Consequences of hierarchical allocation for the evolution of life-history traits

Resource allocation within individuals may often be hierarchical, and this may have important effects on genetic correlations and on trait evolution. For example, organisms may divide energy between reproduction and somatic growth and then subdivide reproductive resources. Genetic variation in allocation to pathways early in such hierarchies (e.g., reproduction) can cause positive genetic correlations between traits that trade off (e.g., offspring size and number) because some individuals invest more resources in reproduction than others. We used quantitative-genetic models to explore the evolutionary implications of allocation hierarchies. Our results showed that when variation in allocation early in the hierarchy exceeds subsequent variation in allocation, genetic covariances and initial responses to selection do not reflect trade-offs occurring at later levels in the hierarchy. This general pattern was evident for many starting allocations and optima and for whether traits contributed multiplicatively or additively to fitness. Finally, artificial selection on a single trait revealed masked trade-offs when variation in early allocation was comparable to subsequent variation in allocation. This result confirms artificial selection as a powerful, but not foolproof, method of detecting trade-offs. Thus, allocation hierarchies can profoundly affect life-history evolution by causing traits to evolve in the opposite direction to that predicted by trade-offs.     

The influence of juvenile and adult environments on life-history trajectories

There is increasing evidence that the environment experienced early in life can strongly influence adult life histories. It is largely unknown, however, how past and present conditions influence suites of life-history traits regarding major life-history trade-offs. Especially in animals with indeterminate growth, we may expect that environmental conditions of juveniles and adults independently or interactively influence the life-history trade-off between growth and reproduction after maturation. Juvenile growth conditions may initiate a feedback loop determining adult allocation patterns, triggered by size-dependent mortality risk. I tested this possibility in a long-term growth experiment with mouthbrooding cichlids. Females were raised either on a high-food or low-food diet. After maturation half of them were switched to the opposite treatment, while the other half remained unchanged. Adult growth was determined by current resource availability, but key reproductive traits like reproductive rate and offspring size were only influenced by juvenile growth conditions, irrespective of the ration received as adults. Moreover, the allocation of resources to growth versus reproduction and to offspring number versus size were shaped by juvenile rather than adult ecology. These results indicate that early individual history must be considered when analysing causes of life-history variation in natural populations.     

Comparative analysis of phylogenetic and fishing effects in life history patterns of teleost fishes

The effects of fishing on life history traits and life history strategies of teleost fishes are analysed by a new comparative method that splits traits into an allometric part (size effect), an autoregressive phylogenetic component, and an environmental component (fishing effect). Both intra- and inter-specific variation of age and size at maturity, fecundity, adult size and egg size are analysed by comparing 84 populations of 49 species submitted to various fishing pressures. Two axes of life history diversification are found among teleosts. One is the well-known slow-fast continuum separating short-lived and early maturing species (like Clupeiformes) from longer-lived species that mature late relative to their size and spawn larger eggs (like salmonids or Scorpaeniformes). An additional strategy involves the schedule of resource allocation to growth and reproduction. Indeterminate growth allows higher teleosts (e.g. Gadiformes) to reach a large size while maturing early and laying small eggs. Increasing fishing pressure decreases age at maturity and egg size, and increases fecundity at maturity, the slope of the fecundity-length relationship and relative size at maturity. These compensations for higher adult mortality differ among life history strategies. Indeterminate growth is associated with a greater flexibility in resource allocation to growth and reproduction that facilitates greater resilience to fishing mortality.     

Effects of parasitic castration on plant resource allocation

It has been proposed that host castration is a parasite strategy to reallocate host resources from reproductive to vegetative functions to increase parasite fitness. Since resource partitioning between reproduction and vegetative growth can affect host life-history traits, parasite effects on resource allocation can affect both plant fitness and host-parasite coevolution. Field and greenhouse experiments were used to investigate the effects of host castration by the fungus Atkinsonella hypoxylon on the resource allocation and architecture of the grass Danthonia spicata. The results indicate that non-infected D. spicata can reallocate resources from reproduction to vegetative growth when resource allocation to reproduction is prevented. However, I found no evidence that fungal castration causes reallocation of resources from host reproduction to vegetative growth. Instead, infection reduces host biomass and the fungus directly utilizes resources that would have been used for host reproduction for its own reproduction. Received: 25 March 1999 / Accepted: 24 October 1999     

