Reconciling nutritional geometry with classical dietary restriction: Effects of nutrient intake,not calories,on survival and reproduction

Dietary restriction (DR) is one of the main experimental paradigms to investigate the mechanisms that determine lifespan and aging. Yet, the exact nutritional parameters responsible for DR remain unclear. Recently, the advent of the geometric framework of nutrition (GF) has refocussed interest from calories to dietary macronutrients. However, GF experiments focus on invertebrates, with the importance of macronutrients in vertebrates still widely debated. This has led to the suggestion of a fundamental difference in the mode of action of DR between vertebrates and invertebrates, questioning the suggestion of an evolutionarily conserved mechanism. The use of dietary dilution rather than restriction in GF studies makes comparison with traditional DR studies difficult. Here, using a novel nonmodel vertebrate system (the stickleback fish, Gasterosteus aculeatus), we test the effect of macronutrient versus calorie intake on key fitness‐related traits, both using the GF and avoiding dietary dilution. We find that the intake of macronutrients rather than calories determines both mortality risk and reproduction. Male mortality risk was lowest on intermediate lipid intakes, and female risk was generally reduced by low protein intakes. The effect of macronutrient intake on reproduction was similar between the sexes, with high protein intakes maximizing reproduction. Our results provide, to our knowledge, the first evidence that macronutrient, not caloric, intake predicts changes in mortality and reproduction in the absence of dietary dilution. This supports the suggestion of evolutionary conservation in the effect of diet on lifespan, but via variation in macronutrient intake rather than calories.     

Effect of host availability on reproduction and survival of the parasitoid wasp Trichogramma minutum

Abstract.

• 1 We tested the hypothesis that females of the egg parasitoid, Trichogramma minutum Riley (Hymenoptera: Trichogrammatidae), could adjust their fecundity schedule according to host availability and that there was a negative correlation between reproduction and survival in these wasps.
• 2 Newly-emerged females were provided with an unlimited or limited number of hosts in the first trial and with either unlimited, limited or zero hosts in the second trial.
• 3 When hosts were unlimited, wasps had the highest rate of reproduction in the first day, which decreased dramatically thereafter. When hosts were limited, wasps from the two trials differed in their response. In Trial I, females with limited hosts had lower first-day fecundity than, and the same subsequent-day fecundity as, those with unlimited hosts. However, in Trial II, females with limited host had a lower first-day but a higher subsequent-day fecundity than those with unlimited hosts. This indicates variation in Trichogramma's ability to shift its fecundity schedule in response to host availability.
• 4 There was a positive (rather than a negative) correlation between reproduction and survival. Wasps that oviposited (in host-unlimited treatment) had greater longevity than those that could not (in host-unavailable treatment).
• 5 The sex ratio of the progeny produced by wasps in both host-unlimited and limited treatments shifted gradually from a female to a male bias as the wasps aged.
• 6 We consider the ability of parasitoids to adjust their fecundity schedule as an adaptation to changing host resources and discuss our findings with regard to theories of life history evolution.

     

限食及重喂食对雄性长爪沙鼠生理指标的影响

限食通常会显著影响鼠类的营养及内分泌等生理指标,但限食后重喂食其生理指标是否能得以恢复尚不
清楚。本文采取70% 的限食水平,研究了限食及重喂食对雄性长爪沙鼠生理指标的影响。将雄性长爪沙鼠分为
限食组、重喂食组和对照组。限食组先自由饮食4 周,后70% 限食4 周;重喂食组先70% 限食4 周,后恢复自
由饮食4 周。对照组自由饮食8 周。实验结束时,检测各组肥满度及血清白蛋白和总蛋白含量、血清甲状腺素
T3 和T4 水平、睾酮和皮质醇含量等各项生理指标的变化。研究结果表明,4 周限食显著降低了雄性长爪沙鼠的肥满度和血清甲状腺素T4 含量,显著升高了其血液皮质醇含量;限食后重喂食4 周后可使上述指标恢复或接近正常,但血清白蛋白含量比对照组低,其他指标与对照组无明显差异,长爪沙鼠的一些生理指标在限食重喂食
后能得以恢复,但其内分泌调节可能存在新的变化,值得进一步研究。     

