Postweaning maternal care increases male chimpanzee reproductive success

Abstract

Humans are unusual among animals for continuing to provision and care for their offspring until adulthood. This "prolonged dependency" is considered key for the evolution of other notable human traits, such as large brains, complex societies, and extended postreproductive lifespans. Prolonged dependency must therefore have evolved under conditions in which reproductive success is gained with parental investment and diminished with early parental loss. We tested this idea using data from wild chimpanzees, which have similarly extended immature years as humans and prolonged mother-offspring associations. Males who lost their mothers after weaning but before maturity began reproducing later and had lower average reproductive success. Thus, persistent mother-immature son associations seem vital for enhancing male reproductive success, although mothers barely provision sons after weaning. We posit that these associations lead to social gains, crucial for successful reproduction in complex social societies, and offer insights into the evolution of prolonged dependency.

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EVOLUTIONARY BIOLOGY
Postweaning maternal care increases male chimpanzee
reproductive success
Catherine Crockford1,2,3*, Liran Samuni1,2,4, Linda Vigilant1, Roman M. Wittig1,2,3
Humans are unusual among animals for continuing to provision and care for their offspring until adulthood. This
“prolonged dependency” is considered key for the evolution of other notable human traits, such as large brains,
complex societies, and extended postreproductive lifespans. Prolonged dependency must therefore have evolved
under conditions in which reproductive success is gained with parental investment and diminished with early
parental loss. We tested this idea using data from wild chimpanzees, which have similarly extended immature
years as humans and prolonged mother-offspring associations. Males who lost their mothers after weaning but
before maturity began reproducing later and had lower average reproductive success. Thus, persistent mother-
immature son associations seem vital for enhancing male reproductive success, although mothers barely provision
sons after weaning. We posit that these associations lead to social gains, crucial for successful reproduction in
complex social societies, and offer insights into the evolution of prolonged dependency.
INTRODUCTION
Among mammals, humans and great apes share an unusually
extended immature phase spanning more than a decade between
weaning and sexual maturity (1,2). In humans, continuous provi-
sioning (1–3) of food to weaned immatures throughout the extended
period before attaining sexual maturity is thought to have pro-
foundly shaped the evolution of humans by enabling extensive
brain growth and affording immatures the social opportunities to
learn complex foraging skills (1,3). As with most mammals, in
humans and great apes, mothers invest most in offspring care, pri-
marily through lactation and carrying, and later potentially through
agonistic support. We therefore posit that for selection to have
favored postweaning maternal investment, immature offspring with
living mothers should later have higher reproductive success rela-
tive to orphans, thereby providing an evolutionary mechanism for
mothers to continue investing in immature offspring. However, the
rarity of cross-generational data in long-lived species, including
humans (4), makes it difficult to examine whether and how extensive
postweaning parental investment affects the reproductive success of
offspring. Here, we examine this topic using data from a closely
related great ape, the chimpanzee.
Although few mammals provide or facilitate acquisition of food
for weaned offspring (5,6), maternal loss during the postweaning
immature period affects offspring survival or development in some
species with shorter life histories and smaller brain to body size
ratios than apes. For example, maternal loss before sexual maturity
(2 to 3 years) in red deer (Cervus elaphus) results in sons with smaller
antlers and daughters giving birth later than those whose mothers
remain alive (6). In baboons (Papio cynocephalus), maternal loss
before sexual maturity (4 years) results in reduced offspring survival
(7). Similar survival gains provided by mothers have also been
demonstrated in two long-lived species with relatively large brain to body
size ratios, orcas (Orcinus orca) and chimpanzees (Pan troglodytes)
(8,9). These findings suggest that even in the absence of provision-
ing, mothers provide key benefits that aid offspring survival. Likely
benefits are support against predators and conspecifics, information
transfer, or acquisition of foraging patterns (7,10).
In long-lived species, determining the impact of maternal loss
upon later reproductive outcomes, a direct test of fitness, is problem-
atic, as cross-generational data take decades to acquire. In humans,
an additional problem is that sociocultural factors can be influential,
such as those that provide buffering effects for orphans via “allopa-
rental” care [e.g., (1,4, 11)]. Hence, studies have examined the
impact of maternal loss on survival, a less direct measure of fitness.
