Naturwissenschaften 85, 307317 (1998) Q Springer-Verlag 1998 307

Of Domestic and WildGuinea Pigs: Studies inSociophysiology,Domestication, and SocialEvolutionNorbert Sachser

Westflische Wilhelms-Universitt Mnster,Institut fr Neuro- und Verhaltensbiologie,Abteilung fr Verhaltensbiologie,Badestrasse 9, D-48149 Mnster, Germany

Among mammals a majority of each individuals daily expecta-tions, motivations, and behaviors are directed to encounterswith conspecifics. Therefore the knowledge of the genesis, con-trol, and consequences of social interactions is crucial for un-derstanding their social life. We present here our research onthe sociophysiology, domestication, and social evolution of wild(Cavia aperea and Galea musteloides) and domestic (Caviaaperea f. porcellus) guinea pigs, which summarizes general rulesfor many group-living mammals. It is shown that social interac-tions have consequences not only for the individuals reproduc-tive success but also for their degrees of stress and welfare. Theway in which individuals interact is controlled not only by thepresent environment but also by the previous social experi-ences which they have gathered during their behavioral devel-opment. Furthermore, the study of ontogeny does not begin atbirth, because prenatal social factors acting on pregnant fe-males can also affect the way in which the offspring will interactwhen adult. In addition, to understand the genesis of interac-tions between domesticated animals implies knowledge of thebehavioral and physiological changes which occurred duringthe process of domestication. Finally, understanding the socialinteractions among individuals of the wild ancestor of the dom-esticated form requires knowledge of how their behavior pat-terns were brought about by natural selection during the proc-ess of social evolution.

Introduction

In higher vertebrates a majority of each individualsdaily expectations, motivations, and behaviors aredirected to encounters with conspecifics (Hendrichs1978). Therefore knowledge of the genesis, control,and consequences of social interactions is crucial forunderstanding the social life of mammals. The studyof the genesis involves the effects of evolution, dom-estication, culture, and ontogeny. Control refers toshort-term regulation by external stimuli impingingon the animals and by internal physiological andmental events. The consequences concern the ef-fects on the organism itsself, on its social and physi-cal environment and on its fitness. [This classifica-tion follows Dewsbury (1992) in most points.] Untilnow mammalian social interactions have rarely beenanalyzed in a way that gives equal attention to thesedifferent levels of analysis. Thus at present behavio-ral biology is far from understanding the social lifeof mammals in a comprehensive way.About 20 years ago we began studying domestic gui-nea pigs using a descriptive ethological approachand were fascinated by the unexpected complexityof these animals social life (Sachser 1986, 1994a;Sachser and Hendrichs 1982). Soon, however, it be-came clear that questions concerning the immediateconsequences of social interactions for the organismin terms of stress and welfare could not be answeredin a satisfactory way by purely behavioral observa-tions. Did subdominants, for example, really suffer ahigher degree of stress than dominants? Was life athigh population densities indeed more stressful thanat low densities? (The answer to both questions isno, as is shown below.) At the beginning of the1980s we developed a technique for taking bloodsamples from guinea pigs ear vessels in a nonstress-ful way (Sachser and Prve 1984), from which theconcentrations of several hormones (cortisol, nore-

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pinephrine, testosterone) were determined (e.g.,Sachser 1987). Thereafter the simultaneous record-ing of ethological and endocrinological parametersprovided a reliable method for studying the physiol-ogical consequences of social interactions (e.g.,Sachser 1994a; Sachser et al. 1994). In addition, itbecame clear that adult guinea pigs interactive be-havior is significantly influenced by their pre- andpostnatal social environment (Sachser and Kaiser1996; Sachser and Lick 1991). The first part of thiscontribution summarizes our sociophysiologicalfindings, which by now have emerged as generalrules for many group-living mammals.Guinea pigs (Cavia aperea f. porcellus) are domesti-cated animals which are adapted to man-made hous-ing conditions, but which are not found in naturalhabitats. In contrast, their ancestor, the wild cavy(Cavia aperea), is among the most common andwidespread rodents of South America (Stahnke andHendrichs 1988). Understanding the genesis of so-cial interactions in the domesticated form requiresconsideration not only of the individuals ontogenybut also of the effects deriving from the process ofdomestication. The second part then summarizes theethological and physiological differences betweenthe domestic guinea pig and its wild ancestors. As isshown below, the process of domestication has ledto typical behavioral developments which are alsofound in comparisons between wild and domesticforms of other species. In addition, some new find-ings on endocrinological changes are presentedwhich have clearly helped domesticated animals toadapt to man-made housing conditions.Understanding the social interactions among indi-viduals of the wild ancestor of the domesticatedform requires knowing the way in which their be-havior patterns have come about by natural selec-tion during the process of social evolution. A mostpromising way to analyze the social evolution of thewild cavy is to compare its patterns of social interac-tions with those of a closely related species and todetermine the consequences for differential repro-duction (the so-called comparative approach). Thethird part of this contribution summarizes the initialresults of our comparison between two species ofwild guinea pigs: the wild cavy (Cavia aperea) andthe yellow-toothed cavy (Galea musteloides). Thiscomparison provides new general insights into theevolution of mammalian mating systems.

