The physiological basis of reaction norms: the interaction among growth rate, the duration of growth and body size

The general effects of temperature and nutritional quality ongrowth rate and body size are well known. We know little, however,about the physiological mechanisms by which an organism translatesvariation in diet and temperature into reaction norms of bodysize or development time. We outline an endocrine-based physiologicalmechanism that helps explain how this translation occurs inthe holometabolous insect Manduca sexta (Sphingidae). Body sizeand development time are controlled by three factors: (i) growthrate, (ii) the timing of the cessation of juvenile hormone secretion(measured by the critical weight) and (iii) the timing of ecdysteroidsecretion leading to pupation (the interval to cessation ofgrowth [ICG] after reaching the critical weight). Thermal reactionnorms of body size and development time are a function of howthese three factors interact with temperature. Body size issmaller at higher temperatures, because the higher growth ratedecreases the ICG, thereby reducing the amount of mass thatcan accumulate. Development time is shorter at higher temperaturesbecause the higher growth rate decreases the time required toattain the critical weight and, independently, controls theduration of the ICG. Life history evolution along altitudinal,latitudinal and seasonal gradients may occur through differentialselection on growth rate and the duration of the two independentlycontrolled determinants of the growth period.     

Predicting the response to simultaneous selection: genetic architecture and physiological constraints

A great deal is known about the evolutionary significance of body size and development time. They are determined by the nonlinear interaction of three physiological traits: two hormonal events and growth rate (GR). In this study we investigate how the genetic architecture of the underlying three physiological traits affects the simultaneous response to selection on the two life-history traits in the hawkmoth Manduca sexta. The genetic architecture suggests that when the two life-history traits are both selected in the same direction (to increase or decrease) the response to selection is primarily determined by the hormonal mechanism. When the life-history traits are selected in opposite directions (one to increase and one to decrease) the response to selection is primarily determined by factors that affect the GR. To determine how the physiological traits affect the response to selection of the life-history traits, we simulated the predicted response to 10 generations of selection. A total of 83% of our predictions were supported by the simulation. The main components of this physiological framework also exist in unicellular organisms, vertebrates, and plants and can thus provide a robust framework for understanding how underlying physiology can determine the simultaneous evolution of life-history traits.     

Sources of Variation in Physiological Phenotypes and Their Evolutionary Significance

We offer the thesis that environmental physiologists and evolutionarybiologists can find fertile common ground in the study of howindividual variation in physiological phenotypes originatesand develops. The sources of such individual variation are oftencomplex; the consequences affect how natural selection willact on a suite of traits, of which some may seem, at first glance,far removed from the usual domain of environmental physiology.We illustrate our thesis in two ways. First, we offer two examplesdrawn from studies of thermal tolerance in the poeciliid fishHeterandria formosa. We show how fitness variation can be acomplex function of the gestational temperature and thermaltolerance and how these effects can produce environmentallyinduced variation among populations in thermal tolerance thatmimics a pattern of adaptive variation. Second, we review twocase studies that illuminate how environmental effects on amultivariate phenotype can channel the action of natural selection.The phenotypic plasticity of male life history in Poecilia latipinnain response to temperature embraces a spectrum of traits; theeffects of each one upon fitness will influence the abilityof selection to mold the response of any one of them to temperature.The phenotypic covariances in thermal tolerance and life-historytraits in Heterandria formosa differ slightly between populationsfrom different parts of the species range, apparently becauseof differences between them in thermal sensitivity; this differenceinsures that the multivariate nature of selection will be correspondinglydifferent in those different populations.     

