State-dependent life-history theory and its implications for optimal clutch size

Summary Life-history theory is usually based on an animal's age or size. McNamara describes a general technique for finding the optimal life-history when an organism's strategy is allowed to depend on other aspects of its state. In this paper we describe the technique in the context of previous work in life-history theory and discuss how it can be used to look at decisions on a finer time scale than the usual annual decisions. We show how it can be used to model optimal clutch size when there is a trade-off between number and quality of offspring. It is shown that the optimal clutch size is typically less than the most productive clutch size. Measuring the value of a clutch in terms of the number of offspring that survive to breed or even the number of grandchildren that survive to breed may give misleading results.     

On the role of body size for life-history evolution

1. Body size is a central element in current theories of life-history evolution. Models for optimal age at maturity are based on the assumptions that there is a trade-off between development time and adult size and that larger size provides a reproductive advantage.
2. The results of large, replicated experiments with the water strider Gerris buenoi (Heteroptera: Gerridae) contradict both these assumptions. Individual rearings under field conditions showed that there is a negative, not a positive, correlation between development time and adult size. The physiological basis of growth, with stretch-induced moulting, may provide a partial explanation for this correlation.
3. This study examined a number of fitness components for their correlations with female size: lifetime fecundity, reproductive life span, average volume per egg, total volume of eggs laid, and the proportion of eggs hatched. None of these traits was correlated with female size.
4. The data on water striders suggest an alternative scenario for life-history evolution, in which size is not an adaptive trait, but evolves as a correlated response to selection on other traits. This expands the range of possible models, and opens life-history theory to the debate about adaptation and optimality.     

Manipulating developmental stress reveals sex-specific effects of egg size on offspring phenotype

The general lack of experimental evidence for strong, positive effects of egg size on offspring phenotype has led to suggestions that avian egg size is a neutral trait. To better understand the functional significance of intra-specific variation in egg size as a determinant of offspring fitness within a life-history (sex-specific life-history strategies) and an environmental (poor rearing conditions) context, we experimentally increased developmental stress (via maternal feather-clipping) in the sexually size-dimorphic European starling (Sturnus vulgaris) and measured phenotypic traits in offspring across multiple biological scales. As predicted by life-history theory, sons and daughters had different responses when faced with developmental stress and variation in egg size. In response to developmental stress, small egg size in normally faster-growing sons was associated with catch-up growth prior to attaining larger adult size, resulting in a reduction in developmental stability. Daughters apparently avoided this developmental instability by reducing growth rate and eventual adult body mass and size. Interestingly, large egg size provided offspring with greater developmental flexibility under poor growth conditions. Large-egg sons and daughters avoided the reduction in developmental stability, and daughters also showed enhanced escape performance during flight trials. Furthermore, large egg size resulted in elevated immune responses for both sexes under developmental stress. These findings show that there can be significant, but complex, context-specific effects of egg size on offspring phenotype at least up to fledging, but these can only be demonstrated by appreciating variation in the quality of the offspring environment and life histories. Results are therefore consistent with egg size playing a significant role in shaping the phenotypic outcome of offspring in species that show even greater intra-specific variation in egg size than starlings.     

Developmental thresholds and the evolution of reaction norms for age and size at life-history transitions

It is quite common in studies of life-history plasticity to find a negative relationship between the age at which various life-history transitions occur and the growth conditions under which individuals develop. In particular, high growth typically results in earlier transitions, often at a larger size. Here, we use a relatively general optimization model for age and size at life-history transitions to argue that current life-history theory cannot adequately explain these results. Specifically, most such theory requires key assumptions that are unlikely to be generally met. This suggests that some important component of the biology of many organisms must be missing from many of the models in life-history theory. We suggest that this missing component might be the phenomenon of developmental thresholds. There are at least two different types of developmental thresholds possible, and we incorporate these into our general optimality model to demonstrate how they can cause a negative relationship between growth conditions and age at a transition. If developmental thresholds are common throughout taxa, then this might explain the empirical results. Our model formulation and analysis also formalizes the popular Wilbur-Collins hypothesis for age and size at metamorphosis in amphibians. The results demonstrate that optimal combinations of age and size, and the slope of the reaction norm connecting them, depend on the existence and type of threshold assumed. Our results also provide an evolutionary framework that can be used to view the data and many of the proximate submodels derived from the Wilbur-Collins hypothesis.     

