Maternal lactational investment is higher for sons in chimpanzees. Iulia Bădescu, David P. Watts, M. Anne Katzenberg & Daniel W. Sellen. Behavioral Ecology and Sociobiology volume 76, Article number: 44 (2022). Mar 10 2022. https://link.springer.com/article/10.1007/s00265-022-03153-1
Abstract: Maternal lactational investment can affect female reproductive rates and offspring survival in mammals and can be biased towards infants of one sex. We compared estimates of lactation effort among mothers, assessed as their potential milk contribution to age-specific infant diets (mother-infant differences in fecal stable nitrogen isotopes, δ15N), to the timing of weaning (infant age at last nursing bout) and to maternal inter-birth interval lengths for male and female infant chimpanzees (Pan troglodytes) at Ngogo, Uganda. Infant males had greater proportions of milk in their age-specific diets, indicated by higher mother-infant differences in δ15N (Generalized Estimating Equation, GEE: p < 0.01). This may mean that mothers of sons showed greater lactation effort than mothers of daughters. Infant males stopped nursing at older ages than infant females (Kaplan–Meier product limit estimate, Breslow estimator: p < 0.05). Mothers of sons showed longer interbirth intervals than mothers of daughters (GEE: p < 0.01). All three measures indicated maternal lactational investment was higher for sons. Male infants may cost mothers more to ensure infant survival than female infants because males are more vulnerable and/or because maternal genetic returns on investment are greater for sons than daughters, as male philopatry means that chimpanzee mothers can have more influence on the reproductive success of sons. Chimpanzee females may trade off growth-related benefits of high lactational investment in male offspring against reduced reproductive rates.
Significance statement: Maternal investment via lactation affects the reproductive success of female mammals and their offspring and can be biased towards infants of one sex. We investigated lactational variation among wild chimpanzees in relation to infant sex using three proxies for maternal lactational investment: fecal stable nitrogen isotopes, a physiological biomarker that may provide an estimate of lactation effort; observations of nursing, which we used to establish weaning ages; and the lengths of intervals between births of surviving infants. Chimpanzee mothers biased lactational investment toward sons on all three indicators and showed reduced fecundity due to longer inter-birth intervals for mothers of sons than for mothers of daughters. These results would be expected if greater maternal investment toward sons leads to better condition and higher reproductive success for sons later in life, thus to greater inclusive fitness for mothers.
Our results collectively indicate that chimpanzee females invest more heavily via lactation in sons than in daughters, which supports the hypothesis. Physiological biomarker data revealed that sons had greater proportions of milk in their diets than daughters, which indicated that mothers could have made greater lactation effort for sons, and that sons were weaned at later ages than daughters. Variation in age at weaning had reproductive implications for adult females. Data on inter-birth intervals showed that mothers of sons experienced more delayed fecundity than mothers of daughters. That results of statistical analyses of demographic, behavioral, physiological data were in the same direction lends support to the argument that this is a true pattern. Our results are in line with previous studies that found evidence for higher maternal investment in sons for chimpanzees at Taï (Boesch 1997; Fahy et al. 2014) and Gombe (Lonsdorf et al. 2020); in other nonhuman primates (spider monkeys, A. paniscus: McFarland Symington 1987; mountain gorillas, G. beringei: Robbins et al. 2007; Eckardt et al. 2016; Robbins and Robbins 2021); and in other mammals (African elephants, L. africana: Lee and Moss 1986; seals, M. angustirostris: Reiter et al. 1978, Arctocephalus spp.: Trillmich 1986; Lunn and Arnould 1997; Iberian deer, C. e. hispanicus: Landete-Castillejos et al. 2005).
