Effects Of Developmental Temperature Research Articles

The effect of developmental temperature on olfaction in a moth revealed by its interaction with body mass

There is a growing interest in the effects of climate warming on olfaction, as temperature may affect this essential sense. In insects, the response of the olfactory system to developmental temperature might be mediated by body size or mass because body size and mass are negatively affected by developmental temperature in most ectotherms. We tested this hypothesis of a mass-mediated effect of developmental temperature on olfaction in the moth Spodoptera littoralis. We measured the olfactory sensitivity of male to female sex pheromone and five plant odors using electroantennography. We compared males reared at an optimal temperature (25 °C with a daily fluctuation of ±5 °C) and at a high temperature (33 ± 5 °C) close to the upper limit of S. littoralis. On average, the olfactory sensitivity of males did not differ between the two developmental temperatures. However, our analyses revealed an interaction between the effects of developmental temperature and body mass on the detection of the six chemicals tested. This interaction is explained by a positive relationship between antennal sensitivity and body mass observed only with the high developmental temperature. Our results show that the effect of developmental temperature may not be detected when organism size is ignored.

Sex and early-life conditions shape telomere dynamics in an ectotherm.

Telomeres, the repetitive DNA regions that protect the ends of chromosomes, and their shortening have been linked to key life history trade-offs among growth, reproduction and lifespan. In contrast to most endotherms, many ectotherms can compensate for telomere shortening throughout life by upregulation of telomerase in somatic tissues. However, during development, marked by rapid growth and an increased sensitivity to extrinsic factors, the upregulation of telomerase may be overwhelmed, resulting in long-term impacts on telomere dynamics. In ectotherms, one extrinsic factor that may play a particularly important role in development is temperature. Here, we investigated the influence of developmental temperature and sex on early-life telomere dynamics in an oviparous ectotherm, Lacerta agilis. While there was no effect of developmental temperature on telomere length at hatching, there were subsequent effects on telomere maintenance capacity, with individuals incubated at warm temperatures exhibiting less telomere maintenance compared with cool-incubated individuals. Telomere dynamics were also sexually dimorphic, with females having longer telomeres and greater telomere maintenance compared with males. We suggest that selection drives this sexual dimorphism in telomere maintenance, in which females maximise their lifetime reproductive success by investing in traits promoting longevity such as maintenance, while males invest in short-term reproductive gains through a polygynous mating behaviour. These early-life effects, therefore, have the potential to mediate life-long changes to life histories.

History matters: Thermal environment before but not during wasp attack determines the efficiency of symbiont-mediated protection.

The outcome of natural enemy attack in insects is commonly impacted by the presence of defensive microbial symbionts residing within the host. The thermal environment is a factor known to affect symbiont-mediated traits in insects. Lower temperatures, for instance, have been shown to reduce Spiroplasma-mediated protection in Drosophila. Our understanding of protective symbiosis requires a deeper understanding of environment-symbiont-protection links. Here, we dissect the effect of the thermal environment on Spiroplasma-mediated protection against Leptopilina boulardi in Drosophila melanogaster by examining the effect of temperature before, during and after wasp attack on fly survival and wasp success. We observed that the developmental temperature of the mothers of attacked larvae, but not the temperature of the attacked larvae themselves during or after wasp attack, strongly determines the protective influence of Spiroplasma. Cooler maternal environments were associated with weaker Spiroplasma protection of their progeny. The effect of developmental temperature on Spiroplasma-mediated protection is probably mediated by a reduction in Spiroplasma titre. These results indicate that historical thermal environment is a stronger determinant of protection than current environment. Furthermore, protection is a character with transgenerational nongenetic variation probably to produce complex short-term responses to selection. In addition, the cool sensitivity of the Spiroplasma-Drosophila symbioses contrasts with the more common failure of symbioses at elevated temperatures, indicating a need to understand the mechanistic basis of low temperature sensitivity on this symbiosis.