Maternal condition influences phenotypic selection on offspring

1. Environmentally induced maternal effects are known to affect offspring phenotype, and as a result, the dynamics and evolution of populations across a wide range of taxa. 2. In a field experiment, we manipulated maternal condition by altering food availability, a key factor influencing maternal energy allocation to offspring. We then examined how maternal condition at the time of gametogenesis affects the relationships among early life-history traits and survivorship during early development of the coral reef fish Pomacentrus amboinensis. 3. Maternal condition did not affect the number of embryos that hatched or the number of hatchlings surviving to a set time. 4. We found no significant difference in egg size in relation to the maternal physiological state. However, eggs spawned by supplemented mothers were provisioned with greater energy reserves (yolk-sac and oil globule size) than nonsupplemented counterparts, suggesting that provision of energy reserves rather than egg size more closely reflected the maternal environment. 5. Among offspring originating from supplemented mothers, those with larger yolk-sacs were more likely to successfully hatch and survive for longer periods after hatching. However, among offspring from nonsupplemented mothers, yolk-sac size was either inconsequential to survival or offspring with smaller yolk-sac sizes were favoured. Mothers appear to influence the physiological capacity of their progeny and in turn the efficiency of individual offspring to utilize endogenous reserves. 6. In summary, our results show that the maternal environment influences the relationship between offspring characteristics and survival and suggest that energy-driven selective mechanisms may operate to determine progeny viability.     

An integrated approach to life-cycle evolution using selective landscapes

A model which defines fitness in terms of the intrinsic rate of increase of phenotypes is used to analyse which life cycles are appropriate to which ecological circumstances. The following predictions are made for asexual animals and those sexual animals producing on average more than one daughter per brood. If there are no behavioural or physiological interactions between variables, then number of offspring per breeding should be maximized, survival until first/next breeding should be maximized, and time to first/next breeding should be minimized. If interactions occur such that altering one life-cycle variable affects another, then there are trade-offs between variables and the optimum trade-off will maximize fitness.Number of offspring per breeding will generally affect adult survivorship until next breeding. Given certain reasonable assumptions about this trade-off, high juvenile survivorship selects towards semelparity (many offspring per brood), low juvenile survivorship selects towards iteroparity (few offspring per brood). If juvenile survival depends on adult feeding, as in altricial birds, then juvenile survivorship declines as clutch size is increased. Optimal clutch size maximizes the number of surviving offspring per brood.Two trade-offs involve parental care. If parents guard their offspring they should take more risks if brood size is larger. The amount that parents feed their offspring should depend on how effective feeding is in enhancing growth. Growth may also be enhanced by taking risks, in juveniles or adults. The extent of risk-taking should depend on how effective risk-taking is in enhancing growth.If the number of offspring per brood is related to growing conditions for offspring, the prediction is that more offspring per brood should be produced if growing conditions for offspring are better. If the adult can protect the offspring, for example by encapsulating them, the amount of protection provided should depend on how effective the protection is in increasing offspring survivorship.     

Why does offspring size affect performance? Integrating metabolic scaling with life-history theory

Within species, larger offspring typically outperform smaller offspring. While the relationship between offspring size and performance is ubiquitous, the cause of this relationship remains elusive. By linking metabolic and life-history theory, we provide a general explanation for why larger offspring perform better than smaller offspring. Using high-throughput respirometry arrays, we link metabolic rate to offspring size in two species of marine bryozoan. We found that metabolism scales allometrically with offspring size in both species: while larger offspring use absolutely more energy than smaller offspring, larger offspring use proportionally less of their maternally derived energy throughout the dependent, non-feeding phase. The increased metabolic efficiency of larger offspring while dependent on maternal investment may explain offspring size effects—larger offspring reach nutritional independence (feed for themselves) with a higher proportion of energy relative to structure than smaller offspring. These findings offer a potentially universal explanation for why larger offspring tend to perform better than smaller offspring but studies on other taxa are needed.     

