Why we cannot always expect life history strategies to directly inform on sensitivity to environmental change.

Variation in life history traits in animals and plants can often be structured along major axes of life history strategies. The position of a species along these axes can inform on their sensitivity to environmental change. For example, species with slow life histories are found to be less sensitive in their long-term population responses to environmental change than species with fast life histories. This provides a tantalizing link between sets of traits and population responses to change, contained in a highly generalizable theoretical framework. Life history strategies are assumed to reflect the outcome of life history tradeoffs that, by their very nature, act at the individual level. Examples include the tradeoff between current and future reproductive success, and allocating energy into growth versus reproduction. But the importance of such tradeoffs in structuring population-level responses to environmental change remains understudied. We aim to increase our understanding of the link between individual-level life history tradeoffs and the structuring of life history strategies across species, as well as the underlying links to population responses to environmental change. We find that the classical association between lifehistory strategies and population responses to environmental change breaks down when accounting for individual-level tradeoffs and energy allocation. Therefore, projecting population responses to environmental change should not be inferred based only on a limited set of species traits. We summarize our perspective and a way forward in a conceptual framework.

Marsupial position on life-history continua and the potential contribution of life-history traits to population growth.

Previous studies have suggested that mammal life history varies along the fast-slow continuum and that, in eutherians, this continuum is linked to variation in the potential contribution of survival and reproduction to population growth rate (λ). Fast eutherians mature early, have large litters and short lifespans, and exhibit high potential contribution of age at first reproduction and fertility to λ, while slow eutherians show high potential contribution of survival to λ. However, marsupials have typically been overlooked in comparative tests of mammalian life-history evolution. Here, we tested whether the eutherian life-history pattern extends to marsupials, and show that marsupial life-history trade-offs are organized along two major axes: (i) the reproductive output and dispersion axis, and (ii) the fast-slow continuum, with an additional association between adult survival and body mass. Life-history traits that potentially drive changes in λ are similar in eutherians and marsupials with slow life histories, but differ in fast marsupials; age at first reproduction is the most important trait contributing to λ and fertility contributes little. Marsupials have slower life histories than eutherians, and differences between these clades may derive from their contrasting reproductive modes; marsupials have slower development, growth and metabolism than eutherians of equivalent size.

Looking to the past to understand the future: linking evolutionary modes of response with functional and life history traits in variable environments.

In a variable world, plants must have strategies to deal with environmental conditions as they change. Understanding these strategies is critical since climate change not only affects mean conditions but also affects variability and predictability of those conditions. Doing so requires identifying how functional and life history traits interact throughout the life cycle to drive responses, as well as exploring how past variability will shape future responses. Here, I highlight relevant life history theory for predicting strategies in relation to the nature of environmental variability, relate theory to empirical studies integrating functional and life history traits to understand responses, and identify key areas for future research that will facilitate the application of this understanding toward predicting responses to climate change.

Life history mediates the trade-offs among different components of demographic resilience.

Accelerating rates of biodiversity loss underscore the need to understand how species achieve resilience-the ability to resist and recover from a/biotic disturbances. Yet, the factors determining the resilience of species remain poorly understood, due to disagreements on its definition and the lack of large-scale analyses. Here, we investigate how the life history of 910 natural populations of animals and plants predicts their intrinsic ability to be resilient. We show that demographic resilience can be achieved through different combinations of compensation, resistance and recovery after a disturbance. We demonstrate that these resilience components are highly correlated with life history traits related to the species' pace of life and reproductive strategy. Species with longer generation times require longer recovery times post-disturbance, whilst those with greater reproductive capacity have greater resistance and compensation. Our findings highlight the key role of life history traits to understand species resilience, improving our ability to predict how natural populations cope with disturbance regimes.

Life-history genotype explains variation in migration activity in Atlantic salmon (Salmo salar).

