Maternal Investment Strategies Research Articles

Maternal risk-management elucidates the evolution of reproductive adaptations in sharks by means of natural selection

Maternal investment theory is the study of how breeding females allocate resources between offspring size and brood size to achieve reproductive success. In classical trade-off models, r/K-selection and bet-hedging selection, the primary predictors of maternal investments in offspring are population density and resource stability. In crowded, stable environments, K-selected females invest in large offspring at an equivalent cost in brood size. In uncrowded, unstable environments, r-selected females invest in large broods at an equivalent cost in offspring size. In unpredictable resource environments, bet-hedging females invest moderately in brood size and offspring size. The maternal risk-management model represents a profound departure from classical trade-off models. Maternal investments in offspring size, brood size, and brood number are shaped independently by autonomous risk factors: the duration of gaps in resources during seasonal cycles, rates of predation, and unpredictable catastrophic events. To date, no single model has risen to a position of preeminence. Here in sharks, we show that maternal investments within and across species do not agree with the predictions of trade-off models and instead agree with the predictions of the maternal risk-management model. Within and across shark species, offspring size and brood size were independent maternal investment strategies. The risk of starvation favored investments in larger offspring. The risk of predation favored investments in larger broods. If empirical studies continue to confirm its predictions, maternal-risk management may yet emerge as a unifying model of diverse reproductive adaptations by means of natural selection.

Forest harvest causes rapid changes of maternal investment strategies in ground beetles.

Species recovery following anthropogenic disturbances will depend on adaptations in survivorship and fecundity. Life-history theory predicts increased environmental stress will result in (1) shifts in resource allocation from fecundity to body growth/maintenance and (2) increased provisioning among offspring at the cost of reproductive output. For remnant populations that persist after forest harvesting, selection mediated through anthropogenic disturbances may affect resilience to additional stressors such as climate change. We tested how rapid changes in environmental conditions affected maternal investment strategies in two ground beetle species, Pterostichus pensylvanicus and Pterostichus coracinus, by comparing fecundity and survivorship in populations from recently clear-cut and uncut habitats. Using parents drawn from clear-cut or uncut stands, we reared progeny in both common garden and reciprocal transplant experiments. In P. pensylvanicus, we found that neither lineage nor rearing habitat affected the number of eggs laid per female or survivorship of offspring. However, eggs laid by females from clear-cuts were more likely to hatch and offspring reached maturity more quickly, suggesting increased provisioning per offspring. In P. coracinus, females from clear-cuts laid more eggs, and their eggs hatched more rapidly and had greater hatching success, suggesting increased investment in overall reproductive output and increased offspring provisioning. In the reciprocal transplant, we observed significant habitat by lineage interactions on survival in P. coracinus, with survivorship increasing when progeny were reared in novel habitats. In both species, increased maternal investment among offspring was not associated with a reduction in overall reproductive output, as anticipated. However, maternal investment among offspring declined with increasing female size, implying trade-offs between increased metabolic demand and fecundity. Taken together, our work suggests that females from more stressful, clear-cut habitats increased investment in fecundity, compared to females from uncut habitats, and may compensate for larval mortality. These changes were driven by smaller individuals, suggesting that increased environmental stress can influence the relationship between female size and maternal investment strategy. Additionally, reciprocal increases in offspring survivorship in habitats other than the parents suggest that adjacent areas between unharvested and clear-cut habitat may be useful in maintaining biodiversity under future climate stressors.

Life history and socioecology of infancy.