Changes in reproductive investment with altitude in an alpine plant

Aims In perennial species, the allocation of resources to reproduction results in a reduction of allocation to vegetative growth and, therefore, impacts future reproductive success. As a consequence, variation in this trade-off is among the most important driving forces in the life-history evolution of perennial plants and can lead to locally adapted genotypes. In addition to genetic variation, phenotypic plasticity might also contribute to local adaptation of plants to local conditions by mediating changes in reproductive allocation. Knowledge on the importance of genetic and environmental effects on the trade-off between reproduction and vegetative growth is therefore essential to understand how plants may respond to environmental changes.Methods We conducted a transplant experiment along an altitudinal gradient from 425 to 1?921 m in the front range of the Western Alps of Switzerland to assess the influence of both altitudinal origin of populations and altitude of growing site on growth, reproductive investment and local adaptation in Poa alpina .Important findings In our study, the investment in reproduction increased with plant size. Plant growth and the relative importance of reproductive investment decreased in populations originating from higher altitudes compared to populations originating from lower altitudes. The changes in reproductive investment were mainly explained by differences in plant size. In contrast to genetic effects, phenotypic plasticity of all traits measured was low and not related to altitude. As a result, the population from the lowest altitude of origin performed best at all sites. Our results indicate that in P. alpina genetic differences in growth and reproductive investment are related to local conditions affecting growth, i.e. interspecific competition and soil moisture content.     

Phenology and fecundity in 11 sympatric pioneer species of Macaranga (Euphorbiaceae)in Borneo

Reproductive traits of tropical tree species vary predictably in relation to successional stage, but this variation may be due to the species' phylogenetic histories rather than selective pressures imposed by regeneration requirements. Reproductive phenology, tree size at the onset of reproduction, and fecundity of 11 sympatric, closely related Macaranga species were studied to investigate within-species variation in reproductive traits in relation to resource availability, and among-species variation in relation to other life-history traits (shade tolerance, seed size and maximum tree size, H(max)) and consequently the requirements for forest-gap colonization. Nine species reproduced in synchronous episodes, and two species reproduced continuously over 32 mo. Episodic reproduction was most intense in 1992 following a severe drought. For several species, reproductive trees had greater light availability, lower fecundity in lower light levels, and lower growth rates than nonreproductive trees, reflecting resource-limited reproduction. Among species, H(max) was negatively correlated with shade tolerance and seed size. Tree size at the onset of reproduction and fecundity was strongly linked to this axis of life-history variation, but phenological pattern was not. Absolute tree size at the onset of reproduction was positively correlated with H(max) and negatively correlated with shade tolerance. Relative size at reproductive onset was not correlated with shade tolerance or H(max). Fecundity ranged four orders of magnitude among species and was correlated positively with H(max) and negatively with seed size and shade tolerance. The interrelationships among these reproductive and other life-history traits are strongly correlated with the species' requirements for gap colonization.     

Age and season impact resource allocation to eggs and nesting behavior in the painted turtle

Theory predicts that in long-lived organisms females should invest less energy in reproduction and more in growth and self-maintenance early in life, with this balance shifting as females age and the relative value of each reproductive event increases. We investigated this potential trade-off by characterizing within-population variation in resource allocation to eggs by female painted turtles (Chrysemys picta) and relating this variation to their nesting ecology and life history. We examined lipid and protein allocation to yolks, accounting for both relative female age and seasonal effects (first vs. second clutches within a female). Older females appear to increase their investment in reproduction by producing larger eggs, but these eggs are not disproportionately more lipid or protein rich than the smaller eggs from younger females. Within the nesting season, first clutches have more lipid and protein than second clutches. We also found that younger females nest closer to the water than older females. Our results indicate that trade-offs involving resource allocation and nesting behavior do occur both seasonally and with age, suggesting ontogenetic variation in life-history strategies in this long-lived organism.     

