Temperature dependence of development rate and adult size in Drosophila species: biophysical parameters

Adult size in Drosophila results from the ratio of the rate of biomass increase and the rate of differentiation, both rates being temperature sensitive. Data on rates and size are collected in two tropical and two temperate Drosophila species; differentiation rate is higher in the two tropical species, growth rate differs between the large and small species of similar climatic origin. A biophysical model is used to evaluate the temperature dependence of adult size in Drosophila. The model is based upon the Sharpe–Schoolfield equation connecting enzyme kinetics and biological rates. Temperature sensitivities of growth rate, development time, and wing and thorax size are characterized by biophysical parameters. The biophysical parameter indicating trait specific temperature sensitivity is lower in tropical species than in temperate species, both for growth rate and for differentiation rate. In the larger species of a climate pair, thorax size and wing size prove to differ in pattern of temperature dependence; in the smaller species of a geographical pair, thorax size and wing size have identical patterns of temperature dependence.     

The temperature-size rule in ectotherms: may a general explanation exist after all?

The majority of ectotherms mature at a larger size at lower rearing temperatures. Although this temperature-size rule is well established, a general explanation for this phenomenon has remained elusive. In this article, we address the problem by exploring the proximate and ultimate reasons for why a temperate grasshopper, Chorthippus brunneus, is an exception to the temperature-size rule. Using a complete set of life-history data to parameterize an established life-history model, we show that it is optimal for this species to mature at a larger size at higher temperatures. We also show that plasticity in adult size is determined by the relative difference between the minimum temperature thresholds for growth and development rates. The mechanism relates to aspects of the biophysical model of van der Have and de Jong. Ectotherms that obey the temperature-size rule are identified as having a higher temperature threshold for development rate than for growth rate; exceptions are identified as having a lower temperature threshold for development rate than for growth rate. The latter scenario may arise broadly in two ways. These are discussed in reference to the thermal biology of temperate grasshoppers and ectotherms in general.     

Temperature-mediated plasticity in egg and body size in egg size-selected lines of a butterfly

We examine genotype–environment interactions by using lines of the butterfly Bicyclus anynana artificially selected for differences in egg size in a full factorial design with two developmental and two oviposition temperatures. In accordance with the temperature–size rule, egg size and pupal mass increased by 4–5 and 8%, respectively, at lower temperatures. Genotype–environment interactions for both traits suggest that plasticity is largely independent of the trait value, and that there is potential for evolutionary change. These findings cast further doubt on the notion that temperature-mediated plasticity might be purely a physiological constraint.     

A comparison of different thermal performance functions describing temperature-dependent development rates

The impact of temperature on developmental duration of insects has been long kept a high profile in the studies of insect pests. The relationship between developmental rate, which is the reciprocal of developmental duration, is generally represented by a straight line over a range of moderate temperature; over two ranges of extreme temperature (i.e., low temperatures and high temperatures), the relationship cannot be accurately reflected by a straight line (Campbell et al., 1974). For describing the effect of constant temperature on developmental rate over the full range of temperature, some non-linear models were proposed. To analyze the effect of temperature on ectothermic performance, twelve non-linear functions, including Gaussian, Logan1, Logan2, Performance, Wang–Lan–Ding, Sharpe–Schoolfield, Ratkowsky, Brière1, Brière2, Weibull, modified Gaussian and exponentially modified Gaussian functions, are compared using the coefficient of determination, adjusted coefficient of determination, Akaike information criterion (AIC), Bayesian information criterion (BIC), corrected Akaike information criterion (AICC) and a new method best on a weighted average of the five listed indicators. These models were compared using the development rate data of two species of insects at the egg stage. We found that the Performance, Brière1 and Brière2 functions are all very suitable for explaining temperature-dependent development rates. The three functions both belong to the asymmetrical skew thermal performance curves, and show better goodness-of-fit than the symmetrical Gaussian function. The Performance function might be the best function, because it can reflect the linearity between temperatures and developmental rates below the optimal developmental temperature.     

