characteristics of lizards.Organisms cannot increase the allocation of limited resources to reproduction without diverting a proportionalamount of energy from another trait. Locomotor performance is an ecologically relevant trait that potentially influ-ences survival by affecting the ability to escape from predators. Most studies have used female lizards as subjectsbecause pregnancy is known to reduce their locomotor abilities, whereas little is known on costs of reproduction inmales. In this study we suggest that in males of the lizard

Lacerta monticola

reproductive investment in mor-phological traits that confer dominance (i.e. head size) might lead to a low probability of survival by decreasinginvestment in other traits that affect locomotor performance (i.e. limb symmetry). We staged laboratory agonisticencounters between males and measured their morphology and burst speed on a race track to examine possible rela-tionships between morphology, social dominance and locomotor capacity. Our results indicate that social dominancewas positively related to relative head height, and that escape speed was negatively related to levels of fluctuatingasymmetry in femur length, but also negatively related to relative head height. Males with greater relative headheight also had more asymmetrical femurs, thus dominant males suffered a decrease in locomotor performance.Males with higher heads tend to dominate male–male interactions and hence may gain access to reproductivefemales, thus increasing their current reproduction success. However, this might occur at the expense of future sur-vivorship mediated by a decrease in escape speed. Therefore, in male

L. monticola

there might be a trade-off betweencurrent reproductive success and survival. © 2002 The Linnean Society of London,

Biological Journal of the Lin-nean Society

, 2002;

77

, 201–209.

ADDITIONAL KEYWORDS:

costs of reproduction – fluctuating asymmetry – locomotor performance – social

status – limb morphology.

INTRODUCTION

The cost of reproduction is defined as a trade-offbetween present and future reproduction (Roff, 1992).A high current reproductive investment may entailcosts by decreasing an organism’s chances of survivingto reproduce again (Reznick, 1992). These costs arebelieved to constrain the evolution of life-history pat-terns, and attempts to predict and explain variation inreproductive investment occupy a central place in life-history theory (Roff, 1992; Stearns, 1992). Lizards

have become ‘model organisms’ in evolutionary ecol-ogy, and there is an extensive scientific literature thatdocuments and interprets patterns in their life-historyvariation (Vitt & Pianka, 1994).

Locomotor performance is an ecologically relevanttrait that potentially influences fitness by affectingescape from predators (Christian & Tracy, 1981; Webb,1986), and is often used as a measure of whole-animalperformance (Hertz, Huey & Garland, 1988; Bonine &Garland, 1999). Because increase in mass associatedwith pregnancy is known to reduce the locomotorcapacity, most studies investigating the costs ofreproduction in lizards have focused on the differencein locomotor performance between gravid and non-

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, 201–209

gravid females (Qualls & Shine, 1998; Miles, Sinervo& Frankino, 2000; but see Olsson, Shine & Bak-Olsson, 2000a for a different view). However, little isknown of the costs of reproduction in male lizards. Thepossible variation in locomotor performance of malelizards has not been previously considered as a possi-ble consequence of their reproductive investment.

In most lizard species, reproductive investment ofmales is directly associated with dominance status.Dominant males often control the largest and mostfavourable home ranges and can have access to ahigher number of females (Martín & Salvador, 1993a,1997). A few studies suggest the existence of domi-nance costs in male lizards that might influence theirsurvival in several different ways. For example, indefending their larger territories dominant males mayexpend greater amounts of energy than subordinates,and this could be reflected in a greater mass lossduring the breeding season (Martín & López, 2000a).Moreover, dominant males require higher activitylevels to search for mates and to exclude opponentsfrom their home ranges (Martín & López, 2000a),which may involve an increased exposure to predators(Magnhagen, 1991). Also, it is known that males witha higher status spend more time in social activitiesand are more involved in agonistic encounters (Martín& López, 2000a), incurring costs from an increase intheir level of aggressive activity (Marler & Moore,1988, 1989). Thus, dominant males may experiencegreater reproductive costs than subordinate ones,which could lead to a decrease in survivorship (Adolph& Porter, 1993; Díaz, 1993; Sinervo

et al

., 2000). Wehypothesized that a high investment in traits thatconfer dominance might reduce investment in traitsthat affect locomotor performance.

