Contrasting patterns of density‐dependent selection at different life stages can create more than one fast–slow axis of life‐history variation

There has been much recent research interest in the existence of a major axis of life‐history variation along a fast–slow continuum within almost all major taxonomic groups. Eco‐evolutionary models of density‐dependent selection provide a general explanation for such observations of interspecific variation in the "pace of life." One issue, however, is that some large‐bodied long‐lived “slow” species (e.g., trees and large fish) often show an explosive “fast” type of reproduction with many small offspring, and species with “fast” adult life stages can have comparatively “slow” offspring life stages (e.g., mayflies). We attempt to explain such life‐history evolution using the same eco‐evolutionary modeling approach but with two life stages, separating adult reproductive strategies from offspring survival strategies. When the population dynamics in the two life stages are closely linked and affect each other, density‐dependent selection occurs in parallel on both reproduction and survival, producing the usual one‐dimensional fast–slow continuum (e.g., houseflies to blue whales). However, strong density dependence at either the adult reproduction or offspring survival life stage creates quasi‐independent population dynamics, allowing fast‐type reproduction alongside slow‐type survival (e.g., trees and large fish), or the perhaps rarer slow‐type reproduction alongside fast‐type survival (e.g., mayflies—short‐lived adults producing few long‐lived offspring). Therefore, most types of species life histories in nature can potentially be explained via the eco‐evolutionary consequences of density‐dependent selection given the possible separation of demographic effects at different life stages.     

Elevational trends in life histories: revising the pace‐of‐life framework

Life‐history traits in birds, such as lifespan, age at maturity, and rate of reproduction, vary across environments and in combinations imposed by trade‐offs and limitations of physiological mechanisms. A plethora of studies have described the diversity of traits and hypothesized selection pressures shaping components of the survival–reproduction trade‐off. Life‐history variation appears to fall along a slow–fast continuum, with slow pace characterized by higher investment in survival over reproduction and fast pace characterized by higher investment in reproduction over survival. The Pace‐of‐Life Syndrome (POLS) is a framework to describe the slow–fast axis of variation in life‐history traits and physiological traits. The POLS corresponds to latitudinal gradients, with tropical birds exhibiting a slow pace of life. We examined four possible ways that the traits of high‐elevation birds might correspond to the POLS continuum: (i) rapid pace, (ii) tropical slow pace, (iii) novel elevational pace, or (iv) constrained pace. Recent studies reveal that birds breeding at high elevations in temperate zones exhibit a combination of traits creating a unique elevational pace of life with a central trade‐off similar to a slow pace but physiological trade‐offs more similar to a fast pace. A paucity of studies prevents consideration of the possibility of a constrained pace of life. We propose extending the POLS framework to include trait variation of elevational clines to help to investigate complexity in global geographic patterns.     

OXIDATIVE DAMAGE INCREASES WITH REPRODUCTIVE ENERGY EXPENDITURE AND IS REDUCED BY FOOD‐SUPPLEMENTATION

A central principle in life‐history theory is that reproductive effort negatively affects survival. Costs of reproduction are thought to be physiologically based, but the underlying mechanisms remain poorly understood. Using female North American red squirrels (Tamiasciurus hudsonicus), we test the hypothesis that energetic investment in reproduction overwhelms investment in antioxidant protection, leading to oxidative damage. In support of this hypothesis we found that the highest levels of plasma protein oxidative damage in squirrels occurred during the energetically demanding period of lactation. Moreover, plasma protein oxidative damage was also elevated in squirrels that expended the most energy and had the lowest antioxidant protection. Finally, we found that squirrels that were food‐supplemented during lactation and winter had increased antioxidant protection and reduced plasma protein oxidative damage providing the first experimental evidence in the wild that access to abundant resources can reduce this physiological cost.     