Fig. 1. Various forms of social organization in guinea pigs. Low densi-ty: arrows among males indicate direction of aggressive behaviors.High density: lines between males and females indicate individual so-cial bondings. Alphas (circled males) dominate nonalphas (noncircledmales). Broken lines, the borders of territories

The Guinea Pig: A Study inSociophysiology

Social Interactions, Social Relationships,Social Organization

Various forms of social interactions are observed inguinea pigs. On the one hand, animals compete witheach other in agonistic encounters. These establishdominance relationships and stratify the individualsinto relative social positions. On the other hand, so-cial interactions can also proceed in a sociopositiveand/or sexual way, which may result in the establish-ment of social bonding. The overall structure ofdominance relationships and social bondings consti-tute the animals social organization.In our first experiment we studied the effects of in-creasing population density on the patterns of socialinteractions and reproductive success. A small num-ber of guinea pigs (four males and two females)were placed in a 16 m2 enclosure. The animals wereallowed to reproduce freely, and after 20 monthsthere were about 50 individuals in the colony. How-ever, the astonishing point was that even at suchhigh population numbers the reproductive successof the females (that is, the number of survivingoffspring/time) did not decline, and the number offights between individuals did not increase distinctly(Sachser 1986, 1994a). The question thus arose:which mechanisms allow guinea pigs in contrast tomany other mammals (Christian 1975) to cope soeffectively with high population numbers? Theanswer to this question is shown in Fig. 1 :guineapigs change their patterns of social interactions andtheir social relationships, that is, their social organi-zation, when population numbers increase (Sachser1986).

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At low population numbers (for example, threemales and three females) the social organization ischaracterized mainly by a linear dominance hierar-chy among the adult males. Subordinate males re-treat whenever a higher ranking conspecific ap-proaches; this largely precludes threat displays andfights. Individuals of identical rank are never found.The highest ranking male shows much more court-ship behavior towards each of the females than anyother male, and he is probably the father of theoffspring. Social bondings do not exist betweenmales and females. Among the females there is alsoa linear rank order (Thyen and Hendrichs 1990).However, their agonistic interactions are less pro-nounced than those among males. Between thesexes fighting and threat displays do not occur.When population numbers increase, guinea pigschange their social organization. Groups of 1015 ormore split into subunits, each consisting of one tofour males and one to seven females. The highestranking male of each subunit, the alpha, establisheslong-lasting social bondings toward all females of hissubunit. The alphas guard and defend their femalesaround estrus, and more than 85% of offspring aresired by them, as shown by DNA fingerprinting (Fis-beck and Sachser, unpublished data). The lowerranking males also have bondings with the femalesof their subunits, that is, they interact predominantlywith these animals. Alphas of different subunits re-spect each others bondings, that is, they do notcourt other alphas females even if these are recep-tive. In general, individuals belonging to a givensubunit live in an area that does not overlap with thearea of other subunits. It is in these areas that mostof the social interactions are displayed, and wherethe individuals have their resting and sleepingplaces. The alphas defend the borders of these areasaround their females estrus (see Sachser 1986,1994a).Social organization at high population numbers istherefore characterized by the following threepoints: (a) splitting of the whole group into subunitsprovides all individuals with social and spatial orien-tation; (b) escalated fighting is rare because alphasrespect the male-female bondings of other alphas;(c) the individuals different social positions are sta-ble over months, and the basic patterns of social or-ganization are independent of individual animals.Thus the change in social organization from a strict-ly dominance-structured system at low populationnumbers to a system in which long-lasting bondingsare predominant at high numbers can be regardedas a mechanism for facilitating adjustment to in-creasing population density.What are the causes for this change? At low density

