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Evolutionary Anthropology 14:170 –185 (2005) ARTICLES Big Times for Dwarfs: Social Organization, Sexual Selection, and Cooperation in the Cheirogaleidae OLIVER SCHÜLKE AND JULIA OSTNER “One can picture a small-bodied ancestral primate moving actively around among the fine branches of trees, foraging on small fruits and on small animal prey, rather like modern . . . mouse lemurs.”1 (p. 658 – 659). This and earlier quotes have shaped the common perception of the dwarf lemurs of the family Cheirogaleidae as being “primitive primates,”2 which inadvertently conveys notions of the archaic, outdated, unelaborated, simple, invariant, inflexible, and hardwired. In this paper, however, we do not focus on the relative level of complexity of cheirogaleids, but instead emphasize the pronounced variation in their social behavior, sexually selected strategies, and kin-selected behavior. By investigating potential causes for this variation, we aim to contribute to further development of general concepts and theories of primate behavioral ecology that apply to all primates, large and small. The latest phylogenetic reconstructions place the cheirogaleid family very close to the root of the lemur tree.3 Today most authors agree that Madagascar was colonized in a single event, that lemurs are monophyletic, and that the aye-aye, Daubentonia madagascariensis, diverged first from their ancestral stock.4 –7 Cheirogaleidae probably were the second family that branched off,3,8 which would Drs. Oliver Schülke and Julia Ostner are in the department of Integrative Primate Socioecology at the Max-Planck Institute for Evolutionary Anthropology, Germany. During the past several years they have focused their research on the behavior and ecology of Malagasy lemurs. They are currently examining the socioecology of macaques in Thailand. Email: [email protected] and [email protected]. *Correspondence: Dr. Oliver Schülke, Integrative Primate Socioecology, Max-Planck Institute for Evolutionary Anthropology, Deutscher Platz 6, Leipzig, 04103, Germany. Tel: ⫹49-(0) 341-3550232, Fax: ⫹49-(0) 341-3550-299, E-mail: schuelke@ eva.mpg.de © 2005 Wiley-Liss, Inc. DOI 10.1002/evan.20081 Published online in Wiley InterScience (www.interscience.wiley.com). support the notion that they retained many characters that are ancestral to all lemurs and primates in general. In addition to the smallest living primates, those of the genus Microcebus (8⫹ species), the family Cheirogaleidae comprises four genera: Phaner (4 species), Cheirogaleus (7 species), Mirza (1 species), and Allocebus (1 species) (Fig. 1). Morphological and genetic traits, but not behavioral traits, suggest that Phaner may be classified as a subfamily or even a separate family.9,10 (Taxonomy within genera has changed rapidly. The first systematic studies covering large areas of the distribution demonstrated high species diversity in Microcebus11,12 and Cheirogaleus,13 and elevated subspecies to the species level in Phaner.14) As a family, the cheirogaleids have colonized the entire Island of Madagascar (Fig. 2), inhabiting the spiny forest and dry forests in the south and west, and wet evergreen forests and marsh habitats in the east and north.15 EVOLUTION OF SOCIAL ORGANIZATION The social organization of cheirogaleids is highly variable. They live truly solitary lives, form dispersed pairs, or live in groups of variable composition. They may form sleeping associations and use large parts of their home ranges together, but they always forage independently at night (Box 1). The distribution of females in space is mainly influenced by ecological factors, namely the abundance, distribution, quality, and size of food resources.16,17 The socioecological model makes explicit predictions about the relationships between food-resource characteristics, the resulting competitive regimens, and consequences for social organization and structure.17,18 Males mainly react to the distribution of females19; this is elegantly demonstrated by an evolutionary time lag between changes in female group size and the subsequent adjustment of male numbers.20 Information on food-resource characteristics is incomplete for most cheirogaleids, precluding larger comparative tests of the socioecological model. Therefore, we will only briefly characterize the diets of the well-studied species. Broadly categorized, Cheirogaleus and Microcebus species are omnivorous, feeding on the reproductive parts of various tree species and small-animal prey they either catch in flight or pursuit or extract from nests and crevices.21–23 Mistletoe (Bakarella grisea) seems to be a staple food resource that is reliably available yearround for M. rufus and perhaps C. major.22,24 In the dry western forest, fallback foods for M. murinus and Mirza coquereli include large amounts of tree exudates and insect secretions.21,25–27 However, the exudate specialist, P. furcifer, proves agonistically dominant whenever encountered in trees yielding exudate.27 In addi- Big Times for Dwarfs 171 ARTICLES Figure 1. Some members of the family, Cheirogaleidae: A) Phaner furcifer, B) Microcebus berthae, C), Cheirogaleus medius, D) Mirza coquereli. Photo credits: A—Julia Ostner, B–D Manfred Eberle. tion, the population density of M. murinus in secondary forest depends on the physical characteristics of the habitat, specifically the thermal-insulation capacity of the crown cover, which influences the economics of torpor and hibernation.28 Apart from tree exudates, M. coquereli feeds on the fruit and nectar of various plants. This species also hunts and consumes several invertebrates and vertebrates, including snakes, chameleons,21,29,30 Circumstantial evidence suggests that it even hunts on Microcebus murinus.30 On a broad scale, invertebrate food availability seems to determine population density in M. coquereli.29 Evolution of Pair-Living in Phaner and Cheirogaleus Phaner furcifer spends more than three-quarters of its feeding time each month on consumption of tree exudates, mainly from baobabs (Adansonia rubrostipa) and taly trees (Terminalia aff. diversipilosa); time spent in the latter makes up 50% of feeding time. This most important resource is scarce, patchily distributed, can be used by only one animal at a time, and is aggressively defended and rapidly depleted. According to socioecological theory16,18,31 these characteristics predict strong within-group scramble and contest competition for food. As expected, scramble competition has a negative group-size effect on female physical condition, so that females living only with a male and no offspring are in better physical condition than are females sharing their territory with one or two offspring.32 The effect of contest competition is reflected in the superior physical condition of agonistically dominant females over subordinate males.32 Delayed natal dispersal is responsible for some of the variation in P. furcifer family size and, thus for female physical condition via scramble competition. It has been proposed that high dispersal costs accruing from the reduced foraging efficiency of specialist gummivores when they are explor- ing unknown habitat keep offspring from dispersing into uninhabited areas. Full-grown offspring are thought to wait and compete for vacancies in existing territories. Offspring’s high dispersal costs are likely responsible for parents’ tolerance of full-grown offspring in the natal territory despite the cost to their own future reproduction.32 This hypothesis gains indirect support from the fact that the number of full-grown offspring in highly gummivorous marmoset groups is higher than that among their closest relatives, the more frugivorous tamarins, as well as from the occurrence of floater males in sympatric C. medius. Although the food resources of C. medius may also be scarce,33 they are larger and do not require repetitive feeding itineraries, and thus do not constrain full-grown offspring from roaming over large areas. None of the established hypotheses for the evolution of pair-living among primates received a priori support with regard to P. furcifer, which led to formulation of the intersexual feeding competition hypothesis.34 The ancestral social organization type in cheirogaleids is believed to be a Mirza-like condition in which solitary males and females have mutually overlapping home ranges.2 Assuming that intense feeding competition within extant families reflects the situation in the past, ancestral