ORI GIN AL PA PER

Maternal investment during pregnancy in wild meerkats

Stuart P. Sharp • Sinead English • Tim H. Clutton-Brock

Received: 4 May 2012 / Accepted: 20 October 2012 / Published online: 31 October 2012� Springer Science+Business Media Dordrecht 2012

Abstract Maternal investment in offspring development is a major determinant of the

survival and future reproductive success of both the mother and her young. Mothers might

therefore be expected to adjust their investment according to ecological conditions in order

to maximise their lifetime fitness. In cooperatively breeding species, where helpers assist

breeders with offspring care, the size of the group may also influence maternal investment

strategies because the costs of reproduction are shared between breeders and helpers. Here,

we use longitudinal records of body mass and life history traits from a wild population of

meerkats (Suricata suricatta) to explore the pattern of growth in pregnant females and

investigate how the rate of growth varies with characteristics of the litter, environmental

conditions, maternal traits and group size. Gestational growth was slight during the first

half of pregnancy but was marked and linear from the midpoint of gestation until birth. The

rate of gestational growth in the second half of pregnancy increased with litter size,

maternal age and body mass, and was higher for litters conceived during the peak of the

breeding season when it is hot and wet. Gestational growth rate was lower in larger groups,

especially when litter size was small. These results suggest that there are ecological and

physiological constraints on gestational growth in meerkats, and that females may also be

able to strategically adjust their prenatal investment in offspring according to the likely

fitness costs and benefits of a particular breeding attempt. Mothers in larger groups may

benefit from reducing their investment because having more helpers might allow them to

lower reproductive costs without decreasing breeding success.

Keywords Cooperative breeding � Foetal growth � Gestation � Load-lightening �Maternal investment � Meerkat

Electronic supplementary material The online version of this article (doi:10.1007/s10682-012-9615-x)contains supplementary material, which is available to authorized users.

S. P. Sharp � S. English � T. H. Clutton-BrockDepartment of Zoology, University of Cambridge, Downing Street, Cambridge CB2 3EJ, UK

S. P. Sharp (&)Lancaster Environment Centre, Lancaster University, Lancaster LA1 4YQ, UKe-mail: s.sharp2@lancaster.ac.uk

123

Evol Ecol (2013) 27:1033–1044DOI 10.1007/s10682-012-9615-x

Introduction

Maternal investment in the development of offspring has a profound impact on the

survival and future reproductive success of both the mother and her young (Mousseau and

Fox 1998; Roff 2002; Maestripieri and Mateo 2009). It has been shown in a wide range of

taxa from invertebrates to humans that the level of investment covaries with the mother’s

age (e.g. Berkeley et al. 2004; Plaistow et al. 2007) and condition (e.g. Fairbanks

and McGuire 1995; Warner et al. 2007), the quality of her mate (e.g. Wedell 1996;

Cunningham and Russell 2000) and the environment that she experiences during various

stages of the reproductive cycle (e.g. Kaplan and Phillips 2006; Roseboom et al. 2006).

Furthermore, the size and growth of offspring are not only constrained by maternal

phenotype and environmental conditions, but mothers may strategically adjust the amount

of resources that they allocate to their young in order to maximise their own lifetime

fitness (Mousseau and Fox 1998; Marshall and Uller 2007; Maestripieri and Mateo 2009).

However, the extent to which mothers are able to make these adjustments according to

predictions about the future quality of the environment remains a source of debate in

evolutionary and biomedical research (Wells 2007; Gluckman et al. 2008; Monaghan

2008).

Cooperatively breeding species, in which parents receive assistance with the care of

their offspring from one or more ‘helpers’, are useful model systems for investigating

maternal investment strategies (Russell and Lummaa 2009). The number of helpers and

their effect on maternal and offspring fitness vary considerably both between and within

species (Wilson 1971; Bourke 1999; Solomon and French 1997; Dickinson and Hatchwell

2004; Russell 2004), making group size an important and predictable source of environ-

mental heterogeneity that may influence the extent to which mothers invest in a given

reproductive attempt (Russell and Lummaa 2009). Reduced maternal care of offspring in

the presence of helpers, or ‘load-lightening’, has been reported in many species and can be

associated with an increase in maternal condition, survival or productivity (Wilson 1971;

Hatchwell 1999; Heinsohn 2004; Russell 2004). However, the majority of research has

focused on birds or insects and, with the exception of work on humans (Sear and Mace

2008; Hrdy 2009; Kramer 2010), there have been relatively few studies of how alloparental

care impacts on maternal investment in mammals (Russell 2004). In particular, prenatal

investment has rarely been investigated (Russell and Lummaa 2009), despite good evi-

dence from other vertebrates that mothers adjust their allocation of resources to eggs

according to the number of helpers in their group (e.g. birds: Russell et al. 2007; fish:

Taborsky et al. 2007).

