Summary 1.Large female insects usually have high potential fecundity. Therefore selection should favour an increase in body size given that these females get opportunities to realize their potential advantage by maturing and laying more eggs. However, ectotherm physiology is strongly temperature-dependent, and activities are carried out sufficiently only within certain temperature ranges. Thus it remains unclear if the fecundity advantage of a large size is fully realized in natural environments, where thermal conditions are limiting. 2. Insect fecundity might be limited by temperature at two levels; first eggs need to mature, and then the female needs time for strategic ovipositing of the egg. Since a female cannot foresee the number of oviposition opportunities that she will encounter on a given day, the optimal rate of egg maturation will be governed by trade-offs associated with egg-and time-limited oviposition. As females of different sizes will have different amounts of body reserves, size-dependent allocation trade-offs between the mother's condition and her egg production might be expected. 3. In the temperate butterfly Pararge aegeria , the time and temperature dependence of oviposition and egg maturation, and the interrelatedness of these two processes were investigated in a series of laboratory experiments, allowing a decoupling of the time budgets for the respective processes. 4. The results show that realized fecundity of this species can be limited by both the temperature dependence of egg maturation and oviposition under certain thermal regimes. Furthermore, rates of oviposition and egg maturation seemed to have regulatory effects upon each other. Early reproductive output was correlated with short life span, indicating a cost of reproduction. Finally, large females matured more eggs than small females when deprived of oviposition opportunities. Thus, the optimal allocation of resources to egg production seems dependent on female size. 5. This study highlights the complexity of processes underlying rates of egg maturation and oviposition in ectotherms under natural conditions. We further discuss the importance of temperature variation for egg-vs. time-limited fecundity and the consequences for the evolution of female body size in insects.
Summary1. It has been postulated that climate warming may pose the greatest threat species in the tropics, where ectotherms have evolved more thermal specialist physiologies. Although species could rapidly respond to environmental change through adaptation, little is known about the potential for thermal adaptation, especially in tropical species. 2. In the light of the limited empirical evidence available and predictions from mutation-selection theory, we might expect tropical ectotherms to have limited genetic variance to enable adaptation. However, as a consequence of thermodynamic constraints, we might expect this disadvantage to be at least partially offset by a fitness advantage, that is, the 'hotter-is-better' hypothesis. 3. Using an established quantitative genetics model and metabolic scaling relationships, we integrate the consequences of the opposing forces of thermal specialization and thermodynamic constraints on adaptive potential by evaluating extinction risk under climate warming. We conclude that the potential advantage of a higher maximal development rate can in theory more than offset the potential disadvantage of lower genetic variance associated with a thermal specialist strategy. 4. Quantitative estimates of extinction risk are fundamentally very sensitive to estimates of generation time and genetic variance. However, our qualitative conclusion that the relative risk of extinction is likely to be lower for tropical species than for temperate species is robust to assumptions regarding the effects of effective population size, mutation rate and birth rate per capita. 5. With a view to improving ecological forecasts, we use this modelling framework to review the sensitivity of our predictions to the model's underpinning theoretical assumptions and the empirical basis of macroecological patterns that suggest thermal specialization and fitness increase towards the tropics. We conclude by suggesting priority areas for further empirical research.
Although the potential to adapt to warmer climate is constrained by genetic trade-offs, our understanding of how selection and mutation shape genetic (co)variances in thermal reaction norms is poor. Using 71 isofemale lines of the fly Sepsis punctum, originating from northern, central, and southern European climates, we tested for divergence in juvenile development rate across latitude at five experimental temperatures. To investigate effects of evolutionary history in different climates on standing genetic variation in reaction norms, we further compared genetic (co)variances between regions. Flies were reared on either high or low food resources to explore the role of energy acquisition in determining genetic trade-offs between different temperatures. Although the latter had only weak effects on the strength and sign of genetic correlations, genetic architecture differed significantly between climatic regions, implying that evolution of reaction norms proceeds via different trajectories at high latitude versus low latitude in this system. Accordingly, regional genetic architecture was correlated to region-specific differentiation. Moreover, hot development temperatures were associated with low genetic variance and stronger genetic correlations compared to cooler temperatures. We discuss the evolutionary potential of thermal reaction norms in light of their underlying genetic architectures, evolutionary histories, and the materialization of trade-offs in natural environments.
