Mounting an immune response requires a relatively substantial investment of energy and marked reductions in energy availability can suppress immune function and presumably increase disease susceptibility. We have previously demonstrated that a moderate reduction in energy stores via partial surgical lipectomy (LIPx) impairs humoural immunity of Siberian hamsters (Phodopus sungorus). Here we tested the hypothesis that LIPx-induced decreases in immunity are mediated by changes in the adipose tissue hormone leptin. Hamsters received bilateral surgical removal of inguinal white adipose tissue (IWATx) or sham surgeries (Sham). Half the animals in each group received osmotic minipumps containing murine leptin (0.5 μl h−1 for 10 days) whereas the remaining animals received minipumps containing vehicle alone; all animals were subsequently challenged with the novel antigen keyhole limpet haemocyanin (KLH). In general, serum leptin and anti-KLH antibodies were significantly correlated with one another with higher levels generally indicating enhanced immunity. In addition, IWATx hamsters had significantly lower serum anti-KLH IgG compared with sham animals. Exogenous leptin, however, attenuated LIPx-induced immune suppression but did not affect humoural immunity in sham animals. These results suggest that reductions in energy availability lead to impairments in humoural immunity and that leptin can serve as a neuroendocrine signal between body fat and immunity regulating humoural immune responses.
body fat; adipose tissue; seasonal; immune; energetics
Animals must balance investments in different physiological activities to allow them to maximize fitness in the environments they inhabit. These adjustments among reproduction, growth and survival are mandated because of the competing high costs of each process. Seasonally breeding rodents generally bias their investments towards reproduction when environmental conditions are benign, but shift these investments towards processes that promote survival, including immune activity, when environmental conditions deteriorate. Because survival probability of non-tropical small mammals is generally low in winter, under certain circumstances, these animals may not allocate resources to survival mechanisms in an effort to produce as many offspring as possible in the face of increased probability of death. Such ‘terminal investments’ have been described in passerines, but there are few examples of such phenomena in small mammals. Here, we show that male Siberian hamsters (Phodopus sungorus) challenged with lipopolysaccharide (a component of gram-negative bacteria that activates the immune system) induced a small, but significant, retardation of seasonal regression of the reproductive system relative to saline-injected hamsters. This delayed reproductive regression likely reflects a strategy to maintain reproductive function when survival prospects are compromised by infection.
photoperiodism; seasonality; Siberian hamsters; terminal investment; life history
Energy balance during lactation critically influences survival and growth of a mother’s offspring, and hence, her reproductive success. Most experiments have investigated the influence of a single factor (e.g., ambient temperature [Ta] or litter size) on the energetics of lactation. Here, we determined the impact of multiple interventions, including increased conductive heat loss consequent to dorsal fur removal, cold exposure (Ta of 5°C versus 23°C), and differential lactational load from litters of different sizes (2 or 4 pups), on maternal energy balance and offspring development of Siberian hamsters (Phodopus sungorus). Lower Ta, fur removal, and larger litters were associated with increased maternal food consumption. Females exposed to multiple challenges (e.g., both fur loss and lower Ta) ate substantially more food than those exposed to a single challenge, with no apparent ceiling to elevated food intake (increases up to 538%). Thus, energy intake of dams under these conditions does not appear to be limited by feeding behavior or the size of the digestive tract. Housing at 5°C attenuated pup weight gain and increased pup mortality to more than 5 times that of litters housed at 23°C. Increases in the dam’s conductive heat loss induced by fur removal did not affect pup weight gain or survival, suggesting that effects of low Ta on pup weight gain and survival reflect limitations in the pups’ ability to ingest or incorporate energy.
maternal care; thermoregulation; fur; food intake; Siberian hamster
Many animals experience marked seasonal fluctuations in environmental conditions. In response, animals display adaptive alterations in physiology and behaviour, including seasonal changes in immune function. During winter, animals must reallocate finite energy stores from relatively costly, less exigent systems (e.g. reproduction and immunity) to systems critical for immediate survival (e.g. thermoregulation). Seasonal changes in immunity are probably mediated by neuroendocrine factors signalling current energetic state. One potential hormonal candidate is insulin, a metabolic hormone released in response to elevated blood glucose levels. The aim of the present study was to explore the potential role of insulin in signalling energy status to the immune system in a seasonally breeding animal, the Siberian hamster (Phodopus sungorus). Specifically, exogenous insulin was administered to male hamsters housed in either long ‘summer-like’ or short ‘winter-like’ days. Animals were then challenged with an innocuous antigen and immune responses were measured. Insulin treatment significantly enhanced humoural immune responses in short, but not long days. In addition, insulin treatment increased food intake and decreased blood glucose levels across photoperiodic treatments. Collectively, these data support the hypothesis that insulin acts as an endocrine signal integrating seasonal energetic changes and immune responses in seasonally breeding rodents.
