Download Big times for dwarfs: Social organization, sexual selection, and

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lemurs of the family Cheirogaleidae as being “primitive primates,”2 which inadvertently conveys notions of the archaic, outdated, unelaborated, simple, invariant, inflexible, and hardwired.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
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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
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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
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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. During our
writing, we were both supported by
Feodor-Lynen-Fellowships of the Alexander von Humboldt Foundation
and by Stony Brook University. We
gratefully acknowledge the invitations
from A. Koenig and C. Borries.
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(2005) The Myth of Syphilis: The
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The Human Fossil Record, Volume 4, Craniodental Morphology
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561 pp. Hoboken: Wiley-Liss
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• Kramer KL. (2005) Maya Children: Helpers at the Farm.
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• Svoboda J, Bar-Yosef O. (2005)
Stránská Skála: Origins of the
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• Kennett DJ. (2005) The Island
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• Rose KD, Archibald JD. (2005)
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• White NM (ed). (2005) Gulf
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ico. xvi⫹416 pp. Gainesville:
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• Burroughs WJ. (2005) Climate
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• Lee RB, Daly R (eds). (2004) The
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• Wessen KP. (2005) Simulating
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• Zollikofer CP, Ponce de Leon M.
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• Palka JW. (2005) Unconquered
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