P. furcifer females may have developed range exclusivity as a reaction to strong within-group feeding competition. Males, however, might still have used home ranges overlapping with those of many females until females began forming pairs with single males by displacing all other males. Under this hypothesis, females benefit from forming pairs by a reduction of independently moving foraging units in their territory, thus increasing the predictability of resource value and facilitating more precise foraging decisions.35,36 In a next step, males take the duty of defending the territory against other males. This service may make it economically worthwhile for females to share their territories and leads to the formation of pairs if males are unable to defend more than one female territory against other males. However, dispersed harems, 172 Schülke and Ostner with one male ranging over two or more exclusive female ranges is the optimal grouping pattern for both males and females. For females this pattern reduces the number of competitors for food; for males, it increases access to mating partners. But dispersed harems may not form for two reasons, reduced foraging efficiency and generally low mate-guarding potential. The foraging efficiency of P. furcifer depends on its knowledge of the current value of resources in the territory. A single individual with exclusive access to a territory’s resources could optimize its return time to exudate trees by taking into account the costs of moving between trees and the relative resource values of current and surrounding patches.37 Deciding to leave a patch or which one to use next becomes more complicated if individuals share resources. To make it even worse, there is circumstantial evidence that males are not well informed about their female partner’s whereabouts,38 which probably is in the females’ interests. Add to this the unconditional female dominance over males and it begins to appear too costly for a male to forage in two female territories, where he will find resources just depleted by one of the females or be aggressively displaced from a resource he just entered. A male sharing a territory with two females would likely suffer decreased foraging efficiency, leaving him with an unbalanced energy budget. The second problem that males encounter when defending two female territories against rivals is related to mating success and its reproductive consequences. The strategy of forming pairs may be stabilized if additional benefits are derived from it. Possible benefits accrue from male services to the female that increase her and her offspring’s likelihood of survival and reproduction.34 A male’s willingness to provide services usually depends on paternity certainty,39 but may also rely on the probability of increasing his future mating success irrespective of his relatedness to the tended infant.40 The latter may play a role in species such as P. furcifer and C. medius, where divorce occurs at very low rates,38,41 so that males that ARTICLES invest during one season will still be around in the next. It has been argued that paternity certainty is likely to be low in all nocturnal pair-living primates due to factors that hamper effective mate guarding.10,39,42 In addition to reduced foraging efficiency, this inability of males to mate guard effectively might be a second factor that prevented the evolution of uni- Occasional nursing of others’ offspring might, therefore, simply be a byproduct of a highly beneficial family insurance that buffers mothers against the overly high risk of dying from predation before their offspring are independent. Hence, haplotypes of cooperating females are less likely to be eliminated in stochastic processes and this feed-back loop enhances cluster formation. form dispersed harems in P. furcifer. In short, pair-living can be regarded as a compromise for both males and females, a possibility not accounted for in any established hypothesis on the evolution of pair-living in primates.43 C. medius accomplishes the preparatory increase in body mass and fat reserve before the seven-month hibernation period mainly during the late wet or early dry season, when animals reduce their energetic costs by reducing locomotor activity and, at the same time, switch their diet to fruit extraordinarily high in sugar.44,45 Because fruiting periods are relatively short, the diet changes rapidly even between successive fortnights. Accordingly, single tree species may be very important during short periods. At Ampijoroa, C. medius food choice is highly selective and concentrated on a few plant species.33 The influence of food-resource characteristics on competitive regime and social structure has not yet been investigated. Females are heavier than males on average, although body size does not differ between the sexes.46 If females were dominant over males, as in M. murinus, P. furcifer, and most large lemurs,23 the sex difference could be a rank effect that demonstrates withingroup contest competition for food resources. Observation of two females in Ampijoroa suggests that sharing a territory with one male is associated with higher female body mass than is living with a male and a two-yearold offspring.47 This may indicate that indirect feeding competition also plays a role for C. medius. It has been argued, however, that scramble competition is weak,41 since fullgrown offspring of age two and older regularly delay dispersal (for one year in Kirindy, two years in Ampijoroa47), resulting in groups of five to six individuals. But delayed dispersal may develop even at a cost to parents’ reproduction.32 Further, the biannual distribution of births in Kirindy suggests strong constraints on female fertility.48 Although physical condition (body weight in relation to body size) could be compared between females living in groups of different sizes, these data have not been published. Pair-living among C. medius is stabilized by paternal care.46,47,49,50 Male care for offspring includes babysitting, playing, and traveling and sleeping with infants in the nest during the day, and responding to their calls.41 Babysitting is likely to have the most profound effect on infant survival and, at the same time, may be the most costly form of parental care. During the first two weeks after birth, infants stay in the tree hole all night. Later, one parent escorts the independently moving infants on their first excursions. Parents take turns staying near or in the tree hole for 28% of the time, on average (20% to 100%).50 Before hi- Big Times for Dwarfs 173 ARTICLES such as reduced foraging efficiency as in P. furcifer, are not obvious. A Model for the Evolution of Microcebus Social Organization Figure 2. Madagascar’s remaining forest and main sites of socioecological studies on cheirogaleids. Forests in the Southwest not shown. bernation and after parental duties, fathers have a tendency to store less fat than do other males.50 A high predation rate (20%) and the observation of active defense against a snake suggest that the major benefit of babysitting is predation reduction. It has been argued that without paternal care females could not raise their young successfully.46,50 Nevertheless, paternal care cannot be the ultimate cause for the evolution of pair-living because it requires female dependence on male help before the helper is available.39,51 Hence, other factors must be responsible for initial pair formation. As described earlier, circumstantial evidence suggests that within-group feeding competition among C. medius is intense and that female range exclusivity might have evolved in response to this competition. As in P. furcifer, females may have benefited from coordinating movements with a single male rather than several males with slightly overlapping home ranges. However, the benefit to males of pair formation remains unknown. With a nightly path length of 1.6 to 2.4 km, a male should be able to defend more than one 2-ha female territory.41 Additional costs from ranging over two territories, Although detailed information about Microcebus diets is lacking, species of the genus represent an interesting test case for the socioecological model because female distribution alone cannot explain why females associate with males in different ways (Box 1). Whereas M. murinus females at Kirindy and Ampijoroa form dispersed all-female groups and never associate with males,52,53 at Mandena females share sleeping sites with central males during the mating