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ABSTRACT: Although fast growth seems to be generally favored by natural selection, growth rates are rarely maximized in nature. Consequently, fast growth is predicted to carry costs resulting in intrinsic trade-offs. Disentangling such trade-offs is of great ecological importance in order to fully understand the prospects and limitations of growth rate variation. A recent study provided evidence for a hitherto unknown cost of fast growth, namely reduced cold stress resistance. Such relationships could be especially important under climate change. Against this background we here investigate the relationships between individual larval growth rate and adult heat as well as cold stress resistance, using eleven data sets from four different insect species (three butterfly species: Bicyclus anynana, Lycaena tityrus, Pieris napi; one Dipteran species: Protophormia terraenovae). Despite using different species (and partly different populations within species) and an array of experimental manipulations (e.g. different temperatures, photoperiods, feeding regimes, inbreeding levels), we were not able to provide any consistent evidence for trade-offs between fast growth and temperature stress resistance in these four insect species.
PLoS ONE 01/2013; 8(4):e62434. · 4.09 Impact Factor
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ABSTRACT: Temperature effects on predator–prey interactions are fundamental to better understand the effects of global warming. Previous studies never considered local adaptation of both predators and prey at different latitudes, and ignored the novel population combinations of the same predator–prey species system that may arise because of northward dispersal. We set up a common garden warming experiment to study predator–prey interactions between Ischnura elegans damselfly predators and Daphnia magna zooplankton prey from three source latitudes spanning >1500 km. Damselfly foraging rates showed thermal plasticity and strong latitudinal differences consistent with adaptation to local time constraints. Relative survival was higher at 24 °C than at 20 °C in southern Daphnia and higher at 20 °C than at 24 °C, in northern Daphnia indicating local thermal adaptation of the Daphnia prey. Yet, this thermal advantage disappeared when they were confronted with the damselfly predators of the same latitude, reflecting also a signal of local thermal adaptation in the damselfly predators. Our results further suggest the invasion success of northward moving predators as well as prey to be latitude-specific. We advocate the novel common garden experimental approach using predators and prey obtained from natural temperature gradients spanning the predicted temperature increase in the northern populations as a powerful approach to gain mechanistic insights into how community modules will be affected by global warming. It can be used as a space-for-time substitution to inform how predator–prey interaction may gradually evolve to long-term warming.
Global Change Biology 01/2013; 19(3):689-696. · 6.86 Impact Factor
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ABSTRACT: 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.
Ecology Letters 10/2012; · 17.56 Impact Factor
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ABSTRACT: 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.
Ecology 06/2012; 93(6):1340-52. · 4.85 Impact Factor
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ABSTRACT: Despite the importance of foraging activity for the growth/predation risk trade-off, studies that demonstrated predator-induced
survival selection on foraging activity under semi-natural conditions are relatively rare. Here, we tested for fish-induced
selection for reduced foraging activity in two larval Enallagma damselflies using a field enclosure experiment. Fish imposed considerable mortality in both damselfly species and survival
selection on foraging activity could be detected in Enallagma geminatum. We did not detect selection in Enallagma hageni, probably because this species already was not eating very much in the absence of fish compared to E. geminatum. Both species responded strongly to the presence of predators by reducing their foraging activity. The documented survival
selection on foraging activity was detected despite the already low activity levels in fish lake prey species and despite
strong predator-induced plasticity in this trait.
KeywordsDamselfly larvae–Foraging activity–Growth/predation risk trade-off–Predation–Survival selection
Behavioral Ecology and Sociobiology 04/2012; 65(2):241-247. · 3.18 Impact Factor
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ABSTRACT: 1. To better predict effects of climate change and predation risk on prey animals and ecosystems, we need studies documenting not only latitudinal patterns in growth rate but also growth plasticity to temperature and predation risk and the underlying proximate mechanisms: behaviour (food intake) and digestive physiology (growth efficiency). The mechanistic underpinnings of predator-induced growth increases remain especially poorly understood. 2. We reared larvae from replicated northern and southern populations of the damselfly Ischnura elegans in a common garden experiment manipulating temperature and predation risk and quantified growth rate, food intake and growth efficiency. 3. The predator-induced and temperature-induced growth accelerations were the same at both latitudes, despite considerably faster growth rates in the southern populations. While the higher growth rates in the southern populations and the high rearing temperature were driven by both an increased food intake and a higher growth efficiency, the higher growth rates under predation risk were completely driven by a higher growth efficiency, despite a lowered food intake. 4. The emerging pattern that higher growth rates associated with latitude, temperature and predation risk were all (partly or completely) mediated by a higher growth efficiency has two major implications. First, it indicates that energy allocation trade-offs and the associated physiological costs play a major role both in shaping large-scale geographic variation in growth rates and in shaping the extent and direction of growth rate plasticity. Secondly, it suggests that the efficiency of energy transfer in aquatic food chains, where damselfly larvae are important intermediate predators, will be higher in southern populations, at higher temperatures and under predation risk. This may eventually contribute to the lengthening of food chains under these conditions and highlights that the prey identity may determine the influence of predation risk on food chain length.