Unique among vertebrates, gestation in mammals is an extended period of maternal

investment and one of the most energetically costly stages of reproduction for females

(Gittleman and Thompson 1988). This generates a strong link between a mother’s con-

dition and her offspring’s size and growth, making gestation a likely time for environ-

mental and social factors to influence maternal investment strategies (Maestripieri and

Mateo 2009). The rate of foetal growth provides a useful measure of gestational investment

that, across species, correlates with various life history traits (Frazer and Huggett 1974;

McKeown et al. 1976; Martin and MacLarnon 1985; Pontier et al. 1993), but most studies

of intraspecific variation have measured the length of the gestation period rather than the

rate of foetal growth itself. Gestation length has been shown to correlate with maternal age

or state (e.g. Silk et al. 1993; Mysterud et al. 2009), environmental conditions (e.g. Byers

and Hogg 1995; Boyd 1996) or offspring sex (e.g. Byers and Hogg 1995; Mysterud et al.

2009), but further work is needed to determine how these factors affect foetal growth rate,

1034 Evol Ecol (2013) 27:1033–1044

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especially in polytocous species where mothers may trade off the per capita investment in

foetal development against litter size (Frazer and Huggett 1974; McKeown et al. 1976;

Pontier et al. 1993). Moreover, while social effects on gestation length have been described

in one cooperatively breeding species (banded mongooses, Mungos mungo: Cant 2000;

Hodge et al. 2011), we know of no study that has investigated whether the presence or

number of helpers impacts on maternal investment in foetal growth rate.

One major impediment to studying foetal growth is the difficulty of obtaining sequential

measures of the mass of foetuses. As yet, most estimates of foetal growth rate are either

derived from measures of gestation length and birth mass (Frazer and Huggett 1974;

Martin and MacLarnon 1985) or are based on samples of mothers culled at different stages

of gestation (Trites 1991; Yunker et al. 2005). Very few studies have been able to track the

development of individual foetuses (see Hildebrandt et al. 2007 for an exception), but it is

sometimes possible to repeatedly weigh individual mothers throughout pregnancy and,

thus, to explore the ecological and life history correlates of the rate of increase in maternal

mass (Boyd 1985; Urison and Buffenstein 1995; Long and Ebensperger 2010). Although

growth of the placentae and other maternal tissues contributes to the gain in mass, the rate

of increase is likely to be strongly correlated with foetal growth rate (Boyd 1985). Fur-

thermore, placental development is an important but often overlooked component of a

mother’s energetic investment during pregnancy (Gittleman and Thompson 1988).

Investigating the combined gestational growth of maternal and foetal tissues therefore

provides important insights into maternal investment, but existing studies of cooperatively

breeding species are entirely restricted to captive or domesticated populations and have not

directly investigated the influence of group size (Urison and Buffenstein 1995; Long and

Ebensperger 2010).

Here, we investigate gestational growth in a wild population of Kalahari meerkats

(Suricata suricatta, Desmarest). Meerkats are cooperatively breeding mongooses that live

in cohesive social groups of up to 50 individuals. Within these groups, reproduction is

monopolised by a single female who is behaviourally dominant to all other female group

members (Doolan and Macdonald 1997; Griffin et al. 2003; Clutton-Brock et al. 2008).

Vacant dominant positions are filled by the oldest subordinate in the group or, where

there is no age difference among the oldest females present, by the heaviest (Hodge et al.

2008). The dominant female produces one to four litters per year, each consisting of up

to seven pups which are raised by all members of the group (Clutton-Brock et al. 2001,

2004; Hodge et al. 2008). Maternal age and body mass are important determinants of

both investment in postnatal care and breeding success in dominant females (Russell

et al. 2003; Hodge et al. 2008; Sharp and Clutton-Brock 2010), and the postnatal growth

rate and survival of pups are higher in larger groups (Russell et al. 2002; Hodge et al.

