The time course of metabolic plasticity and its consequences for growth performance under variable food supply in the northern pike.

Many species up- or downregulate their resting metabolic rate (RMR) when they encounter favourable or unfavourable feeding conditions, respectively. This is thought to promote faster growth when food is abundant and conserve energy reserves when food is scarce. The time it takes to express metabolic plasticity remain little studied. Here, we develop a conceptual model showing how rapid or slow metabolic plasticity alter growth trajectories in response to changes in food supply. We test predictions from the model in a food manipulation experiment with young-of-the-year northern pike, Esox lucius, a species that experience drastic changes in food supply in nature. We find that metabolic plasticity is expressed gradually over several weeks in this species. Rapid changes in food supply thus caused apparent trait-environment mismatches that persisted for at least five weeks. Contrary to predictions, pike grew faster at high food levels when they had previously experienced low food levels and downregulated their RMR. This was not owing to increases in food intake but probably reflected that low RMRs increased the energetic scope for growth when feeding conditions improved. This highlights the important but complex effects of metabolic plasticity on growth dynamics under variable resource levels on ecologically relevant time scales.

The evolution of developmental thresholds and reaction norms for age and size at maturity.

Developing organisms typically mature earlier and at larger sizes in favorable growth conditions, while in rarer cases, maturity is delayed. The rarer reaction norm is easily accommodated by general life history models, whereas the common pattern is not. Theory suggests that a solution to this paradox lies in the existence of critical size thresholds at which maturation or metamorphosis can commence, and in the evolution of these threshold sizes in response to environmental variation. For example, ephemeral environments might favor the evolution of smaller thresholds, enabling earlier maturation. The threshold model makes two unique and untested predictions. First, reaction norms for age and size should steepen, and even change sign, with decreases in threshold size; second, food reductions at sizes below the threshold should delay maturation, while those occurring after the threshold should accelerate maturation. We test these predictions through food manipulations in five damselfly species that theory suggests should differ in threshold size. The results provide strong support for the threshold model's predictions. In all species, early food reductions delayed maturation, while late reductions accelerated maturation. Reaction norms were steeper, and the effect of food reductions changed from decelerating to accelerating at a much smaller size in species from ephemeral habitats. These results support the view that developmental thresholds can account for the widespread observation of negative correlations between age and size at maturity. Moreover, evolution of the threshold appears to be both predictable and central to the observed diversity of reaction norms for age and size at maturity.

Temperate insects with narrow seasonal activity periods can be as vulnerable to climate change as tropical insect species.

The magnitude and ecological impact of climate change varies with latitude. Several recent models have shown that tropical ectotherms face the greatest risk from warming because they currently experience temperatures much closer to their physiological optimum than temperate taxa. Even a small increase in temperature may thus result in steep fitness declines in tropical species but increased fitness in temperate species. This prediction, however, is based on a model that does not account for latitudinal differences in activity periods. Temperate species in particular may often experience considerably higher temperatures than expected during the active season. Here, we integrate data on insect warming tolerance and temperature-dependent development to re-evaluate latitudinal trends in thermal safety margins after accounting for latitudinal trends in insect seasonal activity. Our analyses suggest that temperate and tropical species differ far less in thermal safety margins than commonly assumed, and add to the recent number of studies suggesting that tropical and temperate species might face similar levels of threat from climate change.

Density-dependent offspring interactions do not explain macroevolutionary scaling of adult size and offspring size.

Most life forms exhibit a correlated evolution of adult size (AS) and size at independence (SI), giving rise to AS-SI scaling relationships. Theory suggests that scaling arises because relatively large adults have relatively high reproductive output, resulting in strong density-dependent competition in early life, where large size at independence provides a competitive advantage to juveniles. The primary goal of our study is to test this density hypothesis, using large datasets that span the vertebrate tree of life (fishes, amphibians, reptiles, birds, and mammals). Our secondary goal is to motivate new hypotheses for AS-SI scaling by exploring how subtle variation in life-histories among closely related species is associated with variation in scaling. Our phylogenetically informed comparisons do not support the density hypothesis. Instead, exploration of AS-SI scaling among life-history variants suggests that steeper AS-SI scaling slopes are associated with evolutionary increases in size at independence. We suggest that a positive association between size at independence and juvenile growth rate may represent an important mechanism underlying AS-SI scaling, a mechanism that has been underappreciated by theorists. If faster juvenile growth is a consequence of evolutionary increases in size at independence, this may help offset the cost of delayed maturation, leading to steeper AS-SI scaling slopes.