Evolution of human maternal investment strategies is hypothesized to be tied to biological constraints and environmental cues. It is likely, however, that the socioecological context in which mothers' decisions are made is equally important. Yet, a lack of studies examining maternal investment from a cross-cultural, holistic approach has hindered our ability to investigate the evolution of maternal investment strategies. Here, we take a systems-level approach to study how human life history characteristics, environments, and socioecology influence maternal investment in their children. We test how infant age and sex, maternal age, parity, and child loss, and the composition of a child's cooperative breeding network are associated with maternal investment across three small-scale (hunter-gatherer, horticultural, and agropastoral), sub-Saharan populations (N = 212). Naturalistic behavioral observations also enable us to illustrate the breadth and depth of the human cooperative breeding system. Results indicate that infant age, maternal age and parity, and an infant's cooperative childcare network are significantly associated with maternal investment, controlling for population. We also find that human allomaternal care is conducted by a range of caregivers, occupying different relational, sex, and age categories. Moreover, investment by allomothers is widely distributed. Our findings illustrate the social context in which children are reared in contemporary small-scale populations, and in which they were likely reared throughout our evolutionary history. The diversity of the caregiving network, coupled with life history characteristics, is predictive of maternal investment strategies, demonstrating the importance of cooperation in the evolution of human ontogeny.

Limits to sustained energy intake. XXX. Constraint or restraint? Manipulations of food supply show peak food intake in lactation is constrained.

Lactating mice increase food intake 4- to 5-fold, reaching an asymptote in late lactation. A key question is whether this asymptote reflects a physiological constraint, or a maternal investment strategy (a 'restraint'). We exposed lactating mice to periods of food restriction, hypothesizing that if the limit reflected restraint, they would compensate by breaching the asymptote when refeeding. In contrast, if it was a constraint, they would by definition be unable to increase their intake on refeeding days. Using isotope methods, we found that during food restriction, the females shut down milk production, impacting offspring growth. During refeeding, food intake and milk production rose again, but not significantly above unrestricted controls. These data provide strong evidence that asymptotic intake in lactation reflects a physiological/physical constraint, rather than restraint. Because hypothalamic neuropeptide Y (Npy) was upregulated under both states of restriction, this suggests the constraint is not imposed by limits in the capacity to upregulate hunger signalling (the saturated neural capacity hypothesis). Understanding the genetic basis of the constraint will be a key future goal and will provide us additional information on the nature of the constraining factors on reproductive output, and their potential links to life history strategies.

Age-Specific Reproductive Investment and Offspring Performance in an Orb-web Spider, Argiope radon

Temporal variation in reproductive investment, e.g. maternal egg provisioning, has a substantial effect on offspring fitness therefore has received great attention by evolutionary biologists. Maternal allocation into egg size and egg content directly influences performance of offspring in many taxa, but spiders have rarely been investigated in this regard. In this study, we investigate the temporal changes in maternal reproductive investment and offspring performance in an orb-web, Argiope radon. A group of male and female spiders were mated randomly in the laboratory. Female spiders were kept under standard condition until they laid egg sacs. For each egg sac, egg sac mass, egg size and egg protein content were measured across all egg sacs. Once the spiderlings emerged, emerging time and toleration to starvation of the spiderlings were recorded. Egg sacs laid early in life were heavier, have larger eggs and offspring emerge sooner than the egg sacs laid by the old females. The spiderlings from the early egg sacs were more likely to emerge, however, these offspring had less toleration to starvation than the egg sacs laid by old females. There was no significant correlation between egg size and egg protein content with offspring performance. The results showed how the female spiders strategically allocate resources to egg sacs and its consequences on the offspring emerging time and toleration to starvation. This study suggests an adaptive maternal reproductive investment strategy which allows the female spiders to gain maximum fitness in each reproductive bout.

Resource partitioning between two young-of-year cownose rays Rhinoptera bonasus and R. brasiliensis within a communal nursery inferred by trophic biomarkers.