Effects of food variability on growth and reproduction of Aedes aegypti

Despite a large body of knowledge about the evolution of life histories, we know little about how variable food availability during an individual's development affects its life history. We measured the effects of manipulating food levels during early and late larval development of the mosquito Aedes aegypti on its growth rate, life history and reproductive success. Switching from low to high food led to compensatory growth: individuals grew more rapidly during late larval development and emerged at a size close to that of mosquitoes consistently reared at high food. However, switching to high food had very little effect on longevity, and fecundity and reproductive success were considerably lower than in consistently well‐fed mosquitoes. Changing from high to low food led to adults with similar size as in consistently badly nourished mosquitoes, but even lower fecundity and reproductive success. A rapid response of growth to changing resources can thus have unexpected effects in later life and in lifetime reproductive success. More generally, our study emphasizes the importance of varying developmental conditions for the evolutionary pressures underlying life‐history evolution.     

Juvenile diet restriction and the aging and reproduction of adult Drosophila melanogaster

Mutations of the insulin signal pathway in Drosophila melanogaster produce long-lived adults with many correlated phenotypes. Homozygotes of insulin-like receptor ( InR ) and insulin-like receptor substrate ( chico ) delay time to eclosion, reduce body size, decrease reproduction and increase life span. Because these mutations are expressed through all life stages it is unclear when insulin signals must be reduced to increase life span. As a first analysis of this problem in D. melanogaster we have manipulated the larval diet to determine if changes in metabolic regulation at this stage are sufficient to slow aging. We controlled the dietary yeast fed to third instar larvae and studied the size, mortality, fecundity and hormones of the resulting adults, which were fed a normal, yeast-replete diet. Adults from yeast-deprived larvae phenocopied many traits of InR and chico mutants: small body size, delayed eclosion, reduced ovariole number and reduced age-specific fecundity. But unlike constitutive mutants of the insulin/IGF system, adults from yeast-deprived larvae had normal patterns of demographic senescence, and this was accompanied by normal insulin-like peptide and juvenile hormone syntheses. Surprisingly, the normal aging in these adults was also associated with greatly reduced fecundity. Although nutritional conditions of the larvae can affect the subsequent body size and fecundity of adults, these are not sufficient to slow aging.     

Dietary restriction in two rotifer species: the effect of the length of food deprivation on life span and reproduction

According to resource allocation theory, animals face a trade off between the allocation of resources into reproduction and into individual growth/maintenance. This trade off is reinforced when food conditions decline. It is well established in biological research that many animals increase their life span when food is in suboptimal supply for growth and/or reproduction. Such a situation of reduced food availability is called dietary restriction. An increase in life span under dietary restricted conditions is seen as a strategy to tolerate periods of food shortage so that the animals can start reproduction again when food is in greater supply. In this study, the effect of dietary restriction on life span and reproduction in two rotifer species, Cephalodella sp. and Elosa worallii, was investigated using life table experiments. The food concentration under dietary restricted conditions was below the threshold for population growth. It was (1) tested whether the rotifers start reproduction again after food replenishment, and (2) estimated whether the time scale of dietary restricted conditions is relevant for the persistence of a population in the field. Only E. worallii responded to dietary restriction with an increase in life span at the expense of reproduction. After replenishment of food, E. worallii started to reproduce again within 1 day. With an increase in the duration of dietary restricted conditions of up to 15 days, which is longer than the median life span of E. worallii under food saturation, the life span increased and the life time reproduction decreased. These results suggest that in a temporally (or spatially) variable environment, some rotifer populations can persist even during long periods of severe food deprivation.     

高温对二化螟实验种群生长、存活和繁殖的影响

以2 7℃和30℃恒温为对照,研究了平均温度在2 7～2 9.2℃内的5种变温条件下(每天2 0 h的适温2 7℃和12 :0 0～16 :0 0的高温处理,分别为日最高气温2 7℃、30℃、33℃、36℃、4 0℃)二化螟实验种群的发育历期、存活率和繁殖力的影响,组建了特定年龄生命表和繁殖力生命表。结果表明高温可导致二化螟种群的发育速率延缓、存活率和生殖力下降,主要表现在幼虫历期随日最高温度的升高而延长,36℃时延至12 d以上;在日最高气温高于33℃时,其存活率从2 7℃时的30 .3%降至36℃时的13.1%和4 0℃时的5 .5 % ,繁殖力也从30℃时每雌产卵量14 8.7粒减至36℃时的70 .5粒。因此,夏季异常高温可能是二化螟田间种群数量增长的一个重要抑制因子     