The Rate of Seasonal Changes in Temperature Alters Acclimation of Performance under Climate Change.

How the ability to acclimate will impact individual performance and ecological interactions under climate change remains poorly understood. Theory predicts that the benefit an organism can gain from acclimating depends on the rate at which temperatures change relative to the time it takes to induce beneficial acclimation. Here, we present a conceptual model showing how slower seasonal changes under climate change can alter species' relative performance when they differ in acclimation rate and magnitude. To test predictions from theory, we performed a microcosm experiment where we reared a mid- and a high-latitude damselfly species alone or together under the rapid seasonality currently experienced at 62°N and the slower seasonality predicted for this latitude under climate change and measured larval growth and survival. To separate acclimation effects from fixed thermal responses, we simulated growth trajectories based on species' growth rates at constant temperatures and quantified how much and how fast species needed to acclimate to match the observed growth trajectories. Consistent with our predictions, the results showed that the midlatitude species had a greater capacity for acclimation than the high-latitude species. Furthermore, since acclimation occurred at a slower rate than seasonal temperature changes, the midlatitude species had a small growth advantage over the high-latitude species under the current seasonality but a greater growth advantage under the slower seasonality predicted for this latitude under climate change. In addition, the two species did not differ in survival under the current seasonality, but the midlatitude species had higher survival under the predicted climate change scenario, possibly because rates of cannibalism were lower when smaller heterospecifics were present. These findings highlight the need to incorporate acclimation rates in ecological models.

Antagonistic natural and sexual selection on wing shape in a scrambling damselfly.

Wings are a key trait underlying the evolutionary success of birds, bats, and insects. For over a century, researchers have studied the form and function of wings to understand the determinants of flight performance. However, to understand the evolution of flight, we must comprehend not only how morphology affects performance, but also how morphology and performance affect fitness. Natural and sexual selection can either reinforce or oppose each other, but their role in flight evolution remains poorly understood. Here, we show that wing shape is under antagonistic selection with regard to sexual and natural selection in a scrambling damselfly. In a field setting, natural selection (survival) favored individuals with long and slender forewings and short and broad hindwings. In contrast, sexual selection (mating success) favored individuals with short and broad forewings and narrow-based hindwings. Both types of selection favored individuals of intermediate size. These results suggest that individuals face a trade-off between flight energetics and maneuverability and demonstrate how natural and sexual selection can operate in similar directions for some wing traits, that is, wing size, but antagonistically for others, that is, wing shape. Furthermore, they highlight the need to study flight evolution within the context of species' mating systems and mating behaviors.

Competitive interactions modify the temperature dependence of damselfly growth rates.

Individual growth rates and survival are major determinants of individual fitness, population size structure, and community dynamics. The relationships between growth rate, survival, and temperature may thus be important for predicting biological responses to climate change. Although it is well known that growth rates and survival are affected by competition and predation in addition to temperature, the combined effect of these factors on growth rates, survival, and size structure has rarely been investigated simultaneously in the same ecological system. To address this question, we conducted experiments on the larvae of two species of damselflies and determined the temperature dependence of growth rate, survival, and cohort size structure under three scenarios of increasing ecological complexity: no competition, intraspecific competition, and interspecific competition. In one species, the relationship between growth rate and temperature became steeper in the presence of competitors, whereas that of survival remained unchanged. In the other species, the relationship between growth rate and temperature was unaffected by competitive interactions, but survival was greatly reduced at high temperatures in the presence of interspecific competitors. The combined effect of competitive interactions and temperature on cohort size structure differed from the effects of these factors in isolation. Together, these findings suggest that it will be challenging to scale up information from single-species laboratory studies to the population and community level.

Susceptibility to a metal under global warming is shaped by thermal adaptation along a latitudinal gradient.

