Macroevolutionary pattern of sexual size dimorphism in geckos corresponds to intraspecific temperature‐induced variation

Many animal lineages exhibit allometry in sexual size dimorphism (SSD), known as ‘Rensch’s rule’. When applied to the interspecific level, this rule states that males are more evolutionary plastic in body size than females and that male‐biased SSD increases with body size. One of the explanations for the occurrence of Rensch’s rule is the differential‐plasticity hypothesis assuming that higher evolutionary plasticity in males is a consequence of larger sensitivity of male growth to environmental cues. We have confirmed the pattern consistent with Rensch’s rule among species of the gecko genus Paroedura and followed the ontogeny of SSD at three constant temperatures in a male‐larger species (Paroedura picta). In this species, males exhibited larger temperature‐induced phenotypic plasticity in final body size than females, and body size and SSD correlated across temperatures. This result supports the differential‐plasticity hypothesis and points to the role phenotypic plasticity plays in generating of evolutionary novelties.     

Lipid content of terrestrial arthropods in relation to body size,phylogeny, ontogeny and sex

Energy storage in arthropods has important implications for survival and reproduction. The lipid content of 276 species of adult arthropods with wet mass in the range 0.2–6.13 g is determined to assess how lipid mass scales with body mass. The relative contribution of lipids to total body mass is investigated with respect to phylogeny, ontogeny and sex. The lipid content of adult insects, arachnids, and arthropods in general shows an isometric scaling relationship with respect to body mass (M) (M_{arthropod lipid} = ?1.09 ×M_dry^1.01 and M_{arthropod lipid} = ?1.00 ×M_lean^0.98). However, lipid allocation varies between arthropod taxa, as well as with sex and developmental stage within arthropod taxa. Female insects and arachnids generally have higher lipid contents than males, and larval holometabolous insects and juvenile arachnids have higher lipid contents than adults.     

Rapid prey‐induced shift in body size in an isolated snake population (Notechis scutatus,Elapidae)

Abstract Geographic divergence in phenotypic traits between long‐isolated populations likely has a genetic basis, but can phenotypic plasticity generate such divergence rapidly in the initial stages of isolation? Australian tiger snakes (Notechis scutatus, Elapidae) provide a classic model system for the evolution of body size: mean adult sizes are relatively invariant in mainland populations, but many offshore islands have dwarf or giant populations. Previous work has shown a genetic basis to this divergence in long‐isolated islands (>10 000 years), but what of the initial stages of this process? Human translocation of mainland snakes to Carnac Island 90 years ago gives us a unique opportunity to assess the proximate reasons for the giant size of Carnac Island animals compared with mainland conspecifics. Our data suggest a major role for phenotypic plasticity. Feeding trials on captive snakes from both island and mainland populations showed a strong link between food intake and growth rates, similar in the two populations. Snakes given abundant food grew much larger than we have ever recorded in the wild, demonstrating that observed mean body sizes are driven by food availability rather than genetic limits to growth. In combination with earlier work showing genetic divergence in growth rates in snakes from long‐isolated islands, our data suggest that geographical divergence in mean adult body sizes in this system initially is driven by a rapid shift due to phenotypic plasticity, with the divergence later canalized by a gradual accumulation of genetic differentiation.     

Warming alters the size spectrum and shifts the distribution of biomass in freshwater ecosystems

Organism size is one of the key determinants of community structure, and its relationship with abundance can describe how biomass is partitioned among the biota within an ecosystem. An outdoor freshwater mesocosm experiment was used to determine how warming of～4 °C would affect the size, biomass and taxonomic structure of planktonic communities. Warming increased the steepness of the community size spectrum by increasing the prevalence of small organisms, primarily within the phytoplankton assemblage and it also reduced the mean and maximum size of phytoplankton by approximately one order of magnitude. The observed shifts in phytoplankton size structure were reflected in changes in phytoplankton community composition, though zooplankton taxonomic composition was unaffected by warming. Furthermore, warming reduced community biomass and total phytoplankton biomass, although zooplankton biomass was unaffected. This resulted in an increase in the zooplankton to phytoplankton biomass ratio in the warmed mesocosms, which could be explained by faster turnover within the phytoplankton assemblages. Overall, warming shifted the distribution of phytoplankton size towards smaller individuals with rapid turnover and low standing biomass, resulting in a reorganization of the biomass structure of the food webs. These results indicate future environmental warming may have profound effects on the structure and functioning of aquatic communities and ecosystems.     