Developmental Temperature Shapes the Otolith Morphology of Metamorphosing and Juvenile Gilthead Seabream (Sparus aurata Linnaeus, 1758)

Otolith morphological variability is used as a reliable indicator to discriminate fish that experience different environmental conditions during their lifetimes. The present study examined the effects of developmental temperature (DT) during the egg and yolk-sac larval period on the otolith shape and asymmetry of Gilthead seabream in the later metamorphosis (56–58 days post-hatching, dph) and the early juvenile stage (93–95 dph). The experimental populations were reared at different water temperatures (17, 20, or 23 °C DT) from epiboly onset to the end of the yolk-sac larval stage (5–7 days post-fertilization, dpf) and then at a common rearing temperature (20 °C), up to the end of the trials (93–95 dph). Otolith shape and bilateral asymmetry were analyzed at metamorphosis (20–21 mm standard length, SL) and the early juvenile stage (31–32 mm SL). The results of elliptic Fourier analysis showed that DT significantly affected the otolith shape at both stages examined. Furthermore, elevated DT significantly increased the asymmetry levels of seabream otoliths in the early juvenile stage. The results are discussed in terms of the thermally induced long-term changes of seabream otolith morphology and the potential effects of the raised otolith asymmetry on wild seabream juveniles.

Spatial and temporal variation in phenotypes and fitness in response to developmental thermal environments

AbstractPhenotypic variation within populations is influenced by the environment via plasticity and natural selection. How phenotypes respond to the environment can vary among traits, populations and life stages in ways that can influence fitness.Plastic responses during early development are particularly important because they can affect components of fitness throughout an individual's life. Consequently, how natural selection shapes developmental plasticity could be influenced by fitness consequences across different life stages. Moreover, spatial variation in selection pressures could generate differences in plastic responses among populations.To gain insight into sources of variation in phenotypes and survival, we used a laboratory egg incubation experiment using brown anole lizardsAnolis sagreifrom mainland (ancestral) and island (descendent) populations, combined with a mark–release–recapture experiment in the field. Our study was designed to (a) quantify the effects developmental temperature on embryo development and offspring morphology, (b) assess how developmental temperature influences offspring survival across different life stages and (c) quantify how thermal reaction norms vary among ancestral and descendant populations.Developmental temperature influenced offspring morphology, but thermal reaction norms of embryos showed little variation among populations. Developmental temperature influenced offspring survival, but the patterns differed between embryo and hatchling stages; the optimal temperature for embryos was about 5℃ lower than that for hatchlings. High temperatures were thermally stressful to embryos, but they reduced incubation duration and led to early hatching. In turn, earlier hatching increased the probability of survival to adulthood. Moreover, the effect of developmental temperature on hatchling survival was most pronounced for offspring that hatched late in the season.The difference in optimal developmental temperatures between life stages may be driven by physiological tolerance for embryos and by ecological factors for hatchlings. Moreover, the fitness consequences of the developmental environment depend on the phenology of hatching. Overall, these results highlight how the developmental environment can differentially affect fitness across life stages and show that temporal thermal heterogeneity can influence survival of embryos, but the consequences on post‐hatching stages may vary at different times of the season.A freePlain Language Summarycan be found within the Supporting Information of this article.

The effect of ambient oxygen on the thermal performance of a cockroach, Nauphoeta cinerea.

The oxygen and capacity-limited thermal tolerance (OCLTT) hypothesis proposes that the thermal tolerance of an animal is shaped by its capacity to deliver oxygen in relation to oxygen demand. Studies testing this hypothesis have largely focused on measuring short-term performance responses in animals under acute exposure to critical thermal maximums. The OCLTT hypothesis, however, emphasises the importance of sustained animal performance over acute tolerance. The present study tested the effect of chronic hypoxia and hyperoxia during development on moderate to long-term performance indicators at temperatures spanning the optimal temperature for growth in the speckled cockroach, Nauphoeta cinerea In contrast to the predictions of the OCLTT hypothesis, development under hypoxia did not significantly reduce growth rate or running performance, and development under hyperoxia did not significantly increase growth rate or running performance. The effects of developmental temperature and oxygen on tracheal morphology and metabolic rate were also not consistent with OCLTT predictions, suggesting that oxygen delivery capacity is not the primary driver shaping thermal tolerance in this species. Collectively, these findings suggest that the OCLTT hypothesis does not explain moderate to long-term thermal performance in N.cinerea, which raises further questions about the generality of the hypothesis.

