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Abstract

  1. Top of page
  2. Abstract
  3. Introduction
  4. Methods
  5. Results
  6. Discussion
  7. Acknowledgements
  8. Literature Cited

Alloparents contribute to offspring care and alleviate the workload of breeders. The help provided varies with the age and/or experience of helpers, but it is not known whether breeders vary their investment based on the age of helpers by adjusting the parental care they provide. We studied the alloparental care provided by juvenile and subadult philopatric daughters in biparental African striped mice Rhabdomys pumilio with and without the mother as a measure of alleviation of maternal workload. We showed in a previous study that alleviation of maternal workload directly affects the development of paternal care in their sons, so we studied the expression of paternal care in young males raised by helpers as a proxy of the long-term consequences of helping. Both juvenile and subadult daughters provided care but the level of alloparental care and concomitant alleviation of maternal care was age-dependent. In the absence of the mother, juvenile daughters provided just 6% of care compared with 24% of subadult daughters. Sons raised by mothers and juvenile helpers displayed the expected exaggerated levels of care also observed when mothers raise litters on their own. While our results show the direct value of subadult daughters, juvenile daughters could contribute indirectly (e.g. nest maintenance) to alleviating maternal workload. The development of paternal care indicates that mothers do distinguish between the care provided by different aged helpers. Overall, the type of alloparental care provided by female striped mice is expected to change over their lifetimes, resulting in increased inclusive fitness through caring for siblings and acquisition of parenting skills.


Introduction

  1. Top of page
  2. Abstract
  3. Introduction
  4. Methods
  5. Results
  6. Discussion
  7. Acknowledgements
  8. Literature Cited

Alloparental care describes behaviours, in particular feeding or defence of offspring, performed by a non-parent (helper), which benefits young that are not direct descendents of the alloparent (Crespi & Yanega 1994) and that would not occur in the absence of these young (Woodroffe & Vincent 1994). Alloparental care occurs in diverse taxa, including arthropods (e.g. paper wasps Polistes dominulus, Field & Cant 2006), fish (e.g. fairy cichlid Neolamprologus brichardi, Wisenden 1999), amphibians (e.g. thin-toed frogs Leptodactylus sp., Rodrigues et al. 2011), birds (e.g. tessellated darter Etheostoma olmstedi, Stiver et al. 2012) and mammals (e.g. common marmosets Callithrix jacchus, Barbosa & da Silva Mota 2013). Helpers are usually relatives of breeding adults (Clutton-Brock 2002), being offspring from a previous litter (e.g. cotton-top tamarins Saguinus oedipus oedipus; Ginther et al. 2001) or siblings that have been reproductively suppressed (e.g. house mice Mus domesticus, König 1993).

The primary costs of alloparental care are lost reproductive opportunities and loss of body condition. For example, the breeding success of alpine marmot Marmota marmota helpers is lower than that of dominants (Arnold 1990), and suricates lose approx. 3.8% of body weight over the breeding season due to babysitting (Clutton-Brock et al. 1998). The advantages of alloparental care can be direct, such as by their developing parental care behaviour (e.g. Mongolian gerbils Meriones unguiculatus, Salo & French 1989) or by inheriting the breeding territory and becoming reproductively dominant (e.g. dwarf mongooses Helogale parvula; Creel & Waser 1994). The inclusive fitness of helpers (indirect benefit) can also be enhanced if their helping increases the reproductive output of the breeders (e.g. pine voles Microtus pinetorum, Powell & Fried 1992) or increases survival and growth of related young (e.g. prairie voles Microtus ochrogaster, Solomon 1991). Alloparents can also reduce the workload of the breeders, freeing breeding adults to pursue other activities, such as foraging, thereby maximizing their energy intake and increasing their reproductive fitness and the inclusive fitness of related helpers. Alloparents can alleviate maternal workload, as reported in suricates (Clutton-Brock et al. 2001), and paternal workload in species displaying paternal care, such as Djungarian hamsters Phodopus campbelli (Wynne-Edwards 1995).

