Temperature-related genetic changes in laboratory populations of Drosophila subobscura: evidence against simple climatic-based explanations for latitudinal clines

Parallel latitudinal clines to the long-standing ones in the original Palearctic populations have independently evolved at different rates for chromosomal polymorphism and body size in South and North American populations of Drosophila subobscura since colonization around 25 years ago. This strongly suggests that (micro) evolutionary changes are largely predictable, but the underlying mechanisms are unknown. The putative role of temperature per se was investigated by using three sets of populations at each of three temperatures (13 degrees , 18 degrees , and 22 degrees C) spanning much of the tolerable range for this species. We found a lower chromosomal diversity at the warmest temperature; a quick and consistent shift in gene arrangement frequencies in response to temperature; an evolutionary decrease in wing size, mediated by both cell area and cell number, at 18 degrees C; no relationship between wing size and those inversions involved in latitudinal clines; and a shortening of the basal length of longitudinal vein IV relative to its total length with increasing standard dose. The trends for chromosomal polymorphism and body size were generally inconsistent from simple climatic-based explanations of worldwide latitudinal patterns. The findings are discussed in the light of available information on D. subobscura and results from earlier thermal selection experiments with various Drosophila species.     

Shift in size of bumblebee queens over the last century

Species can respond differently when facing environmental changes, such as by shifting their geographical ranges or through plastic or adaptive modifications to new environmental conditions. Phenotypic modifications related to environmental factors have been mainly explored along latitudinal gradients, but they are relatively understudied through time despite their importance for key ecological interactions. Here we hypothesize that the average bumblebee queen body size has changed in Belgium during the last century. Based on historical and contemporary databases, we first tested if queen body sizes changed during the last century at the intraspecific level among four common bumblebee species and if it could be linked to global warming and/or habitat fragmentation as well as by the replacement by individuals from new populations. Then, we assessed body size changes at the community level, among 22 species, taking into account species population trends (i.e. increasing, stable or decreasing relative abundance). Our results show that the average queen body size of all four bumblebee species increased over the last century. This size increase was significantly correlated to global warming and habitat fragmentation, but not explained by changes in the population genetic structure (i.e. colonization). At the community level, species with stable or increasing relative abundance tend to be larger than declining species. Contrary to theoretical expectations from Bergmann's rule (i.e. increasing body size in colder climates), temperature does not seem to be the main driver of bumblebee body size during the last century as we observed the opposite body size trend. However, agricultural intensification and habitat fragmentation could be alternative mechanisms that shape body size clines. This study stresses the importance of considering alternative global change factors when assessing body size change.     

Latitudinal clines in body size,but not in thermal tolerance or heat‐shock cognate 70 (HSC70), in the highly‐dispersing intertidal gastropod Littorina keenae (Gastropoda: Littorinidae)

Natural populations of widely‐distributed animals often exhibit clinal variation in phenotypic traits or in allele frequencies of a particular gene over their geographical range. A planktotrophic intertidal snail, Littorina keenae is broadly distributed along the north‐eastern Pacific coast through a large latitudinal range (24°50′N–43°18′N). We tested for latitudinal clines in two complex phenotypic traits – thermal tolerance and body size – and one single locus trait – heat shock cognate 70 (HSC70) – in L. keenae along almost its entire geographical range. We found only weak evidence for a latitudinal cline in the thermal tolerance and no evidence for a cline in allele frequencies at HSC70. However, as predicted by Bergmann's rule, we detected a strong latitudinal cline that accounted for 60% of the variance in body size (R² = 0.598; P < 0.001). In contrast, body size did not significantly affect thermal tolerance. HSC70 showed no genetic differentiation among the populations, supporting our previous mitochondrial gene‐based estimate of high gene flow during this snail's free‐swimming larval stage. Given that L. keenae experiences panmixia along its species range, the observed size cline may be partially or entirely caused by a phenotypically plastic response to local thermal environments rather than by genetic divergence in body size among populations in response to locally optimizing natural selection. © 2010 The Linnean Society of London, Biological Journal of the Linnean Society, 2010, 100 , 494–505.     

An experimental study of evolution in progress: Clines for quantitative traits in colonizing and Palearctic populations ofDrosophila

Summary Drosophila subobscura has recently colonized the American continent and is an excellent model for studying evolution in action. Previous analyses have shown that these colonizing populations have significant latitudinal clines for the frequencies of some chromosomal arrangements that parallel those clines found in the Old World. These results strongly suggest that this polymorphism is adaptive. In the present study, significant latitudinal clines for continuous morphometric variables (flies are larger in the north) have been detected in Old World populations ofD. subobscura. The adaptive nature of these clines is reinforced by the fact that parallel latitudinal clines for body size have also been detected inDrosophila obscura, a closely related sympatric species, as well as previously in otherDrosophila. On the other hand, no significant latitudinal clines for continuous morphometric traits, not even when using an overall size index, have been detected in colonizing populations ofD. subobscura. This is a rather surprising result given the number of generations that have elapsed since the species was detected in America and given that significant clines in chromosomal inversions are already established. Thus, the adaptive response of quantitative morphometric variables is not as rapid as that found for chromosomal inversions. Nevertheless, canonical correlation analysis suggests that significant latitudinal clines for body size might soon be detected in the American continent. The results obtained here are included in a projected time series with the aim of documenting size evolution in action.     