Although interspecific trophic interactions plays a principal role within elasmobranch communal nurseries, little is known over variation in foraging strategies adopted by young-of-year of sympatric species. To test the hypothesis of dietary resource partitioning between batoids within a communal nursery, we investigated two cownose ray species, Rhinoptera bonasus and R. brasiliensis, which occur in heterospecific groups, a strategy predicted to increase survival and foraging success. Using two biochemical tracers, fatty acids (FA) and stable isotopes (δ15 N and δ13 C), the combined effects of maternal investment and the formation of heterospecific groups implying competition for, or partitioning of available food resources were investigated. Through univariate and multivariate analyses of biochemical tracers in several tissues (fin clip, muscle, liver, red blood cells; RBC) and plasma, our results revealed significant interspecific differences in tracers between the two species. Total FAs (∑saturated FA, ∑monounsaturated FA and ∑polyunsaturated FA) and trophic biomarkers (i.e., docosahexaenoic acid, arachidonic acid, oleic acid and δ15 N) were the principle tracers responsible for the differences detected. These data revealed that R. brasiliensis was less enriched in physiologically important essential FAs than R. bonasus. Our findings suggest that these congeneric species differ in maternal investment strategy and moderately partition food resources over relatively fine spatial scales within a single nursery habitat to limit competition. These results provide further knowledge on the foraging strategies adopted by batoids in communal nursery areas, information that is required for improving spatial conservation and management planning.

Different maternal investment strategies for male and female calves in a polygynous mammal.

Maternal effects occur when the phenotype of the mother influences that of the young to the detriment of her survival, growth or fitness. The investment of the mother can be affected by maternal body condition and/or experience. Trivers–Willard Hypothesis (TWH) and Local Resource Competition Hypothesis (LRCH) are the main hypotheses used to explain bias in birth sex-ratios in mammals, as well as for sex-biased maternal investment. Both hypotheses suggest that a different amount of investment must be expected according to the sex of the young. However, recent studies suggest that these differences are not in quantity but in the strategies: mechanisms and objectives may differ for each sex. We studied how maternal characteristics (age, body mass, body condition, and dominance status) influence relevant aspects of the birth and early growth of the calf (birth date, birth body mass, body mass at weaning, and body condition at weaning) separately for each sex; and how that investment is mediated by milk production and composition (lactose, fat, and protein). One hundred eighty-eight newborns from 75 captive red deer hinds aged from 2 to 19 years were analyzed. The main differential investment observed was related to birth date: when producing a female, hinds give birth earlier in the season only if they have a good body condition; however, when gestating a male it is the older hinds those which deliver earlier. Subsequently, milk production and composition are correlated with birth body mass in female calves, but to weaning body mass in males. Thus, only hind body mass affects the weaning body mass of female calves, compared with age and hind body mass in males. These results suggest that while TWH fits the maternal investment strategy found for male calves, it is LRCH which correlates with the maternal investment patterns observed for females.

The evolution of different maternal investment strategies in two closely related desert vertebrates.

We compared egg size phenotypes and tested several predictions from the optimal egg size (OES) and bet‐hedging theories in two North American desert‐dwelling sister tortoise taxa, Gopherus agassizii and G. morafkai, that inhabit different climate spaces: relatively unpredictable and more predictable climate spaces, respectively. Observed patterns in both species differed from the predictions of OES in several ways. Mean egg size increased with maternal body size in both species. Mean egg size was inversely related to clutch order in G. agassizii, a strategy more consistent with the within‐generation hypothesis arising out of bet‐hedging theory or a constraint in egg investment due to resource availability, and contrary to theories of density dependence, which posit that increasing hatchling competition from later season clutches should drive selection for larger eggs. We provide empirical evidence that one species, G. agassizii, employs a bet‐hedging strategy that is a combination of two different bet‐hedging hypotheses. Additionally, we found some evidence for G. morafkai employing a conservative bet‐hedging strategy. (e.g., lack of intra‐ and interclutch variation in egg size relative to body size). Our novel adaptive hypothesis suggests the possibility that natural selection favors smaller offspring in late‐season clutches because they experience a more benign environment or less energetically challenging environmental conditions (i.e., winter) than early clutch progeny, that emerge under harsher and more energetically challenging environmental conditions (i.e., summer). We also discuss alternative hypotheses of sexually antagonistic selection, which arise from the trade‐offs of son versus daughter production that might have different optima depending on clutch order and variation in temperature‐dependent sex determination (TSD) among clutches. Resolution of these hypotheses will require long‐term data on fitness of sons versus daughters as a function of incubation environment, data as yet unavailable for any species with TSD.