The level of alloparental care provided by helpers changes with helper age. For example, older helpers carry infants more often than younger helpers in cotton-top tamarins (Tardif et al. 1992). Older helpers are presumably more experienced caregivers (Roberts et al. 1998) or are physically larger and do not themselves require care, such as the ability to thermoregulate independently. What is not evident is whether breeders respond to the age of helpers, and hence the presumed level of experience, by adjusting the parental care provided. In other words, does helper age predict levels of alloparental care and concomitantly the level of parental care?

The African striped mouse Rhabdomys pumilio from the arid Succulent Karoo of South Africa is a small (± 40 g), diurnal, biparental murid rodent. Striped mice are facultatively group-living, displaying social flexibility (i.e. males and females switch social organization mating strategies; Schradin et al. 2012). When population density is low, females favour solitary nesting due to the costs associated with reproductive competition (e.g. infanticide, Schradin et al. 2010; increased female–female aggression, Schubert et al. 2009) and males adopt a roaming strategy, soliciting matings but showing no paternal care (Schradin 2008). In contrast, when population density is high, striped mice form groups comprising 3–4 breeding females and a single dominant territorial breeding male that, through provision of paternal care, can significantly increase offspring development (Schradin & Pillay 2005). In addition to maternal and paternal care (Schradin 2008), breeding females provide allomaternal care in the communal nest (Schubert et al. 2009). Moreover, over-wintering philopatric juveniles of both sexes remain in the nest for a number of months after weaning and provide alloparental care to their younger siblings (Schradin & Pillay 2004). Philopatric helpers participate in territorial defence, nest building (Schradin & Pillay 2004) and group huddling (Schradin 2005; Scantlebury et al. 2006).

Female striped mice adjust levels of maternal care when raising young with and without help, suggesting that helpers alleviate maternal workload. Schubert et al. (2009) found that help provided by sisters (aunts) reduces levels of maternal care of breeding females. Similarly, we showed that when female striped mice raise young without a mate, they compensate for a lack of paternal care by increasing the time spent engaged in maternal care by 1½ times compared with females raising young with a mate (Rymer & Pillay 2011). Compared with other biparental rodents, such as oldfield mice Peromyscus polionotus (Kaufman & Kaufman 1987) and California mice P. californicus (Gubernick & Teferi 2000), compensation of maternal care is unique to striped mice. Maternal compensation has consequences for the development of young striped mice. In particular, the level of care provided by the mother during early rearing is directly related to the level of paternal care displayed by their adult sons, so that sons raised by mothers alone show higher levels of paternal care than those raised by both parents (Rymer & Pillay 2011).

The aim of our study was to assess the level of alloparental care provided by juvenile and subadult philopatric daughters in captive striped mice. We also investigated whether these different aged daughters influenced the development of paternal care of their younger brothers, which we used to assess the long-term consequences of alloparental care. We predicted that, compared with juvenile helpers, subadult helpers would provide higher levels of alloparental care (e.g. huddling), thereby alleviating maternal workload. Based on our previous results that greater maternal investment results in sons displaying greater paternal care (Rymer & Pillay 2011), we also predicted that sons reared by the mother and juvenile daughter would show greater paternal care to their own offspring later because juvenile helpers do not reduce maternal workload. In contrast, males raised by the mother and subadult daughter would display lower levels of paternal care.

Methods

  1. Top of page
  2. Abstract
  3. Introduction
  4. Methods
  5. Results
  6. Discussion
  7. Acknowledgements
  8. Literature Cited

Subjects

Striped mice in this study were F1–F4 generation individuals derived from Goegap Nature Reserve (Succulent Karoo, Northern Cape Province, South Africa; 29.40S, 17.53E). They were housed in the Milner Park Animal Unit at the University of the Witwatersrand, under controlled environmental conditions (14:10 h light: dark regime, lights on at 05:00 h; 20–24°C; 30–60% relative humidity).