Conflicting processes in the evolution of body size and development time

Body size and development time of Manduca sexta are both determined by the same set of three developmental–physiological factors. These define a parameter space within which it is possible to analyse and explain how phenotypic change is associated with changes in the underlying factors. Body size and development time are determined by the identical set of underlying factors, so they are not independent, but because the mechanisms by which these factors produce each phenotype are different, the two phenotypes are only weakly correlated, and the correlation is context dependent. We use a mathematical model of this mechanism to explore the association between body size and development time and show that the correlation between these two life-history traits can be positive, zero or negative, depending entirely on where in parameter space a population is located, and on which of the underlying factors has a greater variation. The gradient within this parameter space predicts the unconstrained evolutionary trajectory under directional selection on each trait. Calculations of the gradients for body size and development time revealed that these are nearly orthogonal through much of the parameter space. Therefore, simultaneous directional selection on body size and development time can be neither synergistic nor antagonistic but leads to conflicting selection on the underlying developmental parameters.     

Response to joint selection on germination and flowering phenology depends on the direction of selection

Flowering and germination time are components of phenology, a complex phenotype that incorporates a number of traits. In natural populations, selection is likely to occur on multiple components of phenology at once. However, we have little knowledge of how joint selection on several phenological traits influences evolutionary response. We conducted one generation of artificial selection for all combinations of early and late germination and flowering on replicated lines within two independent base populations in the herb Campanula americana. We then measured response to selection and realized heritability for each trait. Response to selection and heritability were greater for flowering time than germination time, indicating greater evolutionary potential of this trait. Selection for earlier phenology, both flowering and germination, did not depend on the direction of selection on the other trait, whereas response to selection to delay germination and flowering was greater when selection on the other trait was in the opposite direction (e.g., early germination and late flowering), indicating a negative genetic correlation between the traits. Therefore, the extent to which correlations shaped response to selection depended on the direction of selection. Furthermore, the genetic correlation between timing of germination and flowering varies across the trait distributions. The negative correlation between germination and flowering time found when selecting for delayed phenology follows theoretical predictions of constraint for traits that jointly determine life history schedule. In contrast, the lack of constraint found when selecting for an accelerated phenology suggests a reduction of the covariance due to strong selection favoring earlier flowering and a shorter life cycle. This genetic architecture, in turn, will facilitate further evolution of the early phenology often favored in warm climates.     

Selection for developmental time in bean weevil (Acanthoscelides obtectus): correlated responses for other life history traits and genetic architecture of line differentiation

In this article we investigate the direct and correlated responses to selection for developmental time in order to discern differences between lines in several preadult and adult life history traits of Acanthoscelides obtectus (Coleoptera, Bruchidae). Selection for fast development was about five times as effective as selection for slow development, as judged by realized heritabilities. The correlated responses on the following life‐history traits were studied: egg size, hatching success, embryonic developmental time, egg‐to‐adult viability, body weight, first day of egg laying, total fecundity, and longevity. Analyses of the terminal generation of selection showed that all life history traits examined, except for hatching success, were affected by selection. The findings suggest that body weight, total fecundity, and longevity traded off to preadult developmental time. Unlike the adult traits, none of the preadult traits showed negative correlations with developmental time. We also present data concerning the underlying genetic basis that produces changes in preadult developmental time, body weight, and egg‐to‐adult viability in the lines selected for fast and slow preadult developmental time. Additive‐dominance genetic architecture for both preadult developmental time and body weight was found. In addition, it appears that the responses to selection for preadult developmental time involved between 10 and 28 loci, which were correlated with at least one to four genes for body weight. Epistasis makes a significant contribution to genetic divergence between fast and slow selected lines only with respect to preadult viability. The observed levels of dominance and epistasis underscore the important role of nonadditive genetic effects to the adaptive diversifications of bean weevil populations.     

Sex differences in phenotypic plasticity of a mechanism that controls body size: implications for sexual size dimorphism

