Insular shifts and trade-offs in life-history traits in pond frogs in the Zhoushan Archipelago, China

Island and mainland populations of animal species often differ strikingly in life-history traits such as clutch size, egg size, total reproductive effort and body size. However, despite widespread recognition of insular shifts in these life-history traits in birds, mammals and reptiles, there have been no reports of such life-history shifts in amphibians. Furthermore, most studies have focused on one specific life-history trait without explicit consideration of coordinated evolution among these intimately linked life-history traits, and thus the relationships among these traits are poorly studied. Here we provide the first evidence of insular shifts and trade-offs in a coordinated suite of life-history traits for an amphibian species, the pond frog Rana nigromaculata . Life-history data were collected from eight islands in the Zhoushan Archipelago and neighboring mainland China. We found consistent, significant shifts in all life-history traits between mainland and island populations. Island populations had smaller clutch sizes, larger egg sizes, larger female body size and invested less in total reproductive effort than mainland populations. Significant negative relationships were found between egg size and clutch size and between egg size and total reproductive effort among frog populations after controlling for the effects of body size. Therefore, decreased reproductive effort and clutch size, larger egg size and body size in pond frogs on islands were selected through trade-offs as an overall life-history strategy. Our findings contribute to the formation of a broad, repeatable ecological generality for insular shifts in life-history traits across a range of terrestrial vertebrate taxa.     

Sex Allocation in California Oaks: Trade-Offs or Resource Tracking?

Trade-offs in sex resource allocation are commonly inferred from a negative correlation between male and female reproduction. We found that for three California oak species, aboveground annual net productivity (ANP) differences among individuals were primarily correlated with water availability and soil fertility. Reproductive biomass increased with ANP, but the relative allocation to reproduction was constant, indicating that reproduction tracked productivity, which in turn tracked site quality. Although there was a negative correlation between male and female reproduction, this was not the result of a resource investment trade-off, but rather a byproduct of the positive correlation between female reproductive biomass and ANP combined with the greater overall resource allocation to female, compared to male, function. Thus, we reject the hypothesis of a trade-off between these key life-history components within individuals of these species. For long-lived individuals, a plastic resource tracking response to environmental fluctuations may be more adaptive than directly linking life-history traits through trade-offs.     

Phenotypic plasticity of life history traits in relation to reproductive strategies in <Emphasis Type="Italic">Boa constrictor occidentalis</Emphasis>

The close connection between reproductive ecology and life history in snakes leads to trade-offs between reproductive and other life-history traits. Optimal energy allocation to growth and reproduction is a key factor to determine life history structure. Therefore, elucidating the relationship between body size variations and reproductive characters is essential for a better understanding of life-history plasticity. The aim of this work was to determine to what extent life-history differs among populations of Boa constrictor occidentalis and to identify possible life-history trade-offs between morphological and reproductive traits. We compared two populations from areas that are separated latitudinally, with different climatic conditions and vegetation landscape structure. Reproductive and morphological data of specimens were recorded. Although populations had a similar mean length of mature snakes, the frequency of some size classes tended to be different. Size at sexual maturity differed between populations for females, generating variations in the proportion of mature individuals. Reproductive threshold and follicular size also varied, but female reproductive frequency was similar between populations. Reproductive frequency of males varied between populations although their body condition was similar. We discussed two major issues: (1) implications of size at sexual maturity for body size and fecundity; (2) trade-offs in reproductive characters.     

PLEIOTROPY CAUSES LONG-TERM GENETIC CONSTRAINTS ON LIFE-HISTORY EVOLUTION IN BRASSICA RAPA

Fundamental, long-term genetic trade-offs constrain life-history evolution in wild crucifer populations. I studied patterns of genetic constraint in Brassica rapa by estimating genetic correlations among life-history components by quantitative genetic analyses among ten wild populations, and within four populations. Genetic correlations between age and size at first reproduction were always greater than +0.8 within and among all populations studied. Although quantitative genetics might provide insight about genetic constraints if genetic parameters remain approximately constant, little evidence has been available to determine the constancy of genetic correlations. I found strong and consistent estimates of genetic correlations between life-history components, which were very similar within four natural populations. Population differentiation also showed these same trade-offs, resulting from long-term genetic constraint. For some traits, evolutionary changes among populations were incompatible with a model of genetic drift. Historical patterns of natural selection were inferred from population differentiation, suggesting that correlated response to selection has caused some traits to evolve opposite to the direct forces of natural selection. Comparison with Arabidopsis suggests that these life-history trade-offs are caused by genes that regulate patterns of resource allocation to different components of fitness. Ecological and energetic models may correctly predict these trade-offs because there is little additive genetic variation for rates of resource acquisition, but resource allocation is genetically variable.     