Understanding developmental plasticity as adaptation requires an inter-generational perspective.

In this issue of Evolution, Medicine and Public Health, Lea and colleagues argue that there are major advantages to bringing together biomedical and evolutionary perspectives on plasticity. To develop this approach, they propose two contrasting scenarios for ‘developmental plasticity as adaptation’: that it reflects adjustments to resolve the effects of early ‘constraints’, or that it adjusts phenotype to ecological cues in anticipation of similar conditions in adulthood. Yet neither scenario highlights the unique role of maternal phenotype, mediated by maternal investment strategy, in generating such constraints or cues. Developmental plasticity is greatest during the period when all ecological influences on the offspring are transduced by maternal phenotype. If the offspring adapts during this period, then the target of that adaptation is to maternal phenotype. Ignoring the inter-generational source of early constraints or cues prevents development of a comprehensive adaptive framework, because developmental plasticity is fundamentally relevant to the fitness of both offspring and parents.

Being a weakling and surviving: Keep the fittest siblings close-by when eating

Weaklings serve as a buffer, allowing an increase in the overall prospect of offspring survival. Whereas birds are able to directly determine which offspring to invest in via selective feeding, multiparous mammals have fewer methods of excluding weaklings from milk provision. In pigs the maternal investment strategy is based on the vigorousness of the progeny, whereby weaklings can suffer hunger due to an inability to sufficiently stimulate the mammary gland. However, the vigorous massage might stimulate higher milk production in the surrounding glands and it is possible that a weakling’s survivability is conditioned also by suckling at a position adjacent to heaviest littermate. Results of the present study have confirmed this prediction, showing that the surviving weaklings tended to have the heaviest littermates as nearest neighbours during suckling. It appears, therefore, that weaklings which establish a type of commensal, rather than competitive, relationship with strongest siblings might increase their survivability.

Maternal response to environmental unpredictability.

Mothers are expected to use environmental cues to modify maternal investment to optimize their fitness. However, when the environment varies unpredictably, cues may not be an accurate proxy of future conditions. Under such circumstances, selection favors a diversifying maternal investment strategy. While there is evidence that the environment is becoming more uncertain, the extent to which mothers are able to respond to this unpredictability is generally unknown. In this study, we test the hypothesis that Daphnia magna increase the variance in maternal investment in response to unpredictable variation in temperature consistent with global change predictions. We detected significant variability across temperature treatments in brood size, neonate size at birth, and time between broods. The estimated variability within-brood size was higher (albeit not statistically significant) in mothers reared in unpredictable temperature conditions. We also detected a cross-generational effect with the temperature history of mothers modulating the phenotypic response of F1's. Notably, our results diverged from the prediction that increased variability poses a greater risk to organisms than changes in mean temperature. Increased unpredictability in temperature had negligible effects on fitness-correlated traits. Mothers in the unpredictable treatment, survived as long, and produced as many F1's during lifetime as those produced in the most fecund treatment. Further, increased unpredictability in temperature did not affect the probability of survival of F1's. Collectively, we provide evidence that daphnia respond effectively to thermal unpredictability. But rather than increasing the variance in maternal investment, daphnia respond to uncertainty by being a jack of all temperatures, master of none. Importantly, our study highlights the essential need to examine changes in variances rather than merely on means, when investigating maternal responses.

COOPERATIVE BREEDING FAVORS MATERNAL INVESTMENT IN SIZE OVER NUMBER OF EGGS IN SPIDERS

The transition to cooperative breeding may alter maternal investment strategies depending on density of breeders, extent of reproductive skew, and allo-maternal care. Change in optimal investment from solitary to cooperative breeding can be investigated by comparing social species with nonsocial congeners. We tested two hypotheses in a mainly semelparous system: that social, cooperative breeders, compared to subsocial, solitarily breeding congeners, (1) lay fewer and larger eggs because larger offspring compete better for limited resources and become reproducers; (2) induce egg size variation within clutches as a bet-hedging strategy to ensure that some offspring become reproducers. Within two spider genera, Anelosimus and Stegodyphus, we compared species from similar habitats and augmented the results with a mini-meta-analysis of egg numbers depicted in phylogenies. We found that social species indeed laid fewer, larger eggs than subsocials, while egg size variation was low overall, giving no support for bet-hedging. We propose that the transition to cooperative breeding selects for producing few, large offspring because reproductive skew and high density of breeders and young create competition for resources and reproduction. Convergent evolution has shaped maternal strategies similarly in phylogenetically distant species and directed cooperatively breeding spiders to invest in quality rather than quantity of offspring.

