The relative importance of life-history variables to population growth rate in mammals: Cole's prediction revisited

The relative importance of life-history variables to population growth rate (lambda) has substantial consequences for the study of life-history evolution and for the dynamics of biological populations. Using life-history data for 142 natural populations of mammals, we estimated the elasticity of lambda to changes in age at maturity (alpha), age at last reproduction (omega), juvenile survival (Pj), adult survival (Pa), and fertility (F). Elasticities were then used to quantify the relative importance of alpha, omega, Pj, Pa, and F to lambda and to test theoretical predictions regarding the relative influence on lambda of changes in life-history variables. Neither alpha nor any other single life-history variable had the largest relative influence on lambda in the majority of the populations, and this pattern did not change substantially when effects of phylogeny and body size were statistically removed. Empirical support for theoretical predictions was poor at best. However, analyses of elasticities on the basis of the magnitude (F) and onset (alpha) of reproduction revealed that alpha, followed by F, had the largest relative influence on lambda in populations characterized by early maturity and high reproductive rates, or when F/alpha > 0.60. When maturity was delayed and reproductive rates were low, or when F/alpha < 0.15, survival rates were overwhelmingly most influential, and reproductive parameters (alpha and F) had little relative influence on lambda. Population dynamic consequences of likely responses of biological populations to perturbations in life-history variables are examined, and predictions are made regarding the numerical dynamics of age-structured populations on the basis of values of the F/alpha ratio.     

Age at the onset of senescence in birds and mammals is predicted by early-life performance

Life-history theory predicts that traits involved in maturity, reproduction and survival correlate along a fast–slow continuum of life histories. Evolutionary theories and empirical results indicate that senescence-related traits vary along this continuum, with slow species senescing later and at a slower pace than fast species. Because senescence patterns are typically difficult to estimate from studies in the wild, here we propose to predict the associated trait values in the frame of life-history theory. From a comparative analysis based on 81 free-ranging populations of 72 species of birds and mammals, we find that a nonlinear combination of fecundity, age at first reproduction and survival over the immature stage can account for ca two-thirds of the variance in the age at the onset of actuarial senescence. Our life-history model performs better than a model predicting the onset based on generation time, and it only includes life-history traits during early life as explanatory variables, i.e. parameters that are both theoretically expected to shape senescence and are measurable within relatively short studies. We discuss the good-fit of our life-history model to the available data in the light of current evolutionary theories of senescence. We further use it to evaluate whether studies that provided no evidence for senescence lasted long enough to include the onset of senescence.     

Energetics and life-history of bats in comparison to small mammals

Mammals can be aligned along a slow-fast life-history continuum and a low–high metabolic rate continuum based on their traits. Small non-volant mammals occupy the fast/high end in both continua with high reproductive rates and short life spans linked with high mass-specific metabolic rates. Bats occupy the high end of the metabolic continuum, but the slow end of the life-history continuum with low reproductive rates and long life spans. Typically, both continua are linked, and similar life-history traits of species are reflected in more similar metabolic rates. We therefore hypothesized that metabolic rates are similar in species with similar life-history traits. Resting metabolic rates (RMR) were measured for three ecologically and morphologically similar sympatric bat species (Myotis nattereri, M. bechsteinii, and Plecotus auritus; Vespertilionidae) and compared to data from other similar-sized, temperate insectivorous mammals with other life-history strategies. The bat species share similar life-histories and RMRs, both of which differ from the remaining mammals and therefore supporting our hypothesis. To verify that bats are similar in RMR, two energetically contrasting periods were compared. RMRs in post-lactating females did not differ between bat species. It was, however, positively correlated with parasite load in both Myotis species. However, RMRs differed during energy-demanding pregnancy where M. nattereri had the significantly lowest RMR, suggesting metabolic compensation as an energy-saving strategy. We conclude that the energy requirements of bat species with similar life-history traits resemble each other during periods of low energetic demands and are more similar to each other than to other small temperate mammals.     