Journal of Animal Ecology 04/2012; 81(5):1034-40. · 4.94 Impact Factor
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ABSTRACT: Natural populations are exposed to multiple stressors. These stressors may interact, leading to synergistic or antagonistic
responses. In addition to these direct interaction effects, there may also be an interaction between stressors through a selection
effect: as the population genetically responds to one stressor, it may become more vulnerable to another one, for instance
because of an associated reduction in genetic variation. We here capitalized on a selection experiment involving the exposure
of Daphnia populations to carbaryl pulses to test the hypothesis that selection imposed by this pesticide may increase vulnerability
to fish predation in the resulting population. A direct predation experiment with individuals isolated from carbaryl-exposed
and non-exposed populations revealed no effect of prior selection by carbaryl exposure on mortality due to stickleback predation.
Keywords
Daphnia magna
-Fish predation-Carbaryl selection
Hydrobiologia 04/2012; 643(1):123-128. · 1.78 Impact Factor
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ABSTRACT: Daphnia can reproduce through subitaneous and dormant eggs. The production of dormant eggs is induced by stimuli associated with
deteriorating growth conditions, and enable Daphnia populations to survive temporarily harsh environmental conditions. Dormant eggs are expected to have developed special biochemical
adaptations to bridge this long unfavourable period, but little comparative biochemical data are available for dormant and
subitaneous eggs. We compared levels of the following molecules between subitaneous and dormant eggs: (a) triglycerides, which
are the most abundant energy storage molecules in Daphnia, (b) glycerol, a cryoprotectant also involved in energy storage, and (c) the heat shock protein Hsp60, a molecular chaperone that may assist in maintaining protein structural integrity and inhibiting cell metabolism during
diapause. Unexpectedly, no difference in triglycerides content between egg types was found. As expected, dormant eggs contained
more glycerol and relatively more Hsp60 than subitaneous eggs. The biochemical composition of dormant eggs can therefore be seen as an adaptation to the harsh environmental
conditions these eggs encounter.
Hydrobiologia 04/2012; 594(1):91-96. · 1.78 Impact Factor
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ABSTRACT: Next to imposing direct lethal effects, pollutants may also indirectly impose mortality by making prey organisms more vulnerable to predation. We report that four water boatmen species differed strongly in direct endosulfan-imposed mortality, and only the species that suffered highest mortality, Sigara iactans, also showed a reduction in escape swimming speed. While head AChE activity was inhibited in all four species, body ChE was only inhibited in S. iactans where it covaried with escape swimming speed, indicating a mechanistic link between body ChE and swimming speed. Our study underscores the need for risk assessment to consider sublethal pollutant effects, which may considerably affect survival rates under natural conditions, also when testing concentrations of a pesticide that cause direct mortality. Such sublethal effects may generate discrepancies between laboratory and field studies and should be considered when designing safety factors for toxicants where the risk assessment is solely based on LC50 values.
Environmental pollution (Barking, Essex: 1987) 04/2012; 163:127-33. · 3.43 Impact Factor
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ABSTRACT: We need to understand joint ecological and evolutionary responses to climate change to predict future threats to biological diversity. The ‘evolving metacommunity’ framework emphasizes that interactions between ecological and evolutionary mechanisms at both local and regional scales will drive community dynamics during climate change. Theory suggests that ecological and evolutionary dynamics often interact to produce outcomes different from those predicted based on either mechanism alone. We highlight two of these dynamics: (i) species interactions prevent adaptation of nonresident species to new niches and (ii) resident species adapt to changing climates and thereby prevent colonization by nonresident species. The rate of environmental change, level of genetic variation, source-sink structure, and dispersal rates mediate between these potential outcomes. Future models should evaluate multiple species, species interactions other than competition, and multiple traits. Future experiments should manipulate factors such as genetic variation and dispersal to determine their joint effects on responses to climate change. Currently, we know much more about how climates will change across the globe than about how species will respond to these changes despite the profound effects these changes will have on global biological diversity. Integrating evolving metacommunity perspectives into climate change biology should produce more accurate predictions about future changes to species distributions and extinction threats.