Bird population trends are linearly affected by climate change along species thermal ranges

Beyond the effects of temperature increase on local population trends and on species distribution shifts, how populations of a given species are affected by climate change along a species range is still unclear. We tested whether and how species responses to climate change are related to the populations locations within the species thermal range. We compared the average 20 year growth rates of 62 terrestrial breeding birds in three European countries along the latitudinal gradient of the species ranges. After controlling for factors already reported to affect bird population trends (habitat specialization, migration distance and body mass), we found that populations breeding close to the species thermal maximum have lower growth rates than those in other parts of the thermal range, while those breeding close to the species thermal minimum have higher growth rates. These results were maintained even after having controlled for the effect of latitude per se. Therefore, the results cannot solely be explained by latitudinal clines linked to the geographical structure in local spring warming. Indeed, we found that populations are not just responding to changes in temperature at the hottest and coolest parts of the species range, but that they show a linear graded response across their European thermal range. We thus provide insights into how populations respond to climate changes. We suggest that projections of future species distributions, and also management options and conservation assessments, cannot be based on the assumption of a uniform response to climate change across a species range or at range edges only.     

Urbanization disrupts latitude‐size rule in 17‐year cicadas

Many ectotherms show a decrease in body size with increasing latitude due to changes in climate, a pattern termed converse Bergmann's rule. Urban conditions—particularly warmer temperatures and fragmented landscapes—may impose stresses on development that could disrupt these body size patterns. To test the impact of urbanization on development and latitudinal trends in body size, we launched a citizen science project to collect periodical cicadas (Magicicada septendecim) from across their latitudinal range during the 2013 emergence of Brood II. Periodical cicadas are long‐lived insects whose distribution spans a broad latitudinal range covering both urban and rural habitats. We used a geometric morphometric approach to assess body size and developmental stress based on fluctuating asymmetry in wing shape. Body size of rural cicadas followed converse Bergmann's rule, but this pattern was disrupted in urban habitats. In the north, urban cicadas were larger than their rural counterparts, while southern populations showed little variation in body size between habitats. We detected no evidence of differences in developmental stress due to urbanization. To our knowledge, this is the first evidence that urbanization disrupts biogeographical trends in body size, and this pattern highlights how the effects of urbanization may differ over a species’ range.     

Latitudinal pattern in body size in a cockroach,Eupolyphaga sinensis

Body size of insects with flexible life cycles is expected to conform to the saw‐tooth model, a model in which the relationship between size and developmental time depends on length of the growing season. In species with high variability in terms of voltinism, however, more complex patterns can be expected. Few empirical studies have demonstrated the existence of such relationships, or whether climatic factors contribute to these relationships. In this study, we investigated the geographic variation in body size of the Chinese cockroach, Eupolyphaga sinensis Walker (Blattaria: Polyphagidae), which has a variable life cycle length. The sizes of adults – collected from 14 localities ranging from temperate to subtropical zones in China – were measured, using body length, body width, and pronotum width as parameters. The relationship between size, latitude, and climate factors (encompassing 10 variables) was then investigated. We found that the body size of E. sinensis varied considerably with latitude: cockroaches were larger at low and high latitudes, but smaller at intermediate latitudes. Thus, the relationship between climate and body size conformed to a saw‐tooth pattern. Results indicate that two factors were significantly associated with body size clines: season length and variability in life cycle length. Our results also demonstrated that climatic factors contribute to latitudinal clines in body size, which has important ecological and evolutionary implications. It can be expected that global climate change may alter latitudinal clines in body size of E. sinensis.     

Widespread rapid reductions in body size of adult salamanders in response to climate change

Reduction in body size is a major response to climate change, yet evidence in globally imperiled amphibians is lacking. Shifts in average population body size could indicate either plasticity in the growth response to changing climates through changes in allocation and energetics, or through selection for decreased size where energy is limiting. We compared historic and contemporary size measurements in 15 Plethodon species from 102 populations (9450 individuals) and found that six species exhibited significant reductions in body size over 55 years. Biophysical models, accounting for actual changes in moisture and air temperature over that period, showed a 7.1–7.9% increase in metabolic expenditure at three latitudes but showed no change in annual duration of activity. Reduced size was greatest at southern latitudes in regions experiencing the greatest drying and warming. Our results are consistent with a plastic response of body size to climate change through reductions in body size as mediated through increased metabolism. These rapid reductions in body size over the past few decades have significance for the susceptibility of amphibians to environmental change, and relevance for whether adaptation can keep pace with climate change in the future.     

What determines conformity to Bergmann's rule?