Stochastic population dynamics and life-history variation in marine fish species

Abstract We examined whether differences in life-history characteristics can explain interspecific variation in stochastic population dynamics in nine marine fish species living in the Barents Sea system. After observation errors in population estimates were accounted for, temporal variability in natural mortality rate, annual recruitment, and population growth rate was negatively related to generation time. Mean natural mortality rate, annual recruitment, and population growth rate were lower in long-lived species than in short-lived species. Thus, important species-specific characteristics of the population dynamics were related to the species position along the slow-fast continuum of life-history variation. These relationships were further associated with interspecific differences in ecology: species at the fast end were mainly pelagic, with short generation times and high natural mortality, annual recruitment, and population growth rates, and also showed high temporal variability in those demographic traits. In contrast, species at the slow end were long-lived, deepwater species with low rates and reduced temporal variability in the same demographic traits. These interspecific relationships show that the life-history characteristics of a species can predict basic features of interspecific variation in population dynamical characteristics of marine fish, which should have implications for the choice of harvest strategy to facilitate sustainable yields.     

Ancestral populations perform better in a novel environment: domestication of medfly populations from five global regions

Geographically isolated populations of a species may differ in several aspects of life-history, morphology, behavior, and genetic structure as a result of adaptation in ecologically diverse habitats. We used a global invasive species, the Mediterranean fruit fly to investigate, whether adaptation to a novel environment differs among geographically isolated populations that vary in major life history components such as life span and reproduction. We used wild populations from five global regions (Kenya, Hawaii, Guatemala, Portugal, and Greece). Adult demographic traits were monitored in F(2), F(5), F(7) and F(9) generations in captivity. Although domestication in constant laboratory conditions had a different effect on the mortality and reproductive rates of the different populations, a general trend of decreasing life span and age of first reproduction was observed for most medfly populations tested. However, taking into account longevity of both sexes, age-specific reproductive schedules, and average reproductive rates we found that the ancestral Kenyan population kept the above life history traits stable during domestication compared to the other populations tested. These findings provide important insights in the life-history evolution of this model species, and suggest that ancestral medfly populations perform better than the derived - invasive ones in a novel environment.     

DO VARIATIONS IN SUBSTITUTION RATES AND MALE MUTATION BIAS CORRELATE WITH LIFE‐HISTORY TRAITS? A STUDY OF 32 MAMMALIAN GENOMES

Life-history traits vary substantially across species, and have been demonstrated to affect substitution rates. We compute genome-wide, branch-specific estimates of male mutation bias (the ratio of male-to-female mutation rates) across 32 mammalian genomes and study how these vary with life-history traits (generation time, metabolic rate, and sperm competition). We also investigate the influence of life-history traits on substitution rates at unconstrained sites across a wide phylogenetic range. We observe that increased generation time is the strongest predictor of variation in both substitution rates (for which it is a negative predictor) and male mutation bias (for which it is a positive predictor). Although less significant, we also observe that estimates of metabolic rate, reflecting replication-independent DNA damage and repair mechanisms, correlate negatively with autosomal substitution rates, and positively with male mutation bias. Finally, in contrast to expectations, we find no significant correlation between sperm competition and either autosomal substitution rates or male mutation bias. Our results support the important but frequently opposite effects of some, but not all, life-history traits on substitution rates.     