A Caenorhabditis elegans Wild Type Defies the Temperature–Size Rule Owing to a Single Nucleotide Polymorphism in tra-3

Ectotherms rely for their body heat on surrounding temperatures. A key question in biology is why most ectotherms mature at a larger size at lower temperatures, a phenomenon known as the temperature–size rule. Since temperature affects virtually all processes in a living organism, current theories to explain this phenomenon are diverse and complex and assert often from opposing assumptions. Although widely studied, the molecular genetic control of the temperature–size rule is unknown. We found that the Caenorhabditis elegans wild-type N2 complied with the temperature–size rule, whereas wild-type CB4856 defied it. Using a candidate gene approach based on an N2 × CB4856 recombinant inbred panel in combination with mutant analysis, complementation, and transgenic studies, we show that a single nucleotide polymorphism in tra-3 leads to mutation F96L in the encoded calpain-like protease. This mutation attenuates the ability of CB4856 to grow larger at low temperature. Homology modelling predicts that F96L reduces TRA-3 activity by destabilizing the DII-A domain. The data show that size adaptation of ectotherms to temperature changes may be less complex than previously thought because a subtle wild-type polymorphism modulates the temperature responsiveness of body size. These findings provide a novel step toward the molecular understanding of the temperature–size rule, which has puzzled biologists for decades.     

Could the intrinsic rate of increase represent the fitness in terrestrial ectotherms?

The intrinsic rate of increase (r_m) has been considered as an important indicator of fitness in terrestrial ectotherms since long. It is actually an equivalent to the instantaneous growth rate of the exponential equation for describing the density-independent population growth. In terrestrial ectotherms, r_m has been demonstrated to be temperature-dependent. The temperature at which r_m was maximal, was considered to be the “optimal” temperature for fitness in Amarasekare and Savage (2012), but this definition needs further analysis. Only r_m cannot provide thorough representation of fitness. Because body size can affect the competitive abilities in many terrestrial ectotherms, both population size and body size should be considered in measuring the fitness of ectotherms. The rule of “bigger is better” requires relatively low temperature to increase in body size, whereas relatively high temperature is required for a rapid increase in population size. Thus, there is presumably a trade-off in temperature for adjusting individual body size and population size to achieve maximum fitness. We hypothesized that this temperature could be reflected by the intrinsic optimum temperature for developmental rate in the Sharpe–Schoolfield–Ikemoto model, and it led to a temperature estimate around 20 °C. However, the traditional viewpoint based on the temperature corresponding to the maximal intrinsic rate of increase provides a temperature estimate around 30 °C. This study suggests that a low temperature around 20 °C might authentically represent the optimal ambient temperature for fitness in terrestrial ectotherms. It implies that thermal biologists who are interested in the effect of temperature on the fitness in terrestrial ectotherms should pay more attention to their performance at low temperature rather than high temperature.     

Life-history responses of the rice stem borer Chilo suppressalis to temperature change: Breaking the temperature–size rule

Temperature is a key environmental factor for ectotherms and affects a large number of life history traits. In the present study, development time from hatching to pupation and adult eclosion, pupal and adult weights of the rice stem borer, Chilo suppressalis were examined at 22, 25, 28 and 31 °C under L18:D 6. Larval and pupal times were significantly decreased with increasing rearing temperature and growth rate was positively correlated with temperature. Larval and pupal developmental times were not significantly different between females and males. The relationship between body weight and rearing temperature in C. suppressalis did not follow the temperature–size rule (TSR), both males and females gained the highest body weight at 31 °C. Females were significantly larger than males at all temperatures, showing a female biased sex size dimorphism (SSD). Contrary to Rensch's rule, SSD and body weight in C. suppressalis tended to increase with rising temperature. Male pupae lost significantly more weight at metamorphosis compared to females. We discuss the adaptive significance of the reverse-TSR in the moth's life history.     