One of the most well-known life-history continuums is the fast-slow axis, where 'fast' individuals mature earlier than 'slow' individuals. 'Fast' individuals are predicted to be more active than 'slow' individuals because high activity is required to maintain a fast life-history strategy. Recent meta-analyses revealed mixed evidence for such integration. Here, we test whether known life-history genotypes differ in activity expression by using Atlantic salmon (Salmo salar) as a model. In salmon, variation in Vgll3, a transcription cofactor, explains approximately 40% of variation in maturation timing. We predicted that the allele related to early maturation (vgll3*E) would be associated with higher activity. We used an automated surveillance system to follow approximately 1900 juveniles including both migrants and non-migrants (i.e. smolt and parr fish, respectively) in semi-natural conditions over 31 days (approx. 580 000 activity measurements). In migrants, but not in non-migrants, vgll3 explained variation in activity according to our prediction in a sex-dependent manner. Specifically, in females the vgll3*E allele was related to increasing activity, whereas in males the vgll3*L allele (later maturation allele) was related to increasing activity. These sex-dependent effects might be a mechanism maintaining within-population genetic life-history variation.

Tropical tree growth sensitivity to climate is driven by species intrinsic growth rate and leaf traits.

A better understanding of how climate affects growth in tree species is essential for improved predictions of forest dynamics under climate change. Long-term climate averages (mean climate) drive spatial variations in species' baseline growth rates, whereas deviations from these averages over time (anomalies) can create growth variation around the local baseline. However, the rarity of long-term tree census data spanning climatic gradients has so far limited our understanding of their respective role, especially in tropical systems. Furthermore, tree growth sensitivity to climate is likely to vary widely among species, and the ecological strategies underlying these differences remain poorly understood. Here, we utilize an exceptional dataset of 49 years of growth data for 509 tree species across 23 tropical rainforest plots along a climatic gradient to examine how multiannual tree growth responds to both climate means and anomalies, and how species' functional traits mediate these growth responses to climate. We show that anomalous increases in atmospheric evaporative demand and solar radiation consistently reduced tree growth. Drier forests and fast-growing species were more sensitive to water stress anomalies. In addition, species traits related to water use and photosynthesis partly explained differences in growth sensitivity to both climate means and anomalies. Our study demonstrates that both climate means and anomalies shape tree growth in tropical forests and that species traits can provide insights into understanding these demographic responses to climate change, offering a promising way forward to forecast tropical forest dynamics under different climate trajectories.

Exploring the role of life history traits and introduction effort in understanding invasion success in mammals: a case study of Barbary ground squirrels.

Invasive species-species that have successfully overcome the barriers of transport, introduction, establishment, and spread-are a risk to biodiversity and ecosystem function. Introduction effort is one of the main factors underlying invasion success, but life history traits are also important as they influence population growth. In this contribution, we first investigated life history traits of the Barbary ground squirrel, Atlantoxerus getulus, a species with a very low introduction effort. We then studied if their invasion success was due to a very fast life history profile by comparing their life history traits to those of other successful invasive mammals. Next, we examined whether the number of founders and/or a fast life history influences the invasion success of squirrels. Barbary ground squirrels were on the fast end of the "fast-slow continuum", but their life history was not the only contributing factor to their invasion success, as the life history profile is comparable to other invasive species that do not have such a low introduction effort. We also found that neither life history traits nor the number of founders explained the invasion success of introduced squirrels in general. These results contradict the concept that introduction effort is the main factor explaining invasion success, especially in squirrels. Instead, we argue that invasion success can be influenced by multiple aspects of the new habitat or the biology of the introduced species.

Comparing Life Histories across Taxonomic Groups in Multiple Dimensions: How Mammal-Like Are Insects?

Explaining variation in life histories remains a major challenge because they are multidimensional and there are many competing explanatory theories and paradigms. An influential concept in life-history theory is the fast-slow continuum, exemplified by mammals. Determining the utility of such concepts across taxonomic groups requires comparison of the groups' life histories in multidimensional space. Insects display enormous species richness and phenotypic diversity, but testing hypotheses like the fast-slow continuum has been inhibited by incomplete trait data. We use phylogenetic imputation to generate complete data sets of seven life-history traits in orthopterans (grasshoppers and crickets) and examine the robustness of these imputations for our findings. Three phylogenetic principal components explain 83%-96% of variation in these data. We find consistent evidence of an axis mostly following expectations of a fast-slow continuum, except that "slow" species produce larger, not smaller, clutches of eggs. We show that the principal axes of variation in orthopterans and reptiles are mutually explanatory, as are those of mammals and birds. Essentially, trait covariation in Orthoptera, with "slow" species producing larger clutches, is more reptilelike than mammal-like or birdlike. We conclude that the fast-slow continuum is less pronounced in Orthoptera than it is in birds and mammals, reducing the universal relevance of this pattern and the theories that predict it.