A general model for ontogenetic growth under food restriction

Food restriction (FR) retards animals' growth. Understanding the underlying mechanisms of this phenomenon is important to conceptual problems in life-history theory, as well as to applied problems in animal husbandry and biomedicine. Despite a considerable amount of empirical data published since the 1930s, there is no relevant general theoretical framework that predicts how animals vary their energy budgets and life-history traits under FR. In this paper, we develop such a general quantitative model based on fundamental principles of metabolic energy allocation during ontogeny. This model predicts growth curves under varying conditions of FR, such as the compensatory growth, different age at which FR begins, its degree and its duration. Our model gives a quantitative explanation for the counterintuitive phenomenon that under FR, lower body temperature and lower metabolism lead to faster growth and larger adult size. This model also predicts that the animals experiencing FR reach the same fraction of their adult mass at the same age as their ad libitum counterparts. All predictions are well supported by empirical data from mammals and birds of varying body size, under different conditions of FR.     

Two sexes respond equally to food restriction in a sexually dimorphic but not body mass dimorphic jumping spider

Natural selection favors animals that evolve developmental and behavioral responses that buffer the negative effects of food restrictions. These buffering responses vary both between species and within species. Many studies have shown sex‐specific responses to environmental changes, usually in species with sexual size dimorphism (SSD), less found in species with weak or no SSD, which suggests that sizes of different sexes are experiencing different selections. However, previous studies usually investigated development and behavior separately, and the balanced situation where males and females of sexually dimorphic species respond in the same way to food restriction remains little known. Here, we investigated this in Phintelloides versicolor (Salticidae) that presents sexual dimorphism in color and shape but weak SSD. We examined whether food restriction induced the same responses in males and females in development duration, adult body size and weight, daily time allocated to foraging, and hunting. We found food restriction induced similar responses in both sexes: both exhibited longer development duration, smaller adult body size and weight, higher probability of staying outside nests and noticing prey immediately, and higher hunting success. However, there were sexual differences regardless of food condition: females showed faster development, smaller adult body size, higher probability of staying outside of nests, and higher hunting success. These indicated the differential selection on male and female sizes of P. versicolor could be under a balanced situation, where males and females show equal developmental and behavioral plasticity to environmental constraints.     

Immunity and reproduction during colony foundation in the dampwood termite, Zootermopsis angusticollis

Abstract.  Termite primary reproductives may be exposed to pathogens when dispersing from their parental nest and establishing a new colony. Immunity and reproduction are investigated during colony foundation by implanting a nylon filament into the abdomen of mated and unmated female and male primary reproductives of the dampwood termite Zootermopsis angusticollis. Primary reproductives are paired in combinations of female/male, female/female and male/male and, using confocal microscopy, immune defence is assessed by measuring the degree of encapsulation of nylon implants during three periods of colony foundation: (I) shortly after pairing; (II) during copulation/oocyte maturation; and (III) during oviposition. There are differences in the encapsulation response of mated and unmated termites that are contingent on the period of colony foundation when termites are challenged. Mated females and males have significantly greater encapsulation responses than their unmated counterparts shortly after pairing, perhaps as a prophylactic measure against exposure to disease. The encapsulation response of mated and unmated males does not differ significantly during periods II and III. The onset of oviposition is significantly delayed in mated females that received implants during periods I and II. Mated females have a significantly reduced encapsulation response during the time of copulation and oocyte maturation, but not during oviposition. Overall, males have a significantly greater ability than females to encapsulate a nylon implant. The findings suggest that reproduction can reduce the immune response in female primary reproductives. The results are discussed in light of trade-offs between immunity and reproduction during the critical life-history phase of colony establishment in termites.     

Queen fecundity and reproductive skew in the termite Nasutitermes corniger

A major goal of studies on social animals is to understand variation in reproduction within and between groups. We used hierarchical regressions to analyze oviposition rates in the neotropical termite Nasutitermes corniger, a species with both monogynous and polygynous colonies. Queen fecundity was a non-linear, saturating function of queen weight. Greater queen weight was associated with larger nest size and with lower numbers of queens per nest, suggesting competition among queens for resources acquired by the colony. The collective egglaying rate of pairs of queens exceeded that of single queens, but further increases in queen number did not raise total fecundity. Skew in oviposition rates, as quantified by Morisita’s index I _δ, averaged 1.2, indicating inequalities in reproductive rates that are only moderately greater than expected for random apportionment. The leveling off of oviposition with increasing queen weight suggests that it is costly for individual females to produce eggs at high rates, which could favor tolerance of reproduction by other females, reducing reproductive skew. We hypothesize that the incentive to tolerate reproduction by other females is especially pronounced for heavier queens, because these queens are close to the limit of their own reproductive capacity. Consistent with this hypothesis, skew in oviposition rates was inversely related to the mean weight of queens within a nest. Received 8 March 2007; revised 17 September 2007; accepted 3 October 2007.     