Experimental Design

Experiments involved two phases. In Phase 1 (Ph1), 15 parentally experienced (i.e. individuals had each raised one litter previously, but not with each other) breeding pairs (age at pairing (mean ± SE): males 9 ± 0.52 mo; females 9 ± 0.42 mo) were established and housed in glass tanks (l × b × h: 46 × 30 × 32 cm). The tank floors were covered with a layer of wood shavings for bedding, and a plastic nest box (13 × 9 × 10 cm) was provided. Nesting material comprised of dry grass provided weekly and approx. 5 g of paper towel provided twice weekly. Each mouse received one cardboard toilet roll/paper cup for enrichment. Each mouse received approx. 10 g of food daily (5 g mixed seed and mouse cubes sprinkled throughout the cage to stimulate foraging behaviour; 5 g fresh fruit/vegetables). Water was available ad libitum.

Each pair produced three litters, each representing a different treatment (15 litters per treatment). Males and females (M + F) raised their first litter together until weaning at 21 d of age. At weaning of the first litter, mothers were subjected to a second treatment (mother + young juvenile helper = M + YH), in which a daughter from the first litter was randomly selected and remained with the mother in the breeding tank. The father and all remaining offspring were removed and housed individually or in same-sex sibling pairs in opaque holding cages (42 × 26 × 14 cm) under the conditions described above. Striped mice show post-partum oestrous, so females were pregnant when fathers and the first litter were removed. The mother and juvenile daughter then raised the next litter of young together. Juvenile daughters were approx. 28–30 days old (juvenile stage 30–35 days old; as developed by Brooks 1982) at the time of the second litter's birth. For the third treatment (mother + older subadult helper = M + OH), the original male and female pairs were re-established. At 20 d after pairing, the male was removed and housed elsewhere and an approx. 60-days-old subadult daughter (subadult stage 55–60 days old; Brooks 1982) from the first litter, which had been housed separately from the mother for at least 39 d (i.e. not the daughter used in the second treatment, which was removed to prevent her mating with the male and biasing the results), was randomly selected and returned to the breeding tank after removal of the father to prevent mating. The daughter was separated from her mother for 24 h by inserting a wire mesh barrier (30 × 32 cm, 1 × 1 cm squares) into the tank and placing the mother on one side and the daughter on the other. We did this to prevent aggression and to re-establish familiarity. The wire mesh barrier was then removed, and the mother and subadult helper raised the next litter.

The parental and alloparental care behaviour of the mother and helper (juvenile and sub-adult) for the next litter was video-recorded for 15 min every second day, starting on day 1 (day 0 = day of birth) until day 11. Recordings were only made until day 11, as young striped mice start eating solid food at this time (Pillay 2000) and are often outside the nest. Recordings were made between 07:00 and 11:00 h, coinciding with the peak activity period of striped mice (Rymer & Pillay 2011). No observers were present in the room during taping sessions. Using continuous sampling, we scored the parental care behaviour of test subjects (mothers and helpers) for the 15 min taping session. Parental and alloparental care was scored using the following behaviours (after Schradin & Pillay 2003): huddling, grooming (included sniffing and licking) pups and time spent in close proximity (< 2 cm) of pups (designated ‘near’). For maternal care, we could not distinguish between nursing and huddling pups, so the data were collectively classified as huddling (as described by Schubert et al. 2009). Juvenile helpers were sexually immature, and subadult helpers were not pregnant, so no nursing behaviour was expected by alloparents. To assess the influence of helping by fathers (M + F) and daughters (M + YH, M + OH), we compared our findings to the maternal behaviour of females that raised young alone (M–F; available in Rymer & Pillay 2011).

To assess whether helpers alleviate maternal care, we compared the level of alloparental care provided by juvenile and subadult helpers and paternal care provided by fathers when mothers were not providing care. For these analyses, we compared the time helpers attended pups (huddling and grooming) when the mother was away from the nest (feeding or exploring the tank).