Repeatable inter‐individual variation in the thermal sensitivity of metabolic rate

Assessing whether trait variations among individuals are consistent over time and among environmental conditions is crucial to understand evolutionary responses to new selective pressures such as climate change. According to the universal thermal dependence hypothesis, thermal sensitivity of metabolic rate should not vary strongly and consistently among organisms, implying limited evolutionary response for metabolic traits under climate change. However, this hypothesis has been rarely tested at an individual level, leaving a gap in our understanding of climate change impacts on metabolic responses and their potential evolution. Using the amphipod Gammarus fossarum, we investigated the variability and repeatability of individual metabolic thermal reaction norms over time. We found large variations in both the thermal sensitivity (i.e. slope) and expression level (i.e. intercept) of individual metabolic reaction norms. Moreover, differences among individuals were consistent over time, and therefore repeatable. Inter‐individual variations in body mass resulted in a high repeatability of metabolic expression level but had no significant effect on the repeatability of thermal sensitivity. Overall, our results highlight that inter‐individual variability and repeatability of thermal reaction norms can be substantial. We conclude that these consistent differences among individuals should not be overlooked when apprehending the ecological and evolutionary effects of climate change.     

Experimental evidence of gradual size‐dependent shifts in body size and growth of fish in response to warming

A challenge facing ecologists trying to predict responses to climate change is the few recent analogous conditions to use for comparison. For example, negative relationships between ectotherm body size and temperature are common both across natural thermal gradients and in small‐scale experiments. However, it is unknown if short‐term body size responses are representative of long‐term responses. Moreover, to understand population responses to warming, we must recognize that individual responses to temperature may vary over ontogeny. To enable predictions of how climate warming may affect natural populations, we therefore ask how body size and growth may shift in response to increased temperature over life history, and whether short‐ and long‐term growth responses differ. We addressed these questions using a unique setup with multidecadal artificial heating of an enclosed coastal bay in the Baltic Sea and an adjacent reference area (both with unexploited populations), using before‐after control‐impact paired time‐series analyses. We assembled individual growth trajectories of ~13,000 unique individuals of Eurasian perch and found that body growth increased substantially after warming, but the extent depended on body size: Only among small‐bodied perch did growth increase with temperature. Moreover, the strength of this response gradually increased over the 24 year warming period. Our study offers a unique example of how warming can affect fish populations over multiple generations, resulting in gradual changes in body growth, varying as organisms develop. Although increased juvenile growth rates are in line with predictions of the temperature–size rule, the fact that a larger body size at age was maintained over life history contrasts to that same rule. Because the artificially heated area is a contemporary system mimicking a warmer sea, our findings can aid predictions of fish responses to further warming, taking into account that growth responses may vary both over an individual's life history and over time.     

The underestimated role of temperature–oxygen relationship in large‐scale studies on size‐to‐temperature response

The observation that ectotherm size decreases with increasing temperature (temperature‐size rule; TSR) has been widely supported. This phenomenon intrigues researchers because neither its adaptive role nor the conditions under which it is realized are well defined. In light of recent theoretical and empirical studies, oxygen availability is an important candidate for understanding the adaptive role behind TSR. However, this hypothesis is still undervalued in TSR studies at the geographical level. We reanalyzed previously published data about the TSR pattern in diatoms sampled from Icelandic geothermal streams, which concluded that diatoms were an exception to the TSR. Our goal was to incorporate oxygen as a factor in the analysis and to examine whether this approach would change the results. Specifically, we expected that the strength of size response to cold temperatures would be different than the strength of response to hot temperatures, where the oxygen limitation is strongest. By conducting a regression analysis for size response at the community level, we found that diatoms from cold, well‐oxygenated streams showed no size‐to‐temperature response, those from intermediate temperature and oxygen conditions showed reverse TSR, and diatoms from warm, poorly oxygenated streams showed significant TSR. We also distinguished the roles of oxygen and nutrition in TSR. Oxygen is a driving factor, while nutrition is an important factor that should be controlled for. Our results show that if the geographical or global patterns of TSR are to be understood, oxygen should be included in the studies. This argument is important especially for predicting the size response of ectotherms facing climate warming.     

