Many lifetime growth trajectories for a single mammal

Despite their importance in shaping life history tactics and population dynamics, individual growth trajectories have only been rarely explored in the wild because their analysis requires multiple measurements of individuals throughout their lifetime and some knowledge of age, a key timer of body growth. The availability of long‐term longitudinal studies of two wild boar populations subjected to contrasting environments (rich vs. poor) provided an opportunity to analyze individual growth trajectories. We quantified wild boar growth trajectories at both the population and the individual levels using standard growth models (i.e., Gompertz, logistic, and monomolecular models) that encompass the expected range of growth shapes in determinate growers. Wild boar is a rather altricial species, with a polygynous mating system and is strongly sexually dimorphic in size. According to current theories of life history evolution, we thus expect wild boar to display a sex‐specific Gompertz type growth trajectory and lower sexual size dimorphism in the poorer environment. While wild boar displayed the expected Gompertz type trajectory in the rich site at the population level, we found some evidence for potential differences in growth shapes between populations and individuals. Asymptotic body mass, growth rate and timing of maximum growth rate differed as well, which indicates a high flexibility of growth in wild boar. We also found a cohort effect on asymptotic body mass, which suggests that environmental conditions early in life shape body mass at adulthood in this species. Our findings demonstrate that body growth trajectories in wild boar are highly diverse in relation to differences of environmental context, sex and year of birth. Whether the intermediate ranking of wild boar along the precocial–altricial continuum of development at birth may explain the ability of this species to exhibit this high diversity of growth patterns remains to be investigated.     

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.     

Male immigration triggers increased growth in subordinate female meerkats

There is increasing evidence that some vertebrates can adjust their growth rate in relation to changes in the social context that affect their probability of breeding. Here, we show that, in meerkats (Suricata suricatta), which are singular cooperative breeders, subordinate females increase in body mass after their father is replaced as the dominant male in their natal group by an immigrant male, giving them regular access to an unfamiliar and unrelated mating partner, while their brothers showed no similar increase nor did subordinate females living in other stable groups (where male immigration did not occur did) in this time period. Moreover, subordinate females showed a greater increase in growth rate when their father was succeeded by an unfamiliar immigrant male than when he was replaced by a familiar male who was already resident. These results suggest that female meerkats can adjust their rate of growth to changes in the kinship composition of their groups that provide them with increased access to unrelated breeding partners, which may occur in other mammals as well when breeding opportunities change.     

Effects of Increased Flight on the Energetics and Life History of the Butterfly Speyeria mormonia

Movement uses resources that may otherwise be allocated to somatic maintenance or reproduction. How does increased energy expenditure affect resource allocation? Using the butterfly Speyeria mormonia, we tested whether experimentally increased flight affects fecundity, lifespan or flight capacity. We measured body mass (storage), resting metabolic rate and lifespan (repair and maintenance), flight metabolic rate (flight capacity), egg number and composition (reproduction), and food intake across the adult lifespan. The flight treatment did not affect body mass or lifespan. Food intake increased sufficiently to offset the increased energy expenditure. Total egg number did not change, but flown females had higher early-life fecundity and higher egg dry mass than control females. Egg dry mass decreased with age in both treatments. Egg protein, triglyceride or glycogen content did not change with flight or age, but some components tracked egg dry mass. Flight elevated resting metabolic rate, indicating increased maintenance costs. Flight metabolism decreased with age, with a steeper slope for flown females. This may reflect accelerated metabolic senescence from detrimental effects of flight. These effects of a drawdown of nutrients via flight contrast with studies restricting adult nutrient input. There, fecundity was reduced, but flight capacity and lifespan were unchanged. The current study showed that when food resources were abundant, wing-monomorphic butterflies living in a continuous meadow landscape resisted flight-induced stress, exhibiting no evidence of a flight-fecundity or flight-longevity trade-off. Instead, flight changed the dynamics of energy use and reproduction as butterflies adopted a faster lifestyle in early life. High investment in early reproduction may have positive fitness effects in the wild, as long as food is available. Our results help to predict the effect of stressful conditions on the life history of insects living in a changing world.     