Evolutionary Applications 01/2012; 5(2):154 - 167. · 4.92 Impact Factor
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ABSTRACT: General biochemical biomarkers are widely used in current ecotoxicology and may function as early warning signals. We have, however, poor knowledge on how ecologically similar species differ in their biomarker responsiveness and how predation risk may affect these biomarkers, potentially in an interactive way with pesticides. We evaluated this by exposing four corixid water bug species to combinations of endosulfan and predation risk and quantifying the activity of four general enzymatic biomarkers: acetylcholinesterase (AChE), phenoloxidase (PO), catalase (CAT) and superoxidedismutase (SOD). AChE activity was inhibited at an endosulfan concentration of 2 μg l(-1) and this did not differ significantly among species. Predation risk inhibited AChE activity with the same magnitude as endosulfan in one species, S. striata. Reduction in the investment of immune function following pesticide exposure, as measured by the activity of PO, was only observed in C. coleoptrata at 8 μg l(-1) while we observed an increase of PO levels in S. striata. Overall, PO was suppressed under predation risk at 8 μg l(-1) endosulfan. For SOD we observed a pesticide-induced increase across all species under predation risk, while for CAT the pesticide-induced increase was only present without predation risk. These results indicate that even within this group of ecologically similar and closely related species opposing biomarker responses may exist, as observed for PO. Effects of predation risk on all four enzymes, at a similar magnitude as the pesticide effects, further question their usefulness as general biomarkers.
Ecotoxicology 09/2011; 21(1):268-79. · 2.36 Impact Factor
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ABSTRACT: Although natural populations may evolve resistance to anthropogenic stressors such as pollutants, this evolved resistance may carry costs. Using an experimental evolution approach, we exposed different Daphnia magna populations in outdoor containers to the carbamate pesticide carbaryl and control conditions, and assessed the resulting populations for both their resistance to carbaryl as well as their susceptibility to infection by the widespread bacterial microparasite Pasteuria ramosa. Our results show that carbaryl selection led to rapid evolution of carbaryl resistance with seemingly no cost when assessed in a benign environment. However, carbaryl-resistant populations were more susceptible to parasite infection than control populations. Exposure to both stressors reveals a synergistic effect on sterilization rate by P. ramosa, but this synergism did not evolve under pesticide selection. Assessing costs of rapid adaptive evolution to anthropogenic stress in a semi-natural context may be crucial to avoid too optimistic predictions for the fitness of the evolving populations.
Evolution 09/2011; 65(9):2681-91. · 5.15 Impact Factor
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ABSTRACT: Summary1. The role of spatial processes in ecotoxicology is largely ignored. Yet, together with species-specific sensitivities to the pollutant, spatial processes may determine community recovery and the resulting community composition after a pollution event.2. We investigated the isolation-specific potential for internal recovery by reproduction and external recovery by dispersal after a pesticide pulse in experimental aquatic insect communities along an isolation gradient.3. External recovery was important in the univoltine species and in a multivoltine species that went locally extinct but only when a source population was nearby. Internal recovery occurred in all multivoltine species and was unexpectedly stronger in more isolated communities, probably because of release from a dispersal-limited key predator.4. As a result, community recovery and resulting changes in composition strongly depended on isolation and species differences in the potential for external recovery through dispersal and internal recovery through reproduction.5. Synthesis and applications. Our results indicate that while the immediate impact of a toxicant on natural communities is shaped by species sensitivities, their recovery is primarily dependent on the degree of isolation. Risk assessment and the protection of communities under toxicant threat may improve greatly from considering the spatial context: isolated communities and communities with poor dispersers should receive extra protection to safeguard their member species. Ideally, land use planning should strive to remediate isolation of natural communities under threat in agricultural landscapes. Where this is not possible, spatial regulation of pesticide application may considerably improve protection of extant diversity.