Bigger doesn't mean bolder: behavioral variation of four wild rodent species to novelty and predation risk following a fast-slow continuum.

BACKGROUND: Understanding how wild species respond to novel situations with associated risk can provide valuable insights for inter-specific behavioral variation and associations with pace-of-life (POL). Rodents, a globally distributed and diverse taxonomic group, have been the subjects of countless studies emulating risky situations. Controlled laboratory experiments with a focus on wild-caught species provide the opportunity to test fine-scale behavioral responses to contexts of risk with ecological implications. For example, assessing the importance of predator cues eliciting antipredator responses, as well as whether wild rodents embody behavioral plasticity and repertoires, illustrated by habituation and variation in behavioral traits, respectively. RESULTS: In this comparative study, we examined multiple behavioral responses of four rodent species in eastern Taiwan (three native species Mus caroli, Apodemus agrarius, Rattus losea, and one invasive, Rattus exulans) exposed to an unfamiliar microenvironment and novel cue from an allopatric predator, the leopard cat (Prionailurus bengalensis). All wild-caught animals were subjected to two consecutive nights of experimental trials in a laboratory setting. Behavioral responses to a novel situation during the first trial differed between species; smaller species investing more time in non-defensive behaviors compared to the larger species. More specifically, the smaller species M. caroli and A. agrarius allocated more time to exploration and foraging, whereas the larger rat species R. exulans and R. losea spent more time motionless or concealing. During the second trial, the addition of leopard cat cues did not elicit antipredator behaviors, but rather, rodents were found to exhibit increased non-defensive behaviors, specifically foraging efforts. CONCLUSIONS: Our results suggest that these four species do largely follow a behavioral fast-slow continuum with the two smaller mice species demonstrating increased boldness in a novel context compared to the larger rat species. Also, the wild populations of rodents in eastern Taiwan may be naïve to leopard cats. Finally, the rodents in our study demonstrated habituation to the microenvironment, indicating they possess adaptive capacity.

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 populations with fast life histories the onset of actuarial senescence was earlier and individuals aged at a faster rate than individuals in populations with 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.

Density-dependent survival varies with species life-history strategy in a tropical forest.

Species coexistence in diverse communities likely results from multiple interacting factors. Mechanisms such as conspecific negative density dependence (CNDD) and varying life-history strategies related to resource partitioning are known to influence plant fitness, and thereby community composition and diversity. However, we have little understanding of how these mechanisms interact and how they vary across life stages. Here, we document the interaction between CNDD and life-history strategy, based on growth-mortality trade-offs, from seedling to adult tree for 47 species in a tropical forest. Species' life-history strategies remained consistent across stages: fast-growing species had higher mortality than slow-growing species at all stages. In contrast, mean CNDD was strongest at early life stages (i.e. seedling, sapling). Fast-growing species tended to suffer greater CNDD than slow-growing species at several, but not all life stages. Overall, our results demonstrate that coexistence mechanisms interact across multiple life stages to shape diverse tree communities.

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 λs ) 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 λs 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.

Prey productivity and predictability drive different axes of life-history variation in carnivorous marsupials.