Persistence of Alarm-Call Behaviour in the Absence of Predators: A Comparison Between Wild and Captive-Born Meerkats (Suricata Suricatta)

Performing correct anti‐predator behaviour is crucial for prey to survive. But, are such abilities lost in species or populations living in predator‐free environments? How individuals respond to the loss of predators has been shown to depend on factors such as the degree to which anti‐predator behaviour relies on experience, the type of cues evoking the behaviour, the cost of expressing the behaviour and the number of generations under which relaxed selection has taken place. Here we investigated whether captive‐born populations of meerkats (Suricata suricatta) used the same repertoire of alarm calls previously documented in wild populations and whether captive animals, as wild ones, could recognize potential predators through olfactory cues. We found that all alarm calls that have been documented in the wild also occurred in captivity and were given in broadly similar contexts. Furthermore, without prior experience of odours from predators, captive meerkats seemed to distinguish between faeces of potential predators (carnivores) and non‐predators (herbivores). Despite slight structural differences, the alarm calls given in response to the faeces largely resembled those recorded in similar contexts in the wild. These results from captive populations suggest that direct, physical interaction with predators is not necessary for meerkats to perform correct anti‐predator behaviour in terms of alarm‐call usage and olfactory predator recognition. Such behaviour may have been retained in captivity because relatively little experience seems necessary for correct performance in the wild and/or because of the recency of relaxed selection on these populations.     

Who infects whom? Social networks and tuberculosis transmission in wild meerkats

Transmission of infectious diseases is strongly influenced by who contacts whom. Despite the global distribution of tuberculosis (TB) in free-living wild mammal populations, little is known of the mechanisms of social transmission of Mycobacterium bovis between individuals. Here, I use a network approach to examine for correlations between five distinct types of intra- and intergroup social interaction and changes in TB status of 110 wild meerkats (Suricata suricatta) in five social groups over two years. Contrary to predictions, the most socially interactive animals were not at highest risk of acquiring infection, indicating that in addition to contact frequency, the type and direction of interactions must be considered when quantifying disease risk. Within social groups, meerkats that groomed others most were more likely to become infected than individuals who received high levels of grooming. Conversely, receiving, but not initiating, aggression was associated with M. bovis infection. Incidence of intergroup roving by male meerkats was correlated with the rovers themselves subsequently testing TB-positive, suggesting a possible route for transmission of infection between social groups. Exposure time was less important than these social interactions in influencing TB risk. This study represents a novel application of social network analysis using empirical data to elucidate the role of specific interactions in the transmission of an infectious disease in a free-living wild animal population.     

Plasma proteomic profiles of bovine growth hormone transgenic mice as they age

Attenuation of the growth hormone (GH)/insulin-like growth factor-1 (IGF-1) axis results in extended lifespan in many organisms including mice. Conversely, GH transgenic mice have excess GH action and die prematurely. We have studied bovine (b) GH transgenic mice (n = 9) and their wild type (WT) littermates (n = 8) longitudinally and have determined several age-related changes. Compared to WT mice, bGH mice lost fat mass, became hypoglycemic and had lower insulin levels at older ages despite being hyperinsulinemic when young. To examine plasma protein differences in bGH mice relative to controls, samples at 2, 4, 8, 12 and 16 months of age were analyzed by two-dimensional gel electrophoresis followed by identification using mass spectrometry. We found several differences in plasma proteins of bGH mice compared to controls, including increased apolipoprotein E (five isoforms), haptoglobin (four isoforms) and mannose-binding protein-C (one out of three isoforms), and decreased transthyretin (six isoforms). In addition, clusterin (two out of six isoforms) and haptoglobin (four isoforms) were up-regulated in bGH mice as a function of age. Finally, alpha-2 macroglobulin (seven isoforms) was altered in an isoform-specific manner with two isoforms increased and two decreased in bGH mouse plasma compared to controls. In conclusion, identification of these proteins suggests that bGH mice exhibit an increased inflammatory state with an adverse lipid profile, possibly contributing to their diminished life expectancy. Also, these newly discovered plasma proteins may be indicative or ‘biomarkers’ of a shortened lifespan.     