the highest ranking male monopolizes all females.However, the costs, for example, in time and energyspent in agonistic encounters and in maintaining theexclusive access to all females within the whole area,increases with the population of competitors and fe-males. It is economical to defend all females only aslong as the net benefits (in terms of reproductivesuccess) exceed net costs. When the relationship be-tween benefits and costs becomes unprofitable, analternative behavior yielding a higher reproductivesuccess is preferable, that is, controlling a certainnumber of females within a certain area and respect-ing the same behavior pattern displayed by othermales. Thus the cause for change in the social organ-ization is considered to be the highest rankingmales change in reproductive strategy for maximiz-ing his fitness (Sachser 1986).At low population numbers the highest rankingmale probably sires most offspring. This reproduc-tive advantage results from his dominance. At highpopulation numbers the alphas reproduce withtheir females. This reproductive advantage resultsfrom two mechanisms: (a) alphas respect the own-ership of other alphas, and (b) they dominate non-alphas in agonistic interactions. Thus at low andhigh population numbers a polygynous mating sys-tem is typical for domestic guinea pigs.

Physiological Consequences of SocialStratification

Social interactions have a profound effect on the pi-tuitary adrenocortical (PAC) and the sympatheticadrenomedullary (SAM) systems (e.g., Henry andStephens 1977; Sachser 1994a,b; von Holst 1990).The activation of each of these systems plays a ma-jor role in adjusting an individual to social and non-social challenges by providing the organism with en-ergy and shifting it into a state of heightened reac-tivity. Although the short-term or moderate activa-tion of both systems represents an adaptive mecha-nism to cope with conflict situations, the long-termhyperactivation of both the SAM and the PAC sys-tem is related to the etiology of irreversible injuryand even death (Henry 1982; Henry and Stephens1977; von Holst 1990). Blood glucocorticoid concen-trations cortisol being the major component in gui-nea pigs and man can be used as a measure ofPAC activity; serum catecholamine concentrations epinephrine, norepinephrine and adrenal tyrosinehydroxylase activities are reliable indicators of SAMactivity.When male guinea pigs living at different populationnumbers are compared, they show an increased

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SAM activity at high densities. PAC activity, in con-trast, is not at all affected by population numbers,that is, a male living in a large colony does not showhigher cortisol concentrations than a male living in asmall group or together with one female only. Theseendocrinological data support our behavioral find-ings: a change in density does not necessarily meanan increase in social stress for the individuals as longas a stable social environment is maintained by so-cial mechanisms (Sachser 1990, 1994a).At high and low population numbers males take dif-ferent social positions, which are stable overmonths. Alphas, for example, always clearly domi-nate nonalphas of the same subunit. These domi-nance relationships are independent of place andtime. Alphas bite more often and are less often bit-ten than nonalphas, and they display far more court-ship and sexual behavior than the lower rankingmales (Sachser 1990). Surprisingly, despite theseclear differences in behavior and status, alphas andnonalphas do not differ significantly in indices ofPAC and SAM activities (Sachser 1987, 1994a;Sachser et al. 1998), that is, having low social statusdoes not necessarily entail a higher degree of socialstress than having high social status. Established so-cial relationships resulting in predictable behaviorare seen as a main reason for this, since all individu-als live in a stable social organization.Male-female bonding is very strong in colonies ofguinea pigs (see above; see also Jacobs 1976; Sachs-er 1986). There are three categories of females foran individual colony-living male: (a) his bonded fe-males with whom most amicable interactions takeplace, (b) females which live in the same colony, andwith whom he is familiar but has no social ties, and(c) unfamiliar females which live in a different colo-ny, and which he has never before encountered. In-terestingly, the males endocrine stress responsewhen placed in an unfamiliar cage, that is, his in-crease in PAC activity, is sharply reduced when thebonded female is present. In contrast, the presenceof a strange female or of one with whom he is mere-ly acquainted has little effect. Thus the effect of var-ious types of relationships differ remarkably, andsubstantial social support is given only by the bond-ing partner (Sachser et al. 1998).To summarize, guinea pigs establish complex andlong-lasting stable social structures in which the in-dividuals take different social positions. Establishedsocial relationships resulting in predictable behaviorprovide all members of the social system with highsecurity. Bonding partners give social support inchallenging situations. As a consequence, changes inpopulation parameters such as a rise in populationnumbers and stratification into different social po-

sitions do not seem adversely to affect the animalswelfare and health. The question arises, which fac-tors enable guinea pigs to arrange in such a non-stressful and nonaggressive way even at high densi-ties? The answer is: (a) a great tolerance towardconspecifics, which has been acquired during theprocess of domestication (see below); (b) the abilityto establish and to respect dominance relationships;(c) the ability to establish and to respect socialbondings. As the following section shows, however,whether these abilities are realized depends on thesocial conditions under which the individuals werereared.