Diatoms can be an important exception to temperature–size rules at species and community levels of organization

Climate warming has been linked to an apparent general decrease in body sizes of ectotherms, both across and within taxa, especially in aquatic systems. Smaller body size in warmer geographical regions has also been widely observed. Since body size is a fundamental determinant of many biological attributes, climate‐warming‐related changes in size could ripple across multiple levels of ecological organization. Some recent studies have questioned the ubiquity of temperature–size rules, however, and certain widespread and abundant taxa, such as diatoms, may be important exceptions. We tested the hypothesis that diatoms are smaller at warmer temperatures using a system of geothermally heated streams. There was no consistent relationship between size and temperature at either the population or community level. These field data provide important counterexamples to both James’ and Bergmann's temperature–size rules, respectively, undermining the widely held assumption that warming favours the small. This study provides compelling new evidence that diatoms are an important exception to temperature–size rules for three reasons: (i) we use many more species than prior work; (ii) we examine both community and species levels of organization simultaneously; (iii) we work in a natural system with a wide temperature gradient but minimal variation in other factors, to achieve robust tests of hypotheses without relying on laboratory setups, which have limited realism. In addition, we show that interspecific effects were a bigger contributor to whole‐community size differences, and are probably more ecologically important than more commonly studied intraspecific effects. These findings highlight the need for multispecies approaches in future studies of climate warming and body size.     

The influence of ecological and life history factors on ectothermic temperature–size responses: Analysis of three Lycaenidae butterflies (Lepidoptera)

Body size has been shown to decrease with increasing temperature in many species, prompting the suggestion that it is a universal ecological response. However, species with complex life cycles, such as holometabolous insects, may have correspondingly complicated temperature–size responses. Recent research suggests that life history and ecological traits may be important for determining the direction and strength of temperature–size responses. Yet, these factors are rarely included in analyses. Here, we aim to determine whether the size of the bivoltine butterfly, Polyommatus bellargus, and the univoltine butterflies, Plebejus argus and Polyommatus coridon, change in response to temperature and whether these responses differ between the sexes, and for P. bellargus, between generations. Forewing length was measured using digital specimens from the Natural History Museum, London (NHM), from one locality in the UK per species. The data were initially compared to annual and seasonal temperature values, without consideration of life history factors. Sex and generation of the individuals and mean monthly temperatures, which cover the growing period for each species, were then included in analyses. When compared to annual or seasonal temperatures only, size was not related to temperature for P. bellargus and P. argus, but there was a negative relationship between size and temperature for P. coridon. When sex, generation, and monthly temperatures were included, male adult size decreased as temperature increased in the early larval stages, and increased as temperature increased during the late larval stages. Results were similar but less consistent for females, while second generation P. bellargus showed no temperature–size response. In P. coridon, size decreased as temperature increased during the pupal stage. These results highlight the importance of including life history factors, sex, and monthly temperature data when studying temperature–size responses for species with complex life cycles.     

Within-population variation in body size plasticity in response to combined nutritional and thermal stress is partially independent from variation in development time

Ongoing climate change has forced animals to face changing thermal and nutritional environments. Animals can adjust to such combinations of stressors via plasticity. Body size is a key trait influencing organismal fitness, and plasticity in this trait in response to nutritional and thermal conditions varies among genetically diverse, locally adapted populations. The standing genetic variation within a population can also influence the extent of body size plasticity. We generated near-isogenic lines from a newly collected population of Drosophila melanogaster at the mid-point of east coast Australia and assayed body size for all lines in combinations of thermal and nutritional stress. We found that isogenic lines showed distinct underlying patterns of body size plasticity in response to temperature and nutrition that were often different from the overall population response. We then tested whether plasticity in development time could explain, and therefore regulate, variation in body size to these combinations of environmental conditions. We selected five genotypes that showed the greatest variation in response to combined thermal and nutritional stress and assessed the correlation between response of developmental time and body size. While we found significant genetic variation in development time plasticity, it was a poor predictor of body size among genotypes. Our results therefore suggest that multiple developmental pathways could generate genetic variation in body size plasticity. Our study emphasizes the need to better understand genetic variation in plasticity within a population, which will help determine the potential for populations to adapt to ongoing environmental change.     

