Genotype‐environment interactions rule the response of a widespread butterfly to temperature variation

Understanding how organisms adapt to complex environments is a central goal of evolutionary biology and ecology. This issue is of special interest in the current era of rapidly changing climatic conditions. Here, we investigate clinal variation and plastic responses in life history, morphology and physiology in the butterfly Pieris napi along a pan‐European gradient by exposing butterflies raised in captivity to different temperatures. We found clinal variation in body size, growth rates and concomitant development time, wing aspect ratio, wing melanization and heat tolerance. Individuals from warmer environments were more heat‐tolerant and had less melanised wings and a shorter development, but still they were larger than individuals from cooler environments. These findings suggest selection for rapid growth in the warmth and for wing melanization in the cold, and thus fine‐tuned genetic adaptation to local climates. Irrespective of the origin of butterflies, the effects of higher developmental temperature were largely as expected, speeding up development; reducing body size, potential metabolic activity and wing melanization; while increasing heat tolerance. At least in part, these patterns likely reflect adaptive phenotypic plasticity. In summary, our study revealed pronounced plastic and genetic responses, which may indicate high adaptive capacities in our study organism. Whether this may help such species, though, to deal with current climate change needs further investigation, as clinal patterns have typically evolved over long periods.     

Population‐specific deviations of global human craniometric variation from a neutral model

Past studies have revealed that much of human craniometric variation follows a neutral model of population relationships. At the same time, there is evidence for the influence of natural selection in having shaped some global diversity in craniometrics. In order to partition these effects, and to explore other potential population‐specific influences, this article analyzes residuals of craniometric distances from a geographically based neutral model of population structure. W.W. Howells' global craniometric data set was used for these analyses, consisting of 57 measurements for 22 populations around the world, excluding Polynesia and Micronesia because of the relatively recent settlement of these regions. Phenotypic and geographic distances were derived between all pairs of populations. Three‐dimensional multidimensional scaling configurations were obtained for both distance matrices, and compared using a Procrustes rotation method to show which populations do not fit the geographic model. This analysis revealed three major deviations: the Buriat, Greenland Inuit, and Peru. The deviations of the Buriat and Greenland Inuit appear to be related to long‐term adaptation to cold environments. The Peruvian sample is more similar to other New World populations than expected based on geographic distance alone. This deviation likely reflects the evolutionarily recent movement of human populations into South America, such that these populations are further from genetic equilibrium. This same pattern is seen in South American populations in a comparative analysis of classical genetic markers, but not in a comparative analysis of STR loci, perhaps reflecting the higher mutation rate for the latter. Am J Phys Anthropol, 2010. © 2009 Wiley‐Liss, Inc.     

Landscape effects on the thermotolerance of carabid beetles and the role of behavioral thermoregulation

Physiological thermotolerance and behavioral thermoregulation are central to seasonal cold adaptation in ectothermic organisms. For species with enhanced mobility, behavioral responses may be of greater importance in the cold stress response. Employing the carabid beetles as a study organism, the current study compared physiological thermotolerance and behavioral thermoregulation in carabid species inhabiting cereal fields in different landscape contexts, from fine grain heterogeneous “complex” landscapes to homogenous “simple” landscapes. Physiological thermotolerance was determined via measurement of the CT_min and chill coma temperature. Behavioral responses to cold temperature exposure were determined employing a purpose built arena, and thoracic temperature measured to estimate the efficacy of the behavior as a form of behavioral thermoregulation. Results revealed an influence of landscape composition on the cold tolerance of carabid beetles, although species differed in their sensitivity to landscape intensification. A reduced effect of landscape on the thermotolerance of larger carabid beetles was observed, thought to be the consequence of greater mobility preventing local acclimation to microclimatic variation along the landscape intensification gradient. Investigation into behavioral thermoregulation of the 3 largest species revealed burrowing behavior to be the main behavioral response to cold stress, acting to significantly raise carabid body temperature. This finding highlights the importance of behavioral thermoregulation as a strategy to evade cold stress. The use of behavioral thermoregulation may negate the need to invest in physiological thermotolerance, further offering explanation for the lack of landscape effect on the physiological thermotolerance of larger carabids.     