Fluctuating asymmetry (FA) in individuals resultsfrom non-identical development of a bilateral trait onboth sides of the body (Van Valen, 1962). It has beensuggested that asymmetric locomotor structures mayinvolve a reduction in locomotor performance ofindividuals (Møller & Swaddle, 1997). However, theeffect of asymmetry on locomotor performance hasbeen examined almost exclusively in the flight of birds(Thomas, 1993; Swaddle, 1997), whereas their effectson terrestrial locomotion has scarcely been studied(Manning & Ockenden, 1994). An exception is a studyon the lizard

Psammodromus algirus

, which showedthat escape performance was affected by fluctuatingasymmetry in femur length, resulting in significantlyreduced escape speeds (Martín & López, 2001).This is important, because low asymmetry on locomo-tor structures is predicted to occur for functionalreasons if asymmetry reduces biomechanical perfor-mance (Møller & Swaddle, 1997). Thus, there mightbe strong selection against the most asymmetricalindividuals.

The Iberian rock lizard,

Lacerta monticola

, is a smalldiurnal lacertid found mainly in rocky habitats in highmountains of the Iberian Peninsula. Males of thisspecies defend territories against other males, butoverlap between home ranges is extensive becausemale density is very high, and dominance hierarchiesamong neighbouring males of similar age or size oftenemerge (Martín & Salvador, 1993a, 1997; Martín &López, 2000a). In its natural habitat this lizard suffersa high predation risk as shown by the high rate ofregenerated tails (Martín & Salvador, 1997). Lizardsof this species escape from predators by running rap-idly for cover into the nearest refuge (Carrascal

et al

.,1992). Thus, locomotor performance may constitute animportant trait in male

L. monticola

, because it couldprofoundly affect their probability of survival byaffecting escape from predators. In this study weexamine how social status of male Iberian rock lizardscan be related to their escape performance. In thelaboratory we staged agonistic encounters betweenmales, and measured their morphology and burstspeed on a race track to examine possible relation-ships between morphology, social dominance and loco-motor capacity. Our results suggest that there mightbe a trade-off between dominance and survival medi-ated by sprint speed abilities of males.

METHODS

S

TUDY

ANIMALS

During May 2000 and 2001, we captured (by noosing)12 and 13, respectively, adult male

L. monticola

in different places over a large area (‘Puerto deNavacerrada’, Guadarrama Mountains, CentralSpain) to ensure that individuals had not been in pre-vious contact, which may have affected the outcome ofthe experiments (López & Martín, 2001). Lizards werehoused individually at ‘El Ventorrillo’ Field Station(5 km from the capture site) in outdoor plastic cages(80

×

50 cm) containing rocks for cover. We providedmealworms dusted with a multivitamin powder asfood, and water

ad libitum

. Individuals were held intheir home cages for at least one week to familiarizethem with the novel environment prior to testing.All lizards were healthy during the trials, and werereleased to their capture sites at the end of theexperiments.

M

EASUREMENT

OF

MORPHOLOGICAL

VARIABLES

Lizards were measured (snout–vent length, SVL:mean

±

SE

=

76.1

±

0.6 mm, range

=

73–80 mm) andweighed (body mass: mean

±

SE

=

8.4

±

0.3 g, range

=

6.7–10.0 g). Only individuals with complete tails wereused in this study because tail loss modifies locomotor

LOCOMOTION AND SOCIAL DOMINANCE IN LIZARDS

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patterns (e.g. Martín & Salvador, 1997; Martín &Avery, 1998). We calculated individual values of bodycondition as the residuals from the regression equa-tion of ln mass (g) on ln SVL (mm), which may repre-sent an index of the relative amount of fat stored, andhence an estimation of individual physical condition ornutritional status (Bonnet & Naulleau, 1994).