Life-history variation within a taxon: a comparative analysis of birds and mammals

Most studies on life-history evolution discuss the necessity of distinguishing between extrinsic and intrinsic sources of variability in life-history traits. I use log/log plots of yearly neonate production in daugters (b) versus adult mortality (Ma) for 75 bird species and 88 mammal species to compare graphically life-history "fields" arranged by these selective forces along a "slow-fast continuum". Under the assumptions of steady-state and linear relationship between adult mortality and reproductive effort, as well as between juvenile survival and relative neonate weight, it is possible to place additional axes in the two-dimentional plot, and to predict covariations among demographic and individual growth traits. The functional regression analysis shows, that the assumptions are completely fulfilled, at least for birds, but mammals show nonlinear relationship between adult mortality and reproductive effort. This can be explained by peculiarities of metabolism and parental care in small mammals with high reproductive output. Hence, for birds the axis of relative neonate weight approximately coincides in direction with the juvenile survivorship axis, but this is not a case for mammals. In both taxa, the relative neonate weight is an invariant in relation to fecundity and adult mortality (but not in relation to adult body weight). This important feature, together with other intrinsic (energetic and phylogenetic) constraints, explains well-documented close covariations among traits, even when the effect of body size is factored out. It is argued that life-history and body size variations in birds and mammals mainly depend on a pattern of temporal resource deficiency, although this impact cannot be separated from that of extrinsic juvenile mortality.     

Evolutionary ecology of egg size and number in a seed beetle: genetic trade-off differs between environments

Abstract In many organisms, large offspring have improved fitness over small offspring, and thus their size is under strong selection. However, due to a trade-off between offspring size and number, females producing larger offspring necessarily must produce fewer unless the total amount of reproductive effort is unlimited. Because differential gene expression among environments may affect genetic covariances among traits, it is important to consider environmental effects on the genetic relationships among traits. We compared the genetic relationships among egg size, lifetime fecundity, and female adult body mass (a trait linked to reproductive effort) in the seed beetle, Stator limbatus , between two environments (host-plant species Acacia greggii and Cercidium floridum ). Genetic correlations among these traits were estimated through half-sib analysis, followed with artificial selection on egg size to observe the correlated responses of lifetime fecundity and female body mass. We found that the magnitude of the genetic trade-off between egg size and lifetime fecundity differed between environments–a strong trade-off was estimated when females laid eggs on C. floridum seeds, yet this trade-off was weak when females laid eggs on A. greggii seeds. Also differing between environments was the genetic correlation between egg size and female body mass–these traits were positively genetically correlated for egg size on A. greggii seeds, yet uncorrelated on C. floridum seeds. On A. greggii seeds, the evolution of egg size and traits linked to reproductive effort (such as female body mass) are not independent from each other as commonly assumed in life-history theory.     

Comparative phylogenetic analysis of the evolution of semelparity and life history in salmonid fishes