In humans, motherless children under 2 years old have significantly
reduced chances of survival compared to those with mothers. After
weaning, in the societies tested, there is little effect of maternal loss
on survival, likely due to the impact of effective alloparental care
after weaning (11).
Looking to one of our closest living relatives, recent studies
examining maternal loss in the postweaning immature phase in wild
chimpanzees also reveal reduced survival (9). This is especially the
case for sons (12), where maternal loss after aged 10 years continues
to affect sons’ but not daughters’ survival. In addition, maternal loss
slows growth during development in both sexes (13) and delays sexual
maturity and first reproduction of daughters (14). Chimpanzees
require a similar number of years to reach sexual maturity as
humans (1), and both species maintain a flexible fission-fusion
community structure so not all community members remain together
every day (15). Nonetheless, chimpanzee offspring tend to travel,
nest, and forage alongside their mothers until sexual maturity. After
that point, sons, as well as daughters who do not emigrate, may
continue to associate with their mothers at high rates compared to
association rates with other female group members (16). Because
of female-biased dispersal, typically, the only adult kin of mature
females are their own male offspring. Chimpanzees have a polyan-
drous mating system, with no or limited paternal care (17,18).
Competition among males for reproduction is intense in chimpanzees
(19–21), and while the presence of mothers may facilitate adult and
adolescent son’s paternity success in closely related bonobos, mother
presence has limited effects in the chimpanzee communities studied
thus far (22).
1Department of Primatology, Max Planck Institute for Evolutionary Anthropology,
Leipzig, Germany. 2Taï Chimpanzee Project, CSRS, Abidjan, Ivory Coast. 3Human
Behaviour, Ecology & Culture, Max Planck Institute for Evolutionary Anthropology,
Leipzig, Germany. 4Department of Human Evolutionary Biology, Harvard Univers ity,
Cambridge, USA.
*Corresponding author. Email: crockford@eva.mpg.de
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We examined the impact of maternal loss upon the reproductive
careers of chimpanzee sons using a dataset including demography
and paternity assignments across three communities of the Taï
National Park, Ivory Coast, spanning, on average, 16.7 years (range,
5 to 27 years) per community. Our data include 48 paternity assign-
ments from 12 and 11 males who were or were not “orphaned” by
the mother’s death before the son reached social independence—
aged 12 years in this population (23). We did not assess the impact
of maternal loss on the reproductive careers of daughters, as they
typically disperse at sexual maturity, making assessment of their
reproductive success extremely difficult. This population of chim-
panzees exhibits considerable reproductive skew, wherein alpha
males sire more offspring than any other male, with little variation
between other males (20,21). Thus, arguably the best assessment
for male quality across the reproductive lifetime is alpha tenure
rather than maximum or mean dominance rank, which assume a
more linear distribution of paternities. If maternal loss reduces
competitive ability, then we expect orphans to experience less time
as alpha males. We further predict that maternal loss increases the
age at first siring, effectively affecting the number of reproductive
years available to each male. Last, we expect that maternal loss
results in lower observed reproductive success as measured by the
number of offspring sired per conception opportunity.
Because high rates of mortality occur within the first years of life
in chimpanzees (24) and noninvasive genetic sampling of younger
infants is extremely challenging, we could only estimate siring of
viable offspring, that is, those surviving to ≥2 years of age (n=48
assigned paternities). These represent more than 95% of all off-
spring surviving to 2 years during the study period. We corrected
for the number of conception opportunities of viable offspring that
each male was exposed to after sexual maturity and included those
with ≥4 reproductive years. Sexual maturity is taken as the minimum
known siring age for this population (10 years). Note that this is
earlier than sons’ social independence from mothers (12 years). In
this sample, only two paternities were attributed to males younger
than 12 years, and neither were orphans.
RESULTS
Impact of maternal loss on competitive ability
First, to determine whether maternal loss specifically affects their
sons’ quality over their reproductive lifetime, we tested whether
orphans experience shorter alpha tenure relative to non-orphans
(model 1). Here, we fitted a linear model using a Gaussian error
structure with identity link function, with orphan status as the test
predictor. Alpha tenure is the years spent holding the alpha position
across each males’ reproductive years (means±SD, 1.75±2.49
years; dataset S1). Those who never became alpha (n=11) were
marked as zero. We included a measure of male-male competition,
the average number of sexually mature males in the community per
conception during individuals’ lifetime (aged 10 years until death or
to current age), as a control variable. We also included the number
of reproductive years per male as a control variable, as this is ex-
pected to affect alpha tenure in this high mortality population (24).
