Fast-slow Life-history Continuum Research Articles

Metabolism, population growth, and the fast‐slow life history continuum of marine fishes

AbstractThe maximum intrinsic rate of population increase (rmax) represents a population's maximum capacity to replace itself and is central to fisheries management and conservation. Species with lower rmax typically have slower life histories compared to species with faster life histories and higher rmax. Here, we posit that metabolic rate is related to the fast–slow life history continuum and the connection may be stronger for maximum metabolic rate and aerobic scope compared to resting metabolic rate. Specifically, we ask whether variation in rmax or any of its component life‐history traits – age‐at‐maturity, maximum age, and annual reproductive output – explain variation in resting and maximum metabolic rates and aerobic scope across 84 shark and teleost species, while accounting for the effects of measurement temperature, measurement body mass, ecological lifestyle, and evolutionary history. Overall, we find a strong connection between metabolic rate and the fast‐slow life history continuum, such that species with faster population growth (higher rmax) generally have higher maximum metabolic rates and broader aerobic scopes. Specifically, rmax is more important in explaining variation in maximum metabolic rate and aerobic scope compared to resting metabolic rate, which is best explained by age‐at‐maturity (out of the life history traits examined). In conclusion, teleosts and sharks share a common fast–slow physiology/life history continuum, with teleosts generally at the faster end and sharks at the slower end, yet with considerable overlap. Our work improves our understanding of the diversity of fish life histories and may ultimately improve our understanding of intrinsic sensitivity to overfishing.

Understanding Patterns of Life History Trait Covariation in an Untapped Resource, the Lab Mouse.

AbstractThrough artificial selection and inbreeding, strains of laboratory mice have been developed that vary in the expression of a single or suite of desired traits valuable to biomedical research. In addition to the selected trait(s), these strains also display variation in pelage color, body size, physiology, and life history. This article exploits the broad phenotypic variation across lab mouse strains to evaluate the relationships between life history and metabolism. Life history variation tends to exist along a fast-slow continuum. There has been considerable interest in understanding the ecological and evolutionary factors underlying life history variation and the physiological and metabolic processes that support them. Yet it remains unclear how these key traits scale across hierarchical levels, as ambiguous empirical support has been garnered at the intraspecific level. Within-species investigations have been thwarted by methodological constraints and environmental factors that obscure the genetic architecture underlying the hypothesized functional integration of life history and metabolic traits. In this analysis, we used the publicly available Mouse Phenome Database by the Jackson Laboratory to investigate the relationships among life history traits (e.g., body size, reproduction, and life span) and metabolic traits (e.g., daily energy expenditure and insulin-like growth factor 1 concentration). Our findings revealed significant variation in reproductive characteristics across strains of mice as well as relationships among life history and metabolic traits. We found evidence of variation along the fast-slow life history continuum, though the direction of some relationships among these traits deviated from interspecific predictions laid out in previous literature. Furthermore, our results suggest that the strength of these relationships are strongest earlier in life.

Exceptional parallelisms characterize the evolutionary transition to live birth in phrynosomatid lizards

Viviparity, an innovation enhancing maternal control over developing embryos, has evolved >150 times in vertebrates, and has been proposed as an adaptation to inhabit cold habitats. Yet, the behavioral, physiological, morphological, and life history features associated with live-bearing remain unclear. Here, we capitalize on repeated origins of viviparity in phrynosomatid lizards to tease apart the phenotypic patterns associated with this innovation. Using data from 125 species and phylogenetic approaches, we find that viviparous phrynosomatids repeatedly evolved a more cool-adjusted thermal physiology than their oviparous relatives. Through precise thermoregulatory behavior viviparous phrynosomatids are cool-adjusted even in warm environments, and oviparous phrynosomatids warm-adjusted even in cool environments. Convergent behavioral shifts in viviparous species reduce energetic demand during activity, which may help offset the costs of protracted gestation. Whereas dam and offspring body size are similar among both parity modes, annual fecundity repeatedly decreases in viviparous lineages. Thus, viviparity is associated with a lower energetic allocation into production. Together, our results indicate that oviparity and viviparity are on opposing ends of the fast-slow life history continuum in both warm and cool environments. In this sense, the ‘cold climate hypothesis’ fits into a broader range of energetic/life history trade-offs that influence transitions to viviparity.

The metabolic pace of life histories across fishes.