Early‐life telomere length predicts lifespan and lifetime reproductive success in a wild bird

Poor conditions during early development can initiate trade‐offs that favour current survival at the expense of somatic maintenance and subsequently, future reproduction. However, the mechanisms that link early and late life‐history are largely unknown. Recently it has been suggested that telomeres, the nucleoprotein structures at the terminal end of chromosomes, could link early‐life conditions to lifespan and fitness. In wild purple‐crowned fairy‐wrens, we combined measurements of nestling telomere length (TL) with detailed life‐history data to investigate whether early‐life TL predicts fitness prospects. Our study differs from previous studies in the completeness of our fitness estimates in a highly philopatric population. The association between TL and survival was age‐dependent with early‐life TL having a positive effect on lifespan only among individuals that survived their first year. Early‐life TL was not associated with the probability or age of gaining a breeding position. Interestingly, early‐life TL was positively related to breeding duration, contribution to population growth and lifetime reproductive success because of their association with lifespan. Thus, early‐life TL, which reflects growth, accumulated early‐life stress and inherited TL, predicted fitness in birds that reached adulthood but not noticeably among fledglings. These findings suggest that a lack of investment in somatic maintenance during development particularly affects late life performance. This study demonstrates that factors in early‐life are related to fitness prospects through lifespan, and suggests that the study of telomeres may provide insight into the underlying physiological mechanisms linking early‐ and late‐life performance and trade‐offs across a lifetime.     

Reproductive and post‐reproductive life history of wild‐caught Drosophila melanogaster under laboratory conditions

The life history of the fruit fly (Drosophila melanogaster) is well understood, but fitness components are rarely measured by following single individuals over their lifetime, thereby limiting insights into lifetime reproductive success, reproductive senescence and post‐reproductive lifespan. Moreover, most studies have examined long‐established laboratory strains rather than freshly caught individuals and may thus be confounded by adaptation to laboratory culture, inbreeding or mutation accumulation. Here, we have followed the life histories of individual females from three recently caught, non‐laboratory‐adapted wild populations of D. melanogaster. Populations varied in a number of life‐history traits, including ovariole number, fecundity, hatchability and lifespan. To describe individual patterns of age‐specific fecundity, we developed a new model that allowed us to distinguish four phases during a female's life: a phase of reproductive maturation, followed by a period of linear and then exponential decline in fecundity and, finally, a post‐ovipository period. Individual females exhibited clear‐cut fecundity peaks, which contrasts with previous analyses, and post‐peak levels of fecundity declined independently of how long females lived. Notably, females had a pronounced post‐reproductive lifespan, which on average made up 40% of total lifespan. Post‐reproductive lifespan did not differ among populations and was not correlated with reproductive fitness components, supporting the hypothesis that this period is a highly variable, random ‘add‐on’ at the end of reproductive life rather than a correlate of selection on reproductive fitness. Most life‐history traits were positively correlated, a pattern that might be due to genotype by environment interactions when wild flies are brought into a novel laboratory environment but that is unlikely explained by inbreeding or positive mutational covariance caused by mutation accumulation.     

A meta‐analysis of latitudinal variations in life‐history traits of roach,Rutilus rutilus,over its geographical range: linear or non‐linear relationships?