Maternal investment during pregnancy in wild meerkats

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.

Encephalization, expensive tissues, and energetics: An examination of the relative costs of brain size in strepsirrhines

The evolution of encephalization requires that energetic challenges be met. Several hypotheses, such as the maternal energy and expensive tissue hypotheses, have been proposed to explain how some species are able to provide adequate energetic resources for large brains. The former incorporates maternal investment strategies, such as extended life history and elevated resting metabolic rate, which contribute to the growth of a large brain. The latter incorporates the reduction of gut size, which increases available energy for the maintenance of adult brain size. This study examines a sample of strepsirrhines, testing the hypothesis that encephalized species utilize some combination of the above-mentioned strategies. Infants and juveniles from three species at the Duke Lemur Center (DLC) were measured periodically to arrive at head and body growth trajectories. These data were used to determine the energetic tradeoff among the offspring. The examination of gestation length, weaning age, intestinal size and resting metabolic rate was used to assess adult brain maintenance and maternal energetic contribution. The results reveal that Daubentonia, the most encephalized and thus human-like of the lemurs, does not experience an energetic trade-off between brain and body during ontogeny, but does exhibit a trade-off between extensive brain growth and possibly reduced intestinal growth. Also, maternal energy is utilized. Encephalized lemurs, such as Daubentonia, have higher resting metabolic rate, while encephalized lorisiforms have a longer period of gestation. These results demonstrate that there are several strategies for meeting the energetic demands of encephalization, and they can be manifested differentially across taxa.

Offspring size and timing of hatching determine survival and reproductive output in a lizard

Selection on offspring size and timing of birth or hatching could have important consequences for maternal investment strategies. Here we show consistent viability selection on hatchling body length across 2 consecutive years in a lizard that lays several clutches per season. There was no effect of hatching date on survival to maturity. However, both early hatching and large hatchling size increased adult size, which has a positive effect on total reproductive output. Earlier hatching also led to an earlier onset of reproduction. Overall, increased survival probability for large hatchlings and a positive effect of clutch size on recruitment suggest consistent directional selection on both egg size and clutch size within and across years. Because offspring size and timing of hatching are strongly affected by environmental and maternal effects, there should be potential for strong transgenerational effects on reproductive output in this species. We briefly discuss the implications of these results for the evolutionary ecology of maternal investment and population fluctuations in short-lived lizards.

Maternal Effects Increase Within‐Family Variation in Offspring Survival

Maternal effects are environmental components of phenotypes that complicate relationships between natural selection and evolution because they often affect phenotypes and fitness simultaneously. We studied the effects of egg size variation on juvenile survival in a population of American coots (Fulica americana). We experimentally evaluated egg size variation at three levels: across the population, within natal nests, and within foster nests. Natal nests accounted for the most variation in population egg size. Within clutches, early-laid eggs were larger than later-laid eggs, with the exception of first-laid eggs, which were small. In the fostering experiment, posthatching survival was most strongly related to egg size relative to natal siblings and natal hatching order and less so to egg size within foster nests. These effects on survival were found even though young from natal nests were neither raised together nor raised by genetic parents. These results indicate that females allocate resources unequally among offspring such that offspring from larger, early-laid eggs have higher survival than offspring from smaller, later-laid eggs, regardless of their size relative to foster siblings or to mean population egg size. These results suggest that egg size variation can be maintained through selection on maternal investment strategies and not on egg size per se.