Maternal loss tended to negatively affect alpha tenure (P=0.068),
with orphans’ alpha tenure length less than half that of sons who did
not experience maternal loss before aged 12 years (full-null model
comparison likelihood ratio test, F3,19=3.718, P=0.068; Fig.1A
and Table1). The Taї chimpanzee population has relatively high
reproductive skew (21) with alpha males siring between 38 and 67%
of offspring, when there are less than 10 males in a community (20),
as is the case in this dataset. Each other male sires <20% of offspring
(20,25). However, to control for other possible influences of domi-
nance, we repeated the model exchanging alpha tenure for average
dominance rank across reproductive lifetime, including tenure of
each rank. The full versus null model comparison was nonsignificant
(likelihood ratio test, F3,19=0.026, P=0.872).
Age at first sire
We next asked whether chimpanzee male orphans sire their first
offspring at a later age compared with non-orphans (model 2). To
do this, we fitted a linear model with Gaussian error structure, with
orphan status as the test predictor, and once again, controlling for
male dominance rank as a measure of quality. Here, maximum
dominance rank attained until first siring was used rather than
alpha tenure from model 1, as most males sired their first offspring
before attaining the alpha position. We also controlled for male-
male competition, here, the average number of adult males in the
community per conception from aged 10 years until death or
current age. Orphaned males sired their first offspring, on average,
3 years later (means± SD, 16.32±2.00 years) than non-orphans
(12.93±1.63 years) (full-null model comparison likelihood ratio
test, F3,19=15.454, P=0.0008; Fig.1B and Table1).
Impact of maternal loss on reproductive success
Third, to test whether postweaning maternal loss affects the num-
ber of offspring males sire when adult, we used the same dataset as
in model 1 and fitted a general linear model with Poisson error
structure and log link function, including orphan status as the test
predictor (model 3). We also included alpha male tenure as a con-
trol predictor for male quality. Again, as in model 1, alpha tenure
is likely to better account for reproductive skew than other domi-
nance measures. Siring potential is likely to decrease with increased
male-male competition. Therefore, to account for potential male-
male competition, we included the inverted average number of
males as an offset term. By including the inverted number, we
account for an expected negative effect of the number of males on
siring potential. Siring probabilities are also expected to increase
with increased conception opportunities, and hence, conception
opportunities across each male’s reproductive lifetime are included
in the model as an offset term. The dataset included n=23 males,
n=48 offspring with assigned paternities, and n=21 mothers of adult
sons (dataset S1; table S1 shows the distributions of model variables).
We found that orphans (n=12 males and n=11 mothers) had,
on average, half as many offspring per conception opportunity
(n=12 offspring) as other males (n=11 non-orphans, n=10 mothers,
and n=36 offspring) (full-null model comparison likelihood ratio
test, 2=5.871, df=1, P=0.015; means±SD, orphan=0.08±0.12
and non-orphan=0.2±0.14 offspring/conception opportunity;
Fig.1C and Table1). Males who held the alpha position for longer
also had more offspring (P=0.013; Table1 and Fig.1D). Fifty-two
percent of males became alpha and sired 87.5% of the viable off-
spring. The 48% of males who never became alpha sired only 12.5%
of the offspring, suggesting the potential for strong reproductive
skew in this dataset. To control for other possible influences of
dominance, we repeated the model exchanging alpha tenure for
average dominance rank across each male’s reproductive lifetime,
which did not change the results (table S2).
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Last, if prolonged maternal investment affects the quality and
reproductive success of sons, then we expect age at maternal death
to negatively correlate with alpha tenure and positively correlate
with reproductive success. However, as the dataset was too small for
reliable statistical inference of these effects, we tentatively show the
predicted correlations in a supplementary figure (fig. S1).
DISCUSSION
Our results show that, in a species in which males experience con-
siderable competition over mates, males whose mothers die when
they are weaned immatures are subsequently less competitive than
non-orphaned males in producing offspring. Specifically, orphaned
sons lose out on alpha tenure, sire their first offspring at a later age,
and have fewer offspring that survived to age 2 years during their
reproductive years. Our combined measure of reproductive success
demonstrates that either orphan males lose out on siring or that
their offspring are less likely to survive to 2 years. Either way, we
conclude that mothers continue to provide key benefits to sons
throughout the prolonged postweaning immature phase, at least
until sexual maturity at aged 12 years. It seems that these maternal
benefits contribute both to sons’ competitive ability as an adult and
to sons’ reproductive success.