season.54 M. ravelobensis females form permanent dispersed multi-male, multi-female groups.55 M. berthae also live in dispersed groups, but the modal group contains a single female and several males.56 We propose a model that explains variation in Microcebus social organization as resulting from differences in the ecologically determined potential for cooperative breeding and differences in the choice of sleeping sites (Fig. 3). Where ecological conditions allow high population density, the ranges of many females may overlap and the likelihood of living close to kin will be high. We hypothesize that all Microcebus species have the potential to breed cooperatively with kin if conditions permit, which makes the formation of female sleeping groups highly beneficial. Although cooperative breeding is restricted to a twomonth lactation period, it may nevertheless explain the stability of allfemale groups over time, because cooperative breeders need a period of behavioral adaptation and coordination before successful cooperation.57 Whether females associate with males depends on the costs and benefits of these associations for both. These costs and benefits seem likely to be related to sleeping habits since male foraging ranges overlap with those of females irrespective of mixed-sex group formation. Two potential benefits of communal nesting among Microcebus have been proposed: im- 174 Schülke and Ostner ARTICLES Box 1. Social Organization Among Cheirogaleids Different categories of social organization can be defined according to size, sexual composition, and spatiotemporal cohesion of a social unit.79 As a necessary condition to constitute a social unit, animals that share a common range must also exchange more social interactions than they do with other conspecifics. Each male and female either lives solitarily or with a certain number of other males and females.79 This yields six types of social organization: solitary animals; pairs; one-male, multi-female groups; multi-male, multi-female groups; multi-male, one-female groups, and all-female groups. Units are either cohesive, with members traveling in closed formation, or dispersed (fission-fusion societies in diurnal primates) with members of a unit spending the bulk of their activity time away from one another and meeting only rarely.2 All cheirogaleids live in dispersed societies or solitarily, and thus are encountered alone, making them difficult to follow and observe. Hence, data available on their social organization concern spatial organization proved thermoregulation52,55,58,59 and reduced predation risk.58,59 These two benefits do not accrue for animals sleeping in tree holes. M. murinus choose certain tree holes as preferred sites because of their insulation capacity,52,60 which at least partly determines the amount of energy saved during daily torpor.52 Communal nesting has no effect on the energy budget of C. medius hibernating in tree holes.61 We argue that since the processes involved in hibernation and torpor are functionally very similar it is likely that tree-hole users will not benefit from improved thermoregulation by sharing a sleeping site (but see Schmid,52 Kappeler,58 and Radespiel and coworkers60). The empirical test under natural conditions is pending. Any sleeping site more open than a tree hole will have a lower insulation capacity, which might call for communal nesting. Lemurs’ huddling be- (that is, range size and overlap between and within the sexes): size and composition of sleeping groups; and interaction frequencies among individuals (Table 1). Capture-recapture data are not suitable for defining social organization. Taking population differences into account, the six well-studied species live in six different social-organization types (Fig. 4) Only Mirza coquereli is truly solitary; it never shares sleeping sites and interacts only rarely.88 Phaner furcifer and Cheirogaleus medius live in uniform dispersed pairs with their offspring in well-defined territories,38,46,49 and share sleeping sites to varying degrees. In C. medius, single males may also live as floaters in undefined very large home ranges overlapping those of several pairs.41,47,48 In all Microcebus murinus populations, females form small permanent sleeping groups. The home ranges of female sleepinggroup members overlap with each other more than they do with the ranges of nonmembers.53,54 In Mandena, M. murinus females form population nuclei.54 Only a few cen- havior occurs in response to low ambient temperatures62 and may also be beneficial to torpid animals using semi-occluded shelters, although this has never been tested. At the onset of a torpor bout, an individual allows its body temperature to drop passively to almost ambient levels.52 Huddling closely with warm conspecifics might slow down this process and thus decrease the time spent at energetically preferable low body temperature. When ambient temperature rises again and passively drags up the body temperatures of torpid individuals, huddling partners could serve as ice cubes and beneficially slow down the rewarming process. As long as the cost-benefit ratio cannot be quantified, we might regard communal nesting in shelters other than tree holes as energetically beneficial. The choice of sleeping site may also affect whether there is a predation- tral males have access to these nuclei. Smaller, peripheral males live solitary lives outside of population nuclei. It seems possible that a nucleus is composed of several small, dispersed one-male, multi-female groups. At Ampijoroa and Kirindy, M. murinus lives in all-female groups, males are solitary, an organization type not found in any other primate. M. ravelobensis and M. berthae form stable, dispersed mixed-sex groups and males rarely sleep alone.55,56 Each individual’s home range is smaller than the entire group’s, but the ranges of group members overlap more with each other than with those of nonmembers.55 It is not clear yet whether social interactions follow the same pattern. M. berthae mainly forms multi-male, one-female groups; all-female groups are very rare.56 M. ravelobensis is often found in social units with several females. The fact that not all sleeping-group members have been identified and sexed in M. ravelobensis55 suggests that the modal pattern is a multi-male, multifemale group. avoidance benefit of communal nesting.59 During the day Microcebus faces predation risk from snakes, carnivores, and raptors, all of which inspect tree holes for potential prey.63 Deep tree holes with narrow entrances and solid, intact walls may reduce the overall risk of predation as compared to more open shelters. However, once a predator has access to the hollow it will likely take all individuals sleeping in a tree hole one by one. Hence, there is no benefit from communal nesting. In contrast, sleeping in a more open site may have several benefits: the predator might be detected earlier; might be confused if several individuals flee in different directions, reducing the per capita risk of predation; or individuals might join forces to drive away the attacker64 or even to free an already-captured conspecific.65 None of these benefits apply Big Times for Dwarfs 175 ARTICLES Figure 3. A Theoretical model of the evolution of social organization in Microcebus (see text for details) when animals sleep in tree holes with only one entrance. Differences in sleeping-site choice may be related to the general availability of tree holes in a habitat. Moreover, the number of different animal species using the same tree holes is high in many of Madagascar’s forests, suggesting a strong competition for tree holes even where they occur at high density.65 Hence, niche separation among all tree-hole users, among nocturnal lemurs66 and, importantly, among different Microcebus species may play a major role in sleeping-site choice.67 The description of several new species11,12 has brought about the realization that many forests harbor more than one species of Microcebus.11,12,68,69,70 Pairs of sympatric species such as M. murinus/M. berthae or M. murinus/M. ravelobensis do indeed use different sleeping sites, which promotes the idea of niche separation contributing to the differentiation. The available data match the model shown in Figure 3. M. murinus lives at high to moderate densities in Kirindy and Ampijoroa. Using tree holes, females share sleeping sites with close kin and cooperatively rear their young. Thus, females might not gain extra benefits from allowing