2008; but see Sharp and Clutton-Brock 2010) despite reduced contributions to offspring

care by dominant females (Clutton-Brock et al. 2004). However, the influence of

maternal characteristics and group size on maternal investment during gestation has

never been investigated. In this study, we use longitudinal records of body mass and life

history to: (1) describe the pattern of gestational growth in dominant females; (2)

measure the rate of gestational growth during the linear growth phase; and (3) investigate

how gestational growth rate varies with characteristics of the litter, environmental con-

ditions, maternal traits and group size. In particular, we test the prediction that growth

rates are lower in larger groups because mothers are able to reduce their prenatal

investment when they are likely to have more helpers providing postnatal care to

compensate for this.

Evol Ecol (2013) 27:1033–1044 1035

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Materials and methods

Study population and data collection

A wild population of meerkats (S. suricatta) has been closely monitored at the Kuruman

River Reserve in the South African Kalahari (26�580S, 21�490E) since January 1994. The

present study used data collected up to November 2007, during which time more than

1,500 individuals in 35 social groups were habituated to observation from \2 m. All

individuals were marked with subcutaneous transponder chips and could be identified in

the field by unique dye marks applied to their fur. Groups were visited approximately once

every 3 days to record all key life history events including changes in dominance or

pregnancy status. More than 95 % of individuals were trained to climb onto an electronic

balance and could be weighed (in g) most mornings before they went foraging. Dominance

status was determined from established behavioural assays, and pregnancy could be

identified by swelling of the abdomen and increases in body mass (Clutton-Brock et al.

1998; Hodge et al. 2008). Pregnancy in meerkats lasts around 70 days (Doolan and

Macdonald 1997) and is usually first detected around the midpoint of this period. Litter

mass prior to parturition typically comprises ca. 20 % of female body mass (Doolan and

Macdonald 1997), so although pups are born in an underground burrow and remain there

for around 3 weeks, birth dates could be established reliably from the sudden loss of body

mass and abdomen distention in the mother (Clutton-Brock et al. 1998; Hodge et al. 2008).

Conception dates were then estimated by backdating 70 days from birth, as behavioural

signs of oestrus were rarely observed.

The pattern of gestational growth

In order to determine the pattern of growth throughout the gestation period, we plotted

maternal body mass against time using data from all those pregnancies during which the

mother was the dominant female in her group and had been weighed at least ten times

between the estimated conception date (day 1) and the day before birth (day 70; n = 247

litters, 41 mothers, constituting over 70 % of all litters born to dominant females during the

study period). Preliminary inspection of the data provided unequivocal evidence that the

interbirth interval, and thus the gestation period, was\70 days in a small number of cases

(\10 %). We therefore excluded measures of body mass taken in the first few days of the

estimated gestation period if the female was pregnant with her previous litter.

Calculation of gestational growth rate

Preliminary examination of the data indicated that gestational growth was slight during

the first half of pregnancy but marked and linear thereafter, and that litter size was the

most important determinant of growth rate. We therefore calculated gestational growth rate

(in g per day) for each pregnancy where litter size was known (see below) by obtaining the

slope from a linear regression of maternal body mass against time from day 35 to day 70 of

the gestation period. Analyses were restricted to those pregnancies for which the mother

had been weighed at least ten times during this period (n = 137 pregnancies, 29 mothers).

Litter size could only be determined once pups had emerged from their natal burrow, but

previous ultrasound analyses have shown that few pups are lost between pregnancy and

emergence unless the entire litter is killed: of those pups born to dominant mothers, 85 %

1036 Evol Ecol (2013) 27:1033–1044

123

survived to emergence and, in the few litters (17 %) where some but not all pups were lost

prior to emergence, the mean number of pups per litter that died was 0.6 (Russell et al.

2003; AF Russell unpublished data). Litter size at emergence was therefore considered to

be a reliable measure of litter size at birth.

Factors associated with gestational growth rate

Gestational growth rate was approximately normally distributed and therefore fitted as the

response variable in a series of linear mixed effect models in order to investigate corre-

lations with characteristics of the litter (litter size and litter sex ratio), environmental

conditions (season), maternal traits (maternal age and initial body mass) and group size.

Litter size was measured at emergence from the natal burrow as described above. Simi-

larly, litter sex ratio was calculated for emerged pups only and measured as the number of

males divided by the total number of pups in the litter. In 23 of the litters, one or two pups

died before they could be sexed; to avoid having to exclude these litters from the analyses,

we calculated litter sex ratio for the sexed pups only as this was unlikely to bias the

analyses. The season during which the litter was conceived was fitted in the models in

order to account for environmental variation, as seasonality is thought to have a major

influence on other aspects of growth in meerkats (Russell et al. 2002; English et al. 2012).