The selective pressures involved in the evolution of semelparity and its associated life-history traits are largely unknown. We used species-level analyses, independent contrasts, and reconstruction of ancestral states to study the evolution of body length, fecundity, egg weight, gonadosomatic index, and parity (semelparity vs. degree of iteroparity) in females of 12 species of salmonid fishes. According to both species-level analysis and independent contrasts analysis, body length was positively correlated with fecundity, egg weight, and gonadosomatic index, and semelparous species exhibited a significantly steeper slope for the regression of egg weight on body length than did iteroparous species. Percent repeat breeding (degree of iteroparity) was negatively correlated with gonadosomatic index using independent contrasts analysis. Semelparous species had significantly larger eggs by species-level analysis, and the egg weight contrast for the branch on which semelparity was inferred to have originated was significantly larger than the other egg weight contrasts, corresponding to a remarkable increase in egg weight. Reconstruction of ancestral states showed that egg weight and body length apparently increased with the origin of semelparity, but fecundity and gonadosomatic index remained more or less constant or decreased. Thus, the strong evolutionary linkages between body size, fecundity, and gonadosomatic index were broken during the transition from iteroparity to semelparity. These findings suggest that long-distance migrations, which increase adult mortality between breeding episodes, may have been necessary for the origin of semelparity in Pacific salmon, but that increased egg weight, leading to increased juvenile survivorship, was crucial in driving the transition. Our analyses support the life-history hypotheses that a lower degree of repeat breeding is linked to higher reproductive investment per breeding episode, and that semelparity evolves under a combination of relatively high juvenile survivorship and relatively low adult survivorship.     

The relationship between egg size and fertilization success in broadcast-spawning marine invertebrates

Egg size is a critical life-history trait because it can profoundlyinfluence offspring fitness and the number of offspring thatcan be produced. Recently, interest has grown in how egg sizeinfluences fertilization rate and in turn how sperm availabilitymight influence the evolution of egg size among broadcast-spawningmarine invertebrates. In this article I review the empiricalevidence on the ways in which egg size and egg accessory structuresinfluence fertilization and theoretical models of the ways spermavailability might influence the evolution of egg size. Evidencesuggests that egg size does influence the collision frequencywith sperm, and models suggest that sperm availability can influenceselection on egg size. Sperm availability appears to be oneof the several factors that influence optimal egg size in broadcast-spawningmarine invertebrates.     

Cannibalism as a selective force on offspring size in fish

Cannibalism may cause considerable mortality on juvenile fish and it has been hypothesised that it may exercise selection on offspring size in that larger offspring may enjoy a size refuge. For this to be evolutionarily advantageous the survival of individual offspring must compensate for the reduced fecundity implied by larger offspring size. We develop a model which combines standard assumptions of size‐dependent mortality with adult cannibalism to investigate the potential for cannibalism to act as selective force on offspring size. We find that for this potential to be realised, the mortality due to cannibalism must exceed a threshold value that is a decreasing function of non‐cannibalistic predation intensity, cannibalized size range width and the average cannibalized size. If cannibalism exceeds this threshold, the model predicts evolution of offspring size towards refuges above or below cannibalized size range depending on initial offspring size. Cannibalistic mortality cannot be so great that the population is non‐viable, however, the range of parameter values describing cannibalistic intensity allowed within these boundaries is wide. On this basis, we suggest that cannibalism is a potential mechanism for offspring size selection.     

Life-history variation in closely related generalist predators living in the same habitat: a case study with three Cyclosa spiders

1. Generalist predators sharing similar food resources and phenologies as well as having no competitive interactions are expected to have a similar life-history pattern, but some closely related web spiders show different life-history traits. The present paper clarifies possible selection pressures affecting life-history traits of the three coexisting Cyclosa spiders and explores the significance of the life-history variation.
2. Cyclosa argenteoalba had lower daily survival rate and higher growth rate, C. sedeculata had higher daily survival rate and lower growth rate, and C. octotuberculata showed intermediate levels. This implies that the selection pressures these spiders experience differ appreciably even in the same habitat.
3. The significance of the life-history characteristics of the three species was evaluated by general life-history theories. Cyclosa argenteoalba showed distinguishing reproductive traits: shorter time to maturation, larger reproductive effort, larger relative clutch size, decreased clutch size with the number of clutches, and smaller egg size. These characteristics may have evolved in response to the larger ratio of juvenile to adult survivorship. Cyclosa octotuberculata had a clutch size much larger than the other two species, but relative clutch sizes accounting for body size were similar between C. octotuberculata and C. sedeculata . Also, the two species showed a similar time to maturation despite having different selection pressures. Probably, higher growth rate compensates for lower survivorship, leading to the similarity in some reproductive traits.     