The degree and/or direction of sexual size dimorphism (SSD) varies considerably among species and among populations within species. Although this variation is in part genetically based, much of it is probably due to the sexes exhibiting differences in body size plasticity. Here, we use the hawkmoth, Manduca sexta, to test the hypothesis that moths reared on different diet qualities and at different temperatures will exhibit sex-specific body size plasticity. In addition, we explore the proximate mechanisms that potentially create sex-specific plasticity by examining three physiological variables known to regulate body size in this insect: the growth rate, the critical weight (which measures the cessation of juvenile hormone secretion from the corpora allata) and the interval to cessation of growth (ICG; which measures the time interval between the critical weight and the secretion of the ecdysteroids that regulate pupation and metamorphosis). We found that peak larval mass of males and females did not exhibit sex-specific plasticity in response to diet or temperature. However, the sexes did exhibit sex-specific plasticity in the mechanism that controls size; males and females exhibited sex-specific plasticity in the growth rate and the critical weight in response to both diet and temperature, whereas the ICG only exhibited sex-specific plasticity in response to diet. Our results suggest it is important for the sexes to maintain the same degree of SSD across environments and that this is accomplished by the sexes exhibiting differential sensitivity of the physiological factors that determine body size to environmental variation.     

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

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

A Quantitative Analysis of Growth and Size Regulation in Manduca sexta: The Physiological Basis of Variation in Size and Age at Metamorphosis

Body size and development time are important life history traits because they are often highly correlated with fitness. Although the developmental mechanisms that control growth have been well studied, the mechanisms that control how a species-characteristic body size is achieved remain poorly understood. In insects adult body size is determined by the number of larval molts, the size increment at each molt, and the mechanism that determines during which instar larval growth will stop. Adult insects do not grow, so the size at which a larva stops growing determines adult body size. Here we develop a quantitative understanding of the kinetics of growth throughout larval life of Manduca sexta, under different conditions of nutrition and temperature, and for genetic strains with different adult body sizes. We show that the generally accepted view that the size increment at each molt is constant (Dyar’s Rule) is systematically violated: there is actually a progressive increase in the size increment from instar to instar that is independent of temperature. In addition, the mass-specific growth rate declines throughout the growth phase in a temperature-dependent manner. We show that growth within an instar follows a truncated Gompertz trajectory. The critical weight, which determines when in an instar a molt will occur, and the threshold size, which determines which instar is the last, are different in genetic strains with different adult body sizes. Under nutrient and temperature stress Manduca has a variable number of larval instars and we show that this is due to the fact that more molts at smaller increments are taken before threshold size is reached. We test whether the new insight into the kinetics of growth and size determination are sufficient to explain body size and development time through a mathematical model that incorporates our quantitative findings.     

The plastic fly: the effect of sustained fluctuations in adult food supply on life‐history traits

Many adult traits in Drosophila melanogaster show phenotypic plasticity, and the effects of diet on traits such as lifespan and reproduction are well explored. Although plasticity in response to food is still present in older flies, it is unknown how sustained environmental variation affects life‐history traits. Here, we explore how such life‐long fluctuations of food supply affect weight and survival in groups of flies and affect weight, survival and reproduction in individual flies. In both experiments, we kept adults on constant high or low food and compared these to flies that experienced fluctuations of food either once or twice a week. For these ‘yoyo’ groups, the initial food level and the duration of the dietary variation differed during adulthood, creating four ‘yoyo’ fly groups. In groups of flies, survival and weight were affected by adult food. However, for individuals, survival and reproduction, but not weight, were affected by adult food, indicating that single and group housing of female flies affects life‐history trajectories. Remarkably, both the manner and extent to which life‐history traits varied in relation to food depended on whether flies initially experienced high or low food after eclosion. We therefore conclude that the expression of life‐history traits in adult life is affected not only by adult plasticity, but also by early adult life experiences. This is an important but often overlooked factor in studies of life‐history evolution and may explain variation in life‐history experiments.     

Gall insects and selection on plant vigor: can susceptibility compromise success in competition?