Developmental temperature affects phenotypic means and variability: A meta‐analysis of fish data

AbstractFishes are sensitive to their thermal environment and face an uncertain future in a warming world. Theoretically, populations in novel environments might express greater levels of phenotypic variability to increase the chance of surviving—and eventually thriving—in the new conditions. Most research on the effect of the early thermal environment in fish species focuses on average phenotypic effects rather than phenotypic variability, but to understand how fishes will respond to rising temperatures we need to consider both the average response of the population, as well as the breadth of individual responses. Here we present the first meta‐analysis on the effects of developmental temperature in fishes. Using data from 43 species and over 6,000 individual fish, we show that a change in developmental temperature induces a significant change in phenotypic means and variability, but differently depending on whether the temperature is increased or decreased. Decreases in temperature (cool environments) showed a significant decrease in phenotypic means and no change in phenotypic variability. Increases in temperature (warm environments) showed a non‐significant increase in phenotypic means and a marginally significant increase in phenotypic variability. Larger increases in temperature saw greater increases in phenotypic variability, but no increase in the mean phenotypic response. Together, our results suggest that fishes exhibit both directed and stochastic developmental plasticity in response to warming temperatures, which could facilitate or accelerate adaptation to a changing environment.

Plastic rates of development and the effect of thermal extremes on offspring fitness in a cold-climate viviparous lizard.

Populations at the climatic margins of a species' distribution can be exposed to conditions that cause developmental stress, resulting in developmental abnormalities. Even within the thermal range of normal development, phenotypes often vary with developmental temperature (i.e., thermal phenotypic plasticity). These effects can have significant consequences for organismal fitness and, thus, population persistence. Reptiles, as ectotherms, are particularly vulnerable to thermal effects on development and are, therefore, considered to be at comparatively high risk from changing climates. Understanding the extent and direction of thermal effects on phenotypes and their fitness consequences is crucial if we are to make meaningful predictions of how populations and species will respond as climates warm. Here, we experimentally manipulated the thermal conditions experienced by females from a high-altitude, cold-adapted population of the viviparous skink, Niveoscincus ocellatus, to examine the consequences of thermal conditions at the margins of this population's normal temperature range. We found strong effects of thermal conditions on the development of key phenotypic traits that have implications for fitness. Specifically, we found that offspring born earlier as a result of high temperatures during gestation had increased growth over the first winter of life, but there was no effect on offspring survival, nor was there an effect of developmental temperature on the incidence of developmental abnormalities. Combined, our results suggest that advancing birth dates that result from warming climates may have positive effects in this population via increased growth.

How important is thermal history? Evidence for lasting effects of developmental temperature on upper thermal limits in Drosophila melanogaster.

A common practice in thermal biology is to take individuals directly from the field and estimate a range of thermal traits. These estimates are then used in studies aiming to understand broad scale distributional patterns, understanding and predicting the evolution of phenotypic plasticity, and generating predictions for climate change risk. However, the use of field-caught individuals in such studies ignores the fact that many traits are phenotypically plastic and will be influenced by the thermal history of the focal individuals. The current study aims to determine the extent to which estimates of upper thermal limits (CTmax), a frequently used measure for climate change risk, are sensitive to developmental and adult acclimation temperatures and whether these two forms of plasticity are reversible. Examining a temperate and tropical population of Drosophila melanogaster we show that developmental acclimation has a larger and more lasting effect on CTmax than adult acclimation. We also find evidence for an interaction between developmental and adult acclimation, particularly when flies are acclimated for a longer period, and that these effects can be population specific. These results suggest that thermal history can have lasting effects on estimates of CTmax. In addition, we provide evidence that developmental and/or adult acclimation are unlikely to contribute to substantial shifts in CTmax and that acclimation capacity may be constrained at higher temperatures.