In Phase 2 (Ph2), at sexual maturity (approx. 90 d of age), one male (son) from each litter (M + YH; M + OH) was randomly selected and paired with an unrelated mate (obtained from the breeding colony) of approximately the same age, resulting in two treatments: SM + YH (son from M + YH) and SM + OH (son from M + OH). Pairs were housed in opaque holding cages and kept under the same conditions described above. A few days prior to parturition, pairs were transferred into glass tanks, and males and females were housed together until offspring were weaned (i.e. as described for M + YH). The paternal care behaviour of sons was measured in the same manner as for mothers and helpers.

Offspring Growth

We weighed all male and female pups in litters produced in both phases and recorded the masses (nearest 0.1 g) every day post-natally for the first 7 d and every 3 d thereafter until day 21. Growth rates were then calculated using the formula:

(LN mass day 21−LN mass day 1) ⁄ 20 d.

Ethical Note

All striped mice received environmental enrichment, and the experimental procedures had no obvious negative effects. Individuals were returned to the colony after experiments for use in other studies. This study complied with the current laws and regulations in South Africa and was approved by the Animal Ethics Screening Committee of the University of the Witwatersrand (clearance no. 2005/62/2A).

Statistical Analysis

All analyses were performed using Statistica 7.1 (Statsoft Inc, www.statsoft.com). Parental care data for all treatments met the assumptions of homogeneity of variances (Levene's test) and normality (Shapiro–Wilks test). The model-level significance was determined at α = 0.05, and all tests were two-tailed.

To assess whether breeding pair identity (i.e. to account for individual differences in female and male behaviour) had a random effect on the three behavioural variables (near, huddling, grooming) for paternal (fathers, sons) and alloparental (philopatric daughters) care over the 6 d of video-recording, we first analysed the data with variance components analysis using the Expected Mean Squares method. In all cases, breeding pair identity was not a significant predictor of parental care (p > 0.10) and was not considered further in analyses. Next, we used a general linear model (GLM) with repeated measures, multivariate design, to analyse the data. Treatment was the categorical predictor, which also took into account litter order because the experimental design considered litter 2 for the M + F treatment, litter 3 for the M + YH treatment and litter 4 for the M + OH treatment (above), the behaviours (near, huddling, grooming) were the dependent variables, time (6 d of recording) was the repeated measures variable (to assess changes in behaviours over time), and the covariate was litter size. We used Fisher's HSD post hoc tests to identify specific differences in the main effects (treatment, time). We used an orthogonal polynomial decomposition for linear and quadratic components to assess whether any changes in behaviour over time were random (interaction treatment × time).

We used linear regressions to compare the parental care of mothers (Ph1) and sons (Ph2). Growth rate data did not meet the assumptions of normality, so the data were arcsine-transformed and first analysed using the variance components analysis. Breeding pair identity was a significant predictor of growth rates (p > 0.05). We then analysed male and female offspring growth rates in each phase using a GLM, with a repeated measures design (treatment = categorical predictor; male and female growth rates = repeated measures variable; litter size and sex ratio (proportion of male pups) = covariates).

Results

  1. Top of page
  2. Abstract
  3. Introduction
  4. Methods
  5. Results
  6. Discussion
  7. Acknowledgements
  8. Literature Cited

Maternal Care with Different Helpers (Phase 1)