Alpha tenure—the number of years each son maintained the
alpha position—had a moderate positive effect on reproductive
success, with doubling of tenure length increasing reproductive
success by >50%. Maternal loss negatively affected alpha tenure,
with orphans typically having less than half the alpha tenure length
of non-orphans. A recent study in the same population showed that
chimpanzees orphaned after weaning lose out on growth during
development (13). Together, these results demonstrate that, although
direct provisioning of food by mothers is rare, mothers’ presence
contributes to sons’ growth during development and competitive
ability as adults.
Maternal loss had an additional negative impact on reproductive
success that was independent of alpha tenure (model 3). We posit
that mothers may not only contribute to sons’ competitive ability
but a mothers’ presence may also provide other kinds of benefits,
which contribute to sons’ fitness. In chimpanzees, given that sub-
ordinates do sire some offspring, and at higher rates in populations
with more males than Taï (specifically Ngogo as well as Gombe and
Sonso populations) (21), it is considered that attaining dominance
is not the only reproductive strategy (and may explain why the
number of males had little impact on reproductive success or alpha
tenure). A potential alternative male strategy is building long-term
relationships with females, which has been shown to increase the
likelihood of gaining copulations with that female or of siring her
offspring (16,26, 27). Maintaining long-term affiliative relation-
ships may require certain social skills, which are thought to vary
across individuals (7,28), and may be negatively affected by early
maternal loss (7).
Thus, maternal presence may benefit weaned immature sons in
several ways. First, mothers may provide indirect nutritional benefits.
As ripe fruit specialists, chimpanzees experience contest competition
Fig. 1. The impact of maternal loss on male chimpanzees’ reproductive careers. Impact of maternal loss on (A) alpha tenure, (B) age at first sire, and (C) likelihood of
siring offspring. (D) Impact of alpha tenure on likelihood of siring offspring. Boxes show the median, 25th, and 75th percentiles, and whiskers are interquartile range × 1.5.
(D) Model line (dashed) and 95% confidence intervals (gray), and larger points denote larger number of observations.
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due to the ephemeral patchy nature of ripe fruit (29,30). Thus,
mothers may contribute to their weaned offspring’s nutritional
status through providing agonistic support at food patches and, in
addition, by reducing predation risk (31,32). As weaned offspring
typically travel with their mothers, mothers likely also assist in finding
patchy, ephemeral foods. As well as individual learning opportunities,
mothers may provide food-related social learning opportunities
either directly from themselves (33) or indirectly by facilitating
their sons’ close association with other group members [e.g., (34)].
These social learning opportunities could include better nutrition
obtained from learning extractive foraging techniques on nutrient-rich
foods (33,35) and acquisition of hunting skills (36–39). Mothers
also sometimes directly share energy-rich, difficult-to-access foods
and the tools required for extractive foraging with their offspring,
such as nuts, honey, and insects (33,35), although this is not considered
to be at a frequency to constitute provisioning (1,2).
Second, mothers may provide social benefits, such as through
social buffering in the face of exposure to stressors. Social buffering
can limit the risk of chronic hypothalamic-pituitary-adrenal (HPA)
axis function (23,40), hence having a positive impact on health and
survival (28). Mothers, for example, continue to groom offspring
through the immature years into adulthood, where grooming kin is
associated with the release of a neuropeptide, oxytocin (Fig.2) (41).
Oxytocin is thought to down-regulate HPA axis function, potentially
reducing detrimental effects from repeated exposure to stressors
(40). Little discussed in previous studies, social benefits may also
accrue through social learning opportunities that facilitate adult so-
cial life, either through acquiring skills needed for the building and
maintaining of social bonds or for using complex social and coop-
eration skills required to out-compete out-group members (23,42)
and in-group conspecifics (19,21,43,44). This could be particular-
ly pertinent in highly territorial, fission-fusion social systems,
such as chimpanzees. Successful adult male chimpanzees need
to not only navigate the social complexities of securing coalition
partners to outcompete in-group rivals (19,44) but also maintain
territorial defense by cooperating with the same individuals with
whom they compete intensely over mating opportunities (23,45,46).