In male

L

.

monticola

dominant males won most ago-nistic interactions and have a higher mating success(Martín & Salvador, 1993a). It has been proposed thatmales with large heads tend to dominate male–maleinteractions (e.g. Anderson & Vitt, 1990; Molina-Borja, Padrón-Fumero & Alfonso-Martín, 1998). Thisseems to be one of the causes of sexual dimorphismin head size of many lizard species, including

L. monticola

(unpublished data). Thus, we made mor-phological measurements of the head of males usingdigital callipers (to the nearest 0.1 mm). Head heightwas the greatest distance from the highest portion ofthe head to the bottom of the lower jaw. Head lengthwas the distance between the tip of the snout and theposterior side of the parietal scales. Head width wasthe greatest distance between the external sides of theparietal scales.

Limb morphology and limb proportions have beenidentified as important factors in determining locomo-tor performance in lizards (Arnold, 1998). Thus, foreach lizard we measured the length of the femur, crus,humerus and radius of the left and the right limbs. Weused this terminology to refer to the distinct parts ofthe limb that included these bones in live animals(Martín & López, 2001). Femur length was measuredas the greatest distance from the most anterior pointof insertion of the hindlimb in the body to the knee.Crus length was the greatest distance from the knee tothe sole of the foot (i.e. the plantar surface of the tar-sals and metatarsals). Humerus length was measuredas the greatest distance from the most posterior pointof insertion of the forelimb in the body to the elbow.Radius was the greatest distance from the elbow to theplantar surface of the manus (which includes carpiansand metacarpians). In order to get more precise mea-surements, we placed each lizard on its back overgraph paper and recorded it on videotape using avideo-camera (Hi-8 format, 25 frames s

−

1

) alignedperpendicularly over the centre of the individual. Pre-liminary analyses showed that measurements withdigital callipers of limbs from preserved specimenswere highly correlated with measurements taken fromvideotape with this method. Measurements weremade by the same person from still frames on a mon-itor (to the nearest 1 mm). They were repeated threetimes for different frames where we had slightlymoved the animal between pictures. This procedureallowed for possible measurement error caused by thefact that the camera may not have been exactly per-

pendicular to the limb being measured. Measure-ments were shown to be highly repeatable and themeasurement error small relative to FA (two-waymixed model

ANOVA

s: Femur:

F

24,96

=

271.15,

P

<

0.0001; Crus:

F

24,96

=

346.65,

P

<

0.0001; Humerus:

F

24,96

=

283.14,

P

<

0.0001; Radius:

F

24,96

=

43.12,

P

<

0.0001; see Swaddle, Witter & Cuthill, 1994 fordetails of

ANOVA

analysis).We calculated individual values for relative asym-

metry in each part of the limbs as the unsigned right-minus-left lengths divided by the mean left and rightcharacter value ((|R

−

L|)/0.5(R

+

L); see Palmer &Strobeck, 1986). We tested whether the different partsof the limbs exhibited the properties of FA by usingFilliben correlation coefficients testing for normality(i.e. correlation of raw data with predicted normalprobability scores; Aitken

et al

., 1989), and one-sample

t

-tests testing whether asymmetry valueswere distributed around a mean of zero (Møller &Swaddle, 1997). We used non-parametric Wilcoxonmatched-pairs signed-ranks tests to compare morpho-logical measurements within the same individualsand rank Spearman correlations (Siegel & Castellan,1988) to analyse the relationships between asymme-try and morphological measurements because of theparticular half-normal distribution of unsigned abso-lute asymmetry data (see Swaddle

et al

., 1994). Theinfluence of body size on head and limb measurementswas removed by regressing each against SVL (all vari-ables ln-transformed) and using the residuals in pos-terior analyses.

S

OCIAL

STATUS

To determine social status we staged agonistic encoun-ters between pairs of males in all possible combina-tions within two groups (

N

=

12 in the year 2000, and

N

=

13 in 2001) during May–June, which coincidedwith the mating season of lizards in their original nat-ural population. To avoid the effect of prior-residenceadvantage (Cooper & Vitt, 1987; López & Martín,2001), we performed all experiments in a neutral,previously unoccupied arena, consisting of a 1