1. We collated information from the literature on life history traits of the roach (a generalist freshwater fish), and analysed variation in absolute fecundity, von Bertalanffy parameters, and reproductive lifespan in relation to latitude, using both linear and non-linear regression models. We hypothesized that because most life history traits are dependent on growth rate, and growth rate is non-linearly related with temperature, it was likely that when analysed over the whole distribution range of roach, variation in key life history traits would show non-linear patterns with latitude.
2. As fecundity depends strongly on length, and the length structure of females varied among populations, latitudinal patterns in fecundity were examined based on residuals from the length–fecundity relationship. The reproductive lifespan of roach was estimated as the difference between age at maturity and maximum age of females in each population.
3. The three life history traits of roach analysed all varied among populations and were non-linearly related to latitude. Only the relationship between reproductive lifespan and latitude was a better fit to a linear that to a quadratic model, although Loess smoothing curves revealed that this relationship was actually closer to biphasic than linear in form. A latitude of 50°N formed a break point in all three life history traits.
4. The negative relationships we have described between (i) fecundity and reproductive lifespan and (ii) fecundity and egg mass suggest that lower fecundity is compensated for by longer lifespan, while lower fecundity is compensated for by an increased egg mass, when analysed independently of location.     

Cooperative personalities and social niche specialization in female meerkats

The social niche specialization hypothesis predicts that group‐living animals should specialize in particular social roles to avoid social conflict, resulting in alternative life‐history strategies for different roles. Social niche specialization, coupled with role‐specific life‐history trade‐offs, should thus generate between‐individual differences in behaviour that persist through time, or distinct personalities, as individuals specialize in particular nonoverlapping social roles. We tested for support for the social niche specialization hypothesis in cooperative personality traits in wild female meerkats (Suricata suricatta) that compete for access to dominant social roles. As cooperation is costly and dominance is acquired by heavier females, we predicted that females that ultimately acquired dominant roles would show noncooperative personality types early in life and before and after role acquisition. Although we found large individual differences in repeatable cooperative behaviours, there was no indication that individuals that ultimately acquired dominance differed from unsuccessful individuals in their cooperative behaviour. Early‐life behaviour did not predict social role acquisition later in life, nor was cooperative behaviour before and after role acquisition correlated in the same individuals. We suggest that female meerkats do not show social niche specialization resulting in cooperative personalities, but that they exhibit an adaptive response in personality at role acquisition.     

The predation cost of being a male: implications for sex-specific rates of ageing

Evolutionary theory predicts that the rate of extrinsic (i.e. age- and condition-independent) mortality should affect important life history traits such as the rate of ageing and maximum lifespan. Sex-specific differences in mortality rates due to predation may therefore result in the evolution of important differences in life history traits between males and females. However, quantifying the role of predators as a factor of extrinsic mortality is notoriously difficult in natural populations. We took advantage of the unusual prey caching behaviour of the barn owl Tyto alba and the tawny owl Strix aluco to estimate the sex ratio of their five most common preys. For all prey species, there was a significant bias in the sex ratio of remains found in nests of both these owls. A survey of literature revealed that sex-biased predation is a common phenomenon. These results demonstrate that predation, a chief source of extrinsic mortality, was strongly sex-biased. This may select for alternate life history strategies between males and females, and account for a male life span being frequently lower than female lifespan in many animal species.     

Mediation of vertebrate life histories via insulin‐like growth factor‐1

Life‐history traits describe parameters associated with growth, size, survival, and reproduction. Life‐history variation is a hallmark of biological diversity, yet researchers commonly observe that one of the major axes of life‐history variation after controlling for body size involves trade‐offs among growth, reproduction, and longevity. This persistent pattern of covariation among these specific traits has engendered a search for shared mechanisms that could constrain or facilitate production of variation in life‐history strategies. Endocrine traits are one candidate mechanism that may underlie the integration of life history and other phenotypic traits. However, the vast majority of this research has been on the effects of steroid hormones such as glucocorticoids and androgens on life‐history trade‐offs. Here we propose an expansion of the focus on glucocorticoids and gonadal hormones and review the potential role of insulin‐like growth factor‐1 (IGF‐1) in shaping the adaptive integration of multiple life‐history traits. IGF‐1 is a polypeptide metabolic hormone largely produced by the liver. We summarize a vast array of research demonstrating that IGF‐1 levels are susceptible to environmental variation and that IGF‐1 can have potent stimulatory effects on somatic growth and reproduction but decrease lifespan. We review the few studies in natural populations that have measured plasma IGF‐1 concentrations and its associations with life‐history traits or other characteristics of the organism or its environment. We focus on two case studies that found support for the hypothesis that IGF‐1 mediates adaptive divergence in suites of life‐history traits in response to varying ecological conditions or artificial selection. We also examine what we view as potentially fruitful avenues of research on this topic, which until now has been rarely investigated by evolutionary ecologists. We discuss how IGF‐1 may facilitate adaptive plasticity in life‐history strategies in response to early environmental conditions and also how selection on loci controlling IGF‐1 signaling may mediate population divergence and eventual speciation. After consideration of the interactions among androgens, glucocorticoids, and IGF‐1 we suggest that IGF‐1 be considered a suitable candidate mechanism for mediating life‐history traits. Finally, we discuss what we can learn about IGF‐1 from studies in free‐ranging animals. The voluminous literature in laboratory and domesticated animals documenting relationships among IGF‐1, growth, reproduction, and lifespan demonstrates the potential for a number of new research questions to be asked in free‐ranging animals. Examining how IGF‐1 mediates life‐history traits in free‐ranging animals could lead to great insight into the mechanisms that influence life‐history variation.     