immunity; energy balance; insulin; antibody response
Leptin regulates energy homeostasis and reproductive, neuroendocrine, immune, and metabolic functions. In this review, we describe the role of leptin in human physiology and review evidence from recent “proof of concept” clinical trials using recombinant human leptin in subjects with congenital leptin deficiency, hypoleptinemia associated with energy-deficient states, and hyperleptinemia associated with garden-variety obesity. Since most obese individuals are largely leptin-tolerant or -resistant, therapeutic uses of leptin are currently limited to patients with complete or partial leptin deficiency, including hypothalamic amenorrhea and lipoatrophy. Leptin administration in these energy-deficient states may help restore associated neuroendocrine, metabolic, and immune function and bone metabolism. Leptin treatment is currently available for individuals with congenital leptin deficiency and congenital lipoatrophy. The long-term efficacy and safety of leptin treatment in hypothalamic amenorrhea and acquired lipoatrophy are currently under investigation. Whether combination therapy with leptin and potential leptin sensitizers will prove effective in the treatment of garden-variety obesity and whether leptin may have a role in weight loss maintenance is being greatly anticipated.
leptin; leptin deficiency; obesity; leptin resistance; energy homeostasis; insulin resistance; adipokines; amenorrhea; lipoatrophy
The production of offspring typically requires investment of resources derived from both the environment and maternal somatic reserves. As such, the availability of either of these types of resources has the potential to limit the degree to which resources are allocated to reproduction. Theory and empirical studies have argued that mothers modify reproductive performance relative to exogenous resource availability and maternal condition by adjusting size, number or sex of offspring produced. These relationships have classically been defined relative to availability of energy sources; however, in vertebrates, calcium also plays a critical role in offspring production, as a considerable amount of calcium is required to support the development of offspring skeleton(s). We tested whether the availability of calcium influences reproductive output by providing female white-footed mice with a low-calcium or standard diet from reproductive maturity to senescence. We then compared maternal skeletal condition and reproductive output, based on offspring mass, offspring number and litter sex ratio, between dietary treatments. Mothers on the low-calcium diet exhibited diminished skeletal condition at senescence and produced smaller and strongly female-biased litters. We show that skeletal condition and calcium intake can influence sex ratio and reproductive output following general theoretical models of resource partitioning during reproduction.
The well studied trade-off between offspring size and offspring number assumes that offspring fitness increases with increasing per-offspring investment. Where mothers differ genetically or exhibit plastic variation in reproductive effort, there can be variation in per capita investment in offspring, and via this trade-off, variation in fecundity. Variation in per capita investment will affect juvenile performance directly—a classical maternal effect—while variation in fecundity will also affect offspring performance by altering the offsprings' competitive environment. The importance of this trade-off, while a focus of evolutionary research, is not often considered in discussions about population dynamics. Here, we use a factorial experiment to determine what proportion of variation in offspring performance can be ascribed to maternal effects and what proportion to the competitive environment linked to the size–number trade-off. Our results suggest that classical maternal effects are significant, but that in our system, the competitive environment, which is linked to maternal environments by fecundity, can be a far more substantial influence.