Reproductive allometry and the size-number trade-off for lizards

Fundamental to life-history theory is the assumed inverse proportionality between the number of offspring and the resource allocation per offspring. Lizards have been model organisms for empirical tests of this theory for decades; however, the expected negative relationship between clutch size and offspring size is often not detected. Here we use the approach developed by Charnov and Ernest to demonstrate that this often concealed trade-off can be made apparent in an interspecific comparison by correcting for size-dependent resource allocation. Our data set also shows a tight allometry for annual production that is consistent with life-history models for indeterminate growers. To account for nonindependence of species data we also compare the fit of nonphylogenetic and phylogenetic regression models to test for phylogenetic signal in these allometry and trade-off patterns. When combined, these results demonstrate that the offspring size/clutch size trade-off is not isolated to a single clutch but is shaped by the resource investment made over an entire year. We conclude that, across diverse lizard species, there is strong evidence for the predicted trade-off between offspring size and the annual number of eggs produced.     

Phylogeny determines flower size‐dependent sex allocation at flowering in a hermaphroditic family

• In animal‐pollinated hermaphroditic plants, optimal floral allocation determines relative investment into sexes, which is ultimately dependent on flower size. Larger flowers disproportionally increase maleness whereas smaller and less rewarding flowers favour female function. Although floral traits are considered strongly conserved, phylogenetic relationships in the interspecific patterns of resource allocation to floral sex remain overlooked. We investigated these patterns in Cistaceae, a hermaphroditic family.
• We reconstructed phylogenetic relationships among Cistaceae species and quantified phylogenetic signal for flower size, dry mass and nutrient allocation to floral structures in 23 Mediterranean species using Blomberg's K‐statistic. Lastly, phylogenetically‐controlled correlational and regression analyses were applied to examine flower size‐based allometry in resource allocation to floral structures.
• Sepals received the highest dry mass allocation, followed by petals, whereas sexual structures increased nutrient allocation. Flower size and resource allocation to floral structures, except for carpels, showed a strong phylogenetic signal. Larger‐flowered species allometrically allocated more resources to maleness, by increasing allocation to corollas and stamens.
• Our results suggest a major role of phylogeny in determining interspecific changes in flower size and subsequent floral sex allocation. This implies that flower size balances the male–female function over the evolutionary history of Cistaceae. While allometric resource investment in maleness is inherited across species diversification, allocation to the female function seems a labile trait that varies among closely related species that have diversified into different ecological niches.

     

Body size and the timing of egg production in parasitoid wasps

In insects several key fitness-related variables are positively correlated with intraspecific variation in body size, but little is known about size-related variation in the timing of egg production within species. Female insects are known to vary in the degree to which they concentrate egg production into the early part of life. This variation has been quantified as the ovigeny index, defined as the proportion of the maximum potential lifetime complement of eggs that is mature following emergence from the pupa. We tested the hypothesis that the timing of egg production depends both on body size and on host availability, by means of a dynamic programming model that predicted optimal resource allocation to reproduction and survival together with the resulting ovigeny index, in non-feeding synovigenic parasitoids of different sizes. As body size increases, the proportionate increase in resource allocation to initial egg load is less than the proportionate increase in allocation to lifetime fecundity and potential life span, leading to a deferred investment in reproduction as shown by a decrease in ovigeny index. High habitat quality and high habitat stochasticity in reproductive opportunities have a significant effect on the optimal allocation of resources to reproduction and survival, and thus select for early reproduction, i.e. an increased ovigeny index. The ovigeny concept – ovigeny index together with its life-history correlates – enables understanding of the general occurrence of size-related deferment of reproductive investment in parasitoid wasps and also helps explain a significant part of the considerable life-history variation found among such insects.     