Population-specific effects of developmental temperature on body condition and jumping performance of a widespread European frog.

All physiological processes of ectotherms depend on environmental temperature. Thus, adaptation of physiological mechanisms to the thermal environments is important for achieving optimal performance and fitness. The European Common Frog, Rana temporaria, is widely distributed across different thermal habitats. This makes it an exceptional model for studying the adaptations to different thermal conditions. We raised tadpoles from Germany and Croatia at two constant temperature treatments (15°C, 20°C), and under natural temperature fluctuations (in outdoor treatments), and tested how different developmental temperatures affected developmental traits, that is, length of larval development, morphometrics, and body condition, as well as jumping performance of metamorphs. Our results revealed population‐specific differences in developmental time, body condition, and jumping performance. Croatian frogs developed faster in all treatments, were heavier, in better body condition, and had longer hind limbs and better jumping abilities than German metamorphs. The populations further differed in thermal sensitivity of jumping performance. While metamorphs from Croatia increased their jumping performance with higher temperatures, German metamorphs reached their performance maximum at lower temperatures. These population‐specific differences in common environments indicate local genetic adaptation, with southern populations being better adapted to higher temperatures than those from north of the Alps.

Cellular basis of morphological variation and temperature-related plasticity in Drosophila melanogaster strains with divergent wing shapes.

Organ shape evolves through cross-generational changes in developmental patterns at cellular and/or tissue levels that ultimately alter tissue dimensions and final adult proportions. Here, we investigated the cellular basis of an artificially selected divergence in the outline shape of Drosophila melanogaster wings, by comparing flies with elongated or rounded wing shapes but with remarkably similar wing sizes. We also tested whether cellular plasticity in response to developmental temperature was altered by such selection. Results show that variation in cellular traits is associated with wing shape differences, and that cell number may play an important role in wing shape response to selection. Regarding the effects of developmental temperature, a size-related plastic response was observed, in that flies reared at 16°C developed larger wings with larger and more numerous cells across all intervein regions relative to flies reared at 25°C. Nevertheless, no conclusive indication of altered phenotypic plasticity was found between selection strains for any wing or cellular trait. We also described how cell area is distributed across different intervein regions. It follows that cell area tends to decrease along the anterior wing compartment and increase along the posterior one. Remarkably, such pattern was observed not only in the selected strains but also in the natural baseline population, suggesting that it might be canalized during development and was not altered by the intense program of artificial selection for divergent wing shapes.

Intraspecific hybridization, life history strategies and potential invasion success in a parasitoid wasp

Classical biological control—the introduction of exotic species to permanently control pests—offers an applied framework to test ecological and evolutionary hypotheses derived from invasion biology. One such hypothesis is that intraspecific hybridization can facilitate invasions because hybrids express higher phenotypic mean and/or variance than their parents. We tested this hypothesis using the parasitoid wasp Psyttalia lounsburyi, a candidate biocontrol agent for the olive fly Bactrocera oleae. Under laboratory conditions, we found marked differentiations between two populations of wasps, from South Africa and Kenya, in terms of life history strategies. South African females were better reproducers than Kenyan females, but the opposite was observed for males. Reaction norms showed different effects of developmental temperature on fecundity depending on the genotype. However, neither heterosis nor hybrid breakdown were observed. Hence, in this system, sex-specific effects of hybridization and genotype-by-environment interactions jeopardize any straightforward prediction on the fitness of hybrids. Therefore, our paper contributes to tone down the hybrid advantage hypothesis in invasion biology.