Egg size plasticity corresponding to maternal food conditions in an annual fish,Ayu <Emphasis Type="Italic">Plecoglossus altivelis</Emphasis>

The classic model of Smith and Fretwell predicts that the optimal egg size will vary according to the shape of the relationship between offspring size and offspring fitness, which may vary among environments. Adaptive significance of intrapopulation egg size variation was examined using Ayu (Plecoglossus altivelis). The species has an annual and migratory life history. Fish under controlled rearing conditions become sexually mature with a trend that smaller females produced larger eggs later in the season. Observed egg size variation was explained by the maternal specific growth rate, which was composed of maternal body size and growing period. Hatchlings from larger eggs had a larger notochord length, larger yolk-sac and grew faster. Such offspring traits provide general advantages of increased larval size, which confer competitive ability for assuring early survivorship. In conclusion, egg size plasticity in Ayu suggests higher offspring fitness through enhancement of their accessibility to food.     

Life-history phenotypes in a live-bearing fish Brachyrhaphis episcopi living under different predator regimes: seasonal effects?

Several key life-history attributes in a tropical live-bearing fish, Brachyrhaphis episcopi, have previously been shown to differ between populations that co-occur with large predatory fish (Characin sites) and those that do not (Rivulus sites). Here we show that differences between Characin and Rivulus localities are also repeatable over time; patterns observed in the wet season also persisted during the dry. Both sexes reached maturity at a smaller size at Characin sites. Although there was no difference in fecundity between larger females living in different predator communities, smaller females at Characin sites produced more offspring. Females also produced smaller offspring at Characin localities. These differences are remarkably similar to those reported in two other species of live-bearing fish, B. rhabdophora and Poecilia reticulata suggesting possible convergent adaptation in life-history strategies due to predator-mediated effects or correlates thereof. We also found seasonal changes in life-history traits that were independent of predator community. In the wet season, mature males were larger, females allocated more to reproduction, and offspring mass was also greater. The results of our study generate testable predictions using B. episcopi to further our understanding of life-history evolution.     

Evolution of pleiotropic alleles for maturation and size as a consequence of predation

Understanding life-history evolution requires knowledge about genetic interactions, physiological mechanisms and the nature of selection. For platyfish, Xiphophorus maculatus, extensive information is available about genetic and physiological mechanisms influencing life-history traits. In particular, alleles at the pituitary locus have large and antagonistic effects on age and size at sexual maturation. To examine how predation affects the evolution of these antagonistic traits, I examined pituitary allele evolution in experimental populations differing in predation risk. A smaller size, earlier maturation allele increased in frequency when predators were absent, while a larger size, later maturation allele increased in frequency when predators were present. Thus, predation favours alleles for larger size, at the cost of later maturation and reproduction. These findings are interesting for several reasons. First, predation is often predicted to favour early reproduction at smaller sizes. Second, few studies have shown how selection acts on alleles that affect age and size at sexual maturation. Finally, many studies assume that trade-offs between these life-history traits result from antagonistic pleiotropy, with alleles that positively affect one trait negatively affecting another, yet this is rarely known. This study unequivocally demonstrates that genetically based trade-offs affect life-history evolution in platyfish.     

Selection for increased allocation to offspring number under environmental unpredictability

According to life-history theory, the evolution of offspring size is constrained by the trade-off between allocation of resources to individual offspring and the number of offspring produced. Existing models explore the ecological consequences of offspring size, whereas number is invariably treated simply as an outcome of the trade-off with size. Here I ask whether there is a direct evolutionary advantage of increased allocation to offspring number under environmental unpredictability. Variable environments are expected to select for diversification in the timing of egg hatch and seed germination, yet the dependence of the expression of diversification strategies, and thus parental fitness, on offspring number has not previously been recognized. I begin by showing that well-established sampling theory predicts that a target bethedging diversification strategy is more reliably achieved as offspring number increases. I then use a simulation model to demonstrate that higher offspring number leads to greater geometric mean fitness under environmental uncertainty. Natural selection is thus expected to act directly to increase offspring number under assumptions of environmental unpredictability in season quality.     