the generally subordinate males71 into their groups. Consequently, they form allfemale groups. Despite extreme range overlap among males, they typically sleep alone.53,72 Furthermore M. murinus males at Kirindy may not form permanent groups with females because only females hibernate before the mating season. Males that stay with hibernating females will be less well-informed about mating opportunities in the area. Also, if males hibernate they will be in worse physical condition than will nonhibernating male competitors,73 which will reduce their reproductive success.74 A test of this hypothesis would be a low-density population near Ampijoroa where females cannot find female kin with which to breed cooperatively and where climatic conditions keep females from hibernating. Under these conditions, we predict that the social organization would be similar to that among M. coquereli. The better-studied part of the M. ravelobensis population at Ampijoroa lives at high density. Genetic data and data on cooperative breeding are not available yet. Females typically sleep in open places; the one tree hole used was the site least often used in the study.75 The fact that, in sharp contrast to all M. murinus populations,54,60,76 males almost never sleep alone supports the idea that communal nesting is highly beneficial. The major cost of mixed-sex group formation for females is the risk of infanticide by male group members or immigrant males. Infanticide may pay a male with very low paternity certainty if early loss of infants will increase the mother’s physical condition and allow her to invest more heavily in the next litter. Females may, however, confuse paternity by mating with all group members and many other males that live close by.77 Males seem to have adapted to a high level of polyandry in females, as demonstrated by very large testis size in all Microcebus species investigated so far.42 M. berthae lives at the lowest population densities described for the genus78 (Table 1). Low density is coupled with unusually large female home ranges, very low female intrasexual range overlap, and extremely long travel distances. This suggests that food-resource characteristics and exploitation regimens are indeed responsible for the observed low population density and indicates that intrasexual feeding competition influences female spatial distribution as well.56 Genetic relatedness between females living in close proximity is low and does not differ from levels of related- 176 Schülke and Ostner ARTICLES ecological model stresses that males react to the distribution of females but also recognizes ecological constraints on males,80 which are often overlooked.34,81,82 The mating system acquired by each Microcebus species has to be played out in the arena set up by its social organization. SEXUAL SELECTION: COMPETING FOR MATES Male Mate Competition and Female Choice in Mirza and Microcebus Figure 4. The central part of each diagram shows overlap between group ranges depicted as double lines. Where there are no groups male ranges are shown in dotted and female in solid lines. Arrows point to diagrams representing spatial relationships of individuals within groups. Solid lines: females, dotted lines: males, magnifying glass: 3⫻ magnified. ness between locally distant females.56 Hence, females do not have the opportunity to form cooperative breeding units with close kin. They do not use tree holes.56 Males share a sleeping site more often than do any M. murinus males. The most important test case for the entire model will be a high-density M. berthae population with spatial clusters of female kin, which we predict would live in multi-male, multi-female groups with cooperative breeding. We have demonstrated that the proposed evolutionary model has the po- tential to explain variations in the social organization of Microcebus. We have also proposed several future studies to test the model’s predictive power. Our analysis highlights the necessity to tease apart patterns of social organization and variation in mating systems when evolutionary causes are sought.38,79 Without doing so, the highly explanatory ecological causes for differences in male association patterns would likely have been overlooked and variations in male behavior attributed to differences in male mating strategies. Indeed, the socio- Spatial polygyny has been proposed as the general mating system of primates living in dispersed societies or solitarily.83,84 However, comparative studies of interspecific variation in sexual dimorphism in body and canine size, as well as testis size among strepsirrhine primates revealed that lemurs generally lack sexual dimorphism in these traits and that all solitary and group-living lemurs have very large testes relative to their body size.85– 87 This combination of traits indicates the prevalence of scramble or indirect competition instead of direct spatial monopolization of females and led to the prediction that scramble polygyny is the modal mating system of Mirza and Microcebus.2,88 Only one long-term study of a large number of radio-collared individuals has been conducted on M. coquereli so far.88 This study focused on capturerecapture data over four successive mating seasons, gathering a wealth of morphological data as well as spatial information during focal observations. Results confirmed the lack of sexual dimorphism in canine size as well as large testes. In addition, interand intrasexually overlapping home ranges, as well as a four-times-larger male home range size during the mating season are evidence of the proposed mating system of scramble polygyny.85,86 However, contest competition also plays a role, albeit a smaller one, as indicated by significant sexual dimorphism in body mass, stable throughout the year, as well as the occurrence of more common injuries to males than females.88 While this study was the first to test and confirm the prevalence of scram- Big Times for Dwarfs 177 ARTICLES TABLE 1. Characteristics of Cheirogaleid Social Organizationa Species Population Social Organization Mirza coquereli Kirindy11,88 Phaner furcifer Cheirogaleus medius Microcebus murinus HR Size HR MS HR Overlap solitary 8M 10F M 4 ha F 3.5 ha M 4x FF high MM high FM high none (one FF) Kirindy38,69 dispersed pair 13M 9F pair 5 ha M 0x MF 0.3/d Ampijoroa47,60 dispersed pair 4M 4F pair 2.4 ha M 0x Kirindy41,61 dispersed pair & floaters 22M 14F pair 1.6 ha floater 4 ha M 0x Ampijoroa53,78 all-F group solitary males 12M 12F M 2.8 ha F 1.8 ha M 2x Kirindy74,98 all-F group solitary males 36M 56F M 1.9 ha F 1.3 ha M 1.5x Mandena18,54 oneM, multi F group peripheral M multiM, oneF group 3M 6F nd nd 19M 9F M 5 ha F 2.5 ha M 0.3x oneM, multiF group 15M 14F M 0.55 ha F 0.52 ha M 1.2x FF low MM low FM high FF low MM low FM high FF low MM low FM high FF high MM high MF high FF high MM high MF high FF high MM low MF high FF low MM moderate MF high FF high MM high FM high Microcebus berthae Kirindy56,80 Microcebus ravelobensis Ampijoroa55,79 a Sleeping Gr. N Interactions/hr 0.1/h agon affil 0.03/h affin 0.03 within 1/h between 0.2/h Pop. Density nd 57 MF 0.5/day nd nd MF 0.7/day 0.3/h nd FF group 0.5/h affil/affin 0.4/h 167 FF nd 712 MFF nd nd MMF 0.5/d F 0.5/h M 1/h 36 (or70) MFF F 1.5/h M 2/h 80% affil/affin 967 Social organization: For type see Box 1; N: sample size, number of adult individuals observed; HR: home range; some 100%, some 95% minimum convex polygons; HR MS: home-range during mating season; Pop. Density: population density; M: male; F: female; agon.: agonistic interaction; affin.: affinitive interaction; affil.: affilitative interaction; nd: no data available. ble competition polygyny in a population of solitary lemurs, additional information concerning paternity, temporal distribution of receptive females, and sexual behavior is still unavailable. The available data sets on Microcebus mating strategies fortunately are large and cover different species (M. murinus, M. ravelobensis, M. berthae, and M. rufus), the same species at different sites (M. murinus in Ampijoroa and Kirindy), and animals in both captivity and the wild (M. murinus). Comparing the different studies and species, several common traits emerge, as do striking differences. Males in all studies have spatial access to several females during the mating season.53,55,56,74 In M. murinus, for example, a male’s range overlaps with the centers of activity of eleven females on average.74 Thus, from a male’s perspective, and taking only female spatial