Effect of developmental temperature on swimming performance of zebrafish (Danio rerio) juveniles

It is widely known that water temperature affects the swimming capacity of fish. But the effect of the rearing temperature on the swimming ability of the fish at later stages, has not had similar attention. In this study, four populations of zebrafish, were reared in different water temperatures (22, 25, 28 and 31°C) and after being acclimatized in a common temperature (26.5°C) for over a month, they were subjected to swimming trials in order to evaluate the maximum relative critical velocity (RU crit ) in each case. Fish that were reared in 22°C showed statistically significant lower performance than the ones reared in 31°C (7.72 ± 0.17 vs. 8.79 ± 0.28, means ± S.E.). Possible explanations for the observed differentiation could be the effect of early life temperature on fish muscle ontogeny or on body shape.

Temperature-dependent sex-biased embryo mortality in a bird

Sex ratios have important evolutionary consequences and are often biased by environmental factors. The effect of developmental temperature on offspring sex ratios has been widely documented across a diverse range of taxa but has rarely been investigated in birds and mammals. However, recent field observations and artificial incubation experiments have demonstrated that the hatching sex ratio of a megapode, the Australian brush-turkey (Alectura lathami), varied with incubation temperature; more females hatched at high incubation temperatures and more males hatched at low temperatures. Here, we investigated the causes of this temperature-dependent sex-biasing system. Molecular sexing of chicks and embryos confirmed that male embryo mortality was greater at high temperatures while female embryo mortality is greater at low temperatures, with mortality in both sexes similar at intermediate incubation temperatures. Temperature-dependent sex-biased embryo mortality represents a novel mechanism of altering sex ratios in birds. This novel mechanism, coupled with the unique breeding biology of the brush-turkey, offers a potentially unparalleled opportunity in which to investigate sex allocation theory in birds.

EFFECTS OF DEVELOPMENTAL ENVIRONMENT ON SIGNAL-PREFERENCE COUPLING IN A HAWAIIAN CRICKET

Previous work has suggested that developmental temperature influences expression of the adult male calling song of the cricket, a sexually selected mate recognition signal. The role of developmental temperature in shaping female preference functions, and thus its influence on signal-preference coupling has not been investigated. In this study, the effects of developmental temperature are examined in both males and females of the Hawaiian cricket, Laupala cerasina, to determine the degree of signal-preference matching between male song and female preference due to developmental environment. We found that rearing females in different temperature environments affected adult female acoustic preference functions in the same direction as male calling song, thereby influencing variation in adult reproductive behavior in such a way that male and female components remain coordinated. However, we further demonstrate that for male song, the effect of the rearing environment is not permanent but appears only to exert influence for a period of days. This mid-term temperature effect is distinct from the effect of short-term ambient temperature, which influences song in a matter of minutes and has been well documented. Signal-preference coordination, and sexual selection pressures due to mismatching within natural populations, likely will be influenced by nymphal developmental environments of males and females, as well as by adult singing and preference environments.

Bigger isn't always better: body size, developmental and parental temperature and male territorial success in Drosophila melanogaster

The effect of developmental temperature (18°C versus 25°C) on the body size and territorial success of male fruit flies, Drosophila melanogaster, in paired contests was examined. When tested at ambient temperatures of either 18°C or at 27°C, adult males raised at 25°C were relatively small in size but nevertheless had greater territorial success (control of a food/oviposition resource) than males raised at 18°C. This result negates a ‘size-advantage hypothesis’, which predicts that males raised at 18°C should be more successful at either contest temperature by virtue of their larger size. It also negates an ‘acclimation-advantage hypothesis’, which predicts that males raised at 18°C should be more successful than males raised at 25°C in contests at 18°C, but less successful at 27°C. The data are consistent, however, with an ‘optimal developmental temperature hypothesis’, which suggests that flies raised at 25°C, even though phenotypically small, are physiologically vigorous and will perform relatively well under diverse environmental circumstances. Thus, bigger isn't always better. In a small-scale experiment territoriality scored only at 27°C) in which all males had the same developmental temperature (25°C) males whose parents developed at 25°C were more successful than were males whose parents developed at 18°C. These experiments demonstrate that developmental temperatures, both within and between generations, influence territorial success in male flies.