Sancasania berlesei; maternal effects; size–number trade-off; delayed life history effect
Traditionally, research on life-history traits has viewed the link between clutch size and offspring size as a straightforward linear trade-off; the product of these two components is taken as a measure of maternal reproductive output. Investing more per egg results in fewer but larger eggs and, hence, offspring. This simple size–number trade-off has proved attractive to modellers, but our experimental studies on keelback snakes (Tropidonophis mairii, Colubridae) reveal a more complex relationship between clutch size and offspring size. At constant water availability, the amount of water taken up by a snake egg depends upon the number of adjacent eggs. In turn, water uptake affects hatchling size, and therefore an increase in clutch size directly increases offspring size (and thus fitness under field conditions). This allometric advantage may influence the evolution of reproductive traits such as growth versus reproductive effort, optimal age at female maturation, the body-reserve threshold required to initiate reproduction and nest-site selection (e.g. communal oviposition). The published literature suggests that similar kinds of complex effects of clutch size on offspring viability are widespread in both vertebrates and invertebrates. Our results also challenge conventional experimental methodologies such as split-clutch designs for laboratory incubation studies: by separating an egg from its siblings, we may directly affect offspring size and thus viability.
incubation dynamics; maternal investment; propagule size; size–number trade-off
Offspring provisioning is commonly referenced as the most important influence on men's and women's foraging decisions. However, the provisioning of other adults may be equally important in determining gender differences in resource choice, particularly when the goals of provisioning offspring versus others cannot be met with the acquisition of the same resources. Here, we examine how resources vary in their expected daily energetic returns and in the variance or risk around those returns. We predict that when available resources impose no trade-off between risk and energy, the targets of men's and women's foraging will converge on high-energy, low-risk resources that allow for the simultaneous provisioning of offspring and others. However, when minimizing risk and maximizing energy trade-off with one another, we expect men's foraging to focus on provisioning others through the unreliable acquisition of large harvests, while women focus on reliably acquiring smaller harvests to feed offspring. We test these predictions with foraging data from three populations (Aché, Martu and Meriam). The results uphold the predictions, suggesting that men's and women's foraging interests converge when high-energy resources can be reliably acquired, but diverge when higher-energy resources are associated with higher levels of risk. Social factors, particularly the availability of alloparental support, may also play a major role.
gender division of labour; central place provisioning; risk; variance; human behavioural ecology; hunter–gatherers
Offspring of long-lived species should face costs of parental trade-offs that vary with overall energetic demands encountered by parents during breeding. If sex differences exist in how parents make the trade-off, sex-specific differences may exist in the contribution of each parent to those costs. Adaptations of offspring facing such costs are not well understood, but the hormone corticosterone probably plays a role. We manipulated breeding effort in Cory's shearwaters (Calonectris diomedea) to increase costs to offspring and used an integrated measure of corticosterone from chick feathers to investigate how experimental variation in parental investment influences offspring physiology. Average foraging trip duration and foraging efficiency (FE) of breeding pairs were not related to chick corticosterone, but sex biases in FE were. Adult male investment was more strongly related to chick corticosterone than was female investment. Importantly, we show for the first time suppression of adrenocortical activity in nestling Procellariiform seabirds, and explain how our results indicate an adaptive mechanism invoked by chicks facing increased costs of parental trade-offs.
Cory's shearwater; feather corticosterone; life history; parental investment; stress physiology; trade-offs
Organisms face trade-offs regarding their life-history strategies, such as decisions of single or multiple broods within a year. In passerines displaying facultative multiple breeding, the probability of laying a second clutch is influenced by several life-history factors. However, information about the mechanistic background of these trade-offs is largely lacking. Leptin is a protein hormone produced by white fat cells, and acts as a signal between peripheral energy depots and the central nervous system. In addition, leptin affects cells at all levels of the reproductive axis and plays a critical role in regulating the allocation of metabolic energy to reproduction. As such, it is possible that leptin levels influence the decision of whether or not to invest time and energy into a second clutch. Accordingly, we expect a treatment with exogenous leptin to result in an increased number of second broods.
At a later stage during the first brood, female great tits were treated either with long-term leptin-filled cholesterol pellets (the experimental birds) or with pellets containing only cholesterol (the control birds). We found that leptin-treated females were significantly more likely to have a second brood and that the earlier females were more likely to lay a second clutch than the late females.
As both timing of first brood and treatment with leptin were important in the decision of having multiple broods, the trade-offs involved in the breeding strategy most likely depend on multiple factors. Presumably leptin has evolved as a signal of energy supply status to regulate the release of reproductive hormones so that reproduction is coordinated with periods of sufficient nutrients. This study investigated the role of leptin as a mediator between energy resources and reproductive output, providing a fundamentally new insight into how trade-offs work on a functional basis.