Journal of Applied Ecology 08/2011; 48(6):1480 - 1489. · 5.05 Impact Factor
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ABSTRACT: Genetic adaptation to temperature change can impact responses of populations and communities to global warming. Here we integrate previously published results on experimental evolution trials with follow-up experiments involving the water flea Daphnia as a model system. Our research shows (1) the capacity of natural populations of this species to genetically adapt to changes in temperature in a time span of months to years, (2) the context-dependence of these genetic changes, emphasizing the role of ecology and community composition on evolutionary responses to climatic change, and (3) the impact of micro-evolutionary changes on immigration success of preadapted genotypes. Our study involves (1) experimental evolution trials in the absence and presence of the community of competitors, predators, and parasites, (2) life-table and competition experiments to assess the fitness consequences of micro-evolution, and (3) competition experiments with putative immigrant genotypes. We use these observations as building blocks of an evolving metacommunity to understand biological responses to climatic change. This approach integrates both local and regional responses at both the population and community levels. Finally, we provide an outline of current gaps in knowledge and suggest fruitful avenues for future research.
Integrative and Comparative Biology 07/2011; 51(5):703-18. · 2.45 Impact Factor
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ABSTRACT: Latitudinal variation in thermal reaction norms of key fitness traits may inform about the response of populations to climate warming, yet their adaptive nature and evolutionary potential are poorly known. We assessed the contribution of quantitative genetic, neutral genetic and environmental effects to thermal reaction norms of growth rate for populations of the damselfly Ischnura elegans. Among populations, reaction norms differed primarily in elevation, suggesting that time constraints associated with shorter growth seasons in univoltine, high-latitude as well as multivoltine, low-latitude populations selected for faster growth rates. Phenotypic divergence among populations is consistent with selection rather than drift as Q(ST) was greater than F(ST) in all cases. Q(ST) estimates increased with experimental temperature and were influenced by genotype by environment interactions. Substantial additive genetic variation for growth rate in all populations suggests that evolution of trait means in different environments is not constrained. Heritability of growth rates was higher at high temperature, driven by increased genetic rather than environmental variance. While environment-specific nonadditive effects also may contribute to heritability differences among temperatures, maternal effects did not play a significant role (where these could be accounted for). Genotype by environment interactions strongly influenced the adaptive potential of populations, and our results suggest the potential for microevolution of thermal reaction norms in each of the studied populations. In summary, the observed latitudinal pattern in growth rates is adaptive and results from a combination of latitudinal and voltinism compensation. Combined with the evolutionary potential of thermal reaction norms, this may affect populations' ability to respond to future climate warming.
Molecular Ecology 06/2011; 20(14):2929-41. · 5.52 Impact Factor
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ABSTRACT: Summary1. Natural populations are exposed to multiple stressors, including both anthropogenic challenges such as xenobiotics and natural stressors associated with exposure to parasites and predators. While there is increasing concern and interest in the combined impact of current exposure to multiple stressors, little attention has been given to how past exposure to a stressor and its evolutionary response shapes the effects of current stressors.2. Here, we performed a life-table experiment using the water flea Daphnia magna to study combined effects of current exposure to the pesticide carbaryl, parasite spores and fish predation risk and how these effects depend upon past exposure to carbaryl using clones obtained from a previous carbaryl selection experiment.3. The current exposure to all three treatments affected life-history traits. Exposure to fish kairomones increased intrinsic population growth rate, while carbaryl and parasite exposure decreased this fitness measure. The three treatments interacted only in a few cases: carbaryl and fish kairomone exposure interacted in shaping intrinsic population growth rate and its component individual reproductive performance, yet the latter only in the animals not exposed to carbaryl stress in the past.4. Our data revealed not only adaptive evolution of carbaryl resistance but also associated evolutionary costs in terms of reduced resistance to parasites, corroborating results of an earlier study. Importantly, both the evolutionary benefits and costs of past exposure to carbaryl stress were conditional on current environmental conditions, exposure to predation risk and parasites, respectively.5. The emerging pattern showed that past stress interacted with current stress in shaping life history. Such evolution-driven carry-over effects across generations have been often ignored and may complicate the prediction of effects of current exposure to single and combined stressors even long after the past stress has disappeared.