Treatment, time (6 d of recording) and the interaction between treatment and time were all significant predictors of maternal care (Table 1). Post hoc tests revealed that mothers raising their young together with older daughters (M + OH) and fathers (M + F) spent more time near their pups and groomed pups for longer than mothers raising young with a young daughter (M + YH) (Fig. 1). In contrast, mothers spent more time huddling when they raised pups with a young helper (M + YH: mean ± SE = 3490.97 ± 211.83 s) than when raising pups with an older helper (M + OH: mean ± SE = 2456.40 ± 230.20 s) or with the father (M + F: mean ± SE = 1756.23 ± 100.17 s; Fig. 1). Time spent near pups was lower on days 1 to 7 and then peaked on days 9 and 11. Huddling was greatest shortly after birth (days 1 and 3) and lowest on days 9 and 11. Grooming was lower on days 1 and 11 and peaked on day 9 (Fig. 1, Table 1). For the treatment × time interaction, polynomial components were not significant for any linear components but were significant for all quadratic components for time spent near (linear: t = −094, p = 0.352; quadratic: t = 4.86, p < 0.001), huddling (linear: t = −0.49, p = 0.627; quadratic: t = 4.51, p < 0.001) and grooming (linear: t = 0.86, p = 0.394; quadratic: t = 7.06, p < 0.001) pups, indicating that the behaviours of mothers fluctuated during early and late post-partum for near and huddling and erratically for grooming and varied by treatment (Fig. 1).

Table 1. Predictors (Treatment, time, treatment × time, litter size) of parental care displayed by female (mothers) and male (sons) striped mice. Statistics = general linear model with a repeated measures design. Post hoc comparisons are provided for significant predictors (indicated in bold) for the main effects: homogeneous (non-significant) subsets are given in parentheses. Mothers raised young together with her mate (M + F), young daughter (M + YH) and older daughter (M + OH). D = day
PredictorsStatisticsPost hoc comparisons
Maternal care with different helpers (Phase 1)
TreatmentF6, 78 = 4.99, p < 0.001

Near: (M + F, M + OH) > (M + YH)

Huddling: M + YH > (M + F, M + OH)

Grooming: (M + F, M + OH) > (M + YH)

Time F 15, 27   =   87.18, p   <   0.001

Near: (D11, D9) > (D1, D3) > D5 >  D7

Huddling: (D3, D1, D5) > (D7, D9) > D11

Grooming: D9 > (D5, D3) > (D7, D11) > D1

Treatment × Time F 30, 54   =   3.02, p   <   0.001 See text
Litter sizeF3, 39 = 2.06, p = 0.121 
Helper and father alloparental care behaviour (Phase 1)
TreatmentF2, 56 = 17.83, p < 0.001Pup attendance: OH > M + F > YH
TimeF5, 280 = 3.37, p = 0.001Pup attendance: (D1, D3, D5, D 11) ≤ (D9, D7)
Treatment × TimeF10, 280 = 3.16, p < 0.001See text
Litter sizeF1 56 = 0.01, p = 0.996 
Paternal care behaviour (Phase 2)
TreatmentF3, 23 = 13.164, p < 0.001

Near: SM + YH = SM + OH

Huddling: SM + YH > SM + OH

Grooming: SM + YH = SM + OH

Time F 15, 11  = 6.26, p  =  0.002

Near: D11 > (D7, D3) > (D9, D1) > D5

Huddling: (D1, D3) > (D5, D7) > (D11, D9)

Grooming: D11 > (D1, D7) > (D3, D5, D9)

Treatment × Time F 15, 11  = 2.07, p  =  0.005 See text
Litter sizeF3, 23 = 1.50, p = 0.241 
image

Figure 1. Maternal care during Phase 1. Mean ± SE time (seconds) spent on three parental care behaviours by female striped mice for six taping days (days 1–11). Results of the statistical analyses are presented in Table 1. M + F = mothers and fathers raised young together, M + YH = mothers raised young with a young daughter, M + OH = mothers raised young with an older daughter.