×

0.5 menclosure divided into two equal compartments by aplywood partition. Males were placed in separate com-partments and given 15 min to settle in the new envi-ronment before the partition was removed. All testswere made in outdoor conditions and when lizardswere fully active. Each male was used several times,facing once each of all the other males in randomizedsequence, but participated in only one interaction perday to avoid stress. Staged encounters were spacedsufficiently (at least one day) so that fatigue resultingfrom one trial did not affect subsequent trials, thuseach male participated in only one interaction per day.To avoid disturbing lizards during encounters, we

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made all observations from a hidden point. We consid-ered an aggressive response if a male approachedanother individual with aggressive display and madethe other male retreat or run away either without con-tact, by touching him on the flanks, or, occasionally, bygiving quick bites, specially to the snout or head. Wenoted which male won the interaction and which onewas chased. Thereafter, we calculated a sum of aggres-sive interactions won less interactions lost for eachmale of each pair, and defined the male with the high-est positive sum as the dominant individual (Fox, Rose& Myers, 1981; Martín & Salvador, 1993a). Typically,males considered as winners repeatedly dominatedtheir opponents over a series of interactions in eachencounter. Only in a few cases was it not possible todetermine which male was the dominant of the pair,and we considered it an unknown relationship.

A matrix of dominance was constructed based on theresults of agonistic staged encounters between males.The probability of linearity with hierarchies was cal-culated according to Appleby (1983). To demonstratelinearity of a hierarchy in a group it is necessary toshow that dominace tends to be transitive. Thus, wecalculated the number of circular triads in the group(

d

), and the degree of linearity of a hierarchy (i.e. thecoefficient

K

, which has values from 0, indicating com-plete absence of linearity, to 1, indicating a linear hier-archy; see Appleby, 1983). Social status scores of bothgroups of lizards where standardized for further anal-yses to a scale from 0 to 10, the latter being the mostdominant males. We used forward stepwise multipleregression analysis to determine how snout-to-ventlength, body mass, body condition or head height,head length and head width residuals (independentvariables) influenced social status scores of males(Sokal & Rohlf, 1995).

E

SCAPE

PERFORMANCE

Lizards were individually tested in a linear terrarium(80

×

30 cm) with a carpeted floor, which providedexcellent traction, and where all potential obstacleshad been removed. Individuals were allowed to baskfor at least 2 h before trials to attain a body tempera-ture within the activity temperature range of the spe-cies (Martín & Salvador, 1993b). To study their escaperesponses, lizards were induced to flee at high speedby tapping them close to the tail with a brush. Theescape sequences were spaced sufficiently (at least1 h) so that fatigue resulting from one run did notaffect subsequent runs. The spatial scale of the exper-imental terrarium was realistic in that its lengthapproximates to that of an escape attempt under nat-ural conditions, in which

L. monticola

individuals runrapidly to cover into the nearest refuge (Carrascal

et al

., 1992). Experiments were recorded on videotape

using a video-camera (Hi-8 format, 25 frames s

−

1

)aligned perpendicularly over the centre of thearena. From each individual, we selected fourescape sequences scored as ‘good’ (Tsuji

et al

., 1989;Vanhooydonck & Van Damme, 2001); ‘bad’ trials wereeliminated before further analysis. Lizards passed allthe trials without apparent signs of stress.

We analysed the sequences frame-by-frame to deter-mine the sprint speed of the lizards. Measurementswere based on calibrated distances measured (to thenearest 1 mm) from the video monitor using a whitemark painted on the tip of the snout as a position ref-erence (Martín & Avery, 1998). For each sequence wemeasured the distance between the initial position(lizard paused) of the lizard’s snout mark and the finalposition in the first pause after fleeing (escape dis-tance), and the time interval between the initial andfinal position (escape duration). From these data, wecalculated the burst speed (distance moved divided bytime taken; Martín & Avery, 1998). For each individ-ual, an average value was determined from the foursequences that were analysed. Previous analysesshowed that increasing the number of sequences didnot alter the results. We used forward stepwisemultiple regression analysis (Sokal & Rohlf, 1995) todetermine how snout-to-vent length, body mass, bodycondition, head height residuals, forelimb and hind-limb length, or femur, crus and radius asymmetrylevels (independent variables) influenced burst speedof lizards.