The season was either the hot and wet ‘high’ season (October to April) or the cold and dry

‘low’ season (May to September; Doolan and Macdonald 1997; Russell et al. 2002). Most

litters are conceived during the high season when food availability and long-term growth

rates are relatively high (Doolan and Macdonald 1997; English et al. 2012). Maternal age

was measured (in days) at the birth of the litter, and initial body mass was the mean

maternal mass (in g) in the week after conception. Group size was calculated as the mean

daily group size (excluding pups) in the week prior to conception. Finally, the identity of

the mother and the cohort (the calendar year at conception) were fitted as random terms in

the models to account for the non-independence of multiple litters from the same mother

and interannual variation in seasonal conditions, respectively.

Prior to analysis, we centred and standardised all variables (except season) to facilitate

the direct comparison of parameter estimates and the appropriate interpretation of main

effects involved in interactions (Schielzeth 2010). Colinearity between all explanatory

variables was assessed by calculating correlations and variance inflation factors (VIFs),

following Zuur et al. (2009). All variables were included in the analysis because pairwise

correlations between them were weak (r \ 0.4 in all cases) and VIFs were small (\2 in all

cases). We then used an information theoretical approach for model selection and

parameter estimation (Burnham and Anderson 2002). Preliminary analyses suggested that

the interaction between litter size and group size was the only one of all possible first-order

interactions that was likely to explain variation in gestational growth rate. This interaction,

together with the six explanatory variables described above, produced a set of 48 candidate

models excluding those that did not contain litter size and those that contain the interaction

but not the constituent main effects (see Supplementary Table S1); litter size was fitted in

all models because it is likely to be the most significant determinant of gestational growth

rate. All candidate models were fitted using the package ‘lme4’ (Bates et al. 2011) in the R

environment, version 2.13.0 (R Development Core Team 2011). We then compared these

models using AICc (the second order Akaike Information Criterion), and averaged the

95 % confidence set of models (Burnham and Anderson 2002) in the package MuMIn

(Barton 2011). We validated these models by plotting the distribution of the residuals,

Evol Ecol (2013) 27:1033–1044 1037

123

the residuals versus the fitted values and the residuals versus each of the covariates

(Zuur et al. 2009).

Results

The pattern of gestational growth

Gestational growth was found to be negligible during the first half of pregnancy but

marked and approximately linear from the midpoint of gestation until birth (Fig. 1).

Examining the data for each pregnancy separately showed that this overall pattern was

consistent, but that the rate of linear growth varied between pregnancies, even for litters of

the same size (Fig. 2).

Factors associated with gestational growth rate

Gestational growth rate was most strongly correlated with litter size and season (Table 1;

Table S1). The rate of growth increased with litter size (Fig. 3; Table 1) and was higher for

litters conceived during the high season (Table 1). Although litter sex ratio appeared in the

95 % confidence set of models, the effect size was negligible and unlikely to be biolog-

ically meaningful (Table 1). Both the age and initial body mass of the mother were

positively correlated with gestational growth rate, but there was a strong negative corre-

lation between the rate of growth and group size (Fig. 3; Table 1); an interaction between

litter size and group size revealed that this effect was stronger in smaller litters (Fig. 3;

Table 1).

Day of gestation

Mat

erna

l bod

y m

ass

(g)

0 10 20 30 40 50 60 70

500

600

700

800

900

1100

Fig. 1 The pattern of gestational growth during pregnancy. The boxes show the medians, first and thirdquartiles and the whiskers show the ranges for all data from 247 pregnancies

1038 Evol Ecol (2013) 27:1033–1044

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Discussion

The pattern of gestational growth in wild dominant female meerkats was broadly similar to

that reported in captive studies of two social rodent species (naked mole-rats,

35 40 45 50 55 60 65 70

700

800

900

1000

1100

1200

Day of gestation

Mat

erna

l bod

y m

ass

(g)

Fig. 2 The pattern of gestational growth during the second half of pregnancy. The scatter plot showsthe raw data for three examples of pregnancies in different dominant females with a litter size of four(the median litter size across all litters)

Table 1 The results of linear mixed effect models of the factors associated with gestational growth rateduring the second half of pregnancy