Global warming and contamination represent two major threats to biodiversity that have the potential to interact synergistically. There is the potential for gradual local thermal adaptation and dispersal to higher latitudes to mitigate the susceptibility of organisms to contaminants and global warming at high latitudes. Here, we applied a space-for-time substitution approach to study the thermal dependence of the susceptibility of Ischnura elegans damselfly larvae to zinc in a common garden warming experiment (20 and 24 °C) with replicated populations from three latitudes spanning >1500 km in Europe. We observed a striking latitude-specific effect of temperature on the zinc-induced mortality pattern; local thermal adaptation along the latitudinal gradient made Swedish, but not French, damselfly larvae more susceptible to zinc at 24 °C. Latitude- and temperature-specific differences in zinc susceptibility may be related to the amount of energy available to defend against and repair damage since Swedish larvae showed a much stronger zinc-induced reduction of food intake at 24 °C. The pattern of local thermal adaptation indicates that the predicted temperature increase of 4 °C by 2100 will strongly magnify the impact of a contaminant such as zinc at higher latitudes unless there is thermal evolution and/or migration of lower latitude genotypes. Our results underscore the critical importance of studying the susceptibility to contaminants under realistic warming scenarios taking into account local thermal adaptation across natural temperature gradients.

Latitudinally structured variation in the temperature dependence of damselfly growth rates.

The Metabolic Theory of Ecology predicts that the slope of the rate-temperature relationship, E, remains consistent across traits and organisms, acting as a major determinant of large-scale ecological patterns. Although E has recently been shown to vary systematically, we have a poor understanding of its ecological significance. To address this question, we conducted a common-garden experiment involving six damselfly species differing in distribution, estimating E at the level of full-sib families. Each species was sampled throughout its latitudinal range, allowing us to characterise variation in E along a latitudinal gradient spanning 3600 km. We show that E differs among populations and increases with latitude. E was right-skewness across species, but this was largely an artefact of the latitudinal trend. Increased seasonality towards higher latitude may contribute to the latitudinal trend in E. We conclude that E should be seen as a trait involved in local adaptation.

Growth pattern responses to photoperiod across latitudes in a northern damselfly.

BACKGROUND: Latitudinal clines in temperature and seasonality impose strong seasonal constraints on ectotherms. Studies of population differentiation in phenotypic plasticity of life history traits along latitudinal gradients are important for understanding how organisms have adapted to seasonal environments and predict how they respond to climate changes. Such studies have been scarce for species with a northern distribution. METHODOLOGY/PRINCIPLE FINDING: Larvae of the northern damselfly Coenagrion johanssoni originating from semivoltine central, partivoltine northern, and partivoltine northernmost Swedish populations were reared in the laboratory. To investigate whether larvae use photoperiodic cues to induce compensatory growth along this latitudinal gradient, larvae were reared under two different photoperiods corresponding to a northern and southern latitude. In addition, field adult size was assessed to test the strength of possible compensatory growth mechanisms under natural conditions and hatchling size was measured to test for maternal effects. We hypothesized that populations originating from lower latitudes would be more time constrained than high-latitude populations because they have a shorter life cycle. The results showed that low-latitude populations had higher growth rates in summer/fall. In general northern photoperiods induced higher growth rates, but this plastic response to photoperiod was strongest in the southernmost populations and negligible in the northernmost population. During spring, central populations grew faster under the southern rather than the northern photoperiod. On the other hand, northern and northernmost populations did not differ between each other and grew faster in the northern rather than in the southern photoperiod. Field sampled adults did not differ in size across the studied regions. CONCLUSION/SIGNIFICANCE: We found a significant differentiation in growth rate across latitudes and latitudinal difference in growth rate response to photoperiod. Importantly, growth responses measured at a single larval developmental stage in one season may not always generalize to other developmental stages or seasons.

Generalists and specialists along a latitudinal transect: patterns of thermal adaptation in six species of damselflies.

Tropical organisms colonizing temperate environments face reduced average temperatures and dramatic thermal fluctuations. Theoretical models postulate that thermal specialization should be favored either when little environmental variation is experienced within generations or when among-generation variation is small relative to within-generation variation. To test these predictions, we studied six temperate species of damselflies differing in latitudinal distribution. We developed a computer model simulating how organisms experience environmental variation (accounting for diapause and voltinism) and performed a laboratory experiment assaying thermal sensitivities of growth rates. The computer model showed opposing latitudinal trends in among- and within-generation thermal variability: within-generation thermal variability decreased toward higher latitudes, whereas relative levels of among-generation thermal variability peaked at midlatitudes (where a shift in voltinism occurred). The growth experiment showed that low-latitude species were more thermally generalized than mid- and high-latitude species, supporting the prediction that generalists are favored under high levels of within-generation variation. Northern species had steeper, near-exponential reaction norms suggestive of thermal specialization. However, they had strikingly high thermal optima and grew very slowly over most of the thermal range they are expected to experience in the field. This observation is at present difficult to explain. These results highlight the importance of considering interactions between life history and environmental variation when deriving expectations of thermal adaptation.