Effects of Social Experiences on Physiologyand Behavior

When two adult males that have grown up in differ-ent large colonies are placed into an unfamiliar en-closure in the presence of an unfamiliar female, theyquickly establish stable dominance relationshipswithout displaying overt aggression. No significantchanges in PAC and SAM activities are found,either in the dominant or in the subdominant male(Sachser and Lick 1991). However, such a peace-ful stratification into different social positions re-quires that the opponents have been engaged inagonistic interactions with older dominant malesaround puberty, as is the case in individuals rearedin colonies. In such encounters they experience therole of a subdominant individual, whereby they ac-quire the social skills needed to adapt to conspecif-ics in a nonaggressive and nonstressful way (Sachser1993; Sachser and Lick 1991; the evidence that thetime around puberty is decisive for social develop-ment is summarized in Sachser et al. 1994).In contrast, a male which grows up singly, or with afemale, is prevented from agonistic interactionsaround puberty (since in this species no fighting andthreat displays are found between the sexes). Thusthese social skills cannot be learned. When twomales, both reared in such a way, confront one an-other in the presence of an unfamiliar female in anunfamiliar enclosure, high levels of aggressive be-havior are displayed, and escalated fighting is fre-quent. During the first days of the confrontation nostable dominance relationships are established. Wehad to stop about half of the experiments to avoidirreversible injuries and even death in the losers.Distinct and persistent increases in PAC activitieswere found mainly in the subdominant males(Sachser and Lick 1991; Sachser et al. 1994). Thereis evidence that fighting ability is not what deter-mines the outcome of such contests, but that the

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Fig. 2. Serum glucocorticoid concentrations incolony (solid lines; np6) and individually(dotted lines; np6) reared males before andafter transfer into an unfamiliar colony for20 days. **P~0.01, ***P~0.001. (With per-mission from Sachser and Renninger 1993)

winners are the males that succeed in establishing abond toward the female.The crucial role of social experiences has also beenshown in study taking a different approach (Sachserand Renninger 1993). Colony- and individuallyreared males were introduced singly into unfamiliarcolonies of conspecifics for a period of 20 days. Col-ony-reared males easily adjusted to the new socialsituation. On the first day they explored the new en-vironment but did not court any female, therebypreventing attacks from the male residents whichhad established bondings toward the females. In thecourse of the following days they gradually inte-grated into the social network of the established col-onies and could even gain a higher ranking socialposition than that which they had had in their nativecolonies. In the new colonies changes could not bedetermined in either their body weights or in theirPAC and SAM activities on the 1st, 3rd, 6th, 10th,and 20th days (see Fig. 2). In contrast, individuallyreared males were frequently involved in threat dis-plays and fighting. As a consequence they re-sponded to the new situation with substantial de-creases in body weight and with extreme increases inPAC activity (Sachser and Renninger 1993).

Effects of the Prenatal Social Environmenton Physiology and Behavior

Recently we discovered that even prenatal socialfactors have a profound effect on animals physiol-ogy and behavior when adult (Sachser and Kaiser1996; Kaiser and Sachser 1998). This experimentcompared daughters whose mothers had either lived