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.     

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.     

Genetic differentiation for size at first reproduction through male versus female functions in the widespread Mediterranean tree Pinus pinaster

Background and Aims

The study of local adaptation in plant reproductive traits has received substantial attention in short-lived species, but studies conducted on forest trees are scarce. This lack of research on long-lived species represents an important gap in our knowledge, because inferences about selection on the reproduction and life history of short-lived species cannot necessarily be extrapolated to trees. This study considers whether the size for first reproduction is locally adapted across a broad geographical range of the Mediterranean conifer species Pinus pinaster. In particular, the study investigates whether this monoecious species varies genetically among populations in terms of whether individuals start to reproduce through their male function, their female function or both sexual functions simultaneously. Whether differences among populations could be attributed to local adaptation across a climatic gradient is then considered.

Methods

Male and female reproduction and growth were measured during early stages of sexual maturity of a P. pinaster common garden comprising 23 populations sampled across the species range. Generalized linear mixed models were used to assess genetic variability of early reproductive life-history traits. Environmental correlations with reproductive life-history traits were tested after controlling for neutral genetic structure provided by 12 nuclear simple sequence repeat markers.

Key Results

Trees tended to reproduce first through their male function, at a size (height) that varied little among source populations. The transition to female reproduction was slower, showed higher levels of variability and was negatively correlated with vegetative growth traits. Several female reproductive traits were correlated with a gradient of growth conditions, even after accounting for neutral genetic structure, with populations from more unfavourable sites tending to commence female reproduction at a lower individual size.

Conclusions

The study represents the first report of genetic variability among populations for differences in the threshold size for first reproduction between male and female sexual functions in a tree species. The relatively uniform size at which individuals begin reproducing through their male function probably represents the fact that pollen dispersal is also relatively invariant among sites. However, the genetic variability in the timing of female reproduction probably reflects environment-dependent costs of cone production. The results also suggest that early sex allocation in this species might evolve under constraints that do not apply to other conifers.     

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.     

Variation in reproduction and growth in declining Scots pine populations

Disentangling how variation in reproduction and growth is linked in plants across different ecological scales, and how allocation rules change in response to stress are fundamental aspects of life history theory. Although it is known that reproductive allocation is an allometric process and that environmental conditions can influence demographic traits, patterns of variation in vegetative and reproductive functions across and within individuals of tree species suffering drought-induced decline have rarely been documented. In this study we use Scots pine (Pinus sylvestris L.) as a model species to explore patterns of variation in cone production and growth in two declining populations at the southern edge of its distribution. A Bayesian approach was used to assess how these demographic traits vary as a function of drought effects and competition and covary across different ecological scales. The allometric trajectories relating tree size with cone production and growth differed along gradients of drought impacts and biotic interactions. Although reproduction and growth increased with tree size, cone production reached a maximum at intermediate sized trees and stabilized or decreased at larger sizes. Drought stress effects (defoliation at the tree level and overall decline at the plot level) and competition for resources reduced cone production and growth. Our results also showed differential effects of defoliation on cone production depending on tree size, with stronger effects on larger individuals. After accounting for these effects, much of the variation of demographic traits and correlations among them occurred at small ecological scales across individuals (i.e. within plots) and within individuals across years. This resulted in covariations between demographic traits among nearby individuals and within individuals through time, suggesting a consistent advantage in resource acquisition of some individuals within plots, and trade-offs between growth and cone production within trees across years. In conclusion, this study reports that drought-induced forest decline is associated with lower growth and cone production in Scots pine, which could contribute to explain the long-term impacts of drought in southern populations of this species and, in particular, its low regeneration capacity after severe drought.     

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.     

Regulation of male traits by testosterone: implications for the evolution of vertebrate life histories

The negative co-variation of life-history traits such as fecundity and lifespan across species suggests the existence of ubiquitous trade-offs. Mechanistically, trade-offs result from the need to differentially allocate limited resources to traits like reproduction versus self-maintenance, with selection favoring the evolution of optimal allocation mechanism. Here I discuss the physiological (endocrine) mechanisms that underlie optimal allocation rules and how such rules evolve. The hormone testosterone may mediate life-history trade-offs due to its pleiotropic actions in male vertebrates. Conservation in the actions of testosterone in vertebrates has prompted the 'evolutionary constraint hypothesis,' which assumes that testosterone signaling mechanisms and male traits evolve as a unit. This hypothesis implies that the actions of testosterone are similar across sexes and species, and only the levels of circulating testosterone concentrations change during evolution. In contrast, the 'evolutionary potential hypothesis' proposes that testosterone signaling mechanisms and male traits evolve independently. In the latter scenario, the linkage between hormone and traits itself can be shaped by selection, leading to variation in trade-off functions. I will review recent case studies supporting the evolutionary potential hypothesis and suggest micro-evolutionary experiments to unravel the mechanistic basis of life-history evolution.     