Estimation of fitness from energetics and life‐history data: An example using mussels

Changing environments have the potential to alter the fitness of organisms through effects on components of fitness such as energy acquisition, metabolic cost, growth rate, survivorship, and reproductive output. Organisms, on the other hand, can alter aspects of their physiology and life histories through phenotypic plasticity as well as through genetic change in populations (selection). Researchers examining the effects of environmental variables frequently concentrate on individual components of fitness, although methods exist to combine these into a population level estimate of average fitness, as the per capita rate of population growth for a set of identical individuals with a particular set of traits. Recent advances in energetic modeling have provided excellent data on energy intake and costs leading to growth, reproduction, and other life‐history parameters; these in turn have consequences for survivorship at all life‐history stages, and thus for fitness. Components of fitness alone (performance measures) are useful in determining organism response to changing conditions, but are often not good predictors of fitness; they can differ in both form and magnitude, as demonstrated in our model. Here, we combine an energetics model for growth and allocation with a matrix model that calculates population growth rate for a group of individuals with a particular set of traits. We use intertidal mussels as an example, because data exist for some of the important energetic and life‐history parameters, and because there is a hypothesized energetic trade‐off between byssus production (affecting survivorship), and energy used for growth and reproduction. The model shows exactly how strong this trade‐off is in terms of overall fitness, and it illustrates conditions where fitness components are good predictors of actual fitness, and cases where they are not. In addition, the model is used to examine the effects of environmental change on this trade‐off and on both fitness and on individual fitness components.     

Seasonal environments drive convergent evolution of a faster pace‐of‐life in tropical butterflies

New ecological niches that may arise due to climate change can trigger diversification, but their colonisation often requires adaptations in a suite of life‐history traits. We test this hypothesis in species‐rich Mycalesina butterflies that have undergone parallel radiations in Africa, Asia, and Madagascar. First, our ancestral state reconstruction of habitat preference, using c. 85% of extant species, revealed that early forest‐linked lineages began to invade seasonal savannahs during the late Miocene‐Pliocene. Second, rearing replicate pairs of forest and savannah species from the African and Malagasy radiation in a common garden experiment, and utilising published data from the Asian radiation, demonstrated that savannah species consistently develop faster, have smaller bodies, higher fecundity with an earlier investment in reproduction, and reduced longevity, compared to forest species across all three radiations. We argue that time‐constraints for reproduction favoured the evolution of a faster pace‐of‐life in savannah species that facilitated their persistence in seasonal habitats.     

Pooled energy budgets: Resituating human energy ‐allocation trade‐offs

Across taxa, many life‐history traits vary as a function of differences in body size. 1 - 5 Among primates, including humans, allometric relationships explain many trends in metabolic, growth, reproductive, and mortality rates. 6 - 8 But humans also deviate from nonhuman primates with respect to other developmental, reproductive, and parenting characteristics. 9 - 13 Broad relationships between life‐history traits and body size assume that energy expended in activity (foraging effort) is proportional to body size, and that energy available for growth and reproduction are equivalent. Because human subsistence and parenting are based on food sharing, and cooperation in labor and childrearing, the ways by which energy is acquired and allocated to alternate expenditures are expanded. We present a modification of the general allocation model to include a mechanism for these energy transfers. Our goal is to develop a framework that incorporates this mechanism and can explain the human life‐history paradox; that is, slow juvenile growth and rapid reproduction. We suggest that the central characteristics of human subsistence and energy transfer need to be accounted for in order to more fully appreciate human life‐history variability.     

Testing the effect of early‐life reproductive effort on age‐related decline in a wild insect

The disposable soma theory of ageing predicts that when organisms invest in reproduction they do so by reducing their investment in body maintenance, inducing a trade‐off between reproduction and survival. Experiments on invertebrates in the lab provide support for the theory by demonstrating the predicted responses to manipulation of reproductive effort or lifespan. However, experimental studies in birds and evidence from observational (nonmanipulative) studies in nature do not consistently reveal trade‐offs. Most species studied previously in the wild are mammals and birds that reproduce over multiple discrete seasons. This contrasts with temperate invertebrates, which typically have annual generations and reproduce over a single season. We expand the taxonomic range of senescence study systems to include life histories typical of most temperate invertebrates. We monitored reproductive effort, ageing, and survival in a natural field cricket population over ten years to test the prediction that individuals investing more in early‐reproduction senesce faster and die younger. We found no evidence of a trade‐off between early‐life reproductive effort and survival, and only weak evidence for a trade‐off with phenotypic senescence. We discuss the possibility that organisms with multiple discrete breeding seasons may have greater opportunities to express trade‐offs between reproduction and senescence.     

