Distinguishing between anticipatory and responsive plasticity in a seasonally polyphenic butterfly

Seasonal generations of short-lived organisms often differ in their morphological, behavioural and life history traits, including body size. These differences may be either due to immediate effects of seasonally variable environment on organisms (responsive plasticity) or rely on presumably adaptive responses of organisms to cues signalizing forthcoming seasonal changes (anticipatory plasticity). When directly developing individuals of insects are larger than their overwintering conspecifics, the between-generation differences are typically ascribed to responsive plasticity in larval growth. We tested this hypothesis using the papilionid butterly Iphiclides podalirius as a model species. In laboratory experiments, we demonstrated that seasonal differences in food quality could not explain the observed size difference. Similarly, the size differences are not likely to be explained by the immediate effects of ambient temperature and photoperiod on larval growth. The qualitative pattern of natural size differences between the directly developing and diapausing butterflies could be reproduced in the laboratory as a response to photoperiod, indicating anticipatory character of the response. Directly developing and diapausing individuals followed an identical growth trajectory until the end of the last larval instar, with size differences appearing just a few days before pupation. Taken together, various lines of evidence suggest that between-generation size differences in I. podalirius are not caused by immediate effects of environmental factors on larval growth. Instead, these differences rather represent anticipatory plasticity and are thus likely to have an adaptive explanation. It remains currently unclear, whether the seasonal differences in adult size per se are adaptive, or if they constitute co-product of processes related to the diapause. Our study shows that it may be feasible to distinguish between different types of plasticity on the basis of empirical data even if fitness cannot be directly measured, and contributes to the emerging view about the predominantly adaptive nature of seasonal polyphenisms in insect

Weak sex-specific evolution of locomotor activity of Sepsis punctum (Diptera: Sepsidae) thermal experimental evolution lines

Elevated temperatures are expected to rise beyond what the physiology of many organisms can tolerate. Behavioural responses facilitating microhabitat shifts may mitigate some of this increased thermal selection on physiology, but behaviours are themselves mediated by physiology, and any behavioural response may trade-off against other fitness-related activities. We investigated whether experimental evolution in different thermal regimes (Cold: 15 °C; Hot: 31 °C; Intergenerational fluctuation 15/31 °C; Control: 23 °C) resulted in genetic differentiation of standard locomotor activity in the dung fly Sepsis punctum. We assessed individual locomotor performance, an integral part of most behavioral repertoires, across eight warm temperatures from 24 °C to 45 °C using an automated device. We found no evidence for generalist-specialist trade-offs (i.e. changes in the breadth of the performance curve) for this trait. Instead, at the warmest assay temperatures hot-selected flies showed somewhat higher maximal performance than all other, especially cold-selected flies, overall more so in males than females. Yet, the flies' temperature optimum was not higher than that of the cold-selected flies, as expected under the 'hotter-is-better' hypothesis. Maximal locomotor performance merely weakly increased with body size. These results suggest that thermal performance curves are unlikely to evolve as an entity according to theory, and that locomotor activity is a trait of limited use in revealing thermal adaptation

The evolution of male-biased sexual size dimorphism is associated with increased body size plasticity in males

1. Sexual size dimorphism (SSD) can vary drastically across environments, demonstrating pronounced sex-specific plasticity. In insects, females are usually the larger and more plastic sex. However, the shortage of taxa with male-biased SSD hampers the assessment of whether the greater plasticity in females is driven by selection on size or represents an effect of the female reproductive role. Here, we specifically address the role of sex-specific plasticity of body size in the evolution of SSD reversals to disentangle sex and size effects. 2. We first investigate sex-specific body size plasticity in Sepsis punctum and Sepsis neocynipsea as two independent cases of intraspecific SSD reversals in sepsid flies. In both species, directional variation in SSD between populations is driven by stronger sexual selection on male size. Using controlled laboratory breeding, we find evidence for sex-specific plasticity and increased condition dependence of male size in populations with male-biased SSD, but not of female size in populations with female-biased SSD. 3. To extend the comparative scope, we next estimate sex-specific body size plasticity in eight additional fly species that differ in the direction of SSD under laboratory conditions. In all species with male-biased SSD we find males to be the more plastic sex, while this was only rarely the case in species with female-biased SSD, thus suggesting a more general trend in Diptera. 4. To examine the generality of this pattern in holometabolous insects, we combine our data with data from the literature in a meta-analysis. Again, male body size tends to be more plastic than female size when males are the larger sex, though female size is now also generally more plastic when females are larger. 5. Our findings indicate that primarily selection on size, rather than the reproductive role per se, drives the evolution of sex-specific body size plasticity. However, sepsid flies, and possibly Diptera in general, show a clear sexual asymmetry with greater male than female plasticity related to SSD, likely driven by strong sexual selection on males. Although further research controlling for phylogenetic and ecological confounding effects is needed, our findings are congruent with theory in suggesting that condition dependence plays a pivotal role in the evolution of sexual size dimorphism