Life history trade-offs are more pronounced for a noninvasive,native butterfly compared to its invasive,exotic congener

Life history trade-offs are ubiquitous in nature. Life history theory posits that these trade-offs arise from individuals having limited resources to allocate toward all vital functions, such as survival, growth and reproduction. These trade-offs position most species along a slow-fast life history continuum, where individuals with slow life histories often have higher survival at the cost of delayed reproduction and individuals with fast life histories often live faster and die younger. However, these trade-offs are sometimes less obvious for invasive species. Here, we constructed age-based population models to compare life history strategies and trade-offs between the noninvasive, native mustard white and invasive, exotic cabbage white (Pieris spp.) butterflies. We found that the cabbage white has faster larval growth and higher fecundity at younger ages, suggesting it has a fast life history compared to the mustard white. However, cabbage white also has higher adult survival at younger ages, suggesting that it experiences weaker trade-offs among vital rates than its native counterpart. Our study illustrates the importance of demographic studies in evaluating life history strategies among congener species with different population histories, and emphasizes the many advantages experienced by invasive species in their novel environments.     

Buffering and plasticity in vital rates of oldfield rodents

1. Under the hypothesis of environmental buffering, populations are expected to minimize the variance of the most influential vital rates; however, this may not be a universal principle. Species with a life span <1 year may be less likely to exhibit buffering because of temporal or seasonal variability in vital rate sensitivities. Further, plasticity in vital rates may be adaptive for species in a variable environment with reliable cues. 2. We tested for environmental buffering and plasticity in vital rates using stage-structured matrix models from long-term data sets in four species of grassland rodents. We used periodic matrices to estimate stochastic elasticity for each vital rate and then tested for correlations with a standardized coefficient of variation for each rate. 3. We calculated stochastic elasticities for individual months to test for an association between increased reproduction and the influence of reproduction, relative to survival, on the population growth rate. 4. All species showed some evidence of buffering. The elasticity of vital rates of Peromyscus leucopus (Rafinesque, 1818), Sigmodon hispidus Say & Ord, 1825 and Microtus ochrogaster (Wagner, 1842) was negatively related to vital rate CV. Elasticity and vital rate CV were negatively related in Peromyscus maniculatus (Wagner, 1845), but the relationship was not statistically significant. Peromyscus leucopus and M. ochrogaster showed plasticity in vital rates; reproduction was higher following months where elasticity for reproduction exceeded that of survival. 5. Our results suggest that buffering is common in species with fast life histories; however, some populations that exhibit buffering are capable of responding to short-term variability in environmental conditions through reproductive plasticity.     

From stochastic environments to life histories and back

Environmental stochasticity is known to play an important role in life-history evolution, but most general theory assumes a constant environment. In this paper, we examine life-history evolution in a variable environment, by decomposing average individual fitness (measured by the long-run stochastic growth rate) into contributions from average vital rates and their temporal variation. We examine how generation time, demographic dispersion (measured by the dispersion of reproductive events across the lifespan), demographic resilience (measured by damping time), within-year variances in vital rates, within-year correlations between vital rates and between-year correlations in vital rates combine to determine average individual fitness of stylized life histories. In a fluctuating environment, we show that there is often a range of cohort generation times at which the fitness is at a maximum. Thus, we expect ‘optimal’ phenotypes in fluctuating environments to differ from optimal phenotypes in constant environments. We show that stochastic growth rates are strongly affected by demographic dispersion, even when deterministic growth rates are not, and that demographic dispersion also determines the response of life-history-specific average fitness to within- and between-year correlations. Serial correlations can have a strong effect on fitness, and, depending on the structure of the life history, may act to increase or decrease fitness. The approach we outline takes a useful first step in developing general life-history theory for non-constant environments.     

Fold or hold: experimental evolution in vitro

We introduce a system for experimental evolution consisting of populations of short oligonucleotides (Oli populations) evolving in a modified quantitative polymerase chain reaction (qPCR). It is tractable at the genetic, genomic, phenotypic and fitness levels. The Oli system uses DNA hairpins designed to form structures that self‐prime under defined conditions. Selection acts on the phenotype of self‐priming, after which differences in fitness are amplified and quantified using qPCR. We outline the methodological and bioinformatics tools for the Oli system here and demonstrate that it can be used as a conventional experimental evolution model system by test‐driving it in an experiment investigating adaptive evolution under different rates of environmental change.     