Insect size usually increases greatly in the latter stages of development, while reproductive value increases strongly with adult size. Mechanisms that can balance the benefits associated with increased growth are poorly understood, raising the question: what keeps insects from becoming larger? If predation risk was to increase with juvenile size, it would make an extension of development very risky, favouring smaller final sizes. But field measures of juvenile mortality seldom show any general patterns of size dependence. We here therefore try to estimate a mechanistic relationship between juvenile size and predation risk by exposing the larvae of two closely related butterflies to a generalist invertebrate predator in a laboratory experiment. Predation risk increased with larval size but was not affected by the species-specific growth rate differences. These results indicate that predation risk may increase with the size of the juvenile even when predators are relatively small. By basing a model simulation on our data we also show that size dependent predation of the kind found in this study has potential to stabilise selection on body size in these species. Thus, these findings suggest that more detailed studies of the size dependence of predation risk on juvenile instars will increase the understanding of what it is that keeps insects small.
Laboratory studies of insects suggest that female fecundity may increase very rapidly with adult size and that mass may often increase close to exponentially with time during larval growth. These relationships make it difficult to see how realistic levels of larval mortality can outweigh the fecundity benefit of prolonged growth. Hence, it is unclear why many insects do not become bigger. In this study, we experimentally explore the relationship between female size and fecundity in the butterfly Pararge aegeria and show that thermally induced time limitation during oviposition may substantially reduce the fecundity benefit of larger females. We model time-limited oviposition under natural temperature conditions and show that fecundity is also likely to increase asymptotically with female size in the field. With realistic estimates of juvenile mortality, the model predicts optimal body sizes within the observed range even when larvae grow exponentially. We conclude that one important reason for why insects with a high capacity of larval growth do not evolve toward larger sizes may be that the fecundity benefit is in fact relatively limited under natural conditions. If so, these results may help resolve some of the inconsistencies between theory and empirical patterns in explaining optimal size in insects.
The majority of ectotherms mature at a larger size at lower rearing temperatures. Although this temperature-size rule is well established, a general explanation for this phenomenon has remained elusive. In this article, we address the problem by exploring the proximate and ultimate reasons for why a temperate grasshopper, Chorthippus brunneus, is an exception to the temperature-size rule. Using a complete set of life-history data to parameterize an established life-history model, we show that it is optimal for this species to mature at a larger size at higher temperatures. We also show that plasticity in adult size is determined by the relative difference between the minimum temperature thresholds for growth and development rates. The mechanism relates to aspects of the biophysical model of van der Have and de Jong. Ectotherms that obey the temperature-size rule are identified as having a higher temperature threshold for development rate than for growth rate; exceptions are identified as having a lower temperature threshold for development rate than for growth rate. The latter scenario may arise broadly in two ways. These are discussed in reference to the thermal biology of temperate grasshoppers and ectotherms in general.
Theory predicts the emergence of generalists in variable environments and antagonistic pleiotropy to favour specialists in constant environments, but empirical data seldom support such generalist-specialist trade-offs. We selected for generalists and specialists in the dung fly Sepsis punctum (Diptera: Sepsidae) under conditions that we predicted would reveal antagonistic pleiotropy and multivariate trade-offs underlying thermal reaction norms for juvenile development. We performed replicated laboratory evolution using four treatments: adaptation at a hot (31°C) or a cold (15°C) temperature, or under regimes fluctuating between these temperatures, either within or between generations. After 20 generations, we assessed parental effects and genetic responses of thermal reaction norms for three correlated life-history traits: size at maturity, juvenile growth rate and juvenile survival. We find evidence for antagonistic pleiotropy for performance at hot and cold temperatures, and a temperature-mediated trade-off between juvenile survival and size at maturity, suggesting that trade-offs associated with environmental tolerance can arise via intensified evolutionary compromises between genetically correlated traits. However, despite this antagonistic pleiotropy, we found no support for the evolution of increased thermal tolerance breadth at the expense of reduced maximal performance, suggesting low genetic variance in the generalist-specialist dimension.
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