RESULTS

M

ORPHOLOGY

AND

FLUCTUATING

ASYMMETRY

The hindlimbs (17.7

±

0.3 mm) were significantlylarger than the forelimbs (13.8

±

0.2 mm;

±

SE, Wil-coxon test,

z

=

3.52,

N

=

25,

P

=

0.0005). The averagerelationship of hindlimbs length/forelimbs length was1.28

±

0.01. Within the hindlimbs, the femur (averagevalue of the two sides) was significantly larger thanthe crus (

z

=

3.07,

N

=

25,

P

=

0.002), and within theforelimbs, the radius was significantly larger than thehumerus (

z

=

3.52,

N

=

25,

P

=

0.0004) (Table 1).Except for the humerus measurements, which

showed directional asymmetry (one sample t-test fordeviation from a mean of zero, t = 3.47, d.f. = 24,P = 0.002), the other parts of the limbs exhibited theproperties of FA, i.e. a normal distribution (Fillibencorrelation coefficients, i.e. correlation of raw datawith predicted normal probability scores: Femur:r = 0.87, N = 25, P < 0.001; Crus: r = 0.86, N = 25,P < 0.001; Radius: r = 0.79, N = 25, P < 0.01) around amean of zero (one-sample t-tests, Femur: t = 0.22,d.f. = 24, P = 0.83; Crus: t = 1.18, d.f. = 24, P = 0.25;Radius: t = 0.68, d.f. = 24, P = 0.50).

LOCOMOTION AND SOCIAL DOMINANCE IN LIZARDS 205

© 2002 The Linnean Society of London, Biological Journal of the Linnean Society, 2002, 77, 201–209

Levels of fluctuating asymmetry exhibited by thefemur were lower than those exhibited by the crus(Wilcoxon test, z = 2.54, N = 25, P = 0.01), whereasthere were no differences between humerus andradius asymmetry levels (z = 0.09, N = 25, P = 0.92;Table 1). There was a negative and significant rela-tionship between the residuals of the hindlimb lengthon SVL and asymmetry levels of the crus (rS = −0.65,N = 25, P = 0.0005), but this relationship was notsignificant for the femur (rS = 0.11, N = 25, P = 0.61).Thus, when the hindlimbs were relatively shorter, theasymmertry level of the crus, but not that of the femur,increased. In the forelimbs these relationships werenot significant either for the humerus or crus (P > 0.20in both cases).

Head measurements of males (height: 7.9 ± 0.1 mm;length: 17.0 ± 0.2 mm; width: 10.7 ± 0.1 mm) were sig-nificantly related to SVL (Spearman correlation coef-ficients: rS > 0.7, P < 0.0001 in all cases) and to bodymass (rS > 0.5, P < 0.001 in all cases). Thus, we usedresiduals in posterior analyses. Males with relatively

larger heads also have more asymmetrical femurs(height: rS = 0.52, N = 25, P = 0.007; length: rS = 0.72,P < 0.0001; width: rS = 0.54, P = 0.006), but no signifi-cant relationships were found for the other parts of thelimbs (P > 0.20 in all cases)

SOCIAL STATUS

The results of staged agonistic encounters showedthat males had developed a dominance hierarchy bothin the group from the year 2000 (d = 33.25, N = 12,P < 0.01, k = 0.54) and that from 2001 (d = 30.50,N = 13, P < 0.01, k = 0.66). The results of the stepwisemultiple regression showed that social dominancescores of males were significantly and positivelycorrelated with head height residuals (R2 = 0.49,F1,23 = 22.14, P < 0.0001) (Table 2; Fig. 1). Thus, maleswith relatively higher heads reached superior statusin the dominance hierarchies. Other body measures,

Table 1. Length (mm) and asymmetry values of the differ-ent parts of the limbs on both sides of the body (mean ± SE,range is shown below)

Left Right Asymmetry level

Femur 9.2 ± 0.1 9.2 ± 0.2 0.7 ± 0.1(8.4–11.8) (7.5–11.1) (0.1–1.7)

Crus 8.5 ± 0.2 8.2 ± 0.2 1.2 ± 0.1(6.2–10.5) (6.5–9.8) (0–2.3)