Emergence of sexual size dimorphism and stage‐specific effects of elevated temperature on growth rate and development rate in Harmonia axyridis

Temperature is considered to be the most important environmental factor influencing the performance of ectotherms because it determines the rate of most biochemical reactions and thus the efficiency of metabolism and its function. Unfortunately, most studies investigate the effects of temperature on individuals exposed to a particular temperature regime during their whole pre‐imaginal development and detailed information on variation of the temperature effects during ontogeny is rare. In the present study, the effects of the timing of exposure to a transient period of elevated temperature during ontogeny on development rate and growth rate are investigated for the ladybird Harmonia axyridis Pallas. Control beetles are reared at a constant temperature of 20 °C, whereas treated beetles are reared at 20 °C but are exposed to 33 °C for 48 h either during the early‐larval stage, third‐larval instar, fourth‐larval instar or the pupal stage. The rate of development and the growth rate are both accelerated because the timing of exposure to elevated temperature occurred later in pre‐imaginal development (i.e. development rate and growth rate are highest in individuals exposed to elevated temperature during the pupal stage). An exception to this pattern is the lowering of development rate in individuals exposed to elevated temperature during the fourth‐larval instar. Female H. axyridis have a significantly higher development rate and growth rate than males. However, the relative difference in growth rate between the sexes is much higher than the difference in development rate between sexes, resulting in a female‐biased size (mass) dimorphism in adult beetles.     

Population‐level thermal performance of a cold‐water ectotherm is linked to ontogeny and local environmental heterogeneity

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Whole‐body heat exposure causes developmental stage‐specific apoptosis of male germ cells

Humans are occasionally exposed to extreme environmental heat for a prolonged period of time. Here, we investigated testicular responses to whole‐body heat exposure by placing mice in a warm chamber. Among the examined tissues, the testis was found to be most susceptible to heat stress. Heat stress induces direct responses within germ cells, such as eukaryotic initiation factor 2α phosphorylation and stress granule (SG) formation. Prolonged heat stress (42°C for 6 hr) also disturbed tissue organization, such as through blood‐testis barrier (BTB) leakage. Germ cell apoptosis was induced by heat stress for 6 hr in a cell type‐ and developmental stage‐specific manner. We previously showed that spermatocytes in the early tubular stages (I–VI) form SGs for protection against heat stress. In the mid‐tubular stages (VII–VIII), BTB leakage synergistically enhances the adverse effects of heat stress on pachytene spermatocyte apoptosis. In the late tubular stages (IX–XII), SGs are not formed and severe leakage of the BTB does not occur, resulting in mild apoptosis of late‐pachytene spermatocytes near meiosis. Our results revealed that multiple stress responses are involved in germ cell damage resulting from prolonged heat stress (42°C for 6 hr).     

Cold tolerance in relation to developmental and adult temperature in a butterfly

Abstract. Larvae of the butterfly Lycaena tityrus (Poda) are reared at 20 or 27 °C until adult eclosion, after which they are maintained at the same temperature or are transferred to the alternate temperature. The resulting adults are exposed to −20 °C for 8 min, returned to ambient temperature, and the recovery time to standing position is recorded. On the day of eclosion, individuals reared at 20 °C show 19% shorter recovery times than individuals reared at 27 °C. This effect of developmental temperature disappears when the same animals are tested 3 and 6 days later. However, adult temperature did not affect recovery time in these animals, presumably due to over-riding effects of previous cold shocks. This is suggested by another set of animals, not having experienced previous cold shocks, demonstrating recovery times that are 28% shorter in individuals maintained as adults for 3 days at 20 compared to 27 °C. Thus, L. tityrus appears to be capable of adapting to local temperatures.     

Local genetic adaptation generates latitude‐specific effects of warming on predator–prey interactions

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.     

Combined effect of incubation and ambient temperature on the feeding performance of a small ectotherm

Abstract Many ectothermic animals are subject to fluctuating environmental temperatures during incubation as well as post‐birth. Numerous studies examined the effects of incubation temperature or ambient temperature on various aspects of offspring phenotype. We investigated whether incubation temperature and ambient temperature have an interactive effect on offspring performance. Our study animal, the ectothermic vertebrate Lampropholis delicata (common garden skink; De Vis 1888), experiences fluctuating environmental temperatures caused by differential invasion of an exotic plant Vinca major (blue periwinkle). In the laboratory, eggs from wild‐caught females were assigned to different incubation temperatures that mimicked variation in natural nests. The feeding performance and digestion time of each hatchling was tested at ambient temperatures that represented environments invaded to different degrees by periwinkle. Incubation and ambient temperature interacted to affect a lizard's mobility, the time that it took to capture, subdue and handle a prey, and the number of handling ‘errors’ that it made while foraging. For a number of these characteristics, incubation‐induced changes to a lizard's mass significantly affected this relationship. Irrespective of size, no interaction effect was found for digestion time: lizards digested food faster at warmer temperatures, regardless of incubation temperature. Thus, temperatures experienced during incubation may alter an animal's phenotype so that the surrounding thermal environment differentially affects aspects of feeding performance. Our results also demonstrate that incubation environment can induce changes to morphology and behaviour that carry over into a lizard's early life, and that in some cases these differences in phenotype interact to affect performance. We suggest that the immediate removal of exotic plants as part of a weed control strategy could have important implications for the foraging performance, and presumably fitness, of ectothermic animals.     