Long‐term declines in body size and shifts in run timing of Atlantic salmon in Ireland

Records extending back from three to seven decades from Atlantic salmon Salmo salar fisheries on the Blackwater, Newport and Owenduff River systems in Ireland, were used to test the hypothesis that there have been progressive declines in size and associated shifts in run timing. They showed identical patterns in four respects: 1) peaks of catch, in spring (March to April) and summer (June to July), 2) the largest fish were caught in the spring, with declines in size over the summer and a slight increase in autumn, 3) marked declines over time in average size and in the proportion of the Atlantic salmon taken in spring and 4) reductions in size in most months at all three sites. Correlations were also detected in average fish mass among the rivers over time (especially the Owenduff and Newport systems), showing a slight rise from the late 1960s until the late 1970s, followed by a steep decline. Data from an electronic counter on the Blackwater showed a reduction in the abundance of early migrants. The early fish were apparently much more vulnerable to fishing than later migrants, so the catch records overstated the abundance of early fish. These long‐term declines in size, which have been noted elsewhere, may be due to other factors in addition to changes in marine productivity. Specifically, reduction in the abundance of large, spring‐running Atlantic salmon may be due to selection resulting from heavy angler exploitation.     

Recent spatial and temporal changes in body size of terrestrial vertebrates: probable causes and pitfalls

Geographical and temporal variations in body size are common phenomena among organisms and may evolve within a few years. We argue that body size acts much like a barometer, fluctuating in parallel with changes in the relevant key predictor(s), and that geographical and temporal changes in body size are actually manifestations of the same drivers. Frequently, the principal predictors of body size are food availability during the period of growth and ambient temperature, which often affects food availability. Food availability depends on net primary productivity that, in turn, is determined by climate and weather (mainly temperature and precipitation), and these depend mainly on solar radiation and other solar activities. When the above predictors are related to latitude the changes have often been interpreted as conforming to Bergmann's rule, but in many cases such interpretations should be viewed with caution due to the interrelationships among various environmental predictors. Recent temporal changes in body size have often been related to global warming. However, in many cases the above key predictors are not related to either latitude and/or year, and it is the task of the researcher to determine which particular environmental predictor is the one that determines food availability and, in turn, body size. The chance of discerning a significant change in body size depends to a large extent on sample size (specimens/year). The most recent changes in body size are probably phenotypic, but there are some cases in which they are partly genetic.     

Insular shifts in body size of rice frogs in the Zhoushan Archipelago, China

1. Differences in body size between mainland and island populations have been reported for reptiles, birds and mammals. Despite widespread recognition of insular shifts in body size in these taxa, there have been no reports of such body size shifts in amphibians. 2. We provide the first evidence of an insular shift in body size for an amphibian species, the rice frog Rana limnocharis. We found significant increases in body size of rice frogs on most sampled islands in the Zhoushan archipelago when compared with neighbouring mainland China. 3. Large body size in rice frogs on islands was significantly related to increased population density, in both breeding and non-breeding seasons. Increases in rice frog density were significantly related to higher resource availability on islands. Increased resource availability on islands has led to higher carrying capacities, which has subsequently facilitated higher densities and individual growth rates, resulting in larger body size in rice frogs. We also suggest that large body size has evolved on islands, as larger individuals are competitively superior under conditions of harsh intraspecific competition at high densities. 4. Increases in body size in rice frogs were not related to several factors that have been implicated previously in insular shifts in body size in other taxa. We found no significant relationships between body size of rice frogs and prey size, number of larger or smaller frog species, island area or distance of islands from the mainland. 5. Our findings contribute to the formation of a broad, repeatable ecological generality for insular shifts in body size across a range of terrestrial vertebrate taxa, and provide support for recent theoretical work concerning the importance of resource availability for insular shifts in body size.     

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.     

Smaller,more diverse and on the way to the top: Rapid community shifts of montane wild bees within an extraordinary hot decade

Aim

Global warming is assumed to restructure mountain insect communities in space and time. Theory and observations along climate gradients predict that insect abundance and richness, especially of small-bodied species, will increase with increasing temperature. However, the specific responses of single species to rising temperatures, such as spatial range shifts, also alter communities, calling for intensive monitoring of real-world communities over time.

Location

German Alps and pre-alpine forests in south-east Germany.

Methods

We empirically examined the temporal and spatial change in wild bee communities and its drivers along two largely well-protected elevational gradients (alpine grassland vs. pre-alpine forest), each sampled twice within the last decade.

Results

We detected clear abundance-based upward shifts in bee communities, particularly in cold-adapted bumble bee species, demonstrating the speed with which mobile organisms can respond to climatic changes. Mean annual temperature was identified as the main driver of species richness in both regions. Accordingly, and in large overlap with expectations under climate warming, we detected an increase in bee richness and abundance, and an increase in small-bodied species in low- and mid-elevations along the grassland gradient. Community responses in the pre-alpine forest gradient were only partly consistent with community responses in alpine grasslands.