When it is costly to have a caring mother: food limitation erases the benefits of parental care in earwigs

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.     

Age‐specific reproduction and disposable soma in an urban population of Common Blackbirds Turdus merula

The mechanism of senescence is an important subject of current research, but our knowledge of the factors influencing the rate of ageing in naturally occurring populations remains rudimentary. Evolutionary theories of senescence predict that investment in reproduction in early life should come at the cost of reduced somatic maintenance and thus result in earlier or more rapid senescence. We use data on the complete reproductive histories of 431 Common Blackbirds (222 males and 209 females) collected during a 19‐year study of the ecology of an urban population of this species to test the main hypotheses addressing the issue of senescence. On average, the birds in this population survived for 3.7 (± 1.9 sd) years. Reproductive success in females peaked at the age of 4, but in males remained stable until the 5th year of life. We observed declines in reproductive success, indicative of senescence, after the peak years in both sexes. The mechanism of age‐related changes in the reproduction of females confirms the individual improvement and selective disappearance hypotheses. In the case of males, the increase in reproductive performance comes as a consequence of the disappearance of poor reproducers. The parental investment associated with early life fecundity (the first two breeding seasons in males and females) impairs the breeding success of females later on. Contrary to expectations, there was no negative impact of high early life fecundity on either mortality or lifespan. Individuals of both sexes with a high early life fecundity had a higher lifetime reproductive success than those in which early life fecundity was low. Hence, the most profitable strategy is to maximize reproductive effort in the early stages of life. This yields the highest lifetime reproductive success, despite the increased impact of senescence, especially in females. These results are consistent with the disposable soma hypothesis.     

温度对取食玉米籽粒桃蛀螟生长发育、存活和生殖的影响

为了明确不同温度对取食玉米籽粒桃蛀螟生长发育、存活和生殖的影响,本研究依据年龄-龄期两性生命表理论计算了在21、24、27和30 ℃下取食玉米籽粒的桃蛀螟种群的生命表参数,并基于这些参数预测了未来80 d的种群动态。结果表明: 在21、24、27和30 ℃下桃蛀螟均能完成1个世代,随着温度升高,各阶段的发育历期缩短,且温度间差异显著。24 ℃下的平均单雌产卵量最高(116.7粒),成虫前期存活率最高(84.7%),雌虫占比最高(0.46),均显著高于其他温度。24、27、30 ℃下种群的内禀增长率分别为0.1059、0.1101、0.1045 d^-1,周限增长率分别为1.1117、1.1164、1.1102 d^-1,处理间差异不显著,但均显著高于21 ℃处理。21、24、27和30 ℃下的净增殖率(R₀)分别为17.3、53.7、36.9、19.8个后代个体,其中24 ℃时的R₀最高且显著高于其他温度处理。表明桃蛀螟种群在24～27 ℃下的存活率高、繁殖力大、雌性占比较高,是其生长发育、生存和繁殖的适合温度。     

Trade-off between age of first reproduction and survival in a female primate

Trade-offs are central to life-history theory but difficult to document. Patterns of phenotypic and genetic correlations in rhesus macaques, Macaca mulatta—a long-lived, slow-reproducing primate—are used to test for a trade-off between female age of first reproduction and adult survival. A strong positive genetic correlation indicates that female macaques suffer reduced adult survival when they mature relatively early and implies primate senescence can be explained, in part, by antagonistic pleiotropy. Contrasts with a similar human study implicate the extension of parental effects to later ages as a potential mechanism for circumventing female life-history trade-offs in human evolution.     