Breaking the temperature-size rule: Thermal effects on growth,development and fecundity of a crustacean from temporary waters

The temperature-size rule (TSR) is a well-established phenomenon to describe the growth response of ectotherms to temperature by which individuals maintained at low temperatures grow more slowly, but attain a larger size upon maturity. Although there are adaptive and non-adaptive theories about the plasticity of body size in response to temperature, these cannot be applied to all ectotherms, and little is known about the changes in growth and development rates through ontogeny. The ostracod species Heterocypris bosniaca, an inhabitant of freshwater temporary ponds, was used to examine the growth and development rates of its nine growth stages and female fecundity at four different temperatures (15 °C, 20 °C, 25 °C and 30 °C). The development rate of this species accelerates with increasing temperature, reaching a maximum value at 25 °C. The growth factor has a reverse-TSR in younger instars, and the typical TSR is followed only in the last two moults, resulting in non-monotonic response of adult size to temperature. Fecundity (total offspring per female) was not directly related to adult size and was generally higher at lower temperatures. Our results agree with recent research showing that the TSR may vary during ontogeny, and may not be a general trend in ostracod species from temporary waters. Indeed, adult carapace size seems to follow the pattern of a thermal reaction norm, probably influenced by the reduction of oxygen bioavailability at low temperature and the drastic increase in metabolic demand at the upper extreme of the thermal gradient.     

New modified Square Root and Schoolfield models for predicting bacterial growth rate as a function of temperature

Summary A new modified Square Root model and two new modified Schoolfield models were evaluated for their ability to predict the growth rate ofYersinia enterocolitica as a function of temperature. The new Square Root model fits the data better than both the original Square Root model and the Zwietering Square Root model. Both new Schoolfield models, a six-and a four-parameter equation, fit the data better than the original Schoolfield model. The new four-parameter Schoolfield model was developed by removing the term describing low temperature inactivation from the new six-parameter Schoolfield model. Inclusion of the two extra parameters in the new six-parameter Schoolfield model (F=318) did not significantly improve the fit compared to the new fourparameter Schoolfield model (F=488).     

Effects of temperature on life‐history traits of the newly invasive fall armyworm,Spodoptera frugiperda in Southeast China

In mid‐May, 2019, the fall armyworm (FAW) Spodoptera frugiperda invaded Jiangxi Province, China, and caused extensive damage to corn crops. However, little attention has been given to the life‐history traits of the FAW. In the present study, we systematically investigated the life‐history traits of the newly invasive FAW on corn leaves at 19, 22, 25, 28, and 31°C under a photoperiod of LD 15:9 hr. The FAW thrived on the corn leaves with short developmental periods, high survival rates of larvae and pupae, very high mating success rates, and high fecundity. The pupal developmental stage was significantly longer in males than females at all temperatures, thus resulting in a protogyny phenomenon. The pupal weight was heaviest after a relatively shorter larval development stage at a higher temperature (25°C); thus, the FAW did not follow the temperature–size rule. Females were smaller than males, indicating sexual size dimorphism. A small proportion of females delayed their pre‐oviposition period and began to lay eggs on the 7th to 9th day after adult emergence. There were positive relationships between pupal weight and larval developmental time and between adult weight and fecundity. There was a negative relationship between fecundity and longevity. These findings can help us to predict the population dynamics of the FAW on corn and to develop a suitable and practical management strategy.     

Variation of life‐history traits of the Asian corn borer,Ostrinia furnacalis in relation to temperature and geographical latitude

Life‐history traits from four geographical populations (tropical Ledong population [LD], subtropical Guangzhou [GZ] and Yongxiu populations, and temperate Langfang population [LF]) of the Asian corn borer, Ostrinia furnacalis were investigated at a wide range of temperatures (20–32°C). The larval and pupal times were significantly decreased with increasing rearing temperature, and growth rate was positively correlated with temperature. The relationship between body weight and rearing temperature in O. furnacalis did not follow the temperature–size rule (TSR); all populations exhibited the highest pupal and adult weights at high temperatures or intermediate temperatures. However, development time, growth rate, and body weight did not show a constant latitudinal gradient. Across all populations at each temperature, female were significantly bigger than males, showing a female‐biased sexual size dimorphism (SSD). Contrary to Rensch's rule, the SSD tended to increase with rising temperature. The subtropical GZ population exhibited the largest degree of dimorphism while the temperate LF exhibited the smallest. Male pupae lose significantly more weight at metamorphosis compared to females. The proportionate weight losses of different populations were significantly different. Adult longevity was significantly decreased with increasing temperature. Between sexes, all populations exhibit a rather female‐biased adult longevity. Finally, we discuss the adaptive significance of higher temperature‐inducing high body weight in the moth's life history and why the moth exhibits the reverse TSR.     