Open-cell parasitism shapes maternal investment patterns in the Red Mason bee Osmia rufa

Brood cell parasitism inflicts high fitness costs on solitary, nest-constructing bees. Many of these parasites enter open cells during its provisioning, when the mother bee is absent. Therefore, females can reduce the risk of open-cell parasitism by limiting the time they are away from the nest. However, provisioning efficiency (provisioning time per unit of progeny body mass) decreases due to aging. To limit the increasing risk of open-cell parasitism as the nesting season progresses, female bees could optimize their maternal investment strategy by shifting the sex ratio and the body size of offspring during the nesting season. This prediction was tested in the Red Mason bee Osmia rufa (O. bicornis), a stem- or hole-nesting, polylectic, univoltine megachilid bee. In O. rufa, the risk of open-cell parasitism was found to be correlated with cell provisioning time. Additionally, the provisioning efficiency of females declined during the nesting season to one-fourth of the initial value. However, cell-provisioning time did not increase correspondingly. Bees dealt with their decreasing provisioning efficiency by reducing the amount of stored larval food, leading to a reduction of offspring size and a seasonal shift toward males in the offspring sex ratio. The influence of provisioning efficiency and risk of open-cell parasitism on optimal offspring size was analyzed by means of a statistical model. The observed maternal investment pattern of Red Mason bees is an adaptive strategy to reduce open-cell parasitism.

Selection on social traits in greater spear-nosed bats, Phyllostomus hastatus

Many studies assume that selection molds social traits and have investigated the manner in which this occurs, yet very few studies have measured the strength of selection on social traits in natural populations. In this paper, I report results of phenotypic selection analyses on two social traits – the size of social groups and the frequency of group foraging – in Phyllostomus hastatus, the greater spear-nosed bat. I found significant positive directional selection on individual group foraging frequency, but no directional selection on individuals in different-sized social groups. These results have implications for the structure of social groups, cooperative behavior among group mates, and maternal investment strategies. I argue that combining studies of natural selection on wild populations with experiments to identify the agents and mechanisms of selection can do much to increase our understanding of social evolution.

Male song quality affects circulating but not yolk steroid concentrations in female canaries (Serinus canaria)

Male song complexity is a sexually selected trait found in many songbirds, including strains of the domestic canary. Studies on several species have shown that male song can affect the hormonal state of females and may also influence concentrations of maternal hormones in the yolk of their eggs. In this study, we show that the level of circulating androgens and oestrogens of female canaries, as measured in faeces, varies with the quality of male song to which they are exposed. The female-perceived quality of male canary song depends on the production of special 'sexy syllables' to which females respond with more sexual displays. Using playback of synthetic song we show that females hearing songs with sexy syllables have higher levels of faecal testosterone than control females hearing songs without them. However, unlike previous studies on the canary, we found no evidence that such females laid eggs with more testosterone (or other steroids) in their egg yolks. We discuss these results in relation to the evolution of male signalling and maternal investment strategies.

Common cuckoos (Cuculus canorus) lay eggs with larger yolk but not more testosterone than their great reed warbler (Acrocephalus arundinaceus) hosts

The relatively small common cuckoo Cuculus canorus hatchling evicts its host's propagules, then begs intensively to elicit sufficient parental care. The proximate mechanisms of these behaviours are still obscure. Recent intraspecific studies on avian broods revealed higher competitive ability of nestlings that hatched from eggs with a greater yolk testosterone level. Greater maternal investment in yolk steroids may provide an explanation for the vigour of parasitic chicks. Unexpectedly we found no evidence of higher yolk T concentration and absolute amount of T in cuckoo eggs compared to those of its host, the great reed warbler Acrocephalus arundinaceus. The yolk mass of cuckoo eggs, however, was significantly greater than that of the host, despite egg volumes being similar between these two species. Relatively larger yolks of cuckoo eggs indicates differential maternal investment strategies by parasites as more yolk may contain additional macronutrients to increase the vigour of parasitic young during the early days of its life and/or to enhance its begging display to elicit care from foster parents.