Research in humans and rodents show that the extent of maternal
nurturing received may affect offspring’s later adult social skills
(47,48). Thus, a broader take on the benefits accrued from pro-
longed maternal investment in species with extended immature
periods to include social benefits may be justified in chimpanzees
and other species.
In other long-lived species with prolonged immature periods,
adult sons may continue to gain benefits from their mothers’ presence.
In orcas, living mothers continue to influence their adult son’s
survival, potentially due to maternal knowledge of ephemeral food
sources (8). In primates, for sons, mothers’ presence at the time of
siring increases the reproductive success of sexually mature male
muriquis (Brachyteles arachnoides) (49) and bonobos (Pan paniscus)
but not of chimpanzees (22). In each case, the reported influence is
during adolescence or adulthood, whereby mothers who maintain
bonds with their sons gain indirect fitness benefits in the form of
grandoffspring. In species where females are the philopatric rather
than the dispersing sex, coresidence and social bond maintenance
of adult daughters with mothers is well known to provide direct and
indirect benefits to both mothers and daughters, by increasing the
survival of each other and of their offspring (50–52). In addition, in
Table 1. Models testing the impact of maternal loss on male chimpanzee alpha tenure, age at first siring and reproductive success. Bold, P < 0.05; italic,
P < 0.01. Reference category of factors is in parenthesis. Asterisk (*) indicates test predictor. Full versus null model comparisons: (1) Gaussian: F3,19 = 3.718,
P = 0.068; (2) Gaussian: df = 1, F3,19 = 15.454, P = 0.0008; and (3) Poisson: df = 1, 2 = 5.871, P = 0.015. Offset terms: average number of males present per
conception and number of conceptions resulting in viable births across reproductive years per male. Z transformed: all continuous predictor variables.
Effect sizes = R2.
Term Estimate SE CI F P R2
1. Alpha tenure
Intercept 2.461 0.505 2.121, 2.829 – – –
Orphan (yes)* −1.355 0.702 −1.707 to −1.033 3.718 0.068 0.163
Reproductive years 1.547 0.362 1.191 to1.718 18.240 0.0004 0.489
Average males per
conception −0.572 0.360 −0.797 to 0.374 2.519 0.128 0.117
2. Age at first siring
Intercept 13.435 1.205 12.292 to 13.849 –––
Orphan (yes)*3.041 0.773 2.763 to 3.448 15.453 0.0008 0.448
Maximum dominance 0.725 0.399 0.519 to 0.904 3.287 0.085 0.147
Average males per
conception −0.051 0.176 −0.127 to 0.065 0.085 0.772 0.004
Term Estimate SE CI 2P
3. Number of offspring
Intercept −0.010 0.234 −0.133 to 0.237 –––
Orphan (yes)*−0.863 0.367 −1.103 to −0.718 5.872 0.015 0.297
Alpha tenure 0.337 0.138 0.239 to 0.400 6.133 0.013 0.329
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female baboons, maternal loss in the juvenile period is known to
affect later survival (7). Here, we show specifically that the mother’s
presence during immature periods provides reproductive benefits
to sons, apparently at least in part by enhancing their ability to
out-compete other males in siring offspring. Additional studies
with larger datasets could determine, first, if sons orphaned at
younger ages experience greater deficits and, second, if orphans
adopted by others, as can occur in chimpanzees (53), experience
fewer deficits.
Across species, we see that mothers’ presence after weaning
affects survival, competitive abilities, and reproductive success.
What remains unclear and needs to be addressed in future studies is
by what mechanisms mothers’ presence enhances reproductive
success of her offspring and how much active investment and care
is involved. Of particular interest in socially complex species that
gain fitness through building long-term relationships (50–52) is
how much mothers contribute to learning of social skills required to
maintain these relationships.
We acknowledge the possibility that differences in reproductive
success were driven by hereditary factors rather than maternal loss.
For example, mothers who survive longer may do so, because they
are better quality, and the genes responsible may produce better
quality sons who gain higher reproductive success than rivals. This
potential confound is common to studies of this type (22) and is
difficult to address with the genomic and genealogical data available
from slow life-history wild animals. Although hereditary factors
may play a role in driving the patterns we observe, we argue that the
particular structure of chimpanzee society featuring male philopatry
and life-long associations between males and mothers makes our
inference regarding the importance of the prolonged mother and
offspring relationship highly plausible.