GENETIC CONSTRAINTS ON LIFE-HISTORY EVOLUTION: QUANTITATIVE-TRAIT LOCI INFLUENCING GROWTH AND FLOWERING IN ARABIDOPSIS THALIANA

We have mapped genes causing life-history trade-offs, and they behave as predicted by ecological theory. Energetic and quantitative-genetic models suggest a trade-off between age and size at first reproduction. Natural selection favored plants that flower early and attain large size at first reproduction. Response to selection was opposed by a genetic trade-off between these two components of fitness. Two quantitative-trait loci (QTLs) influencing flowering time were mapped in a recombinant inbred population of Arabidopsis. These QTLs also influenced size at first reproduction, but did not affect growth rate (resource acquisition). Substitutions of small chromosomal segments, which may represent allelic differences at flowering time loci, caused genetic trade-offs between life-history components. One QTL explained 22% of the genetic variation in flowering time. It is within a few centiMorgans (cM) of the gigantea (GI) locus, and may be allelic with GI. Sixteen percent of the genetic variation was explained by another QTL, FDR1, near 18 cM on chromosome II, which does not correspond to any previously identified flowering-time locus. These life-history genes regulate patterns of resource allocation and life-history trade-offs in this population.     

Interactive effects of competition and social environment on the expression of sexual dimorphism

The expression of sexual dimorphism is expected to be influenced by the acquisition of resources available to allocate to trait growth, combined with sex‐specific patterns of resource allocation. Resource acquisition in the wild may be mediated by a variety of ecological factors, such as the density of interspecific competitors. Allocation may in turn depend on social contexts, such as sex ratio, that alter the pay‐off for investment in sexual traits. How these factors interact to promote or constrain the expression and evolution of sexual dimorphism is poorly understood. We manipulated sex ratio and interspecific resource competition over the growing season of red‐spotted newts (Notophthalmus viridescens) in artificial ponds. Fish competitors had a stronger effect on female than male growth, which effectively eliminated the expression of sexual size dimorphism. In addition, newt sex ratio influenced fish growth, leading to reduction in fish mass with an increase in female newt frequency. Fish also reduced the expression of male tail height, a sexually selected trait, but only in tanks with a female‐biased sex ratio. This suggests males alter their resource allocation pattern in response to the strength of sexual selection. Our results demonstrate that ecologically and socially mediated interactions between sex‐specific resource acquisition and allocation can contribute to variation in the expression of sexual dimorphism.     

Seasonality determines patterns of growth and age structure over a geographic gradient in an ectothermic vertebrate

Environmental variation connected with seasonality is likely to affect the evolution of life-history strategies in ectotherms, but there is no consensus as to how important life-history traits like body size are influenced by environmental variation along seasonal gradients. We compared adult body size, skeletal growth, mean age, age at first reproduction and longevity among 11 common frog (Rana temporaria) populations sampled along a 1,600-km-long latitudinal gradient across Scandinavia. Mean age, age at first reproduction and longevity increased linearly with decreasing growth season length. Lifetime activity (i.e. the estimated number of active days during life-time) was highest at mid-latitudes and females had on average more active days throughout their lives than males. Variation in body size was due to differences in lifetime activity among populations??individuals (especially females) were largest where they had the longest cumulative activity period??as well as to differences between populations in skeletal growth rate as determined by skeletochronological analyses. Especially, males grew faster at intermediate latitudes. While life-history trait variation was strongly associated with latitude, the direction and shape of these relationships were sex- and trait-specific. These context-dependent relationships may be the result of life-history trade-offs enforced by differences in future reproductive opportunities and time constraints among the populations. Thus, seasonality appears to be an important environmental factor shaping life-history trait variation in common frogs.     

Are there interactive effects of mate availability and predation risk on life history and defence in a simultaneous hermaphrodite?

Encountering mates and avoiding predators are ubiquitous challenges faced by many organisms and they can affect the expression of many traits including growth, timing of maturity and resource allocation to reproduction. However, these two factors are commonly considered in isolation rather than simultaneously. We examined whether predation risk and mate availability interact to affect morphology and life-history traits (including lifetime fecundity) of a hermaphroditic snail (Physa acuta). We found that mate availability reduced juvenile growth rate and final size. Predator cues from crayfish induced delayed reproduction, but there were no reduced fecundity costs associated with predator induction. Although there were interactive effects on longevity, lifetime fecundity was determined by the number of reproductive days. Therefore, our results indicate a resource-allocation trade-off among growth, longevity and reproduction. Future consideration of this interaction will be important for understanding how resource-allocation plasticity affects the integration of defensive, life-history and mating-system traits.     