Functional Ecology 05/2011; 25(5):974 - 982. · 4.57 Impact Factor
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ABSTRACT: Natural populations that are exposed to pesticides in their environment may at the same time be exposed to natural stressors like parasites and predators, which may interact with pesticide exposure. This may not only impact target pest species but also a wide variety of non-target species. This review reports on a joint research program in the water flea Daphnia magna, a non-target species often used as model organism in ecology and ecotoxicology. The focus is on different aspects that are of key importance to understand the evolutionary ecology of pesticide exposure: (1) the capacity of natural populations to genetically adapt to pesticide exposure (2) the added complexity of synergistic effects caused by simultaneous exposure to natural stressors, and (3) the potential interference of evolutionary costs of adaptation to pesticide exposure. Our results showed that natural populations were able to rapidly evolve resistance to the pesticide carbaryl but at the expense of fitness costs. Individuals selected for carbaryl resistance had higher survival rates when exposed to the pesticide but also a greater susceptibility to the challenge imposed by the bacterial endoparasite Pasteuria ramosa. The evolved resistance to carbaryl was in some cases only expressed in the absence of fish kairomones. Further, it became clear that the responses to both exposure to single and combined stressors was for several life history variables strongly dependent upon past exposure to carbaryl. This indicates that past exposures to pesticides are important and can not be neglected when evaluating responses to current stressors.
Ecotoxicology 03/2011; 20(3):543-51. · 2.36 Impact Factor
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ABSTRACT: The field of ecological immunology strongly relies on indicators of immunocompetence. Two major indicators in invertebrates, the activity of phenoloxidase (PO) and lytic activity have recently been questioned in studies showing that, across a natural range of baseline levels, these indicators did not predict resistance against a manipulated challenge with natural parasites. We confirmed this finding by showing that baseline levels of PO and lytic activity in the host Daphnia magna were not related to spore load of the parasite Pasteuria ramosa. Yet, PO levels in infected hosts did predict spore load, indicating PO activity can be useful as an indicator of immunocompetence in this model parasite-host system.
Biology letters 02/2011; 7(1):156-9. · 3.76 Impact Factor
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ABSTRACT: Global warming and its associated increase in temperature extremes pose a substantial challenge on natural systems. Tropical ectotherms, living close to their (upper) critical thermal limits, may be particularly vulnerable to global warming, yet they are as a group understudied. Most studies assessing fitness effects under global warming focused on life-history correlates such as body size and largely neglected immune function. Furthermore they did not consider to what extent temperature effects may be modulated under resource-based trade-offs. Against this background we here investigate effects of temperature extremes on fitness-related adult traits (viz. body mass, fat content, and two key parameters of arthropod immune function: phenoloxidase (PO) activity and haemocyte numbers) at different levels of larval and adult food stress in the tropical butterfly Bicyclus anynana. Body mass and PO activity decreased after short-term larval food stress, but not fat content and haemocyte numbers (probably owing to compensatory mechanisms during further development). Longer-term food deprivation in the adult stage, in contrast, diminished performance throughout, confirming that the feeding treatments chosen imposed stress. Temperature manipulations yielded contrary responses between life-history correlates and immune function: while body mass and fat content increased by increasing temperatures, PO activity and haemocyte numbers decreased. The latter was particularly pronounced under adult food stress, suggesting a resource-allocation trade-off. Our data suggest that global warming will not only reduce performance through direct effects of thermal stress, but also through secondary effects on adult immune function, which may be missed when exclusively focussing on other life-history correlates.
Global Change Biology 01/2011; 17(2):676 - 687. · 6.86 Impact Factor
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ABSTRACT: Physiological costs of rapid growth may contribute to the observation that organisms typically grow at submaximal rates. Although, it has been hypothesized that faster growing individuals would do worse in dealing with suboptimal temperatures, this type of cost has never been explored empirically. Furthermore, the mechanistic basis of the physiological costs of rapid growth is largely unexplored.
Larvae of the damselfly Ischnura elegans from two univoltine northern and two multivoltine southern populations were reared at three temperatures and after emergence given a cold shock. Cold resistance, measured by chill coma recovery times in the adult stage, was lower in the southern populations. The faster larval growth rates in the southern populations contributed to this latitudinal pattern in cold resistance. In accordance with their assumed role in cold resistance, Hsp70 levels were lower in the southern populations, and faster growing larvae had lower Hsp70 levels. Yet, individual variation in Hsp70 levels did not explain variation in cold resistance.
WE PROVIDE EVIDENCE FOR A NOVEL COST OF RAPID GROWTH: reduced cold resistance. Our results indicate that the reduced cold resistance in southern populations of animals that change voltinism along the latitudinal gradient may not entirely be explained by thermal selection per se but also by the costs of time constraint-induced higher growth rates. This also illustrates that stressors imposed in the larval stage may carry over and shape fitness in the adult stage and highlights the importance of physiological costs in the evolution of life-histories at macro-scales.
PLoS ONE 01/2011; 6(2):e16935. · 4.09 Impact Factor