As assessed by isotopic data, the divergence in dependence on maternal milk between male and female infants was clearest early in infancy (≤ 1 year old, > 1.5 to 2 years old) and late in infancy (> 3.5 years old), when males continued relying on milk while many females were weaned (Figs. 1 and 3; when infants > 5 years old were removed from the analyses, results did not change: Supplementary Information). At some ages, however, infant females relied on milk more than males, and overlap between the mother-infant stable nitrogen isotope differences of male and female infants was considerable for all age categories. Thus, while analyses indicated that infant males relied on milk more than females overall, these results should be interpreted with caution as indications of potentially real effects that warrant further investigation to validate and replicate. Similarly, and consistent with an evolutionary conceptual framework in which infant sex is not expected to be the sole driver of maternal investment, the range of observed weaning ages and female interbirth intervals overlapped, which indicated that some sons were weaned earlier than most daughters and that some mothers of sons had shorter inter-birth intervals than most mothers of daughters. This suggests that other variables, including maternal, ecological, or social factors not measured here, also influenced developmental trajectories. For example, infant carrying is presumably the second most energetically expensive form of maternal investment in most primates (Altmann and Samuels 1992); we do not have data on age-independent variation in the time mothers carried infants, and thus cannot assess its possible contribution to variation in inter-birth intervals. Relatively long inter-birth intervals could result from poor maternal condition, as seems to be the case for olive baboons, Papio anubis (Patterson et al. 2021). However, no obvious reason exists why mothers with daughters would consistently be in poorer condition than mothers with sons. Also, Ngogo provides relatively favorable energetic conditions for chimpanzees, as indicated by data on feeding ecology (Potts et al. 2011; Watts et al. 2012a, b) and C-peptide data (Emery Thompson et al. 2009). Higher mortality of first-born than later-born infants at Ngogo (Wood et al. 2017) is likely to be an effect of maternal condition that results from trade-offs that primiparas face between investing in their own growth versus maternal investment, but we found no effect of parity on weaning ages.
Male infants might have relied more on milk than non-milk foods than same-aged females because they ingested less solid food. If so, this could explain the higher mother-infant δ15N differences for males, because even if absolute milk intake was similar between the sexes, milk would still have contributed a greater proportion of the male infant diet relative to non-milk food. Infant solid food intake data at Ngogo are needed to resolve this issue. At Gombe, there were no differences in the amount of time that male and female infant chimpanzees spent feeding on solid foods up to 5 years of age (Lonsdorf et al. 2014). It may thus be that the higher mother-infant δ15N differences we found for infant males at Ngogo were due to chimpanzee mothers of sons synthesizing more milk, on average, than mothers of daughters. Also, the δ15N differences we obtained probably did not occur because mothers and infants ate different solid foods. Dependent chimpanzee offspring usually foraged at the same time and on the same foods as their mothers, and mothers always shared foods that were difficult to access or extract (Badescu et al. 2017, 2020).
Stable nitrogen isotope ratios primarily reflect the protein component of milk. We therefore cannot exclude the possibility that total energetic lactational investment was similar for mothers of sons and daughters, but mothers of daughters made milk lower in protein and richer in fats and/or sugars compared to mothers of sons. Differences in maternal milk compositions for sons and daughters have been documented in some species (Landete-Castillejos et al. 2005; Hinde 2007, 2009). Nevertheless, our findings that infant males are weaned later than infant females and that mothers of sons have longer IBIs are strong indications of higher total lactational costs of raising males.
In comparing physiological and behavioral assessments of weaning for the four infants for whom we could determine weaning ages isotopically, we found that behavioral and physiological weaning ages matched exactly for one male, but the second was not observed nursing during the two months before he was physiologically weaned. This disparity could have occurred because he was only night-time nursing for the last few months before he stopped drinking milk. If so, he was the only infant in our dataset who exhibited night-time nutritive nursing despite being identified as behaviorally weaned. We could only assess whether physiological and behavioral weaning ages matched for one of two females. This infant nursed during the month that she was physiologically weaned, which indicated that she was comfort nursing without milk transfer, a pattern described among several of our study infants (Bădescu et al. 2017). Because the sample of infants for whom we could establish weaning ages isotopically was so small, we could not conclusively say whether males were physiologically weaned later than females. However, this seems to be a strong possibility given that physiological weaning occurred an average of 23.5 months later for the two males than the two females for whom we had firm data.