Fixed effect Estimate Unconditionalstandard error

Relativeimportance

Intercept 5.26 0.18

Litter size 0.89 0.12 1.00

Litter sex ratio -0.05 0.11 0.23

Season (low relative to high) -0.87 0.28 1.00

Maternal age 0.18 0.14 0.39

Initial body mass 0.17 0.13 0.41

Group size -0.20 0.14 0.62

Litter size 9 group size 0.16 0.11 0.29

Random effect Variance

Mother ID 0.06

Cohort 0.07

Residual 1.70

For details of the full set of models, see Supplementary Table S1

Details of the fixed effects were obtained by averaging the 95 % confidence set of models. Details of therandom effects were obtained from the best-fitting model

Evol Ecol (2013) 27:1033–1044 1039

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Heterocephalus glaber: Urison and Buffenstein 1995; degus, Octodon degus: Long and

Ebensperger 2010), with negligible or slow growth until approximately half way through

the gestation period and marked linear growth thereafter. In contrast, a study of wild

rabbits (Oryctolagus cuniculus) found that growth rate was approximately constant and

linear throughout gestation (Boyd 1985). Gestational growth combines development of the

foetuses, placentae, uterus and mammary tissue in addition to nutrient storage by the

mother (Boyd 1985; Gittleman and Thompson 1988), and the relative investment in each of

these is likely to differ between species (Gittleman and Thompson 1988). In smaller

mammals, for example, mothers typically deposit proportionally less fat (Gittleman and

Thompson 1988), and this may be especially true of species such as meerkats and degus

that live in arid environments. Furthermore, the costs of lactation in both of these species

are often shared between the mother and one or more allolactators (Scantlebury et al. 2002;

Ebensperger et al. 2006), and mothers may therefore investment less in the development of

mammary tissue or fat deposition. In either case, increases in maternal mass would be

relatively small until the onset of significant foetal growth, which in many species occurs a

considerable time after conception (McKeown et al. 1976; Trites 1991; Yunker et al.

2005).

The rate of gestational growth during the second half of pregnancy increased signifi-

cantly with litter size. This is to be expected in all polytocous mammals given that foetal

growth typically accounts for the majority of maternal weight gain in pregnancy (Boyd

1985; Michener 1989). Interestingly, however, there was no clear evidence of a reduction

in the per capita growth rate of foetuses in larger litters, and it may be that trade offs

between pup quality and quantity are difficult to detect without measuring the body mass of

Litter size

Ges

tatio

nal g

row

th r

ate

(g p

er d

ay)

1 2 3 4 5 6

02

46

810

12

Fig. 3 Gestational growth rate during the second half of pregnancy for litters of different sizes and ingroups of different sizes. The solid line shows the relationship predicted by the averaged model for a motherof mean age (1,724 days) and initial body mass (768.6 g) in a group of mean size (18) during the highseason (when most pregnancies occur). The broken lines show the same relationship but for females ingroups of size one standard deviation larger (dotted line) and smaller (dashed line) than the mean. The boxesshow the medians, first and third quartiles and the whiskers show the ranges of the partial residuals for themain effect of litter size

1040 Evol Ecol (2013) 27:1033–1044

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individual foetuses or pups at birth. Alternatively, the potential for such a trade off may be

complicated by the influence of group size on maternal investment. As predicted, the rate

of gestational growth was lower in larger groups, and this supports the hypothesis that

mothers are able to strategically adjust their level of prenatal investment according to the

amount of assistance they are likely to receive with raising their young (Russell and

Lummaa 2009). If postnatal offspring care by helpers compensates for reductions in

maternal investment during gestation, then mothers may benefit from lowering repro-

ductive costs without decreasing offspring fitness. Similar examples of prenatal ‘load-

lightening’ have been found in birds (Russell et al. 2007) and fish (Taborsky et al. 2007),

but we know of no mammalian studies. In meerkats, pup growth rates and survival are

higher in larger groups (Russell et al. 2002; Hodge et al. 2008; but see Sharp and Clutton-

Brock 2010) despite reduced contributions to offspring care by dominant females (Clutton-

Brock et al. 2004). Further work is now needed to determine how variation in maternal

investment during and after gestation impacts on the survival and reproductive success of

dominant females in groups of different sizes. This would help to elucidate whether

reduced investment by females with more helpers is a strategic adjustment or instead the

result of constraints imposed by living in larger groups. For example, competition for food

may increase with group size, or maintaining dominance may be more costly when the

number of subordinate females in the group is higher (Clutton-Brock et al. 2008).