Effects of meal size,meal type,and body temperature on the specific dynamic action of anurans

Specific dynamic action (SDA), the increase in metabolism stemming from meal digestion and assimilation, varies as a function of meal size, meal type, and body temperature. To test predictions of these three determinants of SDA, we quantified and compared the SDA responses of nine species of anurans, Bombina orientalis, Bufo cognatus, Ceratophrys ornata, Dyscophus antongilli, Hyla cinerea, Kassina maculata, Kassina senegalensis, Pyxicephalus adspersus, and Rana catesbeiana subjected to meal size, meal type, and body temperature treatments. Over a three to seven-fold increase in meal size, anurans experienced predicted increases in postprandial rates of oxygen consumption the duration of elevated and SDA. Meal type had a significant influence on the SDA response, as the digestion and assimilation of hard-bodied, chitinous crickets, mealworms, and superworms required 76% more energy than the digestion and assimilation of soft-bodied earthworms, waxworms, and neonate rodents. Body temperature largely effected the shape of the postprandial metabolic profile; peak increased and the duration of the response decreased with an increase in body temperature. Variation in body temperature did not significantly alter SDA for four species, whereas both H. cinerea and R. catesbeiana experienced significant increases in SDA with body temperature. For 13 or 15 species of anurans ranging in mass from 2.4 to 270 g, SMR, postprandial peak and SDA scaled with body mass (log–log) with mass exponents of 0.79, 0.93, and 1.05, respectively.     

Host‐specific thermal profiles affect fitness of a widespread pathogen

Host behavior can interact with environmental context to influence outcomes of pathogen exposure and the impact of disease on species and populations. Determining whether the thermal behaviors of individual species influence susceptibility to disease can help enhance our ability to explain and predict how and when disease outbreaks are likely to occur. The widespread disease chytridiomycosis (caused by the fungal pathogen Batrachochytrium dendrobatidis, Bd) often has species‐specific impacts on amphibian communities; some host species are asymptomatic, whereas others experience mass mortalities and population extirpation. We determined whether the average natural thermal regimes experienced by sympatric frog species in nature, in and of themselves, can account for differences in vulnerability to disease. We did this by growing Bd under temperatures mimicking those experienced by frogs in the wild. At low and high elevations, the rainforest frogs Litoria nannotis, L. rheocola, and L. serrata maintained mean thermal regimes within the optimal range for pathogen growth (15–25°C). Thermal regimes for L. serrata, which has recovered from Bd‐related declines, resulted in slower pathogen growth than the cooler and less variable thermal regimes for the other two species, which have experienced more long‐lasting declines. For L. rheocola and L. serrata, pathogen growth was faster in thermal regimes corresponding to high elevations than in those corresponding to low elevations, where temperatures were warmer. For L. nannotis, which prefers moist and thermally stable microenvironments, pathogen growth was fastest for low‐elevation thermal regimes. All of the thermal regimes we tested resulted in pathogen growth rates equivalent to, or significantly faster than, rates expected from constant‐temperature experiments. The effects of host body temperature on Bd can explain many of the broad ecological patterns of population declines in our focal species, via direct effects on pathogen fitness. Understanding the functional response of pathogens to conditions experienced by the host is important for determining the ecological drivers of disease outbreaks.     

Evidence for sex‐specific selection in brain: a case study of the nine‐spined stickleback

Theory predicts that the sex making greater investments into reproductive behaviours demands higher cognitive ability, and as a consequence, larger brains or brain parts. Further, the resulting sexual dimorphism can differ between populations adapted to different environments, or among individuals developing under different environmental conditions. In the nine‐spine stickleback (Pungitius pungitius), males perform nest building, courtship, territory defence and parental care, whereas females perform mate choice and produce eggs. Also, predation‐adapted marine and competition‐adapted pond populations have diverged in a series of ecologically relevant traits, including the level of phenotypic plasticity. Here, we studied sexual dimorphism in brain size and architecture in nine‐spined stickleback from marine and pond populations reared in a factorial experiment with predation and food treatments in a common garden experiment. Males had relatively larger brains, larger telencephala, cerebella and hypothalami (6–16% divergence) than females, irrespective of habitat. Females tended to have larger bulbi olfactorii than males (13%) in the high food treatment, whereas no such difference was found in the low food treatment. The strong sexual dimorphism in brain architecture implies that the different reproductive allocation strategies (behaviour vs. egg production) select for different investments into the costly brains between males and females. The lack of habitat dependence in brain sexual dimorphism suggests that the sex‐specific selection forces on brains differ only negligibly between habitats. Although significance of the observed sex‐specific brain plasticity in the size of bulbus olfactorius remains unclear, it demonstrates the potential for sex‐specific neural plasticity.     