The maternal effects we observe are in contrast to a recent
meta-analysis demonstrating the different contributions of maternal
and heritable effects across 64 species including short-lived verte-
brates and invertebrates. The meta-analysis showed that, on average,
maternal effects accounted for 10% and heritability for 20% of
phenotypic variation (54). Unlike in this study, the impact of
maternal effects was not elevated for species that provided maternal
care after egg laying or parturition compared to those that did not
[but see (55)]. Thus, the strong effects of postweaning maternal
investment reported in this study—and other studies on long-
lived species (8,9,12)—are more pronounced than the maternal
effects reported for the shorter-lived mammals in (54) and are
greater than the heritable and maternal effects combined in the
meta-analysis (55). This strongly suggests that maternal care in
long-lived species with prolonged immature ontogeny may differ
in kind from that provided by shorter-lived mammal and non-
mammal species.
In summary, we provide evidence that prolonged association of
mothers with their immature sons provides substantial reproduc-
tive benefits, despite evidence of only limited direct postweaning
provisioning of food. In anthropology, a central hypothesis for
explaining rapid encephalization in the hominid lineage, as well as
human’s prolonged juvenile dependency, is related to extended
parental provisioning of food for years beyond weaning (1,2). Our
closest living relatives, the other great apes including chimpanzees,
already show selection for rapid encephalization and prolonged
juvenile dependency since the split from the catarrhine/old world
monkey clade. These traits may then have been shared with the
common ancestor of the great apes including humans and may
be best explained by the social benefits of maternal investment
described here, which we call the social benefits hypothesis. The
addition of extensive food provisioning, potentially facilitated by
alloparenting, may then explain the more extreme juvenile depen-
dence and encephalization seen in humans, as suggested by the pro-
longed juvenile dependency hypothesis.
While further research is needed to ascertain exactly what chim-
panzee mothers provide their sons with, we posit that benefits likely
include both indirect nutritional gains and social benefits. In terms
of social benefits, we expect that offspring are more likely to receive
these benefits from mothers than from other community members.
We expect social benefits to include, first, social buffering, which is
known to be effective in stress reduction and, second, effective
social learning of social skills required for navigating the complexities
of chimpanzee adult social life. We expect both to affect reproduc-
tive success. We posit that the socioecological environment in
which chimpanzees have evolved makes mother-offspring associa-
tion throughout the extended immature period influential in pro-
ducing males that can accrue high paternity success. Chimpanzees
and humans share notable similarities in traits such as life history
(similarly extended immature period), social structure (fission-
fusion societies), and socioecological factors that lead both species
to express highly territorial behavior, requiring group-level cooper-
ation to defend territories. We suggest that these similarities make
chimpanzees a good model species for examining the evolution of
prolonged immature dependency, for which chimpanzee mother-
offspring associations may constitute a precursor.
MATERIALS AND METHODS
Behavioral data
Data were collected at the Taï National Park, Côte d’Ivoire (5°45′N,
7°7′W) (56) on three different chimpanzee communities (north,
south, and east). Systematic observation including collection of
demography data covers the following periods (57) for each
community: north: 1982 to present, mean adult (≥12) group
size=18.894, SD=12.562, range size = 9.25 to 16.24km2; south:
1993 to present, mean adult (≥12) group size=22.962, SD=4.586,
range size = 15.49 to 36.59km2; east: 2000 to present, mean adult
Fig. 2. Mother, Sumatra, grooming her 9 year old son, Solibra. Photograph
by L.S.
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(≥12) group size=19.95, SD =3.103, range size = 20.6 to 34.45km2.
For the spatial location of each territory, see (58). Behavioral
data included nest-to-nest focal follows (59) of individuals of the
different social groups on a daily basis by trained local assistants
and researchers, providing a continuous record of births, deaths,
dominance rank, and alpha male tenure length. We applied a
likelihood- based adaptation of the Elo rating approach (60–62),
standardized to a range between 0 and 1, to assess males’ domi-
nance relationships within each group using submissive unidirec-
tional pant grunt vocalizations (63). To standardize dominance
rank across periods with varying numbers of males, we converted
ranks to a proportion between 0 and 1, depending on the number
of males at any given time. This is necessary because the number
of males varied across years, and thus, the same rank (R) held a
different significance in different years (e.g., the sixth ranking male
is the lowest ranking when the group consists of six males but is
midranking when the group consists of 12 males). Thus, we stan-
dardized R to the number of sexually mature males aged ≥10years
in the hierarchy (nm) using the following formula: (nm− R)/
(nm−1) (64).