Life-history variation in the short-lived herb Rorippa palustris: The role of carbon storage

Carbon storage is commonly found among perennials, but only rarely in annuals. However, many short-lived species may behave as annuals or short-lived perennials depending on the date of germination, photoperiod or disturbance. Due to the trade-off between investments into current reproduction vs. survival, these life-history modes presumably differ in carbon allocation. In this study, we aimed to evaluate how carbon storage is affected by germination date and disturbance in an outdoor pot experiment with the short-lived Rorippa palustris. Plants from autumnal and summer cohorts were injured in different ontogenetic stages (vegetative, flowering and fruiting) and the starch content in roots was assessed. Plants from the autumnal cohort invested more carbon into growth and reproduction, whereas plants from the summer cohort invested preferentially into reserves. However, injury changed the allocation pattern: in plants from the autumnal cohort, injury prevented allocation to reproduction and thus injured plants had a larger carbon storage at the end of the season than control plants; injury at the flowering and fruiting stage caused depletion of reserves for regrowth in plants from the summer cohort, resulting in lower starch reserves compared to control plants. We suggest that life-history variation in R. palustris can be caused by changes in its carbon economy: when all resources could not be used for flowering due to weak photoinduction or loss of flowering organs due to injury, part of the resources is stored for over wintering and reproduction in the next year.     

The ontogeny of postmaturation resource allocation in turtles

Resource-allocation decisions vary with life-history strategy, and growing evidence suggests that long-lived endothermic vertebrates direct resources toward growth and self-maintenance when young, increasing allocation toward reproductive effort over time. Few studies have tracked the ontogeny of resource allocation (energy, steroid hormones, etc.) in long-lived ectothermic vertebrates, limiting our understanding of the generality of life-history strategies among vertebrates. We investigated how reproductively mature female painted turtles (Chrysemys picta) from two distinct age classes allocated resources over a 4-yr period and whether resource-allocation patterns varied with nesting experience. We examined age-related variation in body size, egg mass, reproductive frequency, and yolk steroids and report that younger females were smaller and allocated fewer resources to reproduction than did older females. Testosterone levels were higher in eggs from younger females, whereas eggs from second (seasonal) clutches contained higher concentrations of progesterone and estradiol. These allocation patterns resulted in older, larger females laying larger eggs and producing second clutches more frequently than their younger counterparts. We conclude that resource-allocation patterns do vary with age in a long-lived ectotherm.     

Community-wide germination strategies in an alpine meadow on the eastern Qinghai-Tibet plateau: phylogenetic and life-history correlates

In this study, we built up a database of 633 species (48 families, 205 genera) from an alpine meadow on the eastern Qinghai-Tibet plateau. Our objective was to assess the effects of phylogenetic and life-history (life form, perenniality, seed size, dispersal strategy and period) background on the community-wide germination strategies. We found that the seeds of shrubs, perennials, and well-dispersed plants, and the smaller seeds germinated more and comparatively earlier. In one-way ANOVAs, phylogenetic groups explained 12% of the variance in GT (mean germination time for all seeds germinated of each species); life-history attributes, such as seed size, dispersal strategy, perenniality and life form explained 10%, 7%, 5%, and 1% respectively, and dispersal period had no significant effect on GT. Multifactorial ANOVAs revealed that the three major factors contributing to differences in GT were phylogenetic relatedness, seed size and dispersal strategy (explained 4%, 5% and 4% of the interspecific variation independently, respectively). Thus, seeds germination strategies were significantly correlated with phylogenetic and life-history relatedness. In addition, phylogenetic relatedness had close associations and interactions with seed size and dispersal strategy. Then, we think phylogeny and life-history attributes could not be considered mutual exclusively. Seed germination, like any other trait, is shaped by the natural history of the species and by the evolutionary history of the lineage. And a large percentage of the variance remained unexplained by our model, which suggested important selective factors or parameters may have been left out of this analysis. Electronic Supplementary Material The online version of this article (doi:) contains supplementary material, which is available to authorized users.     