As egg production and offspring care are costly, females should invest resources adaptively into their eggs to optimize current offspring quality and their own lifetime reproductive success. Parasite infections can influence maternal investment decisions due to their multiple negative physiological effects. The act of preening – applying oils with anti-microbial properties to feathers – is thought to be a means by which birds combat pathogens and parasites, but little is known of how preening during the reproductive period (and its expected disease-protecting effects) influences maternal investment decisions at the level of the egg.
Here, we experimentally prevented female mallards (Anas platyrhynchos) from accessing their preen gland during breeding and monitored female immunoresponsiveness (e.g., plasma lysozyme concentration) as well as some egg traits linked to offspring quality (e.g., egg mass, yolk carotenoid content, and albumen lysozyme levels). Females with no access to their preen gland showed an increase in plasma lysozyme level compared to control, normally preening females. In addition, preen-gland-restricted females laid significantly lighter eggs and deposited higher carotenoid concentrations in the yolk compared to control females. Albumen lysozyme activity did not differ significantly between eggs laid by females with or without preen gland access.
Our results establish a new link between an important avian self-maintenance behaviour and aspects of maternal health and reproduction. We suggest that higher yolk carotenoid levels in eggs laid by preen-gland-restricted females may serve to boost health of offspring that would hatch in a comparatively microbe-rich environment.
Mounting an immune response requires substantial energy, and it is well known that marked reductions in energy availability (e.g. starvation) can suppress immune function, thus increasing disease susceptibility and compromising survival. We tested the hypothesis that moderate reductions in energy availability impair humoral immunity. Specifically, we examined the effects of partial lipectomy (LIPx) on humoral immunity in two seasonally breeding rodent species, prairie voles (Microtus ochrogaster) and Siberian hamsters (Phodopus sungorus). Animals received bilateral surgical removal of epididymal white adipose tissue (EWATx), inguinal white adipose tissue (IWATx) or sham surgeries and were injected with the antigen keyhole limpet haemocyanin (KLH) either four or 12 weeks after surgery. In prairie voles, serum anti-KLH immunoglobulin G (IgG) did not differ significantly at four weeks. At 12 weeks, serum IgG was significantly reduced in IWATx, but not EWATx animals, compared with sham-operated animals. In Siberian hamsters, both IWATx and EWATx animals reduced serum IgG at four weeks. At 12 weeks, EWATx hamsters displayed a significant compensatory increase in IWAT pad mass compared with sham-operated hamsters, and serum IgG no longer differed from sham-operated animals. There was no significant increase in EWAT in IWATx hamsters compared with sham animals and IgG remained significantly reduced in IWATx hamsters. These results suggest that reductions in energy availability can impair humoral immunity.
Hypothalamic systems which regulate appetite may be permanently modified during early development. We have previously reported hyperphagia and increased adiposity in the adult offspring of rodents fed an obesogenic diet prior to and throughout pregnancy and lactation. We now report that offspring of obese (OffOb) rats display an amplified and prolonged neonatal leptin surge, which is accompanied by elevated leptin mRNA expression in their abdominal white adipose tissue. At postnatal Day 30, before the onset of hyperphagia in these animals, serum leptin is normal, but leptin-induced appetite suppression and phosphorylation of STAT3 in the arcuate nucleus (ARC) are attenuated; the level of AgRP-immunoreactivity in the hypothalamic paraventricular nucleus (PVH), which derives from neurones in the ARC and is developmentally dependent on leptin, is also diminished. We hypothesise that prolonged release of abnormally high levels of leptin by neonatal OffOb rats leads to leptin resistance and permanently affects hypothalamic functions involving the ARC and PVH. Such effects may underlie the developmental programming of hyperphagia and obesity in these rats.
The energetic resources in an organism’s environment are essential for executing a wide range of life history functions, including immunity and reproduction. Most energetic budgets, however, are limited, which can lead to trade-offs among competing functions. Increasing reproductive effort tends to decrease immunity in many cases; and increasing total energy via supplemental feedings can eliminate this effect. Testosterone (T), an important regulator of reproduction, and food availability are thus both potential factors regulating life-history processes, yet they are often tested in isolation of each other. In this study, we considered the effect of both food availability and elevated T on immune function and reproductive behavior in sagebrush lizards, Sceloporus graciosus, to assess how T and energy availability affect these trade-offs. We experimentally manipulated diet (via supplemental feedings) and T (via dermal patches) in males from a natural population. We determined innate immune response by calculating the bacterial killing capability of collected plasma exposed to E. coli ex vivo. We measured reproductive behavior by counting the number of courtship displays produced in a 20-min sampling period. We observed an interactive effect of food availability and T-patch on immune function, with food supplementation increasing immunity in T-patch lizards. Additionally, T increased courtship displays in control food lizards. Lizards with supplemental food had higher circulating T than controls. Collectively, this study shows that the energetic state of the animal plays a critical role in modulating the interactions among T, behavior and immunity in sagebrush lizards and likely other species.