The relationship between gestational growth rate and group size was weaker in larger

litters. This may be because there are greater constraints on maternal investment when

litter size is large. For example, if mothers reduce the per capita growth rate of foetuses in

larger litters, as has been shown in other mammals (McKeown et al. 1976; Michener 1989),

then further reductions according to group size may not be possible without compromising

offspring fitness. Even if such trade offs do not occur, then mothers may be more likely to

maximise investment in larger litters in order to offset the increased level of sibling

competition. Arguably, the interaction between litter size and group size is more indicative

of strategic investment than of investment constrained by competition within groups, as it

is difficult to imagine why the effects of the latter would be more apparent when litter size

was smaller.

It is important to note that litter size was measured at emergence rather than at birth, and

it is possible that the effects reported for litter size and its interaction with group size are

misleading. However, very few pups die between birth and emergence unless the entire

litter is killed (Russell et al. 2003; see also the ‘‘Materials and methods’’), so fitting litter

size at birth to the models would be very unlikely to change the results presented here

beyond minor differences in effect sizes. Similarly, the lack of any meaningful effect of

litter sex ratio at emergence does not necessarily mean that the sex ratio in utero has no

influence on foetal growth, but sex differences are more likely to occur in those species

with a stronger degree of sexual size dimorphism or sex-biased variance in reproductive

success than meerkats (Trites 1991; Byers and Hogg 1995; Mysterud et al. 2009).

The season during which conception occurred was an important predictor of gestational

growth rate. The rate of growth was higher between October and April, when temperature

and rainfall are also higher, than between May and September, and similar relationships

have been found between seasonality and other aspects of growth in meerkats (Russell

et al. 2002; English et al. 2012). Several studies of other species have reported seasonal

differences in gestation length or foetal growth rates (Byers and Hogg 1995; Boyd 1996;

Yunker et al. 2005), and these differences may be particularly marked in arid environ-

ments, where even sporadic periods of rainfall can dramatically increase food availability

and thus intake rate and growth (English et al. 2012). Further analysis of the relationship

Evol Ecol (2013) 27:1033–1044 1041

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between gestational growth and rainfall at different stages of the reproductive cycle is

needed to investigate whether mothers are able to adjust their prenatal investment

according to the amount of food that is likely to be available during the postnatal period of

offspring care. Similarly, the positive correlations between gestational growth rate and

both maternal age and initial body mass support the findings from studies of other

mammals, including humans, that a mother’s condition influences her prenatal investment

(Michener 1989; Trites 1991; Silk et al. 1993; Scholl et al. 1997), but the extent to which

these relationships result from condition-dependent constraints or strategic investment

remains unclear (Monaghan 2008).

In conclusion, the rate of gestational growth in dominant female meerkats varies

according to characteristics of the litter, season, maternal traits and group size. These

results suggest that there are ecological and physiological constraints on gestational

growth, but also provide the first evidence from mammals that mothers may be able to

strategically adjust their prenatal investment in offspring development according to

environmental and social conditions. The idea that mothers are able to foresee what these

conditions will be like during the lifetime of the offspring remains contentious (Wells

2007; Gluckman et al. 2008; Monaghan 2008) but, in cooperative breeders, the number of

helpers in the group is one source of environmental heterogeneity that mothers may be able

to reliably predict (Russell and Lummaa 2009). Regardless of the mechanism underlying

variation in gestational growth rate, the results presented here indicate that differential

investment during pregnancy may be an important but overlooked component of mam-

malian life history evolution.

Acknowledgments We thank the Kotze family and Northern Cape Conservation for allowing us toconduct research in the Kalahari; the Mammal Research Institute at the University of Pretoria and PennyRoth for logistical support; and Marta Manser for her role in maintaining the Kalahari Meerkat Project. Weare also extremely grateful to the many volunteers, field staff, postgraduate students and postdoctorates whoassisted with data collection and to Shinichi Nakagawa and Andrew Bateman for statistical advice. Twoanonymous reviewers provided feedback that greatly improved the paper. The Biotechnology and BiologicalSciences Research Council, the Isaac Newton Trust, the Leverhulme Trust, the University of Cambridge, theSwiss National Science Foundation and the Earthwatch Institute provided financial support.

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