All life acquires energy through metabolic processes and that energy is subsequently allocated to life-sustaining functions such as survival, growth and reproduction. Thus, it has long been assumed that metabolic rate is related to the life history of an organism. Indeed, metabolic rate is commonly believed to set the pace of life by determining where an organism is situated along a fast-slow life-history continuum. However, empirical evidence of a direct interspecific relationship between metabolic rate and life histories is lacking, especially for ectothermic organisms. Here, we ask whether three life-history traits-maximum body mass, generation length and growth performance-explain variation in resting metabolic rate (RMR) across fishes. We found that growth performance, which accounts for the trade-off between growth rate and maximum body size, explained variation in RMR, yet maximum body mass and generation length did not. Our results suggest that measures of life history that encompass trade-offs between life-history traits, rather than traits in isolation, explain variation in RMR across fishes. Ultimately, understanding the relationship between metabolic rate and life history is crucial to metabolic ecology and has the potential to improve prediction of the ecological risk of data-poor species.

Strong species differences in life history do not predict oxidative stress physiology or sensitivity to an environmental oxidant.

Species typically align along a fast-slow life-history continuum, yet it is not clear to what extent oxidative stress physiology can be integrated with this continuum to form a 'pace-of-life syndrome', especially so in invertebrates. This is important, given the assumed role of oxidative stress in mediating life-history trade-offs, and the prediction that species with a faster pace should be more vulnerable to oxidative stress. We tested whether a species' life-history pace, here represented by its growth rate, can predict species-level differentiation in physiology and sensitivity to oxidative stress. Therefore, we exposed four species of Ischnura damselflies that strongly align along a fast-slow life-history continuum to different levels of ultraviolet (UV) radiation. We measured an extended set of physiological traits linked to the pace-of-life: standard metabolic rate, oxidative stress physiology (antioxidant enzymes and oxidative damage) and defence/condition traits (investment in immune function, energy storage and structural defence). Despite strong species differences in growth rate and physiology, growth rate did not predict species-level differentiation in physiology. Hence there was no support for the integration of metabolic rate, oxidative stress physiology or defence/condition traits into a species-level syndrome. Ultraviolet exposure affected nearly all traits: it reduced growth rate and increased metabolic rate, affected all oxidative stress physiology traits and increased the two defence traits (immune function, and melanin content). Nevertheless, the pace-of-life based on growth rate did not predict sensitivity to UV. Instead, the observed pattern of investment in structural UV defence (melanin) might have reduced the need for enzymatic antioxidant defence, this way potentially decoupling the covariation between the life-history pace and oxidative stress physiology. The absence of an integrated axis of life-history and physiological variation indicates no major constraints for the evolution of these traits among the studied damselfly species. Our study highlights that ecological differences between species may decouple covariation between species' life-history pace and their physiology, as well as their sensitivity to environmental stressors.

Population position along the fast-slow life-history continuum predicts intraspecific variation in actuarial senescence.

Patterns of actuarial senescence can be highly variable among species. Previous comparative analyses revealed that both age at the onset of senescence and rates of senescence are linked to position of a species along the fast-slow life-history continuum. As there are few long-term datasets of wild populations with known-age individuals, intraspecific (i.e. between-population) variation in senescence is understudied and limited to comparisons of wild and captive populations of the same species, mostly birds and mammals. In this paper, we examined how population position along the fast-slow life-history continuum affects intraspecific variation in senescence in an amphibian, Bombina variegata. We used capture-recapture data collected in four populations with contrasting life-history strategies. Senescence trajectories were analysed using Bayesian capture-recapture models. We show that in populationswith fast life histories the onset of actuarial senescence was earlier and individuals aged at a faster rate than individuals in populationswith slow life histories. Our study provides one of the few empirical examples of among-population variation in actuarial senescence patterns in the wild and confirms that the fast-slow life-history gradient is associated with both macroevolutionary and microevolutionary patterns of actuarial senescence.