Humerus 6.2 ± 0.1 5.5 ± 0.1 0.7 ± 0.1(4.7–7.3) (4.1–6.5) (0–2.2)

Radius 7.8 ± 0.1 7.9 ± 0.1 0.8 ± 0.1(6.7–9.0) (6.8–9.2) (0–1.8)

Table 2. Models obtained from stepwise multiple regression analysis on factorsthat explained the variation of social status or burst speed (dependent variables)of male Lacerta monticola. The independent variables were snout-to-vent length,body mass, body condition, head height, head length and head width residuals,limb length, and the asymmetry levels of each part of the limb. Standardized (β)and non-standardized (B) regression coefficients and their standard errors areshown, together with values of t and associated probability levels

Independent variable β B t P

Social statusIntercept 5.40 ± 0.37 14.49 <0.0001Head height residuals 0.70 ± 0.15 109.32 ± 23.25 4.71 <0.0001

Burst speedIntercept 4.82 ± 0.02 214.30 <0.0001Head height residuals −0.50 ± 0.15 −1.78 ± 0.55 −3.26 0.003Femur asymmetry −0.39 ± 0.15 −0.62 ± 0.25 −2.55 0.019

Figure 1. Relationship between males’ social status scores(on scale of 1–10) and head height residuals.

206 PILAR LÓPEZ and JOSÉ MARTÍN


such as snout–vent length, body mass, body conditionor head length and head width residuals did not sig-nificantly affected social status.

ESCAPE PERFORMANCE

Burst speed during escape trials (118.6 ± 2.4 cm s−1;maximum = 143.9 cm s−1) was significantly and nega-tively correlated with head height residuals and withfemur asymmetry levels, but not with SVL, limblength, body weight, body condition or crus and radiusasymmetry levels (R2 = 0.57, F2,22 = 14.54, P = 0.0001;Table 2; Fig. 2).

DISCUSSION

Our results show that social status of males wasdirectly related to relative head height. Males with

larger heads can bite harder (Herrel et al., 1999), andthus can have an advantage in intrasexual agonisticcontests if an escalation occurs. This is in agreementwith the hypothesis that sexual selection accounts forsexual dimorphism in head size of many lizard species,and that head size of males could be an intrasexuallyselected trait (Anderson & Vitt, 1990; Molina-Borjaet al., 1998). In L. monticola we have found that maleshave significantly higher, wider and longer heads thanfemales (unpublished data), and that dominant malesgain access to reproductive females by increasing theirhome ranges in the breeding season and expellingcompetitor males (Martín & Salvador, 1993a, 1997).Thus, our results suggest that males with relativelyhigher heads (dominant males) may experiencegreater reproductive success than subordinates withinthe same breeding season.

On the other hand, our results also show that maleswith relatively higher heads suffer a reduction in theirsprint speed, which suggests that decreased locomotorperformance might constitute a cost of reproduction inthis species. We cannot explain the direct causal linksbehind the inverse relation between social dominanceand locomotor performance. Higher levels of activityand a lower food intake could be reflected in a greaterloss of mass by dominant male L. monticola duringthe breeding season (Martín & López, 2000a), andperhaps also in a lower locomotor capacity. Moreover,dominant males may have higher levels of plasma tes-tosterone, which often result in increased mass loss ortick load (Marler & Moore, 1988, 1989; Salvador et al.,1996; Olsson et al., 2000b). Thus, dominant males maysuffer a worse physiological state and this could bereflected in a reduction of their locomotor performance(but see Klukowski, Jenkinson & Nelson, 1998;Sinervo et al., 2000).

Previous tests of the relationship between socialdominance and sprint capacity in other species oflizards have found results contrary to our findings(Garland, Hankins & Huey, 1990; Hews, 1990). Thismight be explained by differences in protocols, but it ismore likely due to differences in the species tested.While previous studies have used lizards from warmclimates where resources are abundant, we havetested a species inhabiting a cold and limiting habitat.In the high mountains, lizards only have a shortperiod of activity to forage and store reserves (VanDamme et al., 1989; Carrascal et al., 1992). Variationin reptilian growth rate is associated with differencesin food availability and time available for foraging andthermoregulation (Andrews, 1982). We suggest that,at least in some habitats, physiological and energeti-cal constraints might represent a cost of dominance byaffecting locomotor abilities of male lizards.