Desiccation of Panagrolaimus rigidus (Nematoda): survival,reproduction and the influence on the internal clock

Following the life-table experimental schedule, cohorts of aparthenogenetic strain of the free-living nematode Panagrolaimus rigidus were desiccated for six days at theages of4, 8, 12, and 19 d (age effect) and cohorts aged 8 d weredried for15, 20, 40, and 60 days (time effect) to determine theirability torecover and to reproduce.Nematode age had poor effect on recovery after 6 days ofdesiccation until the mean longevity of the nematode (19 daysinhydrated medium) is approached, while increasing times ofdesiccation (from 6 to 60 d) remarkably decreased capacity forrecovery (from 80 to 8%). Anhydrobiosis experienced atdifferentages or for different durations modified the timing of thenematodelife cycle events, but not the pattern of age-specificfecunditynor survival curves. The age-specific fecundity is largelyretainedfollowing anhydrobiosis, but when matched to that of thenematodeskept hydrated (controls), it declines for increasing durationsofdesiccation. Anhydrobiosis appears to cause a reset of theanimalsinternal clock, that is dependent on the duration ofdesiccation.     

Maternal survival costs in an asocial mammal

Maternal characteristics, social dynamics, and environmental factors can all influence reproduction and survival and shape trade‐offs that might arise between these components of fitness. Short‐lived mammals like the golden‐mantled ground squirrel (GMGS; Callospermophilus lateralis) tend to maximize effort toward current reproduction at the expense of survival but may be complicated by other aspects of the species’ life history and environment. Here, we use 25 years of data (1995–2020) collected from a population of GMGS at the Rocky Mountain Biological Research Laboratory in Gothic, Colorado, to test the effect of several maternal characteristics (e.g., age, experience, and timing of litter emergence), social context (e.g., litter sex ratio and kin density), and environmental context (e.g., date of bare ground and length of vegetative growing season) on survival of reproductive female GMGS using Cox proportional hazard models. Our results indicated that social dynamics (i.e., density) and environmental conditions (i.e., standardized first day of permanent snow cover and length of growing season) explained significant variation in annual maternal survival, while maternal characteristics did not. A higher density of related breeding females and the total number of females (both related and unrelated to the focal mother) were associated with an increase in the mortality hazard. A later standardized date of the first day of permanent snow cover and a shorter growing season both reduced the maternal mortality hazard. Together, our results suggest that factors extrinsic to the squirrels affect maternal survival and thus may also influence local population growth and dynamics in GMGS and other short‐lived, territorial mammal species.     

Twinning in humans: maternal heterogeneity in reproduction and survival

While humans usually give birth to singletons, dizygotic twinning occurs at low rates in all populations worldwide. We evaluate two hypotheses that have differing expectations about the effects of bearing twins on maternal lifetime reproduction and survival. The maternal depletion hypothesis argues that mothers of twins will suffer negative outcomes owing to the higher physiological costs associated with bearing multiples. Alternatively, twinning, while costly, may indicate mothers with a greater capacity to bear that cost. Drawing from the vast natural fertility data in the Utah Population Database, we compared the reproductive and survival events of 4603 mothers who bore twins and 54 183 who had not. These mothers were born between 1807 and 1899, lived at least to the age of 50 years and married once to men who were alive when their wives were 50. Results from proportional hazards and regression analyses are consistent with the second hypothesis. Mothers of twins exhibit lower postmenopausal mortality, shorter average inter-birth intervals, later ages at last birth and higher lifetime fertility than their singleton-only bearing counterparts. From the largest historical sample of twinning mothers yet published, we conclude that bearing twins is more likely for those with a robust phenotype and is a useful index of maternal heterogeneity.     

Fecundity and juvenile survival of shape Bembidion lampros and Tachyporus hypnorum

Fecundity and development from first instar larvae to adult beetles were studied for Bembidion lampros Herbst (Coleoptera; Carabidae) and Tachyporus hypnorum F. (Coleoptera; Staphylinidae). Both species reproduce in arable fields, where they are known to contribute to the natural control of cereal aphids. They are univoltine and have similar life cycles and development times. T. hypnorum females laid approximately 3 times more eggs than B. lampros females. Relative lifetime fecundity of B. lampros was very low with an average of 10 eggs per female. Based on the time where half of the populations had dispersed from the overwintering sites into an arable field B. lampros started egg-lay 100°D (°C>9) and T. hypnorum 200°D (°C>3) after dispersal. Mortality in the juvenile stages was found to be an important factor in the population dynamics of both B. lampros and T. hypnorum. The survival from first instar larvae to adults was on average 34% for B. lampros independent of soil type, 21% for T. hypnorum developed in sandy soil and 49% when developed in clayey soil under semi-field conditions. Enlargement of B. lampros and T. hypnorum populations to increase the natural control of aphids during their establishment in cereal fields may be possible if the conditions for juvenile development are improved.