in a stable social environment (SSE) during preg-nancy and lactation (SE mothers) or in an unstablesocial environment (USE) during this period (UEmothers). The SSE was made by keeping the groupcomposition (one male, five females) constant; inthe USE situation every third day two females fromdifferent groups were exchanged. After weaning,groups of daughters were established from UEmothers (UE daughters) and groups of daughtersfrom SE mothers (SE daughters) consisting of fourfemales each. When adult, the spontaneous behav-ior of the daughters was recorded in their homecages. Surprisingly, the UE daughters were charac-terized by a distinct behavioral masculinization: theydisplayed behavioral patterns intensive naso-anallicking, rumba which are essential parts of themale courtship behavior that in mixed-sex groups ofguinea pigs are never shown by females (Fig. 3).This behavioral masculinization corresponds to sig-nificantly higher serum testosterone concentrationsin UE than SE daughters. PAC activity does not dif-fer between the two categories of females. Signifi-cantly higher adrenal tyrosine hydroxylase activities,as an indication of SAM activity (Fig. 3), and adren-al weights in UE than SE daughters, however, indi-cate higher degrees of stress in UE daughters (Kai-ser and Sachser 1998). Interestingly, the behavioraldifferences between UE and SE daughters are dueto the social instability during pregnancy while theperiod of lactation does not seem to be of impor-tance for this phenomenon (Sachser and Kaiser1996).What physiological mechanism caused the UEdaughters behavioral masculinization? We favorthe following hypothesis. The experimentally in-

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Fig. 3. Relative frequencies of male typical court-ship behavior (rumba) and adrenal tyrosine hy-droxylase activities of SE and UE daughters. Left,medians, ranges and 25% and 75% quartiles (eachbox np12). Right, meanscSEM (each columnnp8). **P~0.01, ***P~0.001. (With permissionfrom Sachser and Kaiser 1997)

duced change in group composition (i.e., social in-stability) probably constituted a stressor for thepregnant guinea pigs. As a consequence, an activa-tion of the PAC system can be expected. This wouldresult in increased secretion of glucocorticoids andalso androgens originating from the zona reticularisof the adrenal cortex (Heap 1979). The androgenswould cross the placenta and during a critical phase,which in the precocial guinea pig is during pregnan-cy (MacLusky and Naftolin 1981), would cause amasculinization of the female embryonic hypothala-mus (Breedlove 1992; Suchecki and Neto 1991).This could cause typically male behavior.

Conclusions

What general conclusions can be drawn from ourstudies in sociophysiology? When we look at the rel-evant literature in a comparative way four pointsemerge which obviously apply to many mammalianspecies:1. Social stratification is a general phenomenon inall species studied so far, both in their natural habi-tats and in captivity. Even in species in which closecooperation, social tolerance, and amicable relation-ships predominate, distinct differences in social sta-tus are observed among the adult individuals of agroup (e.g., Frame et al. 1978). Taken together, thefindings from guinea pigs and other nonhumanmammalian species suggest that in stable social sys-tems established dominance relationships result inpredictable behavior, and as a consequence differ-ences in social status do not lead to differences instress and health. Thus both high- and low-ranking

individuals can live in a nonstressful way (Sachser1994b). Under conditions of social instability, how-ever, significant increases are found in disease sus-ceptibility, mediated by hormonal responses. Lowerranking individuals which lose control of their socialposition show an extreme increase in PAC activitythat ultimately leads to deficiencies of the immunesystem. In contrast, animals that attempt to cope ac-tively with recurrent threats to their social positionsare characterized by a heightened SAM activation,ultimately resulting in cardiovascular disease. Sincethis behavioral pattern is often found in dominantsof species in unstable conditions, it is by no meansalways the lower ranking animal which is affectednegatively by its social status (Bradley et al. 1980;Christian 1975; Henry and Stephens 1977; Kaplan etal. 1982; Sachser 1994b; Sapolsky 1983; von Holst1990).2. In group-living mammals the ability to establishand respect dominance relationships is a prerequi-site to establishing stable social systems. Whetherthis ability is realized, however, depends on socialexperiences during behavioral development. Socialrearing conditions significantly affect behavioralpatterns in adulthood (e.g., Harlow and Harlow1962; Immelmann et al. 1982). Furthermore, specificbehavioral patterns in adulthood are related to thecause of stress and disease (Henry and Stephens1977; von Holst 1990). It is generally believed thatearly experiences in mother-offspring and/or sibling-sibling interactions are most important for the de-velopment of behavioral strategies in later life (Im-melmann et al. 1982). Our present data in guineapigs, however, point to the time around puberty ascrucial for the acquisition of those social skills