Reproductive efficiency and shade avoidance plasticity under simulated competition

Plant strategy and life‐history theories make different predictions about reproductive efficiency under competition. While strategy theory suggests under intense competition iteroparous perennial plants delay reproduction and semelparous annuals reproduce quickly, life‐history theory predicts both annual and perennial plants increase resource allocation to reproduction under intense competition. We tested (1) how simulated competition influences reproductive efficiency and competitive ability (CA) of different plant life histories and growth forms; (2) whether life history or growth form is associated with CA; (3) whether shade avoidance plasticity is connected to reproductive efficiency under simulated competition. We examined plastic responses of 11 herbaceous species representing different life histories and growth forms to simulated competition (spectral shade). We found that both annual and perennial plants invested more to reproduction under simulated competition in accordance with life‐history theory predictions. There was no significant difference between competitive abilities of different life histories, but across growth forms, erect species expressed greater CA (in terms of leaf number) than other growth forms. We also found that shade avoidance plasticity can increase the reproductive efficiency by capitalizing on the early life resource acquisition and conversion of these resources into reproduction. Therefore, we suggest that a reassessment of the interpretation of shade avoidance plasticity is necessary by revealing its role in reproduction, not only in competition of plants.     

Adult dietary protein has age‐ and context‐dependent effects on male post‐copulatory performance

The highly conserved effect of dietary protein restriction on lifespan and ageing is observed in both sexes and across a vast range of taxa. This extension of lifespan is frequently accompanied by a reduction in female fecundity, and it has been hypothesized that individuals may reallocate resources away from reproduction and into somatic maintenance. However, effects of dietary protein restriction on male reproduction are less consistent, suggesting that these effects may depend on other environmental parameters. Using the neriid fly, Telostylinus angusticollis, we examined age‐specific effects of adult dietary protein restriction on male post‐copulatory reproductive performance (fecundity and offspring viability). To explore the context dependence of these effects, we simultaneously manipulated male larval diet and adult mating history. We found that protein‐restricted males sired less viable offspring at young ages, but offspring viability increased with paternal age and eventually exceeded that of fully fed males. The number of eggs laid by females was not affected by male dietary protein, whereas egg hatching success was subject to a complex interaction of male adult diet, age, larval diet and mating history. These findings suggest that effects of protein restriction on male reproduction are highly context dependent and cannot be explained by a simple reallocation of resources from reproduction to somatic maintenance. Rather, these effects appear to involve changes in the scheduling of male reproductive investment with age.     

Interactive life‐history traits predict sensitivity of plants and animals to temporal autocorrelation

Temporal autocorrelation in demographic processes is an important aspect of population dynamics, but a comprehensive examination of its effects on different life‐history strategies is lacking. We use matrix population models from 454 plant and animal populations to simulate stochastic population growth rates (log λ_s) under different temporal autocorrelations in demographic rates , using simulated and observed covariation among rates. We then test for differences in sensitivities, or changes of log λ_s to changes in autocorrelation among two major axes of life‐history strategies, obtained from phylogenetically informed principal component analysis: the fast‐slow and reproductive‐strategy continua. Fast life histories exhibit highest sensitivities to simulated autocorrelation in demographic rates across reproductive strategies. Slow life histories are less sensitive to temporal autocorrelation, but their sensitivities increase among highly iteroparous species. We provide cross‐taxonomic evidence that changes in the autocorrelation of environmental variation may affect a wide range of species, depending on complex interactions of life‐history strategies.     