Reaction norms for age and size at maturity in response to temperature: a test of the compound interest hypothesis

In ectotherms, temperature induces similar developmental and evolutionary responses in body size, with larger individuals occurring or evolving in low temperature environments. Based on the occasional occurrence of opposite size clines, showing a decline in body size with increasing latitude, an interaction between generation time and growing season length was suggested to account for the patterns found. Accordingly, multivoltine species with short generation times should gain high compound interest benefits from reproducing early at high temperatures, indicating potential for extra generations, even at the expense of being smaller. This should not apply for obligatorily monovoltine populations. We explicitly test the prediction that monovoltine populations (no compound interest) should be selected for large body size to maximise adult fitness, and therefore size at maturity should respond only weakly to temperature. In two monovoltine populations (an Alpine and a Western German one) of the butterfly Lycaena hippothoe, increasing temperatures had no significant effect on pupal weight and caused a slight decrease in adult weight only. In contrast, two closely related, yet potentially multivoltine Lycaena populations showed a greater weight loss at increasing temperature (in protandrous males, but not in females) and smaller adult sizes throughout. Thus, the results do support our predictions indicating that the compound interest hypothesis may yield causal explanations for the relationship between temperature and insect size at maturity. At all temperatures, the alpine population had higher growth rates and concomitantly shorter development times (not accompanied by a reduction in size) than the other, presumably indicating local adaptations to different climates.     

Why get big in the cold? Towards a solution to a life-history puzzle

The temperature–size rule (TSR), which states that body size increases at lower developmental temperatures, appears to be a near-universal law for ectotherms. Although recent studies seem to suggest that the TSR might be adaptive, the underlying developmental mechanisms are thus far largely unknown. Here, we investigate temperature effects on life-history traits, behaviour and physiology in the copper butterfly Lycaena tityrus in order to disentangle the mechanistic basis for the above rule. In L. tityrus the larger body size produced at a lower temperature was proximately due to a greater increase in mass, which was caused by both behavioural and physiological mechanisms: a much-increased food intake and a higher efficiency in converting ingested food into body matter. These mechanisms, combined with temperature-induced changes at the cellular level, may provide general explanations for the TSR. Body fat and protein content increased in butterflies reared at the higher temperature, indicating favourable growth conditions. As predicted from protandry theory, males showed reduced development times, caused by higher growth rates compared to females. The latter was itself related to a higher daily food consumption, while the total food consumption (due to the females’ longer developmental period) and assimilation was higher in females and may underly the sexual body size dimorphism.     

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.     

Temperature limits to early development of the New Zealand sea urchin Evechinus chloroticus (Valenciennes, 1846)

Seawater temperature is an important environmental factor for the early life stages of marine invertebrates. In this study we evaluated and described the effects of temperature during early development of E. chloroticus, identifying the optimum temperature range and upper thermal limit for successful development. The temperature range evaluated was between 15–24 °C which included the normal seawater temperatures during the spawning season in northern New Zealand, as well as the highest temperature projected by the IPCC for this region due to global warming (1–3 °C by the year 2100). Gametes from several females and males were used in the experiment. Fertilization was carried out at different temperatures and development was monitored at different time points after fertilization in each temperature. The development rate of E. chloroticus increased with an increase in seawater temperature. However, at temperatures higher than 21.5 °C the amount of abnormal development reached ∼30%. The optimum temperature for early development was between 15–21 °C, whereas the upper thermal limit was ∼24 °C. Therefore, early development of E. chloroticus is negatively affected by an increase in seawater temperature of ∼3–4 °C above current seawater temperature levels in northern New Zealand. The thermal sensitivity of early life stages of E. chloroticus could affect survival rates during early development of this species in a global warming scenario, which could impair recruitment in populations which are exposed to higher temperatures, leading to possible distributional shifts of this species.     