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needed to fit into stable social structures and to ad-apt to unfamiliar conspecifics in a nonstressful andnonaggressive way (Sachser 1993; Sachser and Lick1991; review: Sachser et al. 1994). Thus a causal rela-tionship between social rearing conditions aroundpuberty, aggressive behavior as adults, and the de-gree of social stress during the establishment ofdominance relationships is likely, but has not yetbeen verified as a general rule.3. Stress responses can be ameliorated by the pres-ence of members of the same species (e.g., Gust etal. 1994; Hennessy and Ritchey 1987; Henry 1993;Stanton et al. 1985). Frequently, however, such so-cial support cannot be provided by any conspecific(Mendoza et al. 1991; von Holst 1986, 1987), but theability to give social support is restricted to bondingpartners, as is seen very clearly in our present datafrom adult guinea pigs (Sachser et al. 1998).4. The study of behavioral ontogeny does not beginonly after birth, because prenatal factors can affectthe offsprings physiological and behavioral devel-opment (Gandelmann 1992; Hines 1995). Not onlydo artifical physical stressors act on the pregnant fe-male but also mild natural social stressors, such asinstability of the social environment during pregnan-cy, and these factors can have conspicuous effects,such as a distinct masculinization of the females be-havior (Sachser and Kaiser 1996; Kaiser and Sachser1998).

Domestic Guinea Pigs and Wild Cavies: AStudy in Domestication

The Behavior and Physiology of Caviaaperea f. porcellus and Cavia aperea

Guinea pigs were domesticated in South America30006000 years ago (Herre and Rhrs 1990). Inter-estingly, the behavior patterns are similar in thedomesticated and the wild animals; distinct differ-ences, however, occur in behavioral frequencies andthresholds (Knzl and Sachser 1997; Rood 1972;Stahnke 1987). Social interactions between membersof the domesticated form therefore proceed in acompletely different way from those between wildcavies. When a male domestic guinea pig is kept to-gether with one or several females, his mature sonsand daughters will integrate rather peacefully intothe social system of the group, and all animals willcohabitate in a nonaggressive and nonstressful way(as shown above). When wild cavies are kept in thesame group composition, a completely different pic-

Fig. 4. Serum catecholamine concentrations in males of wild cavies(np5) and domestic guinea pigs (np7). MeanscSEM. **P~0.01.(With permission from Knzl and Sachser 1997)

ture emerges: The daughters integrate into the lin-ear dominance hierarchy of the females, which isage dependent, the oldest female filling the highestand the youngest female the lowest position. In con-trast, the father and his sons become rather incom-patible when the sons attain sexual maturity. Thenin most cases they must be taken out of the groupsbecause otherwise the father will injure and evenkill them (Kuczius and Sachser 1992). Thus one ofthe major differences between wild cavies anddomestic guinea pigs is the considerably higher ag-gressiveness of the wild form, which makes it nearlyimpossible to keep adult males together in the pres-ence of females. Correspondingly, domestic maleand female guinea pigs display more sociopositvebehaviors than their wild ancestors. In addition,overt courtship behavior is more frequently ex-pressed, and a lower threshold for vocalization isfound in the domesticated form (Knzl and Sachser1997; Rood 1972; Stahnke 1987).Recently we assessed PAC and SAM activities inwild cavies and domestic guinea pigs to test for pos-sible endocrinological changes during the process ofdomestication (Knzl and Sachser 1997). The ani-mals were housed in groups of one adult male andtwo adult females under standardized conditions.When the males were caught, and a blood samplewas taken from their ear vessels, cortisol titers didnot differ significantly between males of the wildand domesticated forms. In contrast, serum epineph-rine and norepinephrine concentrations were five tosevenfold higher in the wild cavies than in thedomestic guinea pigs (Fig. 4).

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Conclusions

It appears that in the guinea pig the process of dom-estication has led to typical traits reduced aggres-siveness, increased tolerance of conspecifics, largersize that have also been found in comparisons be-tween wild and domestic forms of other species(Boice 1971; Fox 1978; Herre and Rhrs 1990).These results are what one would predict if thosewho originally domesticated the guinea pig for foodhad selected the largest animals for breeding andeliminated aggressive troublemakers (Rood 1972).Our physiological finding the decreased reactivityof the SAM system might explain a further conspi-cious trait of domesticated animals compared totheir wild ancestors: the distinctly reduced degree ofnervousness and timidy (Hemmer 1982; Price 1973;Smith 1972) which obviously helps them to adjust toman-made housing conditions (Knzl and Sachser1997).It nevertheless remains surprising, that such anagreeable animal as the domestic guinea pig shouldhave been derived from highly aggressive ancestors.This obvious paradox might be explained not onlyby changes that occurred during the process of dom-estication but also in the following way: the wildcavy has a wide distribution, from Venezuela andColombia to northern Argentina. The process ofdomestication obviously took place in the Andes(Herre and Rhrs 1990). In contrast, the wild cavieswhich have been studied so far did not originatefrom a mountain region but from the grasslands ofBuenos Aires province. It is well conceivable thatowing to the different ecological conditions underwhich the two populations live, distinct differencesin social tolerance may have evolved by natural se-lection. The guinea pig may therefore have beendomesticated from a population of more tolerantanimals than those which were studied by Rood(1972), Stahnke (1987), and our group (Knzl andSachser 1997; Kuczius and Sachser 1992).