Demography of squirrel monkeys (Saimiri sciureus) in captive environments and its effect on population growth

Understanding which life-history variables have the greatest influence on population growth rate has great ecological and conservation importance. Applying models of population regulation and demographic mechanisms can aid management and conservation of both wild and captive populations. By comparisons of sensitivity, elasticity, and life-table response analyses, we identified demographic processes that were most likely to produce changes in population size (via prospective analyses) and the traits that actually influenced population changes (via retrospective analyses) among sexes, zoological facilities, and generations of captive squirrel monkey populations (Saimiri sciureus). Variation in life-history traits occurs within each group analyzed. Those traits that vary the most include age at maturity, age at last reproduction, and fertility. Zoos with increasing population growth rates maintain earlier ages of maturity, later ages of last reproduction, high rates of juvenile and adult survival, and most importantly greater fertility, reflecting shorter inter-birth intervals. Using prospective analyses, juvenile and adult survivals were predicted to be demographic traits with the greatest effect on population growth. Surprisingly, and despite predictions, retrospective analyses revealed that fertility was the life-history characteristic trait that contributed the most to changes in population size.     

The fast-slow continuum in mammalian life history: an empirical reevaluation

Many life-history traits co-vary across species, even when body size differences are controlled for. This phenomenon has led to the concept of a "fast-slow continuum," which has been influential in both empirical and theoretical studies of life-history evolution. We present a comparative analysis of mammalian life histories showing that, for mammals at least, there is not a single fast-slow continuum. Rather, both across and within mammalian clades, the speed of life varies along at least two largely independent axes when body size effects are removed. One axis reflects how species balance offspring size against offspring number, while the other describes the timing of reproductive bouts.     

Population Dynamics of the Andean Lizard Anolis heterodermus: Fast‐slow Demographic Strategies in Fragmented Scrubland Landscapes

Habitat fragmentation and loss affect population stability and demographic processes, increasing the extinction risk of species. We studied Anolis heterodermus populations inhabiting large and small Andean scrubland patches in three fragmented landscapes in the Sabana de Bogotá (Colombia) to determine the effect of habitat fragmentation and loss on population dynamics. We used the capture‐mark‐recapture method and multistate models to estimate vital rates for each population. We estimated growth population rate and the most important processes that affect λ by elasticity analysis of vital rates. We tested the effects of habitat fragmentation and loss on vital rates of lizard populations. All six isolated populations showed a positive or an equilibrium growth rate (λ = 1), and the most important demographic process affecting λ was the growth to first reproduction. Populations from landscapes with less scrubland natural cover showed higher stasis of young adults. Populations in highly fragmented landscapes showed highest juvenile survival and growth population rates. Independent of the landscape's habitat configuration and connectivity, populations from larger scrubland patches showed low adult survivorship, but high transition rates. Populations varied from a slow strategy with low growth and delayed maturation in smaller patches to a fast strategy with high growth and early maturation in large patches. This variation was congruent with the fast‐slow continuum hypothesis and has serious implications for Andean lizard conservation and management strategies. We suggest that more stable lizard populations will be maintained if different management strategies are adopted according to patch area and habitat structure.     

Lifespan of a Ceratitis fruit fly increases with higher altitude

Variation in lifespan may be linked to geographic factors. While latitudinal variation in lifespan has been studied for a number of species, altitude variation has received much less attention, particularly in insects. We measured the lifespan of different populations of the Natal fruit fly Ceratitis rosa along an altitudinal cline. For the different populations we first measured the residual longevity of wild flies by captive cohort approach and compared F(1) generation from the same populations. We showed an increase in lifespan with higher altitude for a part of our data. For the field collected flies (F0) the average remaining lifespan increased monotonically with altitude for males but not for females. For the F(1) generation, longevity of both males and females of the highest-altitude population was longer than for the two other lower-altitude populations. This relationship between altitude and lifespan may be explained by the effects of temperature on reproduction. Reproductive schedules in insects are linked to temperature: lower temperature, characteristic of high-altitude sites, generally slows down reproduction. Because of a strong trade-off between reproduction and longevity, we therefore observed a longer lifespan for the high- altitude populations. Other hypotheses such as different predation rates in the different sites are also discussed.     