distribution into account, monopolizing several females may be possible. Spatial access to females is, however, only one factor determining a male’s monopolization potential. Equally decisive is the temporal distribution of receptive females: If several females come into estrus simultaneously, a single male has a lower chance of defending exclusive access to all of them at the same time.89,90 Reproduction in Microcebus typically is highly seasonal and photoperiodically induced.60,91 Detailed data are available for the M. murinus populations at Ampijoroa and Kirindy. Females in both populations have a tightly restricted mating season of approximately four weeks, which occurs from mid-September to mid-October at the northern site of Ampijoroa, but from mid-October to mid-November at Kirindy, in western Madagascar.60,74 During this four-week mating season, each individual female mates only during a few hours on a single night of estrus.92,74 However, while Kirindy females enter estrus only once per breeding season, and hence once per year, females in Ampijoroa exhibit a postpartum estrus and can conceive twice during one rainy season.93 A postpartum estrus has also been proposed for M. ravelobensis.93 The mat- ing seasons of M. berthae, M. rufus, and possibly M. ravelobensis are equally restricted in time.55,56,94 The extreme reproductive seasonality does not necessarily imply that the fertile periods of females within a population are synchronous.95 Indeed, there is no evidence of operational synchrony in the Kirindy population of M. murinus.92 On average, two-thirds of females within a single male’s range are receptive on different nights.74 This suggests that the strongest males might try to monopolize several females. Monopolization could take the form of territory defense in which a single male excludes all rivals from the area, as seen in anthropoid species with a high monopolization potential (permanent spatial exclusion). Alternatively, males may monopolize access to each individual female as she comes into estrus (temporal mate guarding).74,92 Since male ranges cover the centers of activity of 2 to 14 rivals during the mating season, and since up to 18 males have spatial access to a receptive female during a 178 Schülke and Ostner given night, spatial monopolization does not seem to be an option for M. murinus males.74,92 Hence, other factors besides the distribution of receptive females in space and time determine mating strategies. Such factors include population density, the costs of mobility, or operational sex ratio (OSR).96,97 The potential causes for a male’s inability to defend an area with several female ranges have not yet been investigated in cheirogaleids. It has been argued, however, that in populations with equal or male-biased adult sex ratios, intruder pressure on “haremholders” might be too high to make the strategy economically feasible. Hence, an additional determinant of male monopolization potential in this population seems to be the skewed OSR; that is, the high number of competing males per receptive female.74,92 Subpopulations with female-biased adult sex ratios or otherwise lower numbers of males competing for access to receptive females constitute a test case for this hypothesis. The observation of a small number of central males spatially monopolizing access to all females in a population nucleus against smaller peripheral males, as in Mandena murinus54 (see Box 1) may indicate that the cost-benefit ratio of spatial defense indeed turns over at an ecologically realistic point. Unfortunately, we do not have the data (OSR and adult sex ratio) from Mandena needed to evaluate this prediction. Other potential constraints on the ability of Microcebus males to defend an area have been discussed. These include the metabolic costs of increased locomotion, costs of injuries inflicted by rivals, and risk of predation due to increased mobility.92,98 Regardless of the potential underlying causes, M. murinus males do not engage in spatial monopolization but may opt for scramble competition instead.85,86 During the mating season, male home ranges have been observed to increase in size in all but one study on any Microcebus species, indicating the prevalence of scramble competition, with males roaming widely for information about fertile females.53,56,74,99 Since female range size does not change widely, ecological factors are unlikely to be respon- ARTICLES sible. In one study of M. ravelobensis, male home-range size did not increase; however, female density at this site is very high (Table 1) and the authors argue that males do not need to increase their range in order to gain access to large numbers of fertile females.55 This interpretation is supported by the observation that males of the same species living at much lower densities show the expected increase in home-range size.99 Hence, we conclude that all Microcebus species employ a roaming strategy in order to increase their rate of encounter with fertile females. Another piece of evidence in line with adaptations to scramble competition is the large testis size of Microcebus species relative to the body mass-testes volume trend among lemurs.42 If males spatially exclude other males from access to females, females will mate monandrously and the potential for sperm competition will be low. Consequently, selection should not promote the evolution of large testes. Instead, scramble polygyny with the potential for female polyandry favors evolution of large testes.100,101 There are also several indications of contest components in these species, as is expected from the moderately high monopolization potential. In M. murinus the direction of sexual dimorphism in body mass fluctuates from females being heavier than males outside the mating season to males being significantly heavier during the mating season.52,102 However, it has been pointed out that the increase in male body mass during the mating season can be attributed mainly to the pronounced increase in testes size.103,104 In this case, the increase in body mass is an adaptation to sperm competition, not a trait favoring contest competition in males. Another potential indicator of contest competition stems from the study of M. murinus at Mandena,54 where a few central males defended access to several females against peripheral males. The data suggest that the two classes of males are morphologically different, with central males being heavier than peripheral males.54 The possibility of a system of two male classes in which central males enjoy mating privileges gains support from captive studies. When several males are housed together they quickly establish a dominance hierarchy. Matings are highly skewed toward dominant males, who have larger testes and are able to suppress the testicular function of subordinate males via urinary pheromones.105,106 However, another captive study, while showing the same pattern of skewed mating success favoring dominant males, failed to show testicular suppression of subordinates, indicated by an equal share of paternity to dominant and subordinate males.107 In addition, no evidence of two morphologically distinct male classes has been found in a wild population of M. murinus.52 Thus, neither seasonal sexual dimorphism in body mass nor reproductive suppression can be unambiguously linked to contest competition among males, although direct competition in the form of mate defense cannot be entirely excluded. To investigate the relative importance of scramble-competition polygyny versus mate defense, a recently published long-term study incorporated frequent capture-recapture methods, detailed focal observations of estrus females, and genetic paternity analysis.74 The study revealed that males employ roaming as well as temporal mate guarding as alternative tactics. Part of the roaming strategy is to increase home-range size during the mating season and to travel longer distances than females do. Male mating success does not depend on age, body mass, or testes size, but on spatial familiarity. Familiarity with an area includes a male’s knowledge of female sleeping sites, which, in combination with knowledge of the estrus state, allows a male to find a receptive female earlier than his competitors, an obviously important advantage of a roaming strategy.74 In addition, older males mate earlier during a female’s receptive period. The success of active mate guarding, and hence the probability of chasing away competitors, depends, among