Wild and Yellow-Toothed Cavies: AStudy in Social Evolution

Mating System, Testis Size, and ReproductiveSuccess

The wild cavy (C. aperea) is one of about ten speciesof wild guinea pigs which belong to four genera(Cavia, Galea, Microcavia, Kerodon) of a subfamily(Caviinae). In wild cavies adult males are incompati-

ble, whereas females organize themselves into a lin-ear dominance hierarchy (as shown above). Escal-ated agonistic interactions between the sexes neveroccur. As a consequence, a polygynous mating sys-tem exists: whenever a female comes into estrus,only one male is present. This male thus mates withseveral females, whereas every female mates with asingle male. The closely related yellow-toothed cavy(G. musteloides) behaves in a completely differentway: these animals can be kept in large mixed-sexcolonies. Brief phases of high activity alternate sev-eral times daily with phases of inactivity, duringwhich all or nearly all members of the group huddletogether with close bodily contact. The mating sys-tem is promiscuous; although the highest rankingmale guards the female during estrous, he is not suc-cessful in preventing the lower ranking males fromcopulating (Rood 1972; Schwarz-Weig and Sachser1996). Promiscuous mating is achieved by the fe-males behavior, which attracts the attention of allthe males and makes it impossible for a single maleto monopolize her. The females thus are actively in-volved in bringing about promiscuity (Schwarz-Weigand Sachser 1996).Variation in mating systems is frequently related torelative testis size (Harcourt et al. 1981; Harvey andHarcourt 1984; Kenagy and Trombulak 1986). Inspecies in which only one male mates (polygynousand monogamous species), low testis weights in rela-tion to body weights are found, whereas males ofpromiscuous species are characterized by high rela-tive testis weights. Presuming that testis size is posi-tively correlated with the volume of ejaculate, spermcounts, and sperm motility (Harvey and May 1989;Mller 1988), it is reasonable to assume that inpromiscuous species males do not compete for ac-cess to females via agonistic encounters but that be-havioral competition is replaced by sperm competi-tion.With this theory in mind, we determined the testissize in both species (Fig. 5). Indeed, the promis-cuous G. musteloides males had distinctly higher ab-solute and relative testes masses than the polygy-nous C. aperea although the latter are characterizedby a 25% higher body weight (Schwarz et al. 1994).The relative testis masses, which were calculated ac-cording to the formula of Kenagy and Trombulak(1986), can be compared directly with those of othermammals. The values found in C. aperea are withinthe range that is typical for polygynous species. Incontrast, the relative testis size of G. musteloidesmales is among the highest ever recorded in a terres-trial mammalian species with a known promiscuousmating system (Kenagy and Trombulak 1986;Schwarz-Weig and Sachser 1996). Interestingly, the

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Fig. 5. Relative testis size in mammals (according to Kenagy andTrombulak 1986). Left, mammalian species with single-male (mono-gamous and polygynous) and multimale (promiscuous) mating sys-tems. (Data from Kanagy and Trombulak; values shown are onlyfrom those species whose type of mating system is known). Each dot,the value of a species; columns, medians. Right, individual values of C.aperea and G. musteloides. Each triangle, the value of a single individ-ual; columns, medians. (With permission from Schwarz-Weig andSachser 1996, extended by unpublished data from Schwarz-Weig andSachser)