Main Conclusion

In well-protected temperate mountain regions, small-bodied bees may initially profit from warming temperatures, by getting more abundant and diverse. Less severe warming, and differences in habitat openness along the forested gradient, however, might moderate species responses. Our study further highlights the utility of standardized abundance data for revealing rapid changes in bee communities over only one decade.     

Estimating the ability of plants to plastically track temperature‐mediated shifts in the spring phenological optimum

One consequence of rising spring temperatures is that the optimum timing of key life‐history events may advance. Where this is the case, a population's fate may depend on the degree to which it is able to track a change in the optimum timing either via plasticity or via adaptation. Estimating the effect that temperature change will have on optimum timing using standard approaches is logistically challenging, with the result that very few estimates of this important parameter exist. Here we adopt an alternative statistical method that substitutes space for time to estimate the temperature sensitivity of the optimum timing of 22 plant species based on >200 000 spatiotemporal phenological observations from across the United Kingdom. We find that first leafing and flowering dates are sensitive to forcing (spring) temperatures, with optimum timing advancing by an average of 3 days °C^?1 and plastic responses to forcing between ?3 and ?8 days °C^?1. Chilling (autumn/winter) temperatures and photoperiod tend to be important cues for species with early and late phenology, respectively. For most species, we find that plasticity is adaptive, and for seven species, plasticity is sufficient to track geographic variation in the optimum phenology. For four species, we find that plasticity is significantly steeper than the optimum slope that we estimate between forcing temperature and phenology, and we examine possible explanations for this countergradient pattern, including local adaptation.     

Elevational variation in adult body size and growth rate but not in metabolic rate in the tree weta Hemideina crassidens

Populations of the same species inhabiting distinct localities experience different ecological and climatic pressures that might result in differentiation in traits, particularly those related to temperature. We compared metabolic rate (and its thermal sensitivity), growth rate, and body size among nine high- and low-elevation populations of the Wellington tree weta, Hemideina crassidens, distributed from 9 to 1171 m a.s.l across New Zealand. Our results did not indicate elevational compensation in metabolic rates (metabolic cold adaptation). Cold acclimation decreased metabolic rate compared to warm-acclimated individuals from both high- and low-elevation populations. However, we did find countergradient variation in growth rates, with individuals from high-elevation populations growing faster and to a larger final size than individuals from low-elevation populations. Females grew faster to a larger size than males, although as adults their metabolic rates did not differ significantly. The combined physiological and morphological data suggest that high-elevation individuals grow quickly and achieve larger size while maintaining metabolic rates at levels not significantly different from low-elevation individuals. Thus, morphological differentiation among tree weta populations, in concert with genetic variation, might provide the material required for adaptation to changing conditions.     

Single rice growth period was prolonged by cultivars shifts,but yield was damaged by climate change during 1981–2009 in China,and late rice was just opposite

Based on the crop trial data during 1981–2009 at 57 agricultural experimental stations across the North Eastern China Plain (NECP) and the middle and lower reaches of Yangtze River (MLRYR), we investigated how major climate variables had changed and how the climate change had affected crop growth and yield in a setting in which agronomic management practices were taken based on actual weather. We found a significant warming trend during rice growing season, and a general decreasing trend in solar radiation (SRD) in the MLRYR during 1981–2009. Rice transplanting, heading, and maturity dates were generally advanced, but the heading and maturity dates of single rice in the MLRYR (YZ_SR) and NECP (NE_SR) were delayed. Climate warming had a negative impact on growth period lengths at about 80% of the investigated stations. Nevertheless, the actual growth period lengths of YZ_SR and NE_SR, as well as the actual length of reproductive growth period (RGP) of early rice in the MLRYR (YZ_ER), were generally prolonged due to adoption of cultivars with longer growth period to obtain higher yield. In contrast, the actual growth period length of late rice in the MLRYR (YZ_LR) was shortened by both climate warming and adoption of early mature cultivars to prevent cold damage and obtain higher yield. During 1981–2009, climate warming and decrease in SRD changed the yield of YZ_ER by ?0.59 to 2.4%; climate warming during RGP increased the yield of YZ_LR by 8.38–9.56%; climate warming and decrease in SRD jointly reduced yield of YZ_SR by 7.14–9.68%; climate warming and increase in SRD jointly increased the yield of NE_SR by 1.01–3.29%. Our study suggests that rice production in China has been affected by climate change, yet at the same time changes in varieties continue to be the major factor driving yield and growing period trends.