Unsociable juvenile male three-spined sticklebacks grow more attractive

An animal’s personality may be an adaptive behavioral response of individuals to consistent differences in physiology and life-history. Studying the relationship between behavior and other fitness-related traits within the pace-of-life syndrome (POLS) framework, which explains the integration of different traits using the concept of a fast-slow life-history continuum, may thus be a useful approach to understanding the evolution and maintenance of animal personality. According to the POLS hypothesis, for example, fast individuals should be behaviorally more active, bolder or less sociable, and potentially invest more in reproduction than slow individuals. Here, we examined whether the sociability of juvenile sticklebacks (Gasterosteus aculeatus) is linked with their key reproductive traits, carotenoid-based nuptial coloration of males and egg production of females. We also tested whether experimental manipulation of environmental conditions (control vs. warm winter) can change pace-of-life and the link between behavioral and reproductive traits. Male sticklebacks prone to shoaling expressed lower peak red coloration at the reproductive stage, during which they were solitary and territorial. In females, fecundity was not correlated with early social behavior. Experimental sticklebacks reared in warm winter conditions decreased their investment in reproduction, but the negative relationship between sociability and sexual signal of males was maintained. Our results suggest that the POLS could partly explain the maintenance of personality under predation pressure or severe mating competition. In natural environments, any benefit to sociable male sticklebacks may be counterbalanced by the cost of growing less attractive. Why do animals vary in personality, and how is such variation maintained within a population? An interesting approach for understanding this is studying how personality traits are correlated with other fitness-related traits within the pace-of-life framework. For the first time, our results show the link between sociability at the juvenile stage and the expression of sexual ornament during reproduction in male three-spined sticklebacks. Sociable juveniles may benefit from reduced predation risk, but they grow less attractive and this may reduce their mating success during reproduction. Thus, the trade-off between survival and reproduction may contribute to the maintenance of among-individual variation in behavior.

Effects of food availability on asexual reproduction and stress tolerance along the fast–slow life history continuum in freshwater hydra (Cnidaria: Hydrozoa)

Life history theory predicts that reproduction and somatic maintenance are negatively related, but the strength of this relationship is expected to depend on food availability. In this study, we investigated asexual reproduction (budding rate) and oxidative stress tolerance as two opposing facets of life history trade-offs in 17 strains of five freshwater hydra species under experimentally simulated low, medium, and high food availability. Stress tolerance was quantified by exposing animals to exogenous H2O2, which mimics reactive oxygen species arising in vivo. The five species differed in life history traits (low budding rate and high stress tolerance in Hydra vulgaris and H. circumcincta and the opposite in H. oligactis and H. viridissima; low budding rate combined with relatively low stress tolerance in H. oxycnida). Stress tolerance and asexual reproduction increased with food, but there were clear interspecific differences in this relationship. Across all strains, stress tolerance and budding rate were significantly negatively related on the low and medium, but not the high food level. These results suggest that resource allocation trade-offs are involved in determining life history traits in hydra; populations/species can be broadly positioned on a fast–slow life history continuum, and response to variation in food varies along this continuum.

Towards cancer-aware life-history modelling.

Studies of body size evolution, and life-history theory in general, are conducted without taking into account cancer as a factor that can end an organism's reproductive lifespan. This reflects a tacit assumption that predation, parasitism and starvation are of overriding importance in the wild. We argue here that even if deaths directly attributable to cancer are a rarity in studies of natural populations, it remains incorrect to infer that cancer has not been of importance in shaping observed life histories. We present first steps towards a cancer-aware life-history theory, by quantifying the decrease in the length of the expected reproductively active lifespan that follows from an attempt to grow larger than conspecific competitors. If all else is equal, a larger organism is more likely to develop cancer, but, importantly, many factors are unlikely to be equal. Variations in extrinsic mortality as well as in the pace of life—larger organisms are often near the slow end of the fast–slow life-history continuum—can make realized cancer incidences more equal across species than what would be observed in the absence of adaptive responses to cancer risk (alleviating the so-called Peto's paradox). We also discuss reasons why patterns across species can differ from within-species predictions. Even if natural selection diminishes cancer susceptibility differences between species, within-species differences can remain. In many sexually dimorphic cases, we predict males to be more cancer-prone than females, forming an understudied component of sexual conflict.