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Helper and Father Alloparental Care Behaviour (Phase 1)

The data for maternal care behaviour showed that mothers modify the maternal investment according to the type of helper. Analyses of the time spent attending pups by helpers without the mother indicated that treatment, time and treatment × time were significant predictors of care provided. Subadult daughters provided the most care, followed by fathers and young helpers (Table 1; Fig. 2). When the mother was away from the nest, the care provided by older daughters accounted for 24% of the total parental care and fathers accounted for 22%, whereas young daughters provided just 6% of care. Helpers, regardless of treatment, provided the most care without the mother during mid to late post-natal development (Table 1). The linear polynomial component was significant (t = 2.80, p = 0.001) for the treatment × time interaction, showing that helpers increased care over time. The quadratic component was not significant (t = 1.72, p = 0.091).

image

Figure 2. Alloparental care provided by fathers (M + F), young helpers (M + YH) and older helpers (M + OH) in absence of the mothers. Mean ± SE time (seconds) spent on with pups for six taping days (days 1–11). Results of the statistical analyses are presented in Table 1.

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Paternal Care Behaviour (Phase 2)

Previously, we showed that changes in maternal investment influence the development and expression of paternal care behaviour in sons (Rymer & Pillay 2011). Because the data for maternal care behaviour in the present study showed that mothers modify the maternal investment according to the type of helper, we next investigated whether the change in maternal investment also influenced the development of paternal care behaviour in sons. For these analyses, we compared the time that adult sons provided paternal care to their own litters (i.e. Ph2 pairs).

Treatment, time and treatment x time were all significant predictors of paternal care displayed by sons (Table 1). Post hoc tests revealed that the SM + YH treatment huddled pups for longer than the SM + OH treatment, but there was no difference in the level of time spent near and grooming pups among the treatments (Fig. 3). A linear regression of parental care for all days combined revealed a significant and strongly positive relationship for the time spent huddling pups between the mothers (Ph1) and their sons (Ph2; R2 = 0.71; F1,28 = 67.28, p < 0.000), but there was no relationship for time spent near (R2 = 0.00; F1,28=0.05, p = 0.826) and grooming (R2 = 0.02; F1,28=0.52, p = 0.477) pups. Time spent near pups was lowest on day 5 and highest on day 11 with intermediate levels during the remaining time periods (Table 1). Huddling was greatest shortly after birth (days 1–5) and lowest on days 9 and 11 (Table 1). Grooming peaked on day 11 and was lowest during days 3, 5 and 9 (Fig. 3, Table 1). For the treatment × time interaction, polynomial components were significant for all linear and quadratic components for time spent near (linear: t = −5.78, p < 0.001; quadratic: t = −4.33, p < 0.001), huddling (linear: t = −6.85, p < 0.001; quadratic: t = −8.50, p < 0.001) and grooming (linear: t = −5.68, p < 0.001; quadratic: t = −758, p < 0.001) pups, indicating that the behaviours of fathers generally increased (near, groom) or decreased (huddling) linearly from early to late development but also fluctuated over time (Fig. 3).

image

Figure 3. Paternal care during Phase 2. Mean ± SE time (seconds) spent on three parental care behaviours by male (adult sons) striped mice for six taping days (days 1–11). Results for the statistical analyses are presented in Table 1. SM + YH = sons from M + YH treatment, SM + OH = sons from M + OH.

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Offspring Growth (Ph1 and Ph2)

In both phases, treatment was not a significant predictor of growth rate for either male or female offspring, indicating that the age and sex of an alloparent (helpers or fathers; Ph1) and the rearing conditions of sons (Ph2) did not influence the growth of offspring (Table 2). Males and females in a litter had similar growth rates, and litter size and sex ratio were not significant predictors of growth (Table 2).