Population‐specific dynamics and selection patterns of transposable element insertions in European natural populations

Transposable elements (TEs) are ubiquitous sequences in genomes of virtually all species. While TEs have been investigated for several decades, only recently we have the opportunity to study their genome‐wide population dynamics. Most of the studies so far have been restricted either to the analysis of the insertions annotated in the reference genome or to the analysis of a limited number of populations. Taking advantage of the European Drosophila population genomics consortium (DrosEU) sequencing data set, we have identified and measured the dynamics of TEs in a large sample of European Drosophila melanogaster natural populations. We showed that the mobilome landscape is population‐specific and highly diverse depending on the TE family. In contrast with previous studies based on SNP variants, no geographical structure was observed for TE abundance or TE divergence in European populations. We further identified de novo individual insertions using two available programs and, as expected, most of the insertions were present at low frequencies. Nevertheless, we identified a subset of TEs present at high frequencies and located in genomic regions with a high recombination rate. These TEs are candidates for being the target of positive selection, although neutral processes should be discarded before reaching any conclusion on the type of selection acting on them. Finally, parallel patterns of association between the frequency of TE insertions and several geographical and temporal variables were found between European and North American populations, suggesting that TEs can be potentially implicated in the adaptation of populations across continents.     

Sex and tissue‐specific evolution of developmental plasticity in Drosophila melanogaster

Developmental plasticity influences the size of adult tissues in insects. Tissues can have unique responses to environmental perturbation during development; however, the prevalence of within species evolution of tissue‐specific developmental plasticity remains unclear. To address this, we studied the effects of temperature and nutrition on wing and femur size in D. melanogaster populations from a temperate and tropical region. Wings were more sensitive to temperature, while wings and femurs were equally responsive to nutrition in both populations and sexes. The temperate population was larger under all conditions, except for femurs of starved females. In line with this, we observed greater femur size plasticity in response to starvation in temperate females, leading to differences in sexual dimorphism between populations such that the slope of the reaction norm of sexual dimorphism in the tropical population was double that of the temperate population. Lastly, we observed a significant trend for steeper slopes of reaction norms in temperate than in tropical females, but not in males. These findings highlight that plasticity divergence between populations can evolve heterogeneously across sexes and tissues and that nutritional plasticity can alter sexual dimorphism in D. melanogaster.     

Cross‐generational effects of temperature on flight performance,and associated life‐history traits in an insect

Nongenetic parental effects may affect offspring phenotype, and in species with multiple generations per year, these effects may cause life‐history traits to vary over the season. We investigated the effects of parental, offspring developmental and offspring adult temperatures on a suite of life‐history traits in the globally invasive agricultural pest Grapholita molesta. A low parental temperature resulted in female offspring that developed faster at low developmental temperature compared with females whose parents were reared at high temperature. Furthermore, females whose parents were reared at low temperature were heavier and more fecund and had better flight abilities than females whose parents were reared at high temperature. In addition to these cross‐generational effects, females developed at low temperature had similar flight abilities at low and high ambient temperatures, whereas females developed at high temperature had poorer flight abilities at low than at high ambient temperature. Our findings demonstrate a pronounced benefit of low parental temperature on offspring performance, as well as between‐ and within‐generation effects of acclimation to low temperature. In cooler environments, the offspring generation is expected to develop more rapidly than the parental generation and to comprise more fecund and more dispersive females. By producing phenotypes that are adaptive to the conditions inducing them as well as heritable, cross‐generational plasticity can influence the evolutionary trajectory of populations. The potential for short‐term acclimation to low temperature may allow expanding insect populations to better cope with novel environments and may help to explain the spread and establishment of invasive species.     

Fitness consequences of variation in developmental temperature in a butterfly

We explored the adaptive significance of developmental plasticity in the tropical butterfly Bicyclus anynana using two experiments including temperature changes during ontogeny. In contrast to previous findings on adult acclimation, we could not find any evidence in support of adaptive developmental plasticity, as survival until adulthood was not enhanced when larval rearing temperatures matched the temperatures experienced during prepupal or pupal development. Extreme temperatures substantially reduced survival, supporting the ‘optimal developmental temperature’ hypothesis. Metamorphosis was more efficient at the higher rearing temperature of 27 °C, where egg hatching success was also higher, indicating that the lower temperature of 20 °C is already slightly stressful for this tropical butterfly.