Convergent maternal care strategies in ungulates and macropods

Mammals show extensive interspecific variation in the form of maternal care. Among ungulates, there is a dichotomy between species in which offspring follow the mother ("following" strategy) versus species in which offspring remain concealed ("hiding" strategy). Here we reveal that the same dichotomy exists among macropods (kangaroos, wallabies and allies). We test three traditional adaptive explanations and one new life history hypothesis, and find very similar patterns among both ungulates and macropods. The three traditional explanations that we tested were that a "following" strategy is associated with (1) open habitat, (2) large mothers, and (3) gregariousness. Our new life-history hypothesis is that a "following strategy" is associated with delayed weaning, and thus with the "slow" end of the slow-fast mammalian life-history continuum, because offspring devote resources to locomotion rather than rapid growth. Our comparative test strongly supports the habitat structure hypothesis and provides some support for this new delayed weaning hypothesis for both ungulates and macropods. We propose that sedentary young in closed habitats benefit energetically by having milk brought to them. In open habitats, predation pressure will select against hiding. Followers will suffer slower growth to independence. Taken together, therefore, our results provide the first quantitative evidence that macropods and ungulates are convergent with respect to interspecific variation in maternal care strategy. In both clades, differences between species in the form of parental care are due to a similar interaction between habitat, social behavior, and life history.     

Intraspecific hybridization and the recovery of fitness in the native legume Chamaecrista fasciculata

Genetic incompatibilities and low offspring fitness are characteristic outcomes of hybridization between species. Yet, the creative potential of recombination following hybridization continues to be debated. Here we quantify the outcome of hybridization and recombination between adaptively divergent populations of the North American legume Chamaecrista fasciculata in a large-scale field experiment. Previously, hybrids between these populations demonstrated hybrid breakdown, suggesting the expression of adaptive epistatic interactions underlying population genetic differentiation. However, the outcome of hybridization ultimately rests on the performance of even later generation recombinants. In experiments that compared the performance of recombinant F6 and F2 generations with nonrecombinant F1 and parental genotypes, we observed that increasing recombination had contrasting effects on different life-history components. Lifetime fitness, defined as the product of survivorship and reproduction, showed a strong recovery of fitness in the F6. The overall gain in fitness with increased recombination suggests that hybridization and recombination may provide the necessary genetic variation for adaptive evolution within species. We discuss the mechanisms that may account for the gain in fitness with recombination, and explore the implications for hybrid speciation and phenotypic evolution.     

Life-history changes that accompany the transition from sexual to parthenogenetic reproduction in Drosophila mercatorum

In spite of the predicted genetic and ecological costs of sex, most natural populations maintain sexual reproduction, even those capable of facultative parthenogenesis. Unfertilized eggs from natural populations of Drosophila mercatorum occasionally develop into viable adults, but obligately parthenogenetic populations are unknown in this species. To evaluate the microevolutionary forces that both favor and constrain the evolution of parthenogenesis in D. mercatorum, we have measured parthenogenetic rates across a natural, sexually reproducing population and characterized the life-history changes that accompany the transition from sexual to parthenogenetic reproduction in laboratory strains. A highly significant difference in parthenogenetic rate was found between two populations in close geographic proximity, with increased rate found with lower population density. Laboratory strains of parthenogenetic females suffered increased mortality and reduced egg viability relative to their virgin counterparts from a sexual strain. Lifetime egg production was similar across all strains, but a shift in peak egg production to an earlier age also occurred. The combination of these life-history traits resulted in a higher net reproductive value for sexual females, but because they also had a longer generation time, intrinsic rate of increase was not as dramatically different from parthenogenetic females. In environments with high early mortality, there may be no fitness disadvantage to parthenogenesis, but the predicted ecological advantage of a twofold increase in intrinsic rate of increase was not realized. These results support the theory of Stalker (1956) that parthenogenesis is favored in environments in which sexual reproduction is difficult or impossible.     