Table 2. Mean (± SE) growth rates for male and female offspring during the first 21 days after birth for treatments in two phases. Statistics: GLM with a repeated measures design, indicate that none of the predictors were significant. For Phase 1, mothers raised pups with young helpers (M + YH), old helpers (M + OH) and fathers (M + F). In Phase 2, the adult sons of two treatments produced in Phase 1 raised pups with their mates SM + YH = sons from M + YH treatment, SM + OH = sons from M + OH
Phase/TreatmentMale growth rateFemale growth rateStatistics
Phase 1
M + YH0.077 (0.002)0.100 (0.011)Treatment: F2, 31 = 2.34, p = 0.113
M + OH0.085 (0.003)0.083 (0.003)Male vs. female: F1, 31 = 3.23, p = 0.082
M + F0.075 (0.008)0.080 (0.003)

Litter size: F1, 31 = 3.45, p = 0.073

Sex ratio: F1, 31 = 0.31, = 0.078

Phase 2
SM + YH0.082 (0.004)0.120 (0.053)Treatment: F1, 16 = 1.38, p = 0.257
SM + OH0.081 (0.002)0.079 (0.002)

Male vs. female: F1, 16 = 0.16, p = 0.692

Litter size: F1, 16 = 0.01, p = 0.896

Sex ratio: F1, 16 = 1.29, p = 0.725

Discussion

  1. Top of page
  2. Abstract
  3. Introduction
  4. Methods
  5. Results
  6. Discussion
  7. Acknowledgements
  8. Literature Cited

Philopatric striped mice, regardless of age, provide alloparental care behaviour in nature (Schradin & Pillay 2004; Schradin 2005; Scantlebury et al. 2006) and in captivity. Mothers, philopatric helpers and offspring all benefit from the provision of alloparental care. Like striped mouse fathers (Rymer & Pillay 2011), subadult helpers alleviate the maternal workload, providing high levels (24%) of care to their siblings when the mother is absent from the nest. Philopatric helpers themselves gain direct benefits from reduced energy expenditure for thermoregulation (huddling; Scantlebury et al. 2006), group defence of territory and resources (Schradin & Pillay 2004) and may have increased opportunities for developing parental care (learning-to-parent hypothesis; Lancaster 1971). Although we found no effects of alloparental care on offspring growth rate, possibly because laboratory conditions minimize the energetic demands associated with parental care (Brown 1993), huddling by both parents enhances offspring growth of semicaptive striped mice (Schradin & Pillay 2005). Therefore, provision of alloparental care by philopatric helpers could also contribute to improving offspring growth and survival under natural conditions. In addition, provision of alloparental care could also enable mothers to invest more time in themselves, through increased foraging (e.g. Mandarin voles Lasiopodomys mandarinus; Smorkatcheva & Smolnyakova 2004), and thereby enhancing maternal care, for example, improving milk production.

The levels of alloparental care provided by philopatric striped mice and concomitant alleviation of maternal care is age-dependent. Females that raised young with a juvenile daughter provided high levels of care, twice that of females that raised young with an older daughter. We showed in an earlier study that striped mice females compensate for the absence of their mate by increasing the level of maternal care (Rymer & Pillay 2011). It is apparent that mothers in the M + YH treatment also compensate for a lack of investment provided by these young helpers. In support, mothers in the M + YH treatment showed similar levels of huddling of their young over the 6 d of sampling (mean ± SE = 3490.97 ± 211.83 s, this study) to mothers raising their young alone (M–F: mean ± SE = 3759.87 ± 101.21 s, Rymer & Pillay 2011) compared with mothers in the M + OH and M + F treatments (this study).

The lower level of care of mothers raising young with subadult daughters indicates that older helpers alleviate maternal workload. The greater level of care shown by mothers raising young with a juvenile helper is contrary to recent reviews of cooperatively breeding mammals (e.g. Solomon & Hayes 2012) and birds (e.g. Hatchwell 1999). We are aware of only two studies, which showed that parents increase parental investment in the presence of helpers. Female meadow voles Microtus pennsylvanicus increased the level of care when raising young with juvenile philopatrics (Wang & Novak 1992) and azure-winged magpies Cyanopica cyanus increased care in the presence of helpers (Valencia et al. 2006). In both cases, females increased care because of other factors: increased maternal investment by female meadow voles was associated with increased maternal stress (Wang & Novak 1992) because females do not usually share a nest with males (Oliveras & Novak 1986), while chick starvation in azure-winged magpies is high, even in the presence of helpers, so any decrease in investment by parents will result in increased offspring mortality (Carranza et al. 2008).