other factors, on male body mass, indicating a contest effect. As a consequence of these mixed male mating tactics, most litters had mixed paternities (scramble effect) but overall male reproductive Big Times for Dwarfs 179 ARTICLES success was biased toward older and heavier males (contest effect).74 As concluded earlier, sperm competition plays a crucial role in Microcebus reproductive competition. Indeed testes are large, matings frequent, and females do not obviously discriminate between males (besides the rejection of familiar, closely related males in captivity108), but mate with most available males.109,110 In a laboratory setting with a fixed mating order, reproductive success does not depend on male body mass or testes size but on the timing of mating, with a higher chance of fertilization during early receptivity.110 The early male advantage may be an additional reason for the higher reproductive success of heavier males in the wild74 because a heavier male in better physical condition might be able to find a receptive female earlier. If this is the case, it may be predicted, first, that earlier mating males are heavier, and second, that there is a positive relationship between travel speed and body mass. If heavier males have a roaming advantage and are more successful in mateguarding contests, this again emphasizes the interaction of direct and indirect mechanisms of male reproductive competition in Microcebus. Extra-Pair Paternity in PairLiving Cheirogaleus and Phaner The well-studied species of the two remaining genera, C. medius and P. furcifer, share similarities in their social organization (see Box 1). They both form uniform stable pairs; pair partners and their offspring share a common home range, which overlaps only slightly with those of neighboring families; and members of a family frequently share sleeping holes. While all P. furcifer males associate with a female and share a home range,38 some so-called floating males of C. medius live solitarily in a home range overlapping with those of several pairs.48 Thus, the question arises of whether the two classes of males employ alternative reproductive tactics. Data from a long-term study of a C. medius population in Kirindy revealed that the classes of males do not differ in body mass or size, but that floater males have significantly smaller testes than do paired males.41 In addition, floater males do not mark or defend their territory and always lose in fights with territorial paired males.48 It may be argued that floater males are younger and not yet fully developed. But floaters ranged in age from two to at least four years, whereas paired males were between two and five years of age.48 All six floater males in the study were excluded from paternity.111 Hence, floating does not seem to be an alternative male reproductive tactic with relevant fitness payoffs. More likely, the occurrence of floaters may be the consequence of high population density and a male-biased sex ratio.41 Studies of wild C. medius and P. furcifer have revealed no male-biased sexual dimorphism in body or canine size, indicating either low direct intrasexual competition or high levels of competition in both males and females.41,42,46,49 But lack of sexual dimorphism characterizes most lemurs.85,87 Males of both C. medius and P. furcifer have testes sizes well below the regression for strepsirrhines of their size,42,86,111 which suggests that sperm competition is not important in these species either. This is contradicted by the finding of high rates of extra-pair paternity (EPP). In the study of C. medius, 44% were sired by males other than their social fathers, as were four out of seven infants in the smaller P. furcifer sample.42,111 This leaves us with several questions: What are male and female reproductive strategies in dispersed pairs? What causes the high EPP rate? Why are testes small, despite obvious potential for sperm competition? Hence, why did males not adapt to a spermcompetition situation? Arguments to explain high rates of EPP include fertilization insurance, genetic benefits, paternal care, and a decreased risk of infanticide.112,113 The benefits of paternal care and infanticide avoidance may not be essential for the explanation of EPP in pairliving cheirogaleids. Females are able to increase total male care if they can recruit several males to help with offspring, leading to a multimale, onefemale organization.114 However, if animals form stable pairs, extra-pair males are not available as helpers. Infanticide, on the other hand, may be an adaptive male strategy even in seasonally and annually breeding species, given that the female will be in better physical condition after the loss of an infant and therefore have a higher chance of conceiving and successfully bringing up her next infant.95 However, it has been argued that in infant-parking species the risk of infanticide is generally low because it is difficult for an infanticidal male to find the infant, and, more importantly, the corresponding mother.34,115 Hence, neither paternal care by extra-pair males nor infanticide avoidance seems to be an essential benefit that females gain from EPP, narrowing down the range of potential causes to genetic advantages and fertilization insurance. In contrast to many species of birds, where pairs form anew each year after arrival at the breeding grounds, primates usually form stable pairs that last several years or even a lifetime. Among C. medius, for example, pairs separate only when one pair partner dies; among P. furcifer, pairs were stable at least for three years.38,41,47 That, however, precludes the potential for females to choose a different male each breeding season or to choose the best male in the population, because most males are already associated with a female. The probability that a female will be paired with a suboptimal male is high. If they are paired with suboptimal partners, females are expected to search for better mating opportunities outside their breeding unit.10 Hence, from the female’s perspective, the observed high rate of EPP in stable pairs is not unexpected. However, extra-pair copulations (EPCs) convey costs as well because the social father may stop investing in the offspring if paternity certainty becomes too low.114 Loss of male investment may have detrimental consequences in C. medius, while P. furcifer females do not risk a lot if they engage in EPCs because males do not participate in infant care.34 Therefore, in P. furcifer pair-living is not expected to be reflected in a monogamous mating system. The finding of high rates of EPP in combination with obligate paternal 180 Schülke and Ostner care in C. medius is more puzzling. Males may invest in others’ offspring for several reasons. If males are not capable of kin recognition they will jeopardize their reproductive success by terminating paternal care.41,50 Therefore males that have mated with a female at least once are expected to care for her young. But males might fine-tune the amount of paternal investment based on mating success or other approximations of paternity such as time spent mate guarding.114 If males are capable of kin recognition, care for unrelated young may still be adaptive when females use paternal care as an indicator of male quality and males benefit by securing future matings.116 At Kirindy, population density is high and the area is saturated with territories. Males there do not have the option of deserting a female as a reaction to cuckoldry and gaining mating opportunities elsewhere instead.50 Because it does not pay a male to desert an unfaithful female, he is expected to reduce the chances of cuckoldry. One way to do so is by mate guarding. Indeed, C. medius males were observed to increase their spatial association from 3 to 5 meetings per night to 60% of the time in association during the night of estrus.41,46 The observation of an estrous female being closely guarded by her partner in P. furcifer indicates that mate guarding is also part of P. furcifer’s behavioral repertoire.42 However, females were not guarded during the day but shared a sleeping site every third day only, as during the nonmating season.42 The observation of mate guarding is in line with a significant increase of agonistic interactions between the pair partners during the mating season, both of which indicate a conflict of interest between the sexes.42 It has been proposed that mate guarding is much harder to maintain in dispersed pairs, leading to