Context-dependent; Energy allocation; Innate immunity; Life history; Resources; Sceloporus; Trade-offs
Life-history theory assumes that animal life histories are a consequence of trade-offs between current activities and future reproductive performance or survival, because resource supply is limited. Empirical evidence for such trade-offs in the wild are common, yet investigations of the underlying mechanisms are rare. Life-history trade-offs may have both physiological and ecological mediated costs. One hypothesized physiological mechanism is that elevated energy metabolism may increase reactive oxygen species production, leading to somatic damage and thus compromising future survival. We investigated the impact of experimentally elevated energy expenditure on oxidative damage, protection and lifespan in short-tailed field voles (Microtus agrestis) maintained in captivity to remove any confounding ecological factor effects. Energy expenditure was elevated via lifelong cold exposure (7±2°C), relative to siblings in the warm (22±2°C). No treatment effect on cumulative mortality risk was observed, with negligible effects on oxidative stress and antioxidant protection. These data suggest that in captive animals physiologically mediated costs on life history do not result from increased energy expenditure and consequent elevations in oxidative stress and reduced survival.
lifespan; metabolic rate; oxidative stress; cold exposure; life-history trade-offs; antioxidant
Hosts may defend themselves against parasitism through a wide variety of defence mechanisms, but due to finite resources, investment in one defence mechanism may trade-off with investment in another mechanism. We studied resistance strategies against the parasitoid wasp Leptopilina boulardi in two Drosophila species. We found that D. melanogaster had significantly lower physiological resistance against L. boulardi than D. simulans, and hypothesized that D. melanogaster might instead invest more heavily in other forms of defence, such as behavioural defence. We found that when given a choice between clean oviposition sites and sites infested with wasps, both D. melanogaster and D. simulans detected and avoided infested sites, which presumably limits later exposure of their offspring to infection. Unlike D. simulans, however, D. melanogaster laid significantly fewer eggs than controls in the forced presence of wasps. Our findings suggest that D. melanogaster relies more heavily on behavioural avoidance as defence against wasp parasitism than D. simulans, and that this may compensate for a lack of physiological defence.
physiological and behavioural defences; Drosophila; parasitoid wasps; resistance; avoidance
A poor prenatal environment brings about perturbations in leptin surge and hypothalamic circuitry that program impaired ability to regulate energy homeostasis in adulthood. Here, using a rat model of moderate maternal caloric restriction during gestation, we aimed to investigate whether leptin supplementation with physiological doses throughout lactation is able to ameliorate the adverse developmental malprogramming effects exerted in offspring hypothalamus structure and function. Three groups of male and female rats were studied: the offspring of ad libitum fed dams (controls), the offspring of 20% calorie restricted dams during the first part of pregnancy (CR), and CR rats supplemented with physiological doses of leptin throughout lactation (CR-Leptin). Animals were sacrificed on postnatal day 25. Morphometric and immunohistochemical studies on arcuate (ARC) and paraventicular (PVN) nucleus were performed and hypothalamic expression levels of selected genes were determined. In CR males, leptin treatment restored, at least in part, the number of immunoreactive neuropeptide Y (NPY+) cells in ARC, the total number of cells in PVN, hypothalamic NPY, cocaine- and amphetamine-regulated transcript (CART) and suppressor of cytokine signalling-3 (SOCS-3) mRNA levels, and plasma leptin levels, which were decreased in CR animals. CR-Leptin males showed higher hypothalamic long-form leptin receptor (ObRb) mRNA levels, compared to control and CR animals. In CR females, leptin treatment reverted the increased number of cells in ARC and cell density in ARC and PVN, and reduced hypothalamic SOCS-3 mRNA expression to levels similar to controls. Leptin treatment also reverted the increased relative area of NPY+ fibers in the PVN occurring in CR animals. In conclusion, leptin supplementation throughout lactation is able to revert, at least partly, most of the developmental effects on hypothalamic structure and function caused by moderate maternal caloric restriction during gestation, and hence making this metabolic malprogramming reversible to some extent.