Variation in life-history strategies has usually been characterized as a single fast-slow continuum of life-history variation, in which mean lifespan increases with age at maturity as reproductive output at each breeding event declines. Analyses of plants and animals suggest that strategies of reproductive timing can vary on an independent axis, with iteroparous species at one extreme and semelparous species at the other. Insectivorous marsupials in the Family Dasyuridae have an unusually wide range of life-history strategies on both purported axes. We test and confirm that reproductive output and degree of iteroparity are independent in females across species. Variation in reproductive output per episode is associated with mean annual rainfall, which predicts food availability. Position on the iteroparity-semelparity axis is not associated with annual rainfall, but species in regions of unpredictable rainfall have longer maximum lifespans, more potential reproductive events per year, and longer breeding seasons. We suggest that these two axes of life-history variation arise because reproductive output is limited by overall food availability, and selection for high offspring survival favours concentrated breeding in seasonal environments. Longer lifespans are favoured when reproductive opportunities are dispersed over longer periods in environments with less predictable food schedules.

Life history tactics shape amphibians' demographic responses to the North Atlantic Oscillation.

Over the last three decades, climate abnormalities have been reported to be involved in biodiversity decline by affecting population dynamics. A growing number of studies have shown that the North Atlantic Oscillation (NAO) influences the demographic parameters of a wide range of plant and animal taxa in different ways. Life history theory could help to understand these different demographic responses to the NAO. Indeed, theory states that the impact of weather variation on a species' demographic traits should depend on its position along the fast-slow continuum. In particular, it is expected that NAO would have a higher impact on recruitment than on adult survival in slow species, while the opposite pattern is expected occur in fast species. To test these predictions, we used long-term capture-recapture datasets (more than 15,000 individuals marked from 1965 to 2015) on different surveyed populations of three amphibian species in Western Europe: Triturus cristatus, Bombina variegata, and Salamandra salamandra. Despite substantial intraspecific variation, our study revealed that these three species differ in their position on a slow-fast gradient of pace of life. Our results also suggest that the differences in life history tactics influence amphibian responses to NAO fluctuations: Adult survival was most affected by the NAO in the species with the fastest pace of life (T. cristatus), whereas recruitment was most impacted in species with a slower pace of life (B. variegata and S. salamandra). In the context of climate change, our findings suggest that the capacity of organisms to deal with future changes in NAO values could be closely linked to their position on the fast-slow continuum.

Fast-slow life history is correlated with individual differences in movements and prey selection in an aquatic predator in the wild.

Fast and slow life histories are proposed to covary with consistent individual differences in behaviour, but little is known whether it holds in the wild, where individuals experience natural fluctuations of the environment. We investigated whether individual differences in behaviour, such as movement traits and prey selection, are linked to variation in life-history traits in Eurasian perch (Perca fluviatilis) in the wild. Using high-resolution acoustic telemetry, we collected the positional data of fish in a whole natural lake and estimated individual movement traits by fitting a two-state correlated random walk model. Prey selection was inferred from stable isotope analysis using scale samples. Life-history traits were estimated by fitting a biphasic growth model to an individual growth trajectory back-calculated from scale samples. Life-history traits were correlated with behavioural traits such as movements and prey selection. Individuals with higher reproductive effort were found to switch more frequently between active and inactive modes and show greater reliance on prey from pelagic pathways (indicated by lower δ13 C). Further, individuals with faster juvenile growth were found to stay active for a longer time during the adult stage. Our results demonstrate the link between individual behavioural differences and fast-slow life-history traits under ecologically relevant conditions.

A bioenergetic framework for aboveground terrestrial food webs.

Bioenergetic approaches have been greatly influential for understanding community functioning and stability and predicting effects of environmental changes on biodiversity. These approaches use allometric relationships to establish species' trophic interactions and consumption rates and have been successfully applied to aquatic ecosystems. Terrestrial ecosystems, where body mass is less predictive of plant-consumer interactions, present inherent challenges that these models have yet to meet. Here, we discuss the processes governing terrestrial plant-consumer interactions and develop a bioenergetic framework integrating those processes. Our framework integrates bioenergetics specific to terrestrial plants and their consumers within a food web approach while also considering mutualistic interactions. Such a framework is poised to advance our understanding of terrestrial food webs and to predict their responses to environmental changes.

Investigating the Relationship Between Body Shape and Life History Traits in Toothed Whales: Can Body Shape Predict Fast-Slow Life Histories?