Parental Support during Childhood Predicts Life History-Related Personality Variation and Social Status in Young Adults

Adaptationist theories of development posit the existence of facultative mechanisms designed to calibrate individual differences in life history strategy to cues available in childhood. Such theories have led to the discovery of links between parenting-related cues and multiple life history phenotypes in offspring (e.g., reproductive timing), but less is known about the influences of parental behavior on the development of stable personality traits. This article reports a preliminary test of the hypothesis that life history-related personality variation is developmentally calibrated in response to the level of parental support received during childhood. Consistent with this, in a sample of young adults (N = 321), (i) subjects’ reports of their parents’ income positively predicted the level of parental support they recall having received during childhood; (ii) these measures of parental income and parental support in childhood positively predicted subjects’ standing on the general factor of personality (GFP), long-term mating orientation, and prestige-based social status; and (iii) path analyses fit a model of the following form: parental income → parental support in childhood → GFP → prestige-based status. Moreover, these effects held when controlling for perceptions of current social support, which implies that associations of parental support in childhood with outcomes in adulthood did not reflect current perceptions or global self-evaluative biases. These findings, though preliminary, are consonant with recent theories positing that the GFP and prestige-based status reflect individual differences along a fast-slow life history continuum, and suggest that life history-related personality variation may be developmentally calibrated to parental support during childhood.

Semelparity in a population of Gracilinanus agilis (Didelphimorphia: Didelphidae) inhabiting the Brazilian cerrado

Although reproducing once in a lifetime (i.e. semelparity) is considered rare among vertebrates, it has evolved at least five times in two distantly related marsupial families; the Australian Dasyuridae and South American Didelphidae. The major aim of this research was to describe the population dynamics, reproductive strategy and associated life-history traits of the agile gracile mouse opossum, Gracilinanus agilis, in order to position the species along the fast-slow life-history continuum. Sampling was carried out through mark-recapture, from August 2010 to April 2013, in a Brazilian area of cerrado. Reproductive activity was seasonal and synchronized among females, and occurred from July to January/February. After mating, population size decreased due to male disappearance, which seems to be explained by post-mating male die-off. Phylogenetic predisposition toward semelparity in Gracilinanus lineage and intense competition for females may contribute to male die-off, as indicated by several evidences such as male-biased sex ratio, signs of aggression in reproductive males, and a pronounced gain in male body mass and size prior to mating. Although two litters were produced, most females disappeared after weaning their young, indicating post-reproductive senescence and resulting in discrete, non-overlapping generations, characterizing semelparity in this population of G. agilis.

Effects of body size and lifestyle on evolution of mammal life histories

It has recently been proposed that life-history evolution is subject to a fundamental size-dependent constraint. This constraint limits the rate at which biomass can be produced so that production per unit of body mass is inevitably slower in larger organisms than in smaller ones. Here we derive predictions for how changes in body size and production rates evolve in different lifestyles subject to this constraint. Predictions are tested by using data on the mass of neonate tissue produced per adult per year in 637 placental mammal species and are generally supported. Compared with terrestrial insectivores with generalized primitive traits, mammals that have evolved more specialized lifestyles have divergent mass-specific production rates: (i) increased in groups that specialize on abundant and reliable foods: grazing and browsing herbivores (artiodactyls, lagomorphs, perissodactyls, and folivorous rodents) and flesh-eating marine mammals (pinnipeds, cetaceans); and (ii) decreased in groups that have lifestyles with reduced death rates: bats, primates, arboreal, fossorial, and desert rodents, bears, elephants, and rhinos. Convergent evolution of groups with similar lifestyles is common, so patterns of productivity across mammalian taxa reflect both ecology and phylogeny. The overall result is that groups with different lifestyles have parallel but offset relationships between production rate and body size. These results shed light on the evolution of the fast-slow life-history continuum, suggesting that variation occurs along two axes corresponding to body size and lifestyle.

Variation in the reproductive rate of bats

In many respects, bats have relatively slow life histories. However, the reproductive rate of bats (i.e., the proportion of females that reproduce in any breeding season) has not been critically examined. We compiled data on the reproductive rates of bats to test predictions based on life-history theory. Among 257 samples from 103 species, reproductive rate varied considerably and was typically under 100%. Temperate-zone species had significantly lower and more variable reproductive rates than did tropical species. Reproductive rate also varied among families, with species in the Vespertilionidae having particularly high rates. As predicted based on life-history theory, reproductive rate was negatively correlated with longevity, and among vespertilionids, species with larger litters had higher reproductive rates. Thus, the data suggest that bats have relatively slow reproductive rates and, as in other life-history traits, fall at the "slow" end of the fast–slow life-history continuum found among mammals. Female bats, especially those in temperate regions, appear to adjust their allocation of resources to reproduction, and at times forego reproduction, perhaps in relation to their body condition, prey availability, and weather conditions.