a higher rate of EPP in dispersed than associated pairs.39 While this prediction is in accord with high EPP in dispersed pairs of P. furcifer and C. medius,42,111 it is not intuitive why the mode of association per se should influence male mate-guarding potential. Instead, mate guarding may be constrained by several other factors.10,42 ARTICLES Nocturnality leading to low visibility may be a crucial factor limiting male mate-guarding potential because it enables females to escape their guards, especially if the male is distracted by fighting off rivals.42 A second factor possibly hampering male mate-guarding potential is female resistance. Female cheirogaleids are dominant over their male partners38,71,117 and thus can not be physically forced to restrain from EPCs. Moreover, punishment of infidelity is unlikely to occur. Both of these factors decrease the efficiency of male mate-guarding.42 Finally, the highly seasonal reproduction of cheirogaleids may enhance female choice and lower male mate-guarding efficiency due to mating opportunity costs. Until his female partner has conceived, a male cannot be sure when she will be in estrus. Thus, he has to guard her for several days or weeks while losing mating opportunities in the neighborhood.42 Nocturnality, the first factor influencing male mate-guarding potential, is not testable in primates because nocturnal activity is a trait common to all dispersed pairs. Female dominance and pronounced reproductive synchrony, however, characterize lemurs.23,118 –120 but not other species living in dispersed pairs.42 The crucial test of the hypothesis that female dominance and seasonal reproduction act on EPP rates via reduced mate-guarding potential could be performed with Tarsius spectrum and Galagoides zanzibaricus, both of which lack strict seasonality in reproduction as well as female dominance.121,122 We argued earlier that efficiency of male mate guarding is low and showed that rates of EPP are high among P. furcifer and C. medius. Thus, the question arises of why males of those species did not evolve large testes as an alternative paternity guard? One possible explanation may be that testes size evolution is constrained. However, pair-living evolved several times independently within the lemur clade.58 Pair-living species with small testes are found in seven genera in four different lemur families. Solitary or dispersed group-living species from those same families or even genera nevertheless have large testes.42 An- other explanation may be that as a result of recent habitat changes the observed EPP rate is exaggerated, leading to unusually high population density and compressed territories, and consequently many potential mates for females in the vicinity. If this change occurred only recently, males may still be in the process of adapting to the new situation.42 However, a comparison of densities across various P. furcifer populations indicates an intermediate density at Kirindy42 where EPP is high. Hence, both explanations are unlikely to account for the small testes size in dispersed pairs. One alternative possibility may be that the relatively small testes are still large enough to serve in sperm competition, given the very restricted period of mating as well as the limited number of potential female partners. The home range of a M. murinus male that relies heavily on sperm competition overlaps with those of up to 21 females that reproduce annually and come into estrus one after the other over approximately four weeks.74,92 Hence, a male has to mate frequently over a comparatively long period, necessitating the evolution of large testes. By contrast, during a given mating season P. furcifer males have to mate on average only for 2.5 days (one-day estruses, five females in adjacent territories, breeding at best every second year32,38). Thus, selection for large testes size seems far less pronounced in dispersed pair-living species, despite high EPP rates, than it does in species competing via scramble polygyny. To test this hypothesis conclusively and to assess the level of sperm competition in pair-living C. medius and P. furcifer, data are needed on mating behavior and temporal distribution of receptive females of these species. KIN-SELECTED COOPERATION AND GENETIC POPULATION STRUCTURE In one of the most elegant studies of cheirogaleids, the M. murinus population in Kirindy was provided with 15 nest boxes made from 30-cm long slices of dead trees with natural hollows and equipped with wooden lids and bottoms.65,123 M. murinus imme- Big Times for Dwarfs 181 ARTICLES diately accepted the artificial sleeping sites, which suggests that sleeping sites per se or sleeping sites of high quality may be limited in the population. The organization of all-female groups did not change, however, indicating that groups form for reasons other than limitation of suitable sleeping sites alone.65,123 Beyond this important insight, the nest boxes provided an opportunity to track activities within the hollow nearly continuously via infrared-light-supported video recording. Motion sensors activated the camera whenever an adult entered or left the sleeping site during nocturnal activity. Regular short recordings allowed instantaneous sampling of behaviors around the clock. Nest boxes are used by all-female groups of two to three females with their offspring. Unlike C. medius infants, those of M. murinus are not continuously guarded during the first weeks.46,50,65 Females return to the nest box individually instead and spend a total of about one hour with the offspring during the first half of the night. Males are never observed in or near the nest or to encounter females during feeding protocols. When sleeping sites are changed, the whole group moves together but each mother transports only her own offspring in her mouth, which demonstrates that females are able to discriminate between their own and others’ offspring without failure.65,123 Nevertheless, females groom and nurse other females’ offspring during the night as well as during the day when all mothers are present in the nest. When only one female is in the box, the time she allows for nursing others’ offspring increases to an average of 20% relative to the time spent nursing own offspring. Most notably, when a female dies the remaining group members take full responsibility and nurse all infants to weaning age, yielding a survival rate of 0.83 for orphans that very likely would otherwise have died.65,123 This behavior is likely to be promoted by kin selection. Although matrilines as a structuring element of social organization and as a prerequisite for cooperative breeding even made it into the textbook description of the typical nocturnal primate,124 the study just described provides the first unambiguous proof of cooperative breeding in any nocturnal primate. First, molecular genetics only recently allowed investigations into relatedness within populations on a larger scale. Second, genetic population structure and kin-selected behaviors are not causally linked in the way that often is perceived.125 Indeed, the first demonstration of the matrilineal spatial clustering of females came from a study of Mirza coquereli, a truly solitary species with overlapping yet independent female home ranges and no sleeping associations.126 In M. coquereli, uncommon haplotypes are represented by males only, whereas all females show one of the few common ones. Individuals with different but frequent haplotypes do not live randomly scattered in space but are spatially clustered, with only low overlap between clusters.126 Whenever a common haplotype occurs in a cluster of another common haplotype, the individual is an adult male. Male haplotypes are not clustered in space. These findings are backed up by relatedness at nuclear satellite-DNA loci: Relatedness is negatively correlated with geographical distance in females but not in males. Matrilineal clusters of the size found in M. coquereli cannot be interpreted as being single mothers with their female offspring, but must span two generations at least. Moreover, spatial association according to haplotype suggests that the observed pattern does not simply result from daughters settling near their mothers. Females have been demonstrated to be capable of long-distance dispersal. In M. coquereli, no obvious benefit from living close to kin has been identified.126 Studies on genetic population structure in the Ampijoroa population of M. murinus have used nuclear DNA from