The greater care provided by striped mouse mothers in the M + YH treatment cannot be explained by a stress response, as occurs in meadow voles, because striped mice regularly nest in social groups (Schradin & Pillay 2004) and are accustomed to receiving help from their sisters (Schubert et al. 2009), mates (Schradin & Pillay 2004; Rymer & Pillay 2011) and philopatric helpers (Schradin & Pillay 2004), and our findings show that older helpers do alleviate maternal workload. In addition, striped mouse females regularly nest alone, and pup survival is not compromised by starvation during this time (D. Hill, unpublished data). Instead, as female striped mice can assess whether their mates provide adequate paternal care and compensate by adjusting their own level of maternal care (Rymer & Pillay 2013), the increased time spent with pups by mothers in the M+YH treatment means that juvenile helpers do not provide adequate direct care to reduce the mother's time to engage in other activities, such as foraging and exploration.

Reduced maternal investment by mothers as a consequence of the help provided by subadult daughters correlated with a reduction in the level of paternal care provided by sons. Sons raised by mothers and subadult daughters (SM + OH) showed lower levels of care than sons raised by mothers alone M-F mothers with juvenile helpers (SM + YH). In a previous study, compensation of maternal care correlated positively with the development of paternal care, illustrating how the early rearing environments shapes paternal care behaviour in striped mice (Rymer & Pillay 2011). The generalizability of the help of fathers and subadult daughters to the maternal care–paternal development relationship also illustrates that the development and expression of paternal care behaviour are useful proxies of the help provided by alloparents.

Our study suggests that temporal changes in alloparental care provided by daughters are independent of their alloparental experience. Although helper age has frequently been confounded with experience (Gittleman 1985), some studies (e.g. cotton-top tamarins; Tardif et al.1992) have shown that age, in the absence of experience, influences how much care an alloparent will provide. Young striped mouse helpers do participate in care but at a low level (only 6%), suggesting that their contribution to alloparental care is marginal. They possibly do not provide a thermal advantage to their younger siblings because of a need to invest in their own growth. Therefore, mothers would need to invest more in huddling to meet the energetic demands of the growing young, as well as young philopatric helpers. In contrast, older philopatric helpers are not constrained in their thermoregulatory capacity (Couture 1980), and they could huddle pups independently of the mothers, which was four times more likely than young helpers.

We conclude that the differences in alloparental care provided by juvenile and subadult daughters reflect ontogenetic changes in their ability to provide care, possibly related to differential investment in their own growth and that of their younger siblings. The consequences of this change in helping affect maternal care and incidentally the development of paternal care behaviour of their younger brothers. In nature, several alloparents, including fathers, sisters and several offspring, provide help so that the effects we observed here may be ameliorated by the different roles of these alloparents. Juvenile daughters would provide indirect care mostly, such as nest building, and accrue benefits of group-living, such as huddling. Subadult helpers would also derive such benefits but they also provide direct alloparental care. The contribution of alloparental care by a daughter is cumulative over her lifetime, in which she improves both her inclusive fitness through caring for her siblings and acquiring skills for nurturing her own offspring later.

Acknowledgements

  1. Top of page
  2. Abstract
  3. Introduction
  4. Methods
  5. Results
  6. Discussion
  7. Acknowledgements
  8. Literature Cited

We are grateful to Megan Jones and Sneha Joshi who assisted with data collection. Funding was provided by the National Research Foundation (Grant Number: 2069110; DOL Scarce Skills scholarship) and the University of the Witwatersrand.

Literature Cited

  1. Top of page
  2. Abstract
  3. Introduction
  4. Methods
  5. Results
  6. Discussion
  7. Acknowledgements
  8. Literature Cited
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