Gall insects select vigorously growing plants and plant parts when initiating gall formation. Vigor is associated with rapid growth rate, and in turn, rapid growth confers competitiveness. Are there conditions under which the cost of vigor, in the form of increased susceptibility to attack, outweighs the benefit of competitive success? I present a simulation model to explore the interaction between susceptibility and competition on the selective advantage of increased growth rate. Assuming size-symmetric competition, the model shows that in general, vigor is favored (benefit > cost) at low to intermediate gall loads. At very high plant densities, however, plants with high gall loads may lose standing in the competitive size hierarchy from which they cannot recover. The details of this result, however, change somewhat when competition is size-asymmetric, that is, when a larger focal plant suppresses smaller neighbors, but smaller neighbors cannot exert a reciprocal effect on the focal. At low densities, the pattern of selection on growth rate is qualitatively similar to the size-symmetric case. At higher plant densities, however, fast-growing genotypes can suppress slow ones so much during the preattack phase that even at the highest gall loads they maintain their standing in the competitive hierarchy. Thus, heavy gall insect attack on vigorous plants can impose selection against high intrinsic growth rates under strong symmetric competition, but not strong asymmetric competition. While life history traits can evolve as a correlated response to selection on defensive traits that reduce susceptibility, this model reveals that susceptibility can evolve as a correlated response to selection on basic life history traits.     

Effects of assay conditions in life history experiments with Drosophila melanogaster

Selection experiments with Drosophila have revealed constraints on the simultaneous evolution of life history traits. However, the responses to selection reported by different research groups have not been consistent. Two possible reasons for these inconsistencies are (i) that different groups used different environments for their experiments and (ii) that the selection environments were not identical to the assay environments in which the life history traits were measured. We tested for the effect of the assay environment in life history experiments by measuring a set of Drosophila selection lines in laboratories working on life history evolution with Drosophila in Basel, Groningen, Irvine and London. The lines measured came from selection experiments from each of these laboratories. In each assay environment, we measured fecundity, longevity, development time and body size. The results show that fecundity measurements were particularly sensitive to the assay environment. Differences between assay and selection environment in the same laboratory or differences between assay environments between laboratories could have contributed to the differences in the published results. The other traits measured were less sensitive to the assay environment. However, for all traits there were cases where the measurements in one laboratory suggested that selection had an effect on the trait, whereas in other laboratories no such conclusion would have been drawn. Moreover, we provide good evidence for local adaptation in early fecundity for lines from two laboratories.     

Nutrient mediation of behavioral plasticity and resource allocation in a xylem-feeding leafhopper

Phenotypic plasticity may be critical for nutrient-limited organisms that allocate ingested nutrients to the competing demands of reproduction and survivorship. Leafhoppers that feed on xylem fluid allow assessment of plasticity in response to the constant selective pressure of nutritional inadequacy. We examined feeding behavior (host selection and consumption rates) and nutrient allocation (fecundity, change in body mass and composition) of the xylem fluid-feeding leafhopper Homalodisca vitripennis (Hemiptera:Cicadellidae) on ten genotypes of related Prunus germplasm when adults first seasonally appear, and later during population peaks, to examine the effects of genotypes and season on plasticity of life history and behavioral traits. Behavior and resource allocation to life history traits were both mediated by xylem nutrients, although nutrients impacting behavior differed from those mediating life history. Host selection and consumption varied with genotype between June and July, yet behavior consistently reflected concentrations of dietary glutamine. Resource allocations also increased linearly with nutrient concentrations, but were best correlated to ingested essential amino acids rather than glutamine. Body mass and composition were highly correlated to dietary essential amino acids in June; 6?weeks later, fecundity was instead proportional to essential amino acids. The discrepancy in nutrients which impact behavior versus those mediating life history may explain the weak preference?Cperformance linkage documented for many insects. The demarcation in allocating resources to biomass in June to fecundity in July suggests increased allocation to reproduction during periods of nutrient stress as predicted by the theory of optimal resource allocation; other contributing biotic and abiotic factors are also discussed.     