Effect of habitat permanence on life-history: extending the Daphnia model into new climate spaces

We use an Australian freshwater invertebrate species, Daphnia carinata, to assess whether variation in habitat permanence influences life-history traits in subpopulations. Using a life table experiment, we measure the life-history traits of populations from both permanent and temporary pools. We show that these habitat classes are associated with clear differences in important life-history traits and evidence of trade-offs in important traits influencing reproduction, diapause, and growth rate and suggest this is evidence for local adaptation. Here we use Daphnia from Australian populations spanning semi-arid and temperate climates generating results that are in broad agreement with similar studies in the northern hemisphere, and so extend these results to a new continent and its particular climate. Variation in habitat permanence, it appears, is a very general driver of life-history divergence.

     

Interpopulation variation in life-history traits of Poeciliopsis prolifica: implications for the study of placental evolution

Placental reproduction is widespread across vertebrate taxa, but little is known about its life-history correlates and putative adaptive value. We studied variation in life-history traits in two populations of the placental poeciliid fish Poeciliopsis prolifica to determine whether differences in post-fertilization maternal provisioning to embryos have a genetic basis and how food availability affects reproduction. Life histories were characterized for wild-caught females and for second-generation lab-born females raised under two levels of food availability. We found that the two populations did not differ significantly in the wild for any life-history traits except for the lipid dry weight in females and in embryos at an advanced stage of development. When environmental effects were experimentally controlled, however, populations exhibited significant differences in several traits, including the degree of maternal provisioning to embryos. Food availability significantly affected female size at first parturition, brood size and offspring dry weight at birth. Altogether, these results demonstrate that population differences in maternal provisioning and other life-history traits have a genetic basis and show a plastic response to food availability. We infer that phenotypic plasticity may mask population differences in the field. In addition, when comparing life-history patterns in these two populations with known patterns in placental and non-placental poeciliids, our results support the hypotheses that placentation is an adaptive reproductive strategy under high-resource conditions but that it may represent a cost under low-food conditions. Finally, our results highlight that age at maturity and reproductive allotment may be key life-history traits accompanying placental evolution.     

Exploiting a window in time. Fate of recruiting populations of two rare fire-dependent Geranium species after forest fire

Fire ephemerals are few in the boreal forest despite a long history of recurrent fires, which suggests such a life-history pose problems here. We analysed the fate of recruiting populations of two rare and fire-dependent annual Geranium species at burnt forest sites in South-eastern Sweden, to extract vital information on their life-history. Seedlings emerged from the soil seed bank only in the year of fire but spread over several weeks. At sites that burnt early in the season, some seedlings exhibited a summer-annual life-cycle, but those were less successful than plants at the same sites that delayed reproduction until the following year (winter-annuals). Herbivory was frequent in the fire year and until the following spring, but later almost absent, and thus hit seed production in summer-annuals badly. Winter mortality was highly variable for rosette-stage winter-annuals, with some populations nearly obliterated. Reproductive success varied greatly between populations mainly due to pre-reproductive mortality, with a return of 0.2–395 (average 79) seeds per seedling. The vast majority of seeds (92–100 %) were produced by the primary generation, emerging from the seed bank. Out of this first seed crop, 0.2–2.5 % germinated within the study period, resulting in secondary generations. Plants in these later generations were small and produced few seeds, showing that the opportunity for high reproductive success is essentially restricted to one year only. This makes populations highly vulnerable to local near-complete reproductive failure due to winter mortality and herbivory and may be the ultimate reason why strict fire ephemerals are so few in northern forests.