No long-term costs of meristem allocation to flowering in stoloniferous Trifolium species

Clonal plants propagate by means of clonal growth and sexual reproduction. The commitment of meristems to branching and flowering govern the expression of these two mutually exclusive life-history functions. We used a modelling and an experimental approach to examine the consequences of a structural trade-off between flowering and clonal growth on future growth and fitness in stoloniferous species with a determinate module architecture. The model revealed negative effects of flowering on vegetative growth due to a structural trade-off at the meristem level. Total fecundity was maximized at intermediate flowering frequencies. In addition, optimal meristem commitment to flowering depended strongly on the time available for growth and reproduction. This indicates an interaction between optimal flowering frequency, the length of the growing period and the rate of ontogenetic development. The greenhouse study made use of 15 genotypes of two closely related, stoloniferous Trifolium species. Despite the existence of a structural trade-off at the meristem level, we found no evidence for costs of flowering on the whole-plant level. High allocation to flowering did not result in reduced plant performance (biomass and module production) and total fecundity, indicating that there were no demographic costs of meristem investment to different life-history functions. Flowering frequencies never exceeded the model prediction for optimal commitment of meristems to sexual reproduction, suggesting strong past selection to eliminate high levels of meristem allocation to flowering. Hence, clonal growth seems to have evolutionary priority over sexual reproduction in our species. This revised version was published online in November 2006 with corrections to the Cover Date.     

Optimal resource allocation of the marine bivalve Yoldia notabilis: The effects of size-limited reproductive capacity and size-dependent mortality

The effects of the morphological constraint of maximum reproductive output (reproductive capacity) and the size at which individuals can avoid heavy mortality (refuge size) on the resource allocation pattern between growth and reproduction are investigated using a dynamic modelling approach for a population of Yoldia notabilis (Mollusca: Bivalvia) in Otsuchi Bay, northeastern Japan. A state variable model is developed using field data on shell length, somatic weight, production, survivorship and reproductive capacity of the bivalve. The optimal allocation pattern is characterized by sudden switching from growth to reproduction without the assumption of reproductive capacity, while simultaneous investment in growth and reproduction becomes optimal when maximum reproductive output is limited by reproductive capacity. Size-specific reproductive effort, size at maturity and the growth curve predicted by the latter model fit more closely to the field data, suggesting that size-limited reproductive capacity can play an important role in the evolution of the observed resource allocation pattern. The mortality pattern affects optimal size at maturity, but not size-specific reproductive effort after maturity. When refuge size is fixed, optimal size at maturity increases with survivorship above refuge size. Optimal size at maturity changes in a more complex way with changes in refuge size. Size at maturity remains constant when refuge size is small, increases when it is intermediate, and decreases when it is large. The results suggest that refuge size is an important factor in the evolution of size at maturity, although its contribution varies depending on the values of other factors, such as size-dependent production and survivorship above refuge size. This revised version was published online in July 2006 with corrections to the Cover Date.     

Heat and drought determine flower female allocation in a hermaphroditic Mediterranean plant family

• In animal‐pollinated hermaphroditic species, larger and xenogamous flowers increase male‐biased resource allocation, whereas smaller and selfing flowers invest disproportionally more resources to female function. In Cistaceae, an entomophilous and hermaphroditic Mediterranean family, this pattern generally follows a phylogenetic signal. However, resource allocation to carpels is independent of phylogeny, which suggests trait divergences among closely related species during the diversification into different environmental conditions.
• We tested this hypothesis across 37 species of Cistaceae along a temperature and precipitation gradient, including semiarid, dry, subhumid and humid sites. We quantified the proportions of dry mass and nutrient investment to carpels and tested the influence of the climatic gradient and site‐specific precipitation on the interspecific variation in carpel resource allocation.
• Lowest and highest percentages of resource allocation to carpels ranged from 1.5–4.2% to 24.2–36.6%, respectively. The proportion of resources comprised in carpels significantly decreased with increasing precipitation/decreasing temperature. Thus, carpels comprised proportionally more resources under drier and hotter conditions, especially in semiarid sites.
• Our results demonstrate how the extent of climatic constraints is more important than phylogenetic relationships in determining stress‐induced differences in carpel resource allocation across species of Cistaceae in a Mediterranean environment. We suggest that allocation of proportionally more resources to carpels in drier and hotter sites lies within a strategy to deal with the most stressful conditions by means of a high reproductive effort.