Age-dependent rates of infection of cassava green mites by a fungal pathogen in Brazil

Age-specific effects of invertebrate pathogens on their hosts can greatly influence the population dynamics in such interactions. Explanations for such differences are usually sought within differing intrinsic susceptibilities of the host life stages but we present data which indicate that host size, behaviour and life history may be the overriding factors determining age-specific effects of a fungal pathogen, Neozygites floridana (Entomophthorales: Neozygitaceae) on spider mites (Mononychellus tanajoa Bondar, Acari: Tetranychidae). Epizootics of N. floridana in spider mites are characterised by much greater relative mortality of adult females compared with other life stages (ca. 99%), despite similar physiological susceptibilities. We present empirical data that demonstrate encounter rates of mites with N. floridana increasing with life stage during an epizootic on cassava in northeastern Brazil. Estimates of the size, walking speeds and patterns, and life history of different life stages (and adult sexes) were used to calculate expected relative encounter rates which were found not to be different from the observed values (although not testable for larvae). This helps explain the different apparent susceptibility of host life stages in the field. Given the low ecological susceptibility of younger life stages to this pathogen, we predict that the interaction time between host and pathogen, determined by climatic conditions, will be critical in determining the degree of host population control in an epizootic. We further hypothesise that such variation in ecological susceptibility to pathogens can generate selection pressures on basic host traits, contributing to the sessile nature of many microarthropods. This revised version was published online in July 2006 with corrections to the Cover Date.     

Interpreting Geographic Variation in Life-History Traits

The geographic variation in the length of the larval periodand the size at metamorphosis of the wood frog,Rana sylvatica,is examined for populations in the tundra of Canada, the mountainsof Virginia, and the lowlands of Maryland. We argue that theobserved differences in developmental plasticity, heriisbilitiesand genetic covariances of traits among localities result fromdifferential selection pressures in each environment, and arerelated to the physiological constraints inherent in developmentand to the degree of compromise between the timing and sizeat metamorphosis allowed in each environment. In Maryland populationsfitness has been maximized by evolutionary changes in size alone;body size in this population is canalized, has low heritabilityand is highly correlated with juvenile survival relative todevelopmental time. In Canada, minimum developmental time yieldsmaximum fitness; the length of the larval period in this populationis canalized and genetically monomorphic relative to body size.In contrast, fitness in the Virginia populations has been determinedby correlated and pleiotropic effects of genes on both developmentaltime and larval body size, and both traits are equally canalized,affect juvenile survivorship equally and display moderate heritabilities.These results stress the importance of interpreting variationin life-history traits relative to constraints inherent in developmentand those imposed by the environment. Heritability and survivorshipdata support the general notion that fitness traits should havelow levels of additive genetic variation, but also suggest thatantagonistic pleiotropy may act to preserve genetic variationin fitness traits under simultaneous selection, and cautionagainst inferring evolutionary importance of individual traitswithout considering the possible presence of pleiotropy.     

Adaptation to developmental diet influences the response to selection on age at reproduction in the fruit fly

Experimental evolution (EE) is a powerful tool for addressing how environmental factors influence life‐history evolution. While in nature different selection pressures experienced across the lifespan shape life histories, EE studies typically apply selection pressures one at a time. Here, we assess the consequences of adaptation to three different developmental diets in combination with classical selection for early or late reproduction in the fruit fly Drosophila melanogaster. We find that the response to each selection pressure is similar to that observed when they are applied independently, but the overall magnitude of the response depends on the selection regime experienced in the other life stage. For example, adaptation to increased age at reproduction increased lifespan across all diets; however, the extent of the increase was dependent on the dietary selection regime. Similarly, adaptation to a lower calorie developmental diet led to faster development and decreased adult weight, but the magnitude of the response was dependent on the age‐at‐reproduction selection regime. Given that multiple selection pressures are prevalent in nature, our findings suggest that trade‐offs should be considered not only among traits within an organism, but also among adaptive responses to different—sometimes conflicting—selection pressures, including across life stages.     

Sexual selection and senescence: do seed beetle males (Acanthoscelides obtectus,Bruchidae, Coleoptera) shape the longevity of their mates?