Luminous capabilities and life-history traits of the polychromatic ophiuroid Amphipholis squamata in two isolated populations from Oliveri-Tindari lagoon system,Sicily

Amphipholis squamata is a small ophiuroid with a worldwide distribution except for Polar regions. Global populations of A. squamata are morphologically uniform but inter- and intrapopulational variability occurs at levels from the population to the genotype. The species is polychromatic and two colour varieties (dark-brown and spotted) from two adjacent populations (separated from each other for only 20 years) in a lagoonal system (Sicily) were compared using bioluminescence and life-history traits as indicators of variability. The dark-brown variety was dominant in Lago Nuovo and the spotted one was dominant in Porto Vecchio. Important variations were observed within populations, however, there were significant differences in life-history traits and luminous capabilities between the dark-brown and spotted varieties. The dark-brown variety invested more energy in somatic growth than reproduction (1 cohort each year and growth rate of 0.279 mm each month), whereas energy was devoted mainly to reproduction in the spotted variety (4 cohorts each year and growth rate of 0.171 mm each month). The chronology of the life cycles was completely different between the two varieties. Fertilization occurred mainly in spring for the spotted but only in autumn for the dark-brown. Recruitment occurred mainly in autumn for spotted and in spring for dark-brown individuals. Finally, significant differences were observed for maximal intensity of emitted light and kinetic parameters between the two varieties.     

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.

     

长江中下游湖泊两种混生苦草属植物生活史特征与共存分布格局

 在对长江中下游流域湖南、湖北、江西和安徽4省25个湖泊苦草属(Vallisneria)植物种群进行广泛的取样调查、鉴定和查明种间共存格局的基 础上,结合同园种植实验,对该属两个混生近缘种刺苦草(V. spinulosa)和苦草(V. natans)有性和无性生活史特征进行了定量测定和比较研究 ,探讨了种间生活史差异对种间共存格局的影响。结果表明：1)刺苦草是长江中下游湖泊的优势物种,苦草为常见种,而密刺苦草(V. denseserrulata)仅有很少分布;2)苦草和刺苦草常混生于这些湖泊中,形成共存分布格局：刺苦草和苦草种间呈明显的的带状相间分布格局, 或苦草只零星分布于刺苦草群落中;3)刺苦草和苦草有性和无性生活史特征显著不同：刺苦草为多年生,主要以无性繁殖为主,只有有限的有 性繁殖投入;相反,苦草在调查的地区为一年生,以有性繁殖为主,只进行微弱的克隆生长,且不能产生克隆繁殖器官(冬芽)。刺苦草和苦草 在有性和无性繁殖生活史对策上的权衡,导致种间资源利用和竞争能力的分异而使这两个近缘种得以共存。     

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.     

High-dimensional coexistence of temperate tree species: functional traits, demographic rates, life-history stages, and their physical context

Theoretical models indicate that trade-offs between growth and survival strategies of tree species can lead to coexistence across life history stages (ontogeny) and physical conditions experienced by individuals. There exist predicted physiological mechanisms regulating these trade-offs, such as an investment in leaf characters that may increase survival in stressful environments at the expense of investment in bole or root growth. Confirming these mechanisms, however, requires that potential environmental, ontogenetic, and trait influences are analyzed together. Here, we infer growth and mortality of tree species given size, site, and light characteristics from forest inventory data from Wisconsin to test hypotheses about growth-survival trade-offs given species functional trait values under different ontogenetic and environmental states. A series of regression analyses including traits and rates their interactions with environmental and ontogenetic stages supported the relationships between traits and vital rates expected from the expectations from tree physiology. A combined model including interactions between all variables indicated that relationships between demographic rates and functional traits supports growth-survival trade-offs and their differences across species in high-dimensional niche space. The combined model explained 65% of the variation in tree growth and supports a concept of community coexistence similar to Hutchinson's n-dimensional hypervolume and not a low-dimensional niche model or neutral model.     