Ontogeny of sexual size dimorphism revisited: Females grow for a longer time and also faster.

Sex-specific mechanisms of the determination of insect body sizes are insufficiently understood. Here we use the common heath moth, Ematurga atomaria (Lepidoptera: Geometridae) to examine how larval growth trajectories differ between males and females. We monitored the development of 1379 larvae in controlled laboratory conditions. Sexually dimorphic development times during the first four instars were associated with sexual size dimorphism (SSD) in the beginning of the fifth (last) instar, when females were on average 15% heavier than males. Similarly, the duration of the last instar was about 13% longer in females. Further, we specifically focussed on the estimates of differential (instantaneous) growth rates of the larvae based on 24h mass increments of the 2nd, 3rd, 4th and 5th day in the beginning of the last instar. We calculated 'allometric' differential growth rates as the per-day increase in cube-root-transformed mass of the larvae. We found that allometric growth rates were slightly but significantly larger in females than in males. As this measure of growth rate (in contrast to the relative growth rate, based on the ratio of masses recorded at consecutive measurements) did not depend on body size, it allows an unambiguous separation of the effects of sex and size. We conclude that in accordance with an emerging general pattern, larger female body size in E. atomaria is achieved primarily by means of a longer growth period. Furthermore, our study shows that the differential growth rate can also be sexually dimorphic and contribute to SSD. This contribution, however, is lower than that of the development time by an order of magnitude. In addition to development periods and growth rates, other parameters of the non-linear growth curves of insect larvae also need to be considered in the context of SSD determination. In particular, weight loss prior to pupation was shown to be considerably larger in females than in males

The evolution of male-biased sexual size dimorphism is associated with increased body size plasticity in males

1. Sexual size dimorphism (SSD) can vary drastically across environments, demonstrating pronounced sex-specific plasticity. In insects, females are usually the larger and more plastic sex. However, the shortage of taxa with male-biased SSD hampers the assessment of whether the greater plasticity in females is driven by selection on size or represents an effect of the female reproductive role. Here, we specifically address the role of sex-specific plasticity of body size in the evolution of SSD reversals to disentangle sex and size effects. 2. We first investigate sex-specific body size plasticity in Sepsis punctum and Sepsis neocynipsea as two independent cases of intraspecific SSD reversals in sepsid flies. In both species, directional variation in SSD between populations is driven by stronger sexual selection on male size. Using controlled laboratory breeding, we find evidence for sex-specific plasticity and increased condition dependence of male size in populations with male-biased SSD, but not of female size in populations with female-biased SSD. 3. To extend the comparative scope, we next estimate sex-specific body size plasticity in eight additional fly species that differ in the direction of SSD under laboratory conditions. In all species with male-biased SSD we find males to be the more plastic sex, while this was only rarely the case in species with female-biased SSD, thus suggesting a more general trend in Diptera. 4. To examine the generality of this pattern in holometabolous insects, we combine our data with data from the literature in a meta-analysis. Again, male body size tends to be more plastic than female size when males are the larger sex, though female size is now also generally more plastic when females are larger. 5. Our findings indicate that primarily selection on size, rather than the reproductive role per se, drives the evolution of sex-specific body size plasticity. However, sepsid flies, and possibly Diptera in general, show a clear sexual asymmetry with greater male than female plasticity related to SSD, likely driven by strong sexual selection on males. Although further research controlling for phylogenetic and ecological confounding effects is needed, our findings are congruent with theory in suggesting that condition dependence plays a pivotal role in the evolution of sexual size dimorphism