Our results also highlight that one of the sources ofvariation in sprint speed between individuals is fluc-

Figure 2. Relationship between burst speed in escapeperformance trials and (a) head height residuals of males,and (b) relative fluctuating asymmetry of their femurlength.



tuating asymmetry in femur length (see also Martín &López, 2001 for a similar result). Thus, males withmore asymmetrical femurs suffered a reduction intheir locomotor performance (about 22% decline inaverage speed between the extremes of FA). Thisimpairment is likely to be of general ecological impor-tance during an encounter with a predator and todirectly affect individual survival: some studies havesuggested that sprinting ability can affect survivalwithin populations of reptiles (Christian & Tracy,1981; Jayne & Bennett, 1990). The significant corre-lation between femur asymmetry and burst speeddo not demonstrate a direct causal relationship, andmany potentially confounding variables may obscurethe real relationship. However, the loss of equilibriumpotentially caused by femur asymmetry may forcelizards to run slowly, and to continuously correct thesmall disequilibrium in each step (Martín & López,2001). The exact biomechanical causes of the lowersprint speed of lizards with more asymmetricalfemurs remain to be analysed in detail. Also, as sym-metry or the lack thereof may be a good indicator ofthe quality of an individual, we cannot exclude thepossibility that reduced performance is not directlyrelated to asymmetry of the limbs but reflects a gen-erally poor phenotypic condition (Qualls & Andrews,1999).

Our results suggest that both relative head heightand femur asymmetry can affect locomotor perfor-mance of males. However, there is also a significativedirect correlation between femur asymmetry andrelative head height of males. Males with relativelyhigher heads (i.e. dominant males) also have moreasymmetrical femurs. Therefore, FA in structuresused in locomotion might be considered as a cost ofreproduction. In order to reach a high social status,energy allocation presumably should be devoted toprocesses such as growth of the head, and productionof testosterone (Sinervo et al., 2000) or pheromones(Martín & López, 2000b). Thus, dominant males mayhave less energy available for non-sexually relatedprocesses such as general growth (Marler & Moore,1988, 1989; Martín & López, 2000a). Variations inasymmetry have been shown to be related to energeticstress (Swaddle & Witter, 1994; Witter & Swaddle,1994), and FA may reflect the physiological state andthe nutritional status during the growth period of aparticular body trait (Møller & Swaddle, 1997). Thus,several studies have shown a lowered control of devel-opmental homeostasis in those parts of the body inwhich less energy is allocated (reviewed in Møller &Swaddle, 1997). We suggest that variation in femurasymmetry may arise from a breakdown of develop-mental homeostasis because of the great energyinvested by dominant males in reproductive charac-teristics. This would agree with findings that energy

allocation is likely to be an important determinant ofreproductive investment in life-history patterns (Roff,1992; Stearns, 1992).

Sexual selection would lead males to increase theiractivity and energetic expenditure in order to increasetheir short-term reproductive success. On the otherhand, a lower escape performance would counterbal-ance these benefits by negatively affecting the male’slong-term survival. Thus, there may be contrastingselective pressures from sexual selection, which is aresult of differential current mating success, andnatural selection, arising from variance in all othercomponents of fitness, principally survival. Dominantmales may achieve higher reproductive success in oneseason, but increased survivorship of subordinatemales might result in similar lifetime reproductivesuccess as dominant males. Thus, competition formates and survivorship may represent two opposingselective forces in L. monticola that could result in anoptimal level of behaviour since both contribute to life-time reproductive success.

ACKNOWLEDGEMENTS

We thank ‘El Ventorrillo’ MNCN Field Station for useof their facilities. Lizards were captured under licensefrom the Agencia del Medio Ambiente de la Comu-nidad de Madrid (Spain). A. Muñoz helped to collectpart of the data for this project under a ‘Contrato deprácticas de empresa’ agreement between Univer-sidad Complutense de Madrid and CSIC. Financialsupport was provided by the DGESIC project PB-98–0505 and a ‘Ramón y Cajal’ MCYT contract to PL.

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