Immune function is a vital physiological process that is often suppressed during times of resource scarcity due to investments in other physiological systems. While energy is the typical currency that has been examined in such trade-offs, limitations of other resources may similarly lead to trade-offs that affect immune function. Specifically, water is a critical resource with profound implications for organismal ecology, yet its availability can fluctuate at local, regional, and even global levels. Despite this, the effect of osmotic state on immune function has received little attention.
Using agglutination and lysis assays as measures of an organism’s plasma concentration of natural antibodies and capacity for foreign cell destruction, respectively, we tested the independent effects of osmotic state, digestive state, and energy balance on innate immune function in free-ranging and laboratory populations of the Gila monster, Heloderma suspectum. This desert-dwelling lizard experiences dehydration and energy resource fluctuations on a seasonal basis. Dehydration was expected to decrease innate immune function, yet we found that dehydration increased lysis and agglutination abilities in both lab and field studies, a relationship that was not simply an effect of an increased concentration of immune molecules. Laboratory-based differences in digestive state were not associated with lysis or agglutination metrics, although in our field population, a loss of fat stores was correlated with an increase in lysis.
Depending on the life history of an organism, osmotic state may have a greater influence on immune function than energy availability. Thus, consideration of osmotic state as a factor influencing immune function will likely improve our understanding of ecoimmunology and the disease dynamics of a wide range of species.
Dehydration; Digestion; Energy balance; Hemagglutination; Hemolysis; Osmolality; Water
Seasonal variation in behavior and physiology, including changes in immune function, are common. This variability is elicited by changes in photoperiod and often covaries with fluctuations in both energy reserves and reproductive state. It is unclear, however, whether changes in either variable alone drive seasonal changes in immunity. We investigated the relative contributions of reproduction and energy balance to changes in immune function. To accomplish this, we uncoupled seasonal changes in reproduction from those related to energy balance via daily injections of N-methyl-D-Aspartate (NMDA) in Siberian hamsters (Phodopus sungorus). NMDA is a glutamatergic agonist that blocks short-day induced gonadal regression while leaving short-day declines in body mass unaffected. In Experiment 1, we examined the effect of differing doses of NMDA on testosterone production as a proxy for NMDA effects on reproduction; a dose-dependent rise in testosterone was observed. In Experiment 2, animals were maintained on long or short days and received daily injections of NMDA. After eight weeks all animals underwent a humoral immune challenge. Short-day animals receiving daily injections of NMDA maintained long-day-like gonads, however contrary to our predictions, no trade-off between reproduction or energy balance and immune function was observed. Unexpectedly, NMDA treatment increased immunoglobulin levels in all groups, suggesting NMDA may provide an immunomodulatory signal, presumably through actions on peripheral glutamate receptors. These results support a previous finding that NMDA blocks reproductive regression. In addition, these findings demonstrate a general immunoenhancing effect of NMDA that appears independent of changes in reproductive or energetic state of the animal.
Evolutionary explanations for life history diversity are based on the idea of costs of reproduction, particularly on the concept of a trade-off between age-specific reproduction and parental survival, and between expenditure on current and future offspring. Such trade-offs are often difficult to detect in population studies of wild mammals. Terminal investment theory predicts that reproductive effort by older parents should increase, because individual offspring become more valuable to parents as the conflict between current versus potential future offspring declines with age. In order to demonstrate this phenomenon in females, there must be an increase in maternal expenditure on offspring with age, imposing a fitness cost on the mother. Clear evidence of both the expenditure and fitness cost components has rarely been found. In this study, we quantify costs of reproduction throughout the lifespan of female antechinuses. Antechinuses are nocturnal, insectivorous, forest-dwelling small (20–40 g) marsupials, which nest in tree hollows. They have a single synchronized mating season of around three weeks, which occurs on predictable dates each year in a population. Females produce only one litter per year. Unlike almost all other mammals, all males, and in the smaller species, most females are semelparous. We show that increased allocation to current reproduction reduces maternal survival, and that offspring growth and survival in the first breeding season is traded-off with performance of the second litter in iteroparous females. In iteroparous females, increased allocation to second litters is associated with severe weight loss in late lactation and post-lactation death of mothers, but increased offspring growth in late lactation and survival to weaning. These findings are consistent with terminal investment. Iteroparity did not increase lifetime reproductive success, indicating that terminal investment in the first breeding season at the expense of maternal survival (i.e. semelparity) is likely to be advantageous for females.