Although the reasons why organisms age and die are generally well understood, it has recently been suggested that an optimal life span has evolved not only as the result of trade‐offs between reproductive performances early and late in life, but also that a balance between the costs and benefits of the number of mating has also played an important role in the evolution of ageing in both sexes. By using four seed beetle (Acanthoscelides obtectus) lines selected for different life history traits, but which have also inadvertently created monoandrous and polyandrous conditions, we showed that males evolved to affect the mortality patterns of females in a way consistent to the postmating sexual selection generated by sexually antagonistic co‐evolution theory. Monoandrous males, irrespectively of body weight and other life history traits specific to their lines, evolved to increase the longevity of control females kept under starvation and suppressed fecundity, compared with males that originated in the lines with effectively polyandrous conditions. When females were allowed to lay eggs, the effects of males from different lines and mating type history on the senescence of females were substantially weaker. We found that males in the line that was evolved to decelerate senescence and polyandrous conditions stimulate the earlier onset of females’ oviposition, relative to males stemmed from the line with accelerated senescence and monoandrous conditions. This fact may explain the absence of difference in the mean longevities between the control females mated to these males and highlight the importance of sexual selection in the evolution of ageing.     

Geographic and clonal variation in the milkweed-oleander aphid,Aphis nerii (Homoptera: Aphididae), for winged morph production,life history,and morphology in relation to host plant permanence

Summary Populations of the milkweed-oleander aphid,Aphis nerii, were sampled in California, Iowa and Puerto Rico. Among these localities the aphid's host plants differ greatly in permanence. I compared populations for migratory potential, measured as the proportion of winged offspring produced in response to being crowded, and for life history and morphometric traits of the subsequent adult winged aphids. I predicted a negative correlation between degree of host plant permanence and migratory potential. As predicted, aphids from Iowa, where migration on to temporary hosts must occur each year, produce a greater proportion of winged offspring (37.7%) than those from California (25.7%) or Puerto Rico (31.6%) where hosts are more permanent. However, hosts in Puerto Rico appear to be more permanent than those in California, yet the difference between populations for migratory potential was opposite to that predicted. Within California the prediction again held: aphids collected from the most impermanent sites produce the greatest proportion of winged offspring. There were no population differences for any life history or morphometric traits of winged aphids that are important contributors to fitness or migratory ability such as time to reproductive maturity, fecundity or wing length. Nor did any traits covary with migratory potential. Thus, there does not appear to be an association of life history and morphology with migratory potential that could enhance the colonizing ability of migrant aphids. I was unable to detect population differentiation for life history and morphology even though there is ample genetic variation within populations on which selection could act and an absence of constraints arising from genetic correlations that could prevent appropriate evolution of traits within populations. The exploitation of temporary host plants therefore occurs by an increase in the number of colonists produced and not by change in life history or morphology of those colonists.     

The effect of developmental nutrition on life span and fecundity depends on the adult reproductive environment in Drosophila melanogaster

Both developmental nutrition and adult nutrition affect life‐history traits; however, little is known about whether the effect of developmental nutrition depends on the adult environment experienced. We used the fruit fly to determine whether life‐history traits, particularly life span and fecundity, are affected by developmental nutrition, and whether this depends on the extent to which the adult environment allows females to realize their full reproductive potential. We raised flies on three different developmental food levels containing increasing amounts of yeast and sugar: poor, control, and rich. We found that development on poor or rich larval food resulted in several life‐history phenotypes indicative of suboptimal conditions, including increased developmental time, and, for poor food, decreased adult weight. However, development on poor larval food actually increased adult virgin life span. In addition, we manipulated the reproductive potential of the adult environment by adding yeast or yeast and a male. This manipulation interacted with larval food to determine adult fecundity. Specifically, under two adult conditions, flies raised on poor larval food had higher reproduction at certain ages – when singly mated this occurred early in life and when continuously mated with yeast this occurred during midlife. We show that poor larval food is not necessarily detrimental to key adult life‐history traits, but does exert an adult environment‐dependent effect, especially by affecting virgin life span and altering adult patterns of reproductive investment. Our findings are relevant because (1) they may explain differences between published studies on nutritional effects on life‐history traits; (2) they indicate that optimal nutritional conditions are likely to be different for larvae and adults, potentially reflecting evolutionary history; and (3) they urge for the incorporation of developmental nutritional conditions into the central life‐history concept of resource acquisition and allocation.