On the developmental theory of ageing. II. The effect of developmental temperature on longevity in relation to adult body size in D. melanogaster.

Flies from a wild type strain of Drosophila melanogaster, previously kept at 25 degrees C, were reared at either 20, 25 or 29 degrees C. As expected, developmental time and adult body size decreased with increasing temperature. Adult longevity of flies reared at 25 degrees C was slightly greater than that of flies raised at 20 or 29 degrees C when measured at all three temperatures. This may reflect the laboratory history of the strain. On the whole, it appeared that longevity was independent of adult body size. These results support our previous conclusion (Zwaan et al., 1991) that developmental time and body size are not causally related to longevity in 'environmental' studies. It is stressed, that genetic analysis is needed to investigate the reputed correlation between development and ageing.

Low Temperature Development under Intermittent Light Conditions Results in the Formation of Etiochloroplasts

Summary The effects of developmental temperature on etioplast to chloroplast conversion were examined in winter rye ( Secale cereale L. cv. Muskateer) upon exposure to intermittent light. One cycle of intermittent light is defined as exposure to 2 min of incandescent light (10 µE m- 2 ·s -1 ) followed by 118 min of darkness. Although 5 °C intermittent light seedlings developed almost 2-fold higher chlorophyll levels after 48 to 80 cycles than 20 °C seedlings, both exhibited similar maximum photosystem I activities. Development of maximum photosystem I and photosystem II activity was delayed at 5 °C relative to that observed at 20 °C. Etiolated seedlings exposed to 48 cycles of intermittent light at 20 °C exhibited the normal light-dependent breakdown of prolamellar bodies and protochlorophyllide oxidoreductase followed by the appearance of thylakoid membranes. In contrast, the plastids developed at 5 °C appeared to be etiochloroplasts which exhibited prolamellar bodies, high levels of protochlorophyllide reductase in addition to thylakoid membranes. We suggest that during chloroplast biogenesis intermittent light at low developmental temperature inhibits the plastid proteases involved in the light-dependent breakdown of protochlorophyllide reductase.

IRREVERSIBLE NONGENETIC TEMPERATURE ADAPTATION OF OXYGEN UPTAKE IN CLONES OF THE SEA ANEMONE HALIPLANELLA LUCIAE (VERRILL).

1. Isogenic clones of H. luciae were raised at each of two developmental temperatures, 18° and 28° C. Despite prolonged acclimation to common thermal conditions, oxygen uptake rates differ according to the temperature of reproduction, regeneration and development. 2. The effects of developmental temperature, however, are masked by body size differences. Only when this variable is eliminated can the underlying effect of developmental temperature be detected. 3. The irreversible change is not due to an increase in the gas exchange surface area at the primary site of O2 uptake, the tentacles. 4. No qualitative changes in banding patterns for five enzymes (HK, PGI, IDH, MDH, G-6-PDH) were found.

The effect of developmental temperature on population flexibility in Drosophila melanogaster and D. simulans

Ten strains each of D. melanogaster and D. simulans were derived from single inseminated females of the same population. For each strain the influence of developmental temperatures in the range 12-30�C was considered for developmental time, egg to adult development percentage, sex ratio, longevity of adults, mating speed, fecundity and fertility. The species showed similar responses for all characters, although for the latter four D. simulans was more affected by extreme temperatures. Analyses of variance demonstrated temperature, strain, and temperature x strain effects to be generally significant. For sex ratio, however, temperature effects alone were significant. The results are discussed in relation to the level of genetical integration existing in a population and how such integration allows for considerable population flexibility.