multiple microsatellite loci,98 while studies of this species at Kirindy have used a combination of information from both mtDNA and microsatellite loci.74,109,127,128 These studies have found the same pattern of male dispersal and female philopatry as in M. coquereli. M. murinus males have fewer relatives in the study area and related males live further apart than do related females.98 In the part of the Kirindy population where most studies have been conducted,52,76,92,102,109 80% of females share the same common haplotype.127 Twelve additional haplotypes occur at very low frequencies and, apart from one smaller female cluster, belong to males only.127 Studies disagree on how to define a matriline, but in both populations females in all-female groups are more closely related to each other than they are to females in other such groups. All-female groups are comprised mainly of mother-daughter or sister dyads, but may also contain grandmother-granddaughter, aunt-niece, or even cousin dyads; group members are never unrelated.65 As cooperative breeding occurs within those all-female groups,65 the prediction that cooperative breeding is kin-selected is supported to a degree rarely matched in the literature on primates. As in M. coquereli, clusters of M. murinus females sharing an mtDNA haplotype were found to be perfectly isolated in space in the first study conducted in a 9-ha forest plot at Kirindy.127 Due to the close proximity of female clusters and the absence of barriers indicated by the almost ideal free distribution of males, these clusters do not represent population nuclei like those found in Mandena.54 The distribution of M. murinus across an area of more than 12 km2 is highly patchy, with large uninhabitated areas.128 Unlike the population nuclei in Mandena, the male spatial distribution pattern does not vary from female distribution and the sex ratio within spatial clusters is not female-biased. Highly mobile males seem to promote gene flow across long distances, but the distribution of mtDNA haplotypes indicates that females may also disperse from their natal areas. Where many individuals live closely together they may, as described, form clusters of relatedness. However, spatial clusters of females were not always comprised of individuals of the same haplotype, a point that further distinguishes the population structure from the Mandena nuclei. The existence of closely related females in spatial accumulations that are stable in time favors the evolution of kin-selected cooperative breeding.128 The investigation of infant-care behavior in genetically more diverse areas of the Kirindy population is 182 Schülke and Ostner mandatory to test this proposition once and for all. Population turnover is tremendously high in Microcebus, reaching 50% annually,129 most likely due to intense predation by various diurnal and nocturnal raptors, carnivores, and snakes. We think that this process may randomly eliminate haplotypes but may also enhance clustering. Once a female can find a sister or aunt to raise her offspring cooperatively, the probability of cooperation in the progeny will increase. During mothers’ nocturnal activities, cooperative efforts may reduce the time interval between nursing and grooming bouts, which may be favorable for the absolutely small infants with high metabolic rates. However, the larger impact of cooperative breeding is brought about by the adoption of unweaned offspring whose mother had died. Occasional nursing of others’ offspring might, therefore, simply be a byproduct of a highly beneficial family insurance that buffers mothers against the overly high risk of dying from predation before their offspring are independent. Hence, haplotypes of cooperating females are less likely to be eliminated in stochastic processes, and this feed-back loop enhances cluster formation. This hypothesis ought to be investigated by mathematical modeling of the feedback process using the conditions found in Kirindy. It is unclear why M. coquereli does not breed cooperatively despite the spatial aggregation of closely related females. However, the hypothesis we propose suggests that, irrespective of the costs involved, the major benefit of cooperative breeding is back-up for the loss of a mother. If predation pressure on M. coquereli is markedly lower, which is likely, given its seven times larger body size, this benefit may not outweigh the costs. M. coquereli females do not always settle in close proximity to their birth place.126 Crowding seems to make dispersal away from the mother, but not away from the cluster, necessary, indicating that there are indeed costs to the communal use of foraging areas. Within an mtDNA cluster, relatedness between cooperative partners may fall well below the level necessary to select for adoption of kin, so that dispersing ARTICLES females may end up without cooperation partners. Lack of cooperative breeding among M. coquereli and probably P. furcifer (Schülke, unpublished data) indicate that among cheirogaleids the phenomenon is unique to Microcebus. One observation on C. medius, however, suggests otherwise.46,50 In an unusual group of two closely related females and one male, both females bred in the same year. Both gave birth in the same tree hole and took turns babysitting the young and sleeping with them during the day. Once the infants started moving independently, they all followed either mother for their first excursions and foraging trips. Although it is not known whether allonursing occurred, this case demonstrates that a certain predisposition toward cooperation in infant care exists among cheirogaleids and may be activated when conditions permit. CONCLUSIONS In this paper we have laid out the marked variation in various socioecological traits among cheirogaleids. The testable hypotheses we have derived from these comparisons may help to identify evolutionary explanations for variation in social organization and cooperative breeding. We have identified areas for further research, including year-round feeding ecology in most cheirogaleids, feeding competition and the evolution of pair living in C. medius, variation in foraging efficiency with group size in P. furcifer, changes in male competitive regimens as operational sex ratio varies, explanations for parental care with low paternity certainty, the relationship between roaming success and physical condition in M. murinus, and cooperative breeding where haplotypes are less clustered. Apart from these topics, our understanding of cheirogaleid behavioral evolution will gain from investigating the unstudied or less studied of the 21 species; this review is based mainly on information about only six species. Nevertheless, the results extend and refine theory in primate behavioral ecology because a positive feed-back loop may exist between cooperative breeding and the spatial clustering of closely related females that is evident from microgeographic population genetics. Moreover, it has become obvious that modes of male mating competition and male social organization cannot be predicted from the distribution of fertile females in space and time if the operational sex ratio, hence potential intruder pressure, is neglected. Finally, we have identified more of the rare pieces of evidence of a strong ecological influence on male social organization. Despite the primacy of sexual competition, these need to be incorporated more thoroughly into our theoretical models. ACKNOWLEDGMENTS We are grateful to J. Fleagle for inviting us to contribute this review. We especially thank P. Kappeler, who initially drew our attention to the awkward societies of cathemeral and nocturnal lemurs and since then has supported us in countless ways. We thank the Commission Tripartite of the Malagasy Government, the Direction des Eaux et Forêts Madagascar for making these studies possible, and the Centre de Formation Professionelle Forestière de Morondava, Professor B. Rakotosamimanana from Université d’Antananarivo, and F. Rakotodraparany at PBZT Antananarivo for hospitality and cooperation. We thank C. Borries, K. Dausmann, M. Eberle, W. Erb, J. Fietz, P. Kappeler, and A. Koenig for long discussions and comments on the manuscript. M. Craul, M. Dammhahn, K. Dausmann, M. Eberle, P. Kappeler, U. Radespiel, O. Rakotonirainy, and E. Zimmermann generously shared unpublished data and manuscripts with us. J. Ganzhorn provided the Madagascar map and M. Irwin adjusted it. 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