Time spent in distinct life history stages has sex‐specific effects on reproductive fitness in wild Atlantic salmon

In species with complex life cycles, life history theory predicts that fitness is affected by conditions encountered in previous life history stages. Here, we use a 4‐year pedigree to investigate if time spent in two distinct life history stages has sex‐specific reproductive fitness consequences in anadromous Atlantic salmon (Salmo salar). We determined the amount of years spent in fresh water as juveniles (freshwater age, FW, measured in years), and years spent in the marine environment as adults (sea age, SW, measured in sea winters) on 264 sexually mature adults collected on a river spawning ground. We then estimated reproductive fitness as the number of offspring (reproductive success) and the number of mates (mating success) using genetic parentage analysis (>5,000 offspring). Sea age is significantly and positively correlated with reproductive and mating success of both sexes whereby older and larger individuals gained the highest reproductive fitness benefits (females: 62.2% increase in offspring/SW and 34.8% increase in mate number/SW; males: 201.9% offspring/SW and 60.3% mates/SW). Younger freshwater age was significantly related to older sea age and thus increased reproductive fitness, but only among females (females: ?33.9% offspring/FW and ?32.4% mates/FW). This result implies that females can obtain higher reproductive fitness by transitioning to the marine environment earlier. In contrast, male mating and reproductive success was unaffected by freshwater age and more males returned at a younger age than females despite the reproductive fitness advantage of later sea age maturation. Our results show that the timing of transitions between juvenile and adult phases has a sex‐specific consequence on female reproductive fitness, demonstrating a life history trade‐off between maturation and reproduction in wild Atlantic salmon.     

Investment in survival and reproduction along a semelparity–iteroparity gradient in the Beta species complex

The Beta species complex shows a gradient of life histories from pronounced semelparity (big‐bang reproduction) to pronounced iteroparity (repeated reproduction). Models assume a trade‐off between investment in reproduction and survival. Reproductive effort is thought to increase with decreasing life span, and to be invariable in semelparous plants and susceptible to environmental conditions in iteroparous plants. These assumptions and hypotheses were verified by a greenhouse experiment testing six different life cycles at three contrasting nutrient levels. This study suggests that reproductive effort is negatively correlated with mean life span along the life‐cycle gradient. Unlike semelparous beets, reproductive effort in iteroparous beets is extremely sensitive to nutrient level. Phenotypic correlation between allocation to reproduction and allocation to survival generally appeared significantly negative in the longest‐lived iteroparous beets, nonsignificant in intermediate life histories and obviously positive in semelparous beets (no trade‐off control).     

Food availability as a major driver in the evolution of life‐history strategies of sibling species

Life‐history theory predicts trade‐offs between reproductive and survival traits such that different strategies or environmental constraints may yield comparable lifetime reproductive success among conspecifics. Food availability is one of the most important environmental factors shaping developmental processes. It notably affects key life‐history components such as reproduction and survival prospect. We investigated whether food resource availability could also operate as an ultimate driver of life‐history strategy variation between species. During 13 years, we marked and recaptured young and adult sibling mouse‐eared bats (Myotis myotis and Myotis blythii) at sympatric colonial sites. We tested whether distinct, species‐specific trophic niches and food availability patterns may drive interspecific differences in key life‐history components such as age at first reproduction and survival. We took advantage of a quasi‐experimental setting in which prey availability for the two species varies between years (pulse vs. nonpulse resource years), modeling mark‐recapture data for demographic comparisons. Prey availability dictated both adult survival and age at first reproduction. The bat species facing a more abundant and predictable food supply early in the season started its reproductive life earlier and showed a lower adult survival probability than the species subjected to more limited and less predictable food supply, while lifetime reproductive success was comparable in both species. The observed life‐history trade‐off indicates that temporal patterns in food availability can drive evolutionary divergence in life‐history strategies among sympatric sibling species.     