Mothers may be under direct selective pressures to invest more in sons because infant males require greater maternal investment to survive. Infant males could also be more demanding of maternal investment and may solicit greater lactation effort from their mothers than infant females. In some highly sexually dimorphic species, infant growth is faster in males than females, and males therefore require more lactation effort (e.g., mountain gorillas, G. beringei: Eckardt et al. 2016; western gorillas, G. gorilla: Meder 1990; Leigh and Shea 1996; California sea lion, Zalophus californianus: Oftedal et al. 1987; Galápagos sea lion, Zalophus wollebaeki: Piedrahita et al. 2014). However, chimpanzee body mass dimorphism is moderate, and while growth data are not available for wild chimpanzee infants younger than 3 years old, the absence of sex differences in body mass at age 3 at Kasekela (Pusey et al. 2005) and the similarity of male and female growth trajectories there and at Kanyawara (Emery Thompson et al. 2016) imply that no consistent sex difference in infant growth exists. Second, male offspring may be biologically less resilient and more sensitive and may therefore be less buffered in the face of hardship than female offspring (“fragile male hypothesis”: Clutton-Brock et al. 1985; Stinson 1985; Lindstrom 1999; Wells 2000; Battles 2016). Higher infant mortality rates for males than females have been demonstrated in several mammals including Galápagos sea lions, Z. wollebaeki (Kraus et al. 2013), red deer, Cervus elaphus (Clutton-Brock et al. 1985), and humans, Homo sapiens (Kraemer 2000), as expected under this hypothesis. Infant mortality at Ngogo is substantial and resembles that at other chimpanzee research sites, but whether a sex difference exists is unclear because mortality is highest for very young infants, for whom determining sex is difficult (Wood et al. 2017). At Gombe, immature male chimpanzees between 10 and 15 years of age (but not at younger ages) showed higher mortality than females after maternal loss (Stanton et al. 2020); this suggests that early life mortality in chimpanzees is higher for males. Male offspring could suffer injuries more often, given that (as in other nonhuman primates), they spend more time in social play and engage in rough and tumble play more than females (Owens 1975; Forster and Cords 2005; Lonsdorf et al. 2014). Chimpanzee mothers may therefore face selective pressure to provide high maternal investment in sons, via higher lactation effort and longer lactation length, to increase the probability that sons survive, especially during times of food scarcity or infectious disease epidemics (Clutton-Brock et al. 1985; Stinson 1985; Lindstrom 1999; Wells 2000; Battles 2016). However, food scarcity probably did not affect the differential maternal investment of infants in our study, as noted above. Also, none of our study infants suffered major injuries during data collection. A respiratory virus outbreak at Ngogo in 2016–2017 led to a spike in infant mortality (Negrey et al. 2019), but we cannot assess whether a sex bias in mortality occurred because some young infants died before observers had been able to ascertain their sex.
Female chimpanzees may stand to gain greater inclusive fitness by investing more in sons than in daughters. Female mammals generally produce a limited number of offspring in their lifetimes, whereas males can theoretically produce few or no offspring, or many, depending on their condition and access to fertile females (Trivers 1972). Especially when conditions are good, such as when food availability is high, maximum potential reproductive output is much higher for males than for females (Trivers and Willard 1973; Bercovitch 2002). Similarly, mothers in good condition are predicted to bias investment towards offspring of the sex that is most likely to benefit from the increased maternal contribution (Trivers and Willard 1973; Bercovitch 2002). In male philopatric species, sons are more likely to benefit from the added maternal investment under good conditions than are daughters. At Taï, females identified as high-ranking, who were presumably in better condition than lower-ranking females because of better access to high quality resources, had longer inter-birth intervals following births of sons than births of daughters. Boesch (1997) argued that this showed they invested more via lactation in sons. In contrast, low-ranking females, who were presumably in worse condition, had longer inter-birth intervals after producing daughters and apparently made more lactational investment in daughters than sons (Boesch 1997). Compared to other chimpanzee research sites, food abundance at Ngogo is high and feeding competition is low (Potts et al. 2009, 2011, 2020), and female energetic condition there is probably generally good (Potts et al. 2011; Potts 2013), which helps explain why females do not form dominance hierarchies there (Wakefield 2008). All mothers in this favorable ecological context could benefit from investing more heavily in sons because the potential for high reproductive success, and hence greater inclusive fitness for the mothers, is higher for males than for females (Trivers and Willard 1973; Bercovitch 2002). However, how well the Trivers and Willard (1973) hypothesis applies to chimpanzees is still unclear. Moreover, the relatively high gregariousness of Ngogo females and relatively low variation in fruit abundance there argue against competition effects on female fecundity like those proposed for Gombe (Pusey et al. 1997) and Kanyawara (Kahlenberg et al. 2008). As Riedel et al. (2011) argue, chimpanzee socioecological circumstances are not universally the same, and care should be taken before generalizing findings from any one community to the species level.