A widespread pattern in vertebrate life-history evolution is for species to evolve towards either fast or slow life histories; however, the underlying causes of this pattern remain unclear. Toothed whales (Odontoceti) are a diverse group with a range of body sizes and life histories, making them an ideal model to investigate potential drivers of this dichotomy. Using ancestral reconstruction, we identified that certain groups of odontocetes evolved more-streamlined, presumably faster, body shapes around the same time that killer whales (Orcinus orca) evolved into whale predators approximately 1 Mya during the Pleistocene. This suggests that the evolution of a streamlined body shape may have been an adaptation to escape killer whale predation, leading to longer life-history events. To test this hypothesis, we performed a cluster analysis of odontocete whales and confirmed the dual pattern of life-history traits, with one group referred to as 'reproducers' characterized by early age of maturity, short gestation, short interbirth interval, and short lifespan, and the other group referred to as 'bet-hedgers' exhibiting the opposite pattern. However, we found that life history grouping was relatively unrelated to whale shape (i.e., more streamlined or less streamlined). Therefore, we incorporated principal component results into mixed effects models, and the model results indicated that body shape was positively related to neonate length (a measure of investment in progeny), but not significantly related to the temporal life-history traits. Thus, whale body shape is not a sufficient explanation for the evolution of fast-slow life histories in odontocete whales. Supplementary Information: The online version contains supplementary material available at 10.1007/s11692-023-09605-4.

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.

A Double-Track Pathway to Fast Strategy in Humans and Its Personality Correlates.

The fast-slow paradigm of life history (LH) focuses on how individuals grow, mate, and reproduce at different paces. This paradigm can contribute substantially to the field of personality and individual differences provided that it is more strictly based on evolutionary biology than it has been so far. Our study tested the existence of a fast-slow continuum underlying indicators of reproductive effort-offspring output, age at first reproduction, number and stability of sexual partners-in 1,043 outpatients with healthy to severely disordered personalities. Two axes emerged reflecting a double-track pathway to fast strategy, based on restricted and unrestricted sociosexual strategies. When rotated, the fast-slow and sociosexuality axes turned out to be independent. Contrary to expectations, neither somatic effort-investment in status, material resources, social capital, and maintenance/survival-was aligned with reproductive effort, nor a clear tradeoff between current and future reproduction was evident. Finally, we examined the association of LH axes with seven high-order personality pathology traits: negative emotionality, impulsivity, antagonism, persistence-compulsivity, subordination, and psychoticism. Persistent and disinhibited subjects appeared as fast-restricted and fast-unrestricted strategists, respectively, whereas asocial subjects were slow strategists. Associations of LH traits with each other and with personality are far more complex than usually assumed in evolutionary psychology.

Life-history strategy and extinction risk in the warm desert perennial spring ephemeral Astragalus holmgreniorum (Fabaceae).

This study of Astragalus holmgreniorum examines its adaptations to the warm desert environment and whether these adaptations will enable it to persist. Its spring ephemeral hemicryptophyte life-history strategy is unusual in warm deserts. We used data from a 22-year demographic study supplemented with reproductive output, seed bank, and germinant survival studies to examine the population dynamics of this species using discrete-time stochastic matrix modeling. The model showed that A. holmgreniorum is likely to persist in the warm desert in spite of high dormant-season mortality. It relies on a stochastically varying environment with high inter-annual variation in precipitation for persistence, but without a long-lived seed bank, environmental stochasticity confers no advantage. Episodic high reproductive output and frequent seedling recruitment along with a persistent seed bank are adaptations that facilitate its survival. These adaptations place its life-history strategy further along the spectrum from "slower" to "faster" relative to other perennial spring ephemerals. The extinction risk for small populations is relatively high even though mean λ s > 1 because of the high variance in year quality. This risk is also strongly dependent on seed bank starting values, creating a moving window of extinction risk that varies with population size through time. Astragalus holmgreniorum life-history strategy combines the perennial spring ephemeral life form with features more characteristic of desert annuals. These adaptations permit persistence in the warm desert environment. A promising conclusion is that new populations of this endangered species can likely be established through direct seeding.