Determinants of reproductive success in dominant female meerkats

1. In cooperative societies with high reproductive skew, selection on females is likely to operate principally through variation in the probability of acquiring dominant status and variation in reproductive success while dominant. Despite this, few studies of cooperative societies have investigated the factors that influence which females become dominant, and/or their reproductive output while in the dominant position. 2. Here we use long-term data from a wild meerkats population to describe variation in the breeding success of dominant female meerkats Suricata suricatta and investigate its causes. 3. Female meerkats compete intensely for breeding positions, and the probability of acquiring the breeding role depends upon a female's age in relation to competitors and her weight, both at the time of dominance acquisition and early in life. 4. Once dominant, individual differences in breeding success depend principally on the duration of dominance tenure. Females remain for longer in the dominant position if they are heavier than their competitors at the start of dominance, and if the number of adult female competitors at the start is low. 5. Female breeding success is also affected by variation in fecundity and pup survival, both of which increase with group size. After controlling for these effects, female body weight has a positive influence on breeding rate and litter size, while the number of adult female competitors reduces litter survival. 6. These findings suggest that selection for body weight and competitive ability will be high in female meerkats, which may moderate their investment in cooperative activities. We suggest that similar consequences of competition may occur among females in other cooperative societies where the benefits of attaining dominance status are high.     

The Importance of Population Growth and Regulation in Human Life History Evolution

Explaining the evolution of human life history traits remains an important challenge for evolutionary anthropologists. Progress is hindered by a poor appreciation of how demographic factors affect the action of natural selection. I review life history theory showing that the quantity maximized by selection depends on whether and how population growth is regulated. I show that the common use of R, a strategy’s expected lifetime number of offspring, as a fitness maximand is only appropriate under a strict set of conditions, which are apparently unappreciated by anthropologists. To concretely show how demography-free life history theory can lead to errors, I reanalyze an influential model of human life history evolution, which investigated the coevolution of a long lifespan and late age of maturity. I show that the model’s conclusions do not hold under simple changes to the implicitly assumed mechanism of density dependence, even when stated assumptions remain unchanged. This analysis suggests that progress in human life history theory requires better understanding of the demography of our ancestors.     

Insulin-like growth factor-1 is associated with life-history variation across Mammalia

Despite the diversity of mammalian life histories, persistent patterns of covariation have been identified, such as the ‘fast–slow’ axis of life-history covariation. Smaller species generally exhibit ‘faster’ life histories, developing and reproducing rapidly, but dying young. Hormonal mechanisms with pleiotropic effects may mediate such broad patterns of life-history variation. Insulin-like growth factor 1 (IGF-1) is one such mechanism because heightened IGF-1 activity is related to traits associated with faster life histories, such as increased growth and reproduction, but decreased lifespan. Using comparative methods, we show that among 41 mammalian species, increased plasma IGF-1 concentrations are associated with fast life histories and altricial reproductive patterns. Interspecific path analyses show that the effects of IGF-1 on these broad patterns of life-history variation are through its direct effects on some individual life-history traits (adult body size, growth rate, basal metabolic rate) and through its indirect effects on the remaining life-history traits. Our results suggest that the role of IGF-1 as a mechanism mediating life-history variation is conserved over the evolutionary time period defining mammalian diversification, that hormone–trait linkages can evolve as a unit, and that suites of life-history traits could be adjusted in response to selection through changes in plasma IGF-1.     