The aggregation of parents with offspring is generally associated with different forms of care that improve offspring survival at potential costs to parents. Under poor environments, the limited amount of resources available can increase the level of competition among family members and consequently lead to adaptive changes in parental investment. However, it remains unclear as to what extent such changes modify offspring fitness, particularly when offspring can survive without parents such as in the European earwig, Forficula auricularia. Here, we show that under food restriction, earwig maternal presence decreased offspring survival until adulthood by 43 per cent. This effect was independent of sibling competition and was expressed after separation from the female, indicating lasting detrimental effects. The reduced benefits of maternal presence on offspring survival were not associated with higher investment in future reproduction, suggesting a condition-dependent effect of food restriction on mothers and local mother–offspring competition for food. Overall, these findings demonstrate for the first time a long-term negative effect of maternal presence on offspring survival in a species with maternal care, and highlight the importance of food availability in the early evolution of family life.
family life; conflicts; food restriction
We investigated the effects of population fluctuation on the offspring’s sex allocation by a weakly polygynous mouse, Apodemus argenteus, for 3 years. In acorn-poor seasons, heavier mothers invested more in sons, and lighter mothers invested more in daughters. In acorn-rich seasons, heavier mothers invested more in daughters, and lighter mothers invested more in sons. Maternal body condition and litter size affected the sex allocation. Furthermore, there was a maternal investment trade-off between a son’s birth mass and the number of daughters. Based upon the effect of population fluctuation on the lifetime reproductive success of each sex, we proposed the new “safe bet hypothesis”. This hypothesis predicts that frequent and unpredictable change in female distribution, which is often caused by abrupt fall in food condition, favors female-biased maternal investment to offspring by polygynous mammals and is applicable to many small mammals inhabiting in unstable environments.
Apodemus argenteus; Trivers and Willard’s hypothesis; Sex allocation; Maternal investment trade-off; Safe bet hypothesis
Life-history theory posits a fundamental trade-off between number and size of offspring that structures the variability in parental investment across and within species. We investigate this ‘quantity–quality’ trade-off across primates and present evidence that a similar trade-off is also found across natural-fertility human societies. Restating the classic Smith–Fretwell model in terms of allometric scaling of resource supply and offspring investment predicts an inverse scaling relation between birth rate and offspring size and a −¼ power scaling between birth rate and body size. We show that these theoretically predicted relationships, in particular the inverse scaling between number and size of offspring, tend to hold across increasingly finer scales of analyses (i.e. from mammals to primates to apes to humans). The advantage of this approach is that the quantity–quality trade-off in humans is placed into a general framework of parental investment that follows directly from first principles of energetic allocation.
quantity–quality trade-off; Smith–Fretwell model; number and size of offspring; natural-fertility human societies; primate life histories; quarter-power scaling
The reproductive costs associated with the upregulation of immunity have been well-documented and constitute a fundamental trade-off between reproduction and self-maintenance. However, recent experimental work suggests that parents may increase their reproductive effort following immunostimulation as a form of terminal parental investment as prospects for future reproduction decline. We tested the trade-off and terminal investment hypotheses in a wild population of house wrens (Troglodytes aedon) by challenging the immune system of breeding females with lipopolysaccharide, a potent but non-lethal antigen. Immunized females showed no evidence of reproductive costs; instead, they produced offspring of higher phenotypic quality, but in a sex-specific manner. Relative to control offspring, sons of immunized females had increased body mass and their sisters exhibited higher cutaneous immune responsiveness to phytohaemagglutinin injection, constituting an adaptive strategy of sex-biased allocation by immune-challenged females to enhance the reproductive value of their offspring. Thus, our results are consistent with the terminal investment hypothesis, and suggest that maternal immunization can induce pronounced transgenerational effects on offspring phenotypes.
immune challenge; life-history trade-off; maternal effect; sex allocation; terminal investment