relative testis size of the domestic guinea pig is quitesimilar to that of the C. aperea, its wild ancestor(Sachser, unpublished data). This finding corre-sponds well to a polygynous mating system which istypical not only for the wild but also for the domes-ticated form (see above).Recent findings from DNA fingerprinting have con-firmed what behavioral observations and testis sizesuggest for G. musteloides: the existence of a prom-iscuous mating system. In three mixed-sex groups ofthis species (four males and six/seven females) mul-tiple paternity was found on average in more than80% of the litters, that is, more than one and up tothree males were represented as fathers (Keil et al.,submitted). To our knowledge, a comparably highpercentage of multiple paternities has been de-scribed only in Beldings ground squirrels (Hankenand Sherman 1981).Traditionally it was thought that multiple matingsare without any benefits for females. Their role inachieving promiscuous matings should therefore berather passive. From our behavioral observations itappears, however, that female G. musteloides are ac-tively involved in bringing about promiscuity(Schwarz-Weig and Sachser 1996). We thereforestudied whether a reproductive benefit exists for fe-

males which mate with more than one male. Indeed,females which in a mating experiment were pairedwith four males and became pregnant, weaned sig-nificantly more surviving offspring than femaleswhich were paired with a single male. Litter sizes didnot differ between the groups (Keil and Sachser1998). The data support the hypothesis that promis-cuous females copulate with several males to inducesperm competition and/or zygote selection andthereby increase the viability of their offspring(Eberhard 1996). The physiological mechanism be-hind this phenomenon remains to be clarified.

Conclusions

Many questions concerning the proximate mecha-nisms which help to establish and maintain differentsocial and mating systems can only be answered un-der controlled laboratory conditions. The same mayapply when specific hypotheses concerning the evo-lution of mating systems are tested. In our case sucha laboratory approach revealed that C. aperea andG. musteloides are two closely related species withdivergent mating systems and functional variationsin testis size. The polygynous mating system of C.aperea is brought about mainly by the incompatibili-ty of the adult males. The promiscuous mating sys-tem of G. musteloides results from the higher com-patibility of the males and the females soliciting be-havior when receptive. Moreover, it is shown for thefirst time that a female mammal has a reproductiveadvantage from promiscuous mating. However, a la-boratory approach cannot elucidate the ultimate fac-tors which have resulted in different individual be-haviors, in different interaction patterns, and thus indifferent social and mating systems in these two spe-cies of wild guinea pigs. For this, differences in be-havior must be related to differences in ecologicalconditions (e.g., distribution of food and/or preda-tors) in the natural habitats of C. aperea and G. mus-teloides. Until now these data are largely lacking.We have therefore recently begun to carry out suchfield studies in cooperation with colleagues fromSouth America to understand how each species be-havior is adapted to the specific environmental con-ditions under which it lives.

Conclusions

In 1963 Niko Tinbergen, one of the founders ofethology, formulated the famous four problems ofbehavioral biology: the problem of causation, the

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problem of survival value, the problem of ontogeny,and the problem of evolution. He insisted that acomprehensive, coherent science of behavioral bio-logy must give equal attention to each of these andto their integration. Recently Dewsbury (1992) sug-gested an up-to-date reformulation of Tinbergensfour problems, that is, to consider them in relationto the genesis, control, and consequences of behav-ior. One might differ over whether he was able tosucceed in this. (I personally think that he did, butfor a criticism see Alcock and Sherman 1994). In anycase agreement has existed for decades that a com-prehensive understanding of behavioral phenomenarequires research at quite different levels of analy-sis.However, in practice such multilevel approaches arerare. This is a pity, for we have also had to learn inour research that a comprehensive understanding ofthe social life of guinea pigs is possible only if theirbehavior is analyzed from different points of view.In doing this a complex picture emerged: social in-teractions have consequences for the individuals re-productive success not only but also for their de-grees of stress and welfare. The way in which indi-viduals interact is controlled not only by their sex,age, physiological state, and present environmentbut also by the social experiences which they haveundergone. Furthermore, the study of ontogenydoes not begin at birth, because prenatal social fac-tors can also affect the animals behavior when ad-ult. In addition, to understand the genesis of interac-tions between domesticated animals requires knowl-edge of the behavioral and physiological changeswhich have occurred during the process of domesti-cation. Finally, understanding the social interactionsbetween the wild ancestors of the domesticatedform includes knowing how their behavior patternshave evolved by natural selection.

Acknowledgements. I thank Claudia Bger, Trevor G. Cooper, GertiDcker, and Sylvia Kaiser for critical comments on the manuscript.This work was supported by grants form the Deutsche Forschungsge-meinschaft (Sa389/1-3). All experiments comply with current Germanlaws.

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