Mapping the adaptive landscape of a major agricultural pathogen reveals evolutionary constraints across heterogeneous environments

The adaptive potential of pathogens in novel or heterogeneous environments underpins the risk of disease epidemics. Antagonistic pleiotropy or differential resource allocation among life-history traits can constrain pathogen adaptation. However, we lack understanding of how the genetic architecture of individual traits can generate trade-offs. Here, we report a large-scale study based on 145 global strains of the fungal wheat pathogen Zymoseptoria tritici from four continents. We measured 50 life-history traits, including virulence and reproduction on 12 different wheat hosts and growth responses to several abiotic stressors. To elucidate the genetic basis of adaptation, we used genome-wide association mapping coupled with genetic correlation analyses. We show that most traits are governed by polygenic architectures and are highly heritable suggesting that adaptation proceeds mainly through allele frequency shifts at many loci. We identified negative genetic correlations among traits related to host colonization and survival in stressful environments. Such genetic constraints indicate that pleiotropic effects could limit the pathogen’s ability to cause host damage. In contrast, adaptation to abiotic stress factors was likely facilitated by synergistic pleiotropy. Our study illustrates how comprehensive mapping of life-history trait architectures across diverse environments allows to predict evolutionary trajectories of pathogens confronted with environmental perturbations.Subject terms: Population genetics, Plant sciences, Molecular evolution, Fungi     

Competition and the evolution of reproductive restraint in malaria parasites

All organisms must trade off resource allocation between different life processes that determine their survival and reproduction. Malaria parasites replicate asexually in the host but must produce sexual stages to transmit between hosts. Because different specialized stages are required for these functions, the division of resources between these life-history components is a key problem for natural selection to solve. Despite the medical and economic importance of these parasites, their reproductive strategies remain poorly understood and often seem counterintuitive. Here, we tested recent theory predicting that in-host competition shapes how parasites trade off investment in in-host replication relative to between-host transmission. We demonstrate, across several genotypes, that Plasmodium chabaudi parasites detect the presence of competing genotypes and facultatively respond by reducing their investment in sexual stages in the manner predicted to maximize their competitive ability. Furthermore, we show that genotypes adjust their allocation to sexual stages in line with the availability of exploitable red blood cell resources. Our findings are predicted by evolutionary theory developed to explain life-history trade-offs in more traditionally studied multicellular taxa and suggest that the answer to the long-standing question of why so few transmission stages are produced is that in most natural infections heavy investment in reproduction may compromise in-host survival.     

Reproduction and the energy cost of defense in a Batesian mimicry complex

Summary The amount of energy invested in reproduction and in defense was examined in a Batesian mimicry complex consisting of the modelEleodes obscura and the mimicStenomorpha marginata (both Coleoptera: Tenebrionidae). Models live up to 4 y as adults while mimic adults live only 3 mo. The energy content of the eggs of the model and mimic was determined by microbomb calorimetry. The energy content of the defensive secretions produced by the model was determined by computational chemistry and MNDO computer programming. Contrary to the predictions of some life-history theory, the long-lived model annually produces many small eggs each of low energetic content, while the short-lived mimic annually produces fewer, larger eggs each of high energetic content. However, in terms of total energy, the long-lived model has an annual investment in reproduction equal to that of the short-lived mimic. During the 3 mo of co-ocurrence of models and mimics within a year, an average individual model's cost in using defensive secretions against potential predators is 12% of the amount of energy tied up in the eggs that it produces within the year. The annual cost of defense for the model is 18% of the energy contained in the mean number of eggs produced. When the energy allocated to eggs is added to that allocated to defense, the model has an annual investiment that is greater than the annual investment in reproduction by the mimic. Although the energy invested in defense by the model is small relative to the energy invested in egg production, it buys the model considerable protection from predation. Nevertheless, the cost of defense does not explain the deviations from the predictions of life-history theory.     

Life-History and Spatial Determinants of Somatic Growth Dynamics in Komodo Dragon Populations

Somatic growth patterns represent a major component of organismal fitness and may vary among sexes and populations due to genetic and environmental processes leading to profound differences in life-history and demography. This study considered the ontogenic, sex-specific and spatial dynamics of somatic growth patterns in ten populations of the world’s largest lizard the Komodo dragon (Varanus komodoensis). The growth of 400 individual Komodo dragons was measured in a capture-mark-recapture study at ten sites on four islands in eastern Indonesia, from 2002 to 2010. Generalized Additive Mixed Models (GAMMs) and information-theoretic methods were used to examine how growth rates varied with size, age and sex, and across and within islands in relation to site-specific prey availability, lizard population density and inbreeding coefficients. Growth trajectories differed significantly with size and between sexes, indicating different energy allocation tactics and overall costs associated with reproduction. This leads to disparities in maximum body sizes and longevity. Spatial variation in growth was strongly supported by a curvilinear density-dependent growth model with highest growth rates occurring at intermediate population densities. Sex-specific trade-offs in growth underpin key differences in Komodo dragon life-history including evidence for high costs of reproduction in females. Further, inverse density-dependent growth may have profound effects on individual and population level processes that influence the demography of this species.