Parentage analysis using microsatellite genotyping of DNA ob-
tained from noninvasive samples has been carried out on members
of these study groups since 1999. The current dataset includes 259
individuals with an average of 83% complete genotypes at 19 loci.
Briefly, ~100-mg samples of feces were extracted using either the
QIAamp DNA Mini Stool Kit (QIAGEN) or the GeneMATRIX
Stool DNA Purification Kit (Roboklon) as instructed. Aliquots were
first amplified at all 19 loci simultaneously and then subsequently
reamplified using fluorescently labeled primers as detailed in (65).
Resultant genotypes were compared using the “identity analysis”
function of CERVUS (66) to confirm identities, and the “parentage
analysis” function was used to confirm maternities and assign
paternities, using confidence assessments of 80 and 95%. Each of
the paternity assignments received a high likelihood, and other po-
tential sires were excluded by two or more mismatches. Parentage
analyses revealed fathers and confirmed mothers for adult males for
north group from 1990, south group from 1999, and east group
from 2012.
We limited the dataset to males who survived at least four repro-
ductive years, taken from the age of the youngest siring age known
for this population (10 years old) until 14 years of age, and for
whom we have a near-complete siring history (i.e., were at least
10 years old when fecal sample collection and paternity analysis
were established such that >90% of offspring reaching 2 years old
had assigned paternities). Last, we limited siring to viable offspring,
those who survived ≥2 years of age. This gave us a sample across
groups of n=23 sexually mature males (≥10 years old) with known
mothers (n=21) and a near-complete siring history of offspring
that survived to ≥2 years (with 95% of paternities known across the
study period). n=12 of these were orphans, defined as the mother
dying before the sons reached social independence from their
mothers, when males in this population associate and travel more
with the adult males than with their mothers (12 years old) (37,62).
These orphans, who reached the minimum age of 14 years, lost their
mothers between the ages of 4and 12 years old (dataset S1), where
weaning occurs between 4 and 5 years old (9,31). Thus, the sample
of orphans represents maternal loss during the postweaning period.
This sample included n=48 offspring with genetically identified
fathers.
Statistical analysis
We conducted a series of models to assess the impact of maternal
loss on male reproductive success.
First, to determine whether maternal loss affected alpha tenure,
we fitted a linear model with orphan status (y/n) as the test predic-
tor, using a Gaussian error structure and an identity link function.
To control for the impact of the number of sexually mature males
in the group influencing the likelihood of achieving alpha position,
we included the average number of males present across concep-
tions that lead to viable offspring. To control for number of repro-
ductive years until death or current age, we included the number of
reproductive years per male as a control variable. We reran the
model switching alpha tenure for average dominance rank, such
that we calculated the average dominance rank across each males’
reproductive lifetime while considering the duration each male
held each dominance position [if a male held a position a for x du-
ration, b for y duration, and c for z duration, then we calculated
the average dominance rank as follows: (a * x+b * y+c * z)/
(x+y+z)].
We fitted all models in R (version 3.5.3) (67), using the functions
glm and lm of the R package “lme4” (68). For all models, we con-
ducted appropriate checks on collinearity with all variables with
variance inflation factor (<3), model stability, and model assump-
tions. We verified the assumptions of normally distributed and
homogeneous residuals by visual inspection of Q-Qplots and residuals
plotted against fitted values. These evaluations did not reveal obvious
deviations from model assumptions.
For the Poisson model, we checked for overdispersion, which
did not reveal any issue, being <1. We log-transformed the response
variable of alpha tenure (model 1) to better approximate a normal
distribution. We analyzed the statistical significance of models
using full-null comparisons and a likelihood ratio test for the Poisson
model and with F tests for the Gaussian models. We measured the
significance of each single term by comparing reduced models to
the full model using the drop1 function in R (69). Model stability
tests revealed no influential identities.