Trade‐offs between life‐history traits at range‐edge and central locations

The allocation of resources to different life‐history traits should represent the best compromise in fitness investment for organisms in their local environment. When resources are limiting, the investment in a specific trait must carry a cost that is expressed in trade‐offs with other traits. In this study, the relative investment in the fitness‐related traits, growth, reproduction and defence were compared at central and range‐edge locations, using the seaweed Ascophyllum nodosum as a model system. Individual growth rates were similar at both sites, whereas edge populations showed a higher relative investment in reproduction (demonstrated by a higher reproductive allocation and extended reproductive periods) when compared to central populations that invested more in defence. These results show the capability of A. nodosum to differentially allocate resources for different traits under different habitat conditions, suggesting that reproduction and defence have different fitness values under the specific living conditions experienced at edge and central locations. However, ongoing climate change may threaten edge populations by increasing the selective pressure on specific traits, forcing these populations to lower the investment in other traits that are also potentially important for population fitness.     

Food intake rates of inactive fish are positively linked to boldness in three‐spined sticklebacks Gasterosteus aculeatus

To investigate the link between personality and maximum food intake of inactive individuals, food‐deprived three‐spined sticklebacks Gasterosteus aculeatus at rest in their home compartments were provided with ad libitum prey items. Bolder individuals ate considerably more than shyer individuals, even after accounting for body size, while sociability did not have an effect. These findings support pace‐of‐life theory predicting that life‐history strategies are linked to boldness.     

A pre‐breeding immune challenge delays reproduction in the female dark‐eyed junco Junco hyemalis

Precise timing of life‐history transitions in predictably changing environments is hypothesized to aid in individual survival and reproductive success, by appropriately matching an animal's physiology and behavior with prevailing environmental conditions. Therefore, it is imperative for individuals to time energetically costly life‐history stages (i.e. reproduction) so they overlap with seasonal peaks in food abundance and quality. Female lifetime reproductive fitness is affected by several factors that influence energy balance, including arrival date, timing of egg production, and energetic condition. Therefore, any extra energetic costs during reproduction may negatively affect timing of egg production, and ultimately a female's fitness. For example, mounting an immunological response elicits a high energetic cost, and this transfer of resources towards cell and immune system maintenance could have direct negative effects on reproductive timing. In order to determine whether an immune challenge delays onset of breeding (i.e. egg production), we administered either a humoral immune challenge (keyhole limpet hemocyanin (KLH)) (treatment) or physiological saline (control) to free‐living female dark‐eyed juncos Junco hyemalis in the period immediately prior to egg‐laying (～4 weeks). We found that KLH‐injected females artificially delayed clutch initiation when compared to control females. These data help to refine our understanding of how free‐living birds allocate resources between reproduction and self‐maintenance processes during the critical pre‐laying period of the annual cycle.     

The early‐life environment and individual plasticity in life‐history traits

We tested whether the early‐life environment can influence the extent of individual plasticity in a life‐history trait. We asked: can the early‐life environment explain why, in response to the same adult environmental cue, some individuals invest more than others in current reproduction? Moreover, can it additionally explain why investment in current reproduction trades off against survival in some individuals, but is positively correlated with survival in others? We addressed these questions using the burying beetle, which breeds on small carcasses and sometimes carries phoretic mites. These mites breed alongside the beetle, on the same resource, and are a key component of the beetle's early‐life environment. We exposed female beetles to mites twice during their lives: during their development as larvae and again as adults during their first reproductive event. We measured investment in current reproduction by quantifying average larval mass and recorded the female's life span after breeding to quantify survival. We found no effect of either developing or breeding alongside mites on female reproductive investment, nor on her life span, nor did developing alongside mites influence her size. In post hoc analyses, where we considered the effect of mite number (rather than their mere presence/absence) during the female's adult breeding event, we found that females invested more in current reproduction when exposed to greater mite densities during reproduction, but only if they had been exposed to mites during development as well. Otherwise, they invested less in larvae at greater mite densities. Furthermore, females that had developed with mites exhibited a trade‐off between investment in current reproduction and future survival, whereas these traits were positively correlated in females that had developed without mites. The early‐life environment thus generates individual variation in life‐history plasticity. We discuss whether this is because mites influence the resources available to developing young or serve as important environmental cues.     