Life expectancy,maximum longevity and lifetime reproductive success in female Thornicroft's giraffe in Zambia

Gestation and longevity scale with body mass across taxa, yet within size dimorphic taxa, males tend to have reduced lifespans compared with females. Testing life history models, and accounting for sex differences in longevity, requires obtaining accurate longitudinal data from wild populations. We provide the first report describing key life history parameters from a long‐term study of giraffes in Africa. We followed a population of Thornicroft's giraffe (Giraffa camelopardalis thornicrofti) in Zambia for over 40 years. Maximum longevity among females was approximately 28 years, with lifespan accounting for 81% of the variance in lifetime reproductive success. Average adult female life expectancy was no different than average adult male life expectancy. However, the breeding lifespan of males was about half that of females, while maximum lifespan of males was 75% that of females. Our findings support the suggestion that sex differences in maximum lifespan arise from stronger selection for lengthy lives in females than in males. Among females, longer lives are associated with greater reproductive output.     

Disentangling the Evolution of Early and Late Life History Traits in Humans

Some aspects of human life history are unique among primates. Most notably, humans have a younger weaning age, a later age at first parturition, a shorter female reproductive period, and a longer lifespan than other living hominoid species. Obtaining a better understanding of when and how life history changed during human evolution is important to those studying the evolutionary developmental biology of extinct hominins, as life history traits pace developmental processes. Life history traits are thought to be linked via tradeoffs, such that changes in early life history traits directly affect those that follow later in life, and vice versa. However, it is also worth considering how changes to a single life history trait may indirectly affect other traits by way of modifying selective pressures acting on individuals and groups. For example, because they affect the size and demographic structure of a group, late life history traits (e.g., lifespan) may also affect the evolution of life history traits that occur earlier in life, but by modifying selective pressures acting on juveniles rather than by triggering a physiological tradeoff. This review marks an effort to begin to disentangle the ways in which early and late life history traits may affect each other both directly and indirectly. We concentrate on female life history characteristics. First, we review previous research on the evolution of the postmenopausal lifespan in women. Next we discuss recent findings concerning the relationship between the optimal length of the female reproductive period, mortality, and weaning age that show that selection favors a shorter female reproductive period in the presence of a younger weaning age. We discuss the implications this finding holds for understanding the evolution of life history traits that are of particular interest to developmental biologists.     

四种不同生活型树种细根寿命及影响因素

以4种不同生活型树种(常绿阔叶和针叶树种、落叶阔叶和针叶树种)为研究对象,通过微根管法现地观测细根的生长动态,比较不同生活型树种细根寿命在种内和种间的差异,探讨影响细根寿命的主要因子,研究结果对理解和预测森林生态系统碳及养分循环过程具有重要的理论意义。结果表明:(1)细根形态特征(分枝结构和直径)显著影响种内细根寿命,分枝等级越低、直径越小,细根的寿命越短;(2)4个树种的细根寿命表现出明显的土层效应和季节效应,即随土壤深度增加,细根的累积存活率逐渐增加,寿命延长;而不同季节出生的细根其寿命长短模式在树种间不一致,春季或夏季出生的细根寿命要长于秋冬季;(3)常绿树种(柳杉、石栎)的细根寿命要长于落叶树种(池杉、麻栎),同时,针叶树种(池杉、柳杉)的细根寿命要长于阔叶树种(麻栎、石栎)。在同一树种内,细根寿命受细根直径、根系分枝结构、土壤环境因子(土层)等因素显著影响,但在不同树种间,细根寿命可能更依赖于树木生长速率、碳分配模式等树木整体的功能性状差异。