Data from: The evolution of male-biased sexual size dimorphism is associated with increased body size plasticity in males

1.Sexual size dimorphism (SSD) can vary drastically across environments, demonstrating pronounced sex-specific plasticity. In insects, females are usually the larger and more plastic sex. However, the shortage of taxa with male-biased SSD hampers the assessment of whether the greater plasticity in females is driven by selection on size or represents an effect of the female reproductive role. Here we specifically address the role of sex-specific plasticity of body size in the evolution of SSD reversals to disentangle sex and size effects. 2.We first investigate sex-specific body size plasticity in Sepsis punctum and S. neocynipsea as two independent cases of intraspecific SSD reversals in sepsid flies. In both species, directional variation in SSD between populations is driven by stronger sexual selection on male size. Using controlled laboratory breeding, we find evidence for sex-specific plasticity and increased condition dependence of male size in populations with male-biased SSD, but not of female size in populations with female-biased SSD, indicating no adaptive canalization of female size. 3.To extend the comparative scope, we next estimate sex-specific body size plasticity in eight additional fly species that differ in the direction of SSD under laboratory conditions. In all species with male-biased SSD we find males to be the more plastic sex, while this was only rarely the case in species with female-biased SSD, thus suggesting a more general trend in Diptera. 4.To examine the generality of this pattern in holometabolous insects, we combine our data with data from the literature in a meta-analysis. Again, male body size tends to be more plastic than female size when males are the larger sex, though female size is now also generally more plastic when females are larger. 5.Our findings indicate that primarily selection on size, rather than the reproductive role per se, drives the evolution of sex-specific body size plasticity. However, sepsid flies, and possibly Diptera in general, show a clear sexual asymmetry with greater male than female plasticity related to SSD, likely driven by strong sexual selection on males. Although further research controlling for phylogenetic and ecological confounding effects is needed, our findings are congruent with theory in suggesting that condition dependence plays a pivotal role in the evolution of sexual size dimorphism

Data from: Plastic and evolutionary responses to heat stress in a temperate dung fly: negative correlation between basal and induced heat tolerance?

Extreme weather events such as heat waves are becoming more frequent and intense. Populations can cope with elevated heat stress by evolving higher basal heat tolerance (evolutionary response) and/ or stronger induced heat tolerance (plastic response). However, there is ongoing debate about whether basal and induced heat tolerance are negatively correlated and whether adaptive potential in heat tolerance is sufficient under ongoing climate warming. To evaluate the evolutionary potential of basal and induced heat tolerance, we performed experimental evolution on a temperate source population of the dung fly Sepsis punctum. Offspring of flies adapted to three thermal selection regimes (Hot, Cold and Reference) were subjected to acute heat stress after having been exposed to either a hot- or non-acclimation pre-treatment. As different traits may respond differently to temperature stress, several physiological and life history traits were assessed. Condition-dependence of the response was evaluated by exposing juveniles to different levels of developmental (food restriction/ rearing density) stress. Heat knockdown times were highest while acclimation effects were lowest in the Hot selection regime, indicating a negative association between basal and induced heat tolerance. However, survival, adult longevity, fecundity and fertility did not show such a pattern. Acclimation had positive effects in heat-shocked flies, but in the absence of heat stress hot-acclimated flies had reduced lifespans relative to non-acclimated ones, thereby revealing a potential cost of acclimation. Moreover, body size positively affected heat tolerance and unstressed individuals were less prone to heat stress than stressed flies, offering support for energetic costs associated with heat tolerance. Overall, our results indicate that heat tolerance of temperate insects can evolve under rising temperatures, but this response could be limited by a negative relationship between basal and induced thermotolerance, and may involve some but not other fitness-related traits

S. punctum heat shock experiment

Responses to heat shock (15 minutes at 42C) in thermal experimental evolution lines of Sepsis punctum (originating from Zurich, Switzerland