An optimum body size for mammals? Comparative evidence from bats

1. The distribution of body sizes among mammalian species has been modelled by Brown, Marquet & Taper (1993), who suggest that reproductive power (the rate at which energy from the environment is channelled into offspring production) is maximized at a size of 100 g, and the observed size distribution among species reflects the way reproductive power depends on size. The model makes a testable prediction about life-history allometries: namely, that components of reproductive power should not scale linearly with body size but should change sign at the optimum size.
2. A large set of life-history data from a single clade of small mammals, the bats (Order: Chiroptera), was analysed to test this key prediction. The analyses in this study offer no support for the idea that allometries of reproductive power change sign in bats, either at 100 g or at any other size. Furthermore the life-history allometries of bats, which are mostly below the 100 g optimum, were broadly the same as in mammalian taxa larger than the optimum size.
3. These findings together contradict a key prediction of Brown et al. 's (1993) model to explain the skewed body size distribution across mammalian species.     

Offspring size plasticity in response to intraspecific competition: an adaptive maternal effect across life-history stages

When provisioning offspring, mothers balance the benefits of producing a few large, fitter offspring with the costs of decreased fecundity. The optimal balance between offspring size and fecundity depends on the environment. Theory predicts that larger offspring have advantages in adverse conditions, but in favorable conditions size is less important. Thus, if environmental quality varies, selection should favor mothers that adaptively allocate resources in response to local conditions to maximize maternal fitness. In the bryozoan Bugula neritina, we show that the intensity of intraspecific competition dramatically changes the offspring size/performance relationship in the field. In benign or extremely competitive environments, offspring size is less important, but at intermediate levels of competition, colonies from larger larvae have higher performance than colonies from smaller larvae. We predicted mothers should produce larger offspring when intermediate competition is likely and tested these expectations in the field by manipulating the density of brood colonies. Our findings matched expectations: mothers produced larger larvae at high densities and smaller larvae at low densities. In addition, mothers from high-density environments produced larvae that have higher dispersal potential, which may enable offspring to escape crowded environments. It appears mothers can adaptively adjust offspring size to maximize maternal fitness, altering the offspring phenotype across multiple life-history stages.     

Allocation of offspring size and sex by female black ratsnakes

How females allocate resources to each offspring and how they allocate the sex of their offspring are two powerful potential avenues by which mothers can affect offspring fitness. Previous research has focussed extensively on mean offspring size, with much less attention given to variance in offspring size. Here we focussed on variation in offspring size in black ratsnakes, Elaphe obsoleta . We collected and hatched 105 clutches (1283 eggs) over 9 years. We predicted that females should lay larger eggs, or more variable eggs, when the environment is less predictable. We also predicted that females laying early or laying larger eggs should produce mostly sons because adult males are larger than adult female ratsnakes. The largest hatchling was more than twice the length and almost four times the mass of the smallest hatchling. Variation in offspring size was itself highly variable, with CVs in offspring mass among clutches ranging from 1% to 25%. With one exception, the variables we expected should influence variation in offspring size had little effect. We found that clutch size increased with maternal size and that egg size decreased with clutch size, but we found no evidence that variance in egg size among clutches increased as the season progressed or that females increased the mean size of their offspring the later in the season they laid their eggs. Females in better condition after they finish laying their eggs did produce larger eggs. There was no relationship between within-clutch variation in egg size and laying date or mean egg size. Finally, sex ratio did not vary with mean egg size or hatching date. Given evidence that offspring size in snakes affects survival, selection should reduce variation in offspring size unless that variance enhances maternal fitness and yet we found little support for hypothesized advantages of varying offspring size.