Compared to other long-term research sites, reproductive skew among males at Ngogo is low and mean male reproductive success is high (Langergraber et al. 2017). Prior to the permanent community fission, all Ngogo males gained long-term reproductive benefits from participating in cooperative territory defense (Langergraber et al. 2017). Thus, females at Ngogo, in favorable ecological circumstances that allow a large community with many males who can do well in intergroup competition, could benefit from investing more heavily in sons because success in intergroup competition increases mean male reproductive success (Potts et al. 2009, 2011, 2020; Langergraber et al. 2017).
In contrast, daughters might benefit from relatively early nutritional independence. This could facilitate social independence, which is important because most chimpanzee females must establish social relationships with strangers in their new communities. In ursine red howler monkeys (Alouatta arctoidea), females who emigrated from natal groups were weaned faster than those who stayed in their natal groups (Crockett and Rudran 1987), which suggests that early weaning provides benefits associated with dispersal. However, the benefits of faster development for female chimpanzees, if any, are unclear, especially because juvenile and young adolescent females at Gombe associated more closely, not less, with their mothers than males did (Pusey 1983, 1990). Thus, it seems unlikely that chimpanzee females acquire social competence faster than males.
Whether early maternal investment in sons influences the sons’ reproductive success in chimpanzees is unclear, partly because we do not have data on infant and juvenile growth. Bonobos (Pan paniscus) are also male philopatric, and female bonobos can influence the mating opportunities, rank, and reproductive success of their sons after weaning. Such influence seems mostly due to the effect of mother-adult son alliances on male-male competition (Surbeck et al. 2011, 2019). Female chimpanzees rarely intervene in contests between adult males and do not directly influence their adult sons’ dominance ranks (Surbeck et al. 2019). Whether early maternal investment influences adult male chimpanzee competitive ability is unknown. At Taï, the presence of mothers was positively associated with post-weaning growth, although this applied to both offspring sexes (Samuni et al. 2020). Likewise, association between mothers and sons before maturity, but after weaning, was positively associated with male reproductive success (Crockford et al. 2020), but causality, if any, was unclear. Any causal influence is likely to act via early growth and nutrition provided by maternal milk, as happens in bighorn sheep (Festa-Bianchet et al. 2000). Adult body size presumably influences male dominance ranks in chimpanzees, and male rank and reproductive success are positively correlated (Wroblewski et al. 2009; Langergraber et al. 2013). If adult body size is also positively associated with early growth and size at weaning, high lactational investment for male offspring could indeed bring fitness payoffs (Clutton-Brock et al. 1984; Clutton-Brock 1991; Lee et al. 1991). Differential maternal investment in sons by chimpanzee females in our study may translate into better condition for male offspring later in life, which could lead to higher male reproductive success and greater inclusive fitness for mothers. Cross-sectional data showing longer inter-birth intervals following births of sons than births of daughters imply that females trade off any growth-related benefits of high lactational investment in males against reduced reproductive rates, as Emery Thompson et al. (2016) argued for chimpanzees at Kanyawara. Continued documentation of within-female variation in inter-birth intervals as a function of offspring sex will help address this issue.
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