Evaluation of data transformations used with the square root and schoolfield models for predicting bacterial growth rate.

A comparison was made between mathematical variations of the square root and Schoolfield models for predicting growth rate as a function of temperature. The statistical consequences of square root and natural logarithm transformations of growth rate use in several variations of the Schoolfield and square root models were examined. Growth rate variances of Yersinia enterocolitica in brain heart infusion broth increased as a function of temperature. The ability of the two data transformations to correct for the heterogeneity of variance was evaluated. A natural logarithm transformation of growth rate was more effective than a square root transformation at correcting for the heterogeneity of variance. The square root model was more accurate than the Schoolfield model when both models used natural logarithm transformation.     

Growth temperature and phenotypic plasticity in two Drosophila sibling species: probable adaptive changes in flight capacities

In the sibling species Drosophila melanogaster and D. simulans, growth and development at constant temperatures, from 12 to 30 °C, resulted in extensive variations of adult size and flight parameters with significant differences between species. Changes in body weight, thorax length and wing length were nonlinear, with maximum values of each trait at lower temperatures for D. simulans than for its sibling species. By contrast, the wing/thorax ratio and the wing loading varied monotonically with growth temperature. These traits were negatively correlated, the wing/thorax ratio decreasing with growth temperature while the wing loading increased. Wing/thorax ratio, which is easier to measure, thus appears as a convenient predictor of wing loading. During tethered flight at the same ambient temperature, the wingbeat frequency changed linearly as a function of the wing moment of inertia. More interestingly, the beat rate was strongly correlated with the increase of wing loading at growth temperature above 13 °C. The likely adaptive significance of these morphometrical changes for flight efficiency is discussed.     

Inter- and intraspecific relationships between performance and temperature in a cryptic species complex of the rotifer Brachionus plicatilis

The strategy of decreasing size with increasing temperature operates at regional and phenotypic scale and presents a puzzle to researchers. In this work, we studied two aspects of the temperature–performance relationship along a temperature gradient, (i) comparing the population growth rates of three cryptic Brachionus species differing in adult size, and (ii) assessing the phenotypic plasticity of adult size, in one clone per species. The working hypotheses were that (i) the bigger the species the lower its optimal temperature for population growth, and (ii) the higher the temperature the smaller the individual within each focal species. The results showed that (i) the optimal temperature for population growth is related to species size in a manner foreseen by Bergmanns’ rule for two of the three species (the third, biggest species, performed evenly well at all temperatures examined, what could be explained by its generally eurioic character), and that (ii) the strategy of body size adjustment to environmental temperature differs between species and may depend on the level of temperature specialization. This work demonstrated the usefulness of inter- and intraspecific comparisons for studying the role of growth strategies in adaptation to temperature.     

Postembryonic growth in two species of freshwater Ostracoda (Crustacea) shows a size-age sigmoid model fit and temperature effects on development time, but no clear temperature-size rule (TSR) pattern

Although the temperature-size rule is a widespread phenomenon that describes the impact of temperature on the intraspecific size of ectotherms, what determines the wide intrinsic variation in moult increment and the intermoult period within and between Crustacea species remains unknown. This work characterizes the growth of freshwater ostracods Chlamydotheca incisa and Strandesia bicuspis under different controlled temperatures and identifies growth patterns. Animals were collected from temporary ponds in Argentina. The experiment was done at two constant temperatures: 17 and 23 °C. The intermoult time and the time from hatching to the final moult were calculated. Three different growth regression equations were tested: von Bertalanffy and two sigmoidal models (Sigmoid and Gompertz). For both species, significant differences in the duration of each instar were found by comparing individuals grown at 17 and at 23 °C. A strong temperature effect was noted on intermoult time but not on growth factors. The best model selected for the size-age relationship was a sigmoid growth type, indicating accelerated growth in the earliest juvenile instars. These results challenge the widely-accepted application of nonsigmoidal growth models and are in agreement with recent analyses of growth patterns in aquatic invertebrates when early juvenile instars are considered.