Second, to determine whether chimpanzee male orphans sire
their first offspring at a later age compared with non-orphans, we
fitted a linear model using a Gaussian error structure and an identity
link function. We tested the age at first sire as the response variable
with orphan (y/n) as the test predictor. To account for male quality
and potential male-male competition, we added the control predic-
tors of maximum dominance rank reached by the age at first sire
and the average number of males present across conceptions that
led to viable offspring from age 10 years until age of first sire, re-
spectively. Given that chimpanzees had sired their first offspring
before they became alpha, we used maximum dominance rank
rather than alpha tenure in this analysis.
Third, to test whether postweaning maternal loss affects the
number of viable offspring males sire when adult, we fitted a general
linear model using a Poisson error structure and log link function.
We tested the response variable, the number of offspring sired,
against the categorical test predictor, orphan (y/n). To control for
variation in male quality across each male’s reproductive lifetime,
we added the control predictor that we expected to best reflect their
lifetime dominance rank history: alpha male tenure length (in
years). Those who never became alpha were marked as zero. Siring
potential is likely to decrease with increased male-male competi-
tion. Therefore, to account for potential male-male competition, we
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included the log of the inverted average number of males present
for each conception during each male’s reproductive lifetime as an
offset term. In addition, as siring probabilities are expected to in-
crease with increased conception opportunities, we accounted for
the conception opportunities using the number of conceptions that
led to viable offspring (2 years old) across each male’s reproductive
years by adding an offset term of the log of total number of births
that reached 2 years of age during each males’ reproductive years.
By this, we simultaneously considered both the length of reproduc-
tive age and conception opportunities per male. Last, we reran the
model switching alpha tenure for average dominance rank, such
that we calculated the average dominance rank across each males’
reproductive lifetime while considering the duration each male held
each dominance position [if a male held a position a for x duration,
b for y duration and c for z duration, then we calculated the average
dominance rank as follows: (a*x+b*y+c*z)/(x+y+z); table S2].
To determine effect sizes, for the Gaussian models, we calculated R2
from the residuals’ sum of squares (RSS) using the drop1 output
and used the following formula: (RSS predictor A – RSS intercept)/
RSS predictor A. For Poisson models, we calculated the log likelihood
of the full model and reduced models, with the model missing one
predictor at a time.
SUPPLEMENTARY MATERIALS
Supplementary material for this article is available at http://advances.sciencemag.org/cgi/
content/full/6/38/eaaz5746/DC1
View/request a protocol for this paper from Bio-protocol.
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Acknowledgments: We thank the Ministère de l’Enseignement Supérieur et de la Recherche
Scientifique and the Ministère de Eaux et Fôrests in Côte d’Ivoire and the Office Ivoirien des
Parcs et Réserves for permitting the study. We are grateful to the Centre Suisse de Recherches
Scientifiques en Côte d’Ivoire and the staff members of the Taï Chimpanzee Project for
support. We are grateful to R. Mundry for statistical support and A. Nicklisch, V. Staedele, and
C. Rowney for lab work. We thank K. Langergraber for valuable comments reading an early
version of this manuscript. Funding: This study was funded by the Max Planck Society under
the Evolution of Brain Connectome Project and the European Research Council (ERC) under
the European Union’s Horizon 2020 research and innovation programme (grant agreement
no. 679787) awarded to C.C. Ethics statement: All methods were noninvasive and were
approved by Ethics Committee of the Max Planck Society (4 August 2014) and the European
Research Council. Author contributions: C.C. and R.M.W. conceived the study and compiled
data from long-term Taï Chimpanzee Project database, including data from L.S. Genetic
analyses were conducted by L.V. C.C. and L.S. compiled the data, conducted the behavioral
analyses, and devised the figures. C.C. wrote the paper with important contributions from L.S.,
L.V., and R.M.W. All authors gave final approval for publication and agree to be held
accountable for the work performed therein. Competing interests: The authors declare that
they have no competing interests. Data and materials availability statement: All data
needed to evaluate the conclusions in the paper are present in the Supplementary Materials.
Additional data related to this paper may be requested from the authors.
Submitted 13 December 2019
Accepted 28 July 2020
Published 18 September 2020
10.1126/sciadv.aaz5746
Citation: C. Crockford, L. Samuni, L. Vigilant, R. M. Wittig, Postweaning maternal care increases
male chimpanzee reproductive success. Sci. Adv. 6, eaaz5746 (2020).
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Postweaning maternal care increases male chimpanzee reproductive success
Catherine Crockford, Liran Samuni, Linda Vigilant and Roman M. Wittig
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