Selection on age at first and at last reproduction in the long‐lived Alpine Swift Apus melba

The way an organism spreads its reproduction over time is defined as a life‐history trait, and selection is expected to favour life‐history traits associated with the highest fitness return. We use a long‐term dataset of 277 life histories to investigate the shape and strength of selection acting on the age at first reproduction and at last reproduction in the long‐lived Alpine Swift. Both traits were under strong directional selection, but in opposite directions, with selection favouring birds starting their reproductive career early and being able to reproduce for longer. There was also evidence for stabilising selection acting on both traits, suggesting that individuals should nonetheless refrain from reproducing in their first 2 years of life (i.e. when inexperienced), and that reproducing after 7 years of age had little effect on lifetime fitness, probably due to senescence.     

Interpopulation Variations in Behavioral Syndromes of a Jumping Spider from Insecticide‐Treated and Insecticide‐Free Orchards

Variations in environmental conditions can influence behavioral syndromes (correlated tendencies in behaviors), and understanding the factors that shape trait covariation is particularly relevant when species are challenged by environmental changes. We investigated how behavioral syndromes varied at extremes of a gradient of anthropogenic disturbance, using apple orchards with different histories of insecticidal applications as a model system. Eris militaris (Araneae: Salticidae) jumping spiders were sampled from an insecticide‐free orchard and an insecticide‐treated orchard from Southern Québec. Spiders were tested for activity, aggression, boldness, and voracity under standardized conditions. Behavioral syndrome structure was compared between the two populations using Bayesian multiresponse models and structural equation modeling. Syndrome structure differed significantly between the two populations. The insecticide‐free population showed evidence of a syndrome involving all measured traits, while only aggression, boldness and voracity were correlated in the insecticide‐treated population. The insecticide‐free population showed negative correlations between active and voracious behavioral types vs. aggressive and bold types while the insecticide‐treated population showed a negative correlation between aggression‐boldness and voracity. This research is a first step in investigating the impact of anthropogenic disturbances on behavioral syndromes and demonstrates that behavioral syndromes may vary with respect to insecticidal applications.     

Condition‐dependent mortality exacerbates male (but not female) reproductive senescence and the potential for sexual conflict

Disentangling the relationship between age and reproduction is central to understand life‐history evolution, and recent evidence shows that considering condition‐dependent mortality is a crucial piece of this puzzle. For example, nonrandom mortality of ‘low‐condition’ individuals can lead to an increase in average lifespan. However, selective disappearance of such low‐condition individuals may also affect reproductive senescence at the population level due to trade‐offs between physiological functions related to survival/lifespan and the maintenance of reproductive functions. Here, we address the idea that condition‐dependent extrinsic mortality (i.e. simulated predation) may increase the age‐related decline in male reproductive success and with it the potential for sexual conflict, by comparing reproductive ageing in Drosophila melanogaster male/female cohorts exposed (or not) to condition‐dependent simulated predation across time. Although female reproductive senescence was not affected by predation, male reproductive senescence was considerably higher under predation, due mainly to an accelerated decline in offspring viability of ‘surviving’ males with age. This sex‐specific effect suggests that condition‐dependent extrinsic mortality can exacerbate survival‐reproduction trade‐offs in males, which are typically under stronger condition‐dependent selection than females. Interestingly, condition‐dependent extrinsic mortality did not affect mating success, hinting that accelerated reproductive senescence is due to a decrease in male post‐copulatory fitness components. Our results support the recent proposal that male ageing can be an important source of sexual conflict, further suggesting this effect could be exacerbated under more natural conditions.