Aim  Bergmann's rule, the tendency of body size within species in bird and mammal populations to be positively correlated with latitude, is among the best known biogeographical generalizations. The factors behind such clines, however, are not well understood. Here we use a large data base of 79 mammalian carnivore species to examine the factors affecting latitudinal size clines.
Location  Worldwide.
Methods  We measured the skulls and teeth of carnivores in natural history museums, and calculated the amount of variation in size explained by latitude, supplementing our measurements with published data. We examined the effects of a number of variables on the tendency to show latitudinal clines.
Results  We found that geographical range and latitudinal extent are strongly related to size clines. Minimum temperatures across the range, net primary productivity and habitat diversity also have some, albeit much less, influence.
Main conclusions  We suggest that species with large geographical ranges are likely to encounter significant heterogeneity in those factors that influence body size, and are thus likely to exhibit size clines. However, the key factors that determine body size may not always operate along a latitudinal (or other geographical) cline, but be spatially linked to patches in the species range. One such important factor is likely to be food availability, which we show is a strong predictor of size in the brown bear ( Ursus arctos ) but is not associated with a latitudinal cline. We argue that the spatial distribution of key resources within the species range constitutes a significant predictor of carnivore body size.     

WHEN RENSCH MEETS BERGMANN: DOES SEXUAL SIZE DIMORPHISM CHANGE SYSTEMATICALLY WITH LATITUDE?

Bergmann's and Rensch's rules describe common large-scale patterns of body size variation, but their underlying causes remain elusive. Bergmann's rule states that organisms are larger at higher latitudes (or in colder climates). Rensch's rule states that male body size varies (or evolutionarily diverges) more than female body size among species, resulting in slopes greater than one when male size is regressed on female size. We use published studies of sex-specific latitudinal body size clines in vertebrates and invertebrates to investigate patterns equivalent to Rensch's rule among populations within species and to evaluate their possible relation to Bergmann's rule. Consistent with previous studies, we found a continuum of Bergmann (larger at higher latitudes: 58 species) and converse Bergmann body size clines (larger at lower latitudes: 40 species). Ignoring latitude, male size was more variable than female size in only 55 of 98 species, suggesting that intraspecific variation in sexual size dimorphism does not generally conform to Rensch's rule. In contrast, in a significant majority of species (66 of 98) male latitudinal body size clines were steeper than those of females. This pattern is consistent with a latitudinal version of Rensch's rule, and suggests that some factor that varies systematically with latitude is responsible for producing Rensch's rule among populations within species. Identifying the underlying mechanisms will require studies quantifying latitudinal variation in sex-specific natural and sexual selection on body size.     

Are long‐term widespread avian body size changes related to food availability? A test using contemporaneous changes in carotenoid‐based color

Recent changes in global climate have been linked with changes in animal body size. While declines in body size are commonly explained as an adaptive thermoregulatory response to climate warming, many species do not decline in size, and alternative explanations for size change exist. One possibility is that temporal changes in animal body size are driven by changes in environmental productivity and food availability. This hypothesis is difficult to test due to the lack of suitable estimates that go back in time. Here, we use an alternative, indirect, approach and assess whether continent‐wide changes over the previous 100 years in body size in 15 species of Australian birds are associated with changes in their yellow carotenoid‐based plumage coloration. This type of coloration is strongly affected by food availability because birds cannot synthesize carotenoids and need to ingest them, and because color expression depends on general body condition. We found significant continent‐wide intraspecific temporal changes in body size (wing length) and yellow carotenoid‐based color (plumage reflectance) for half the species. Direction and magnitude of changes were highly variable among species. Meta‐analysis indicated that neither body size nor yellow plumage color showed a consistent temporal trend and that changes in color were not correlated with changes in size over the past 100 years. We conclude that our data provide no evidence that broad‐scale variation in food availability is a general explanation for continent‐wide changes in body size in this group of species. The interspecific variability in temporal changes in size as well as color suggests that it might be unlikely that a single factor drives these changes, and more detailed studies of museum specimens and long‐term field studies are required to disentangle the processes involved.     

Inter‐ and intraspecific variation in body‐ and genome size in calanoid copepods from temperate and arctic waters

The tendency of ectotherms to get larger in the cold (Bergmann clines) has potentially great implications for individual performance and food web dynamics. The mechanistic drivers of this trend are not well understood, however. One fundamental question is to which extent variation in body size is attributed to variation in cell size, which again is related to genome size. In this study, we analyzed body and genome size in four species of marine calanoid copepods, Calanus finmarchicus, C. glacialis, C. hyperboreus and Paraeuchaeta norvegica, with populations from both south Norwegian fjords and the High Arctic. The Calanus species showed typical interspecific Bergmann clines, and we assessed whether they also displayed similar intraspecific variations—and if correlation between genome size and body size differed between species. There were considerable inter‐ as well as intraspecific variations in body size and genome size, with the northernmost populations having the largest values of both variables within each species. Positive intraspecific relationships suggest a functional link between body and genome size, although its adaptiveness has not been settled. Impact of additional drivers like phylogeny or specific adaptations, however, was suggested by striking divergences in body size – genome size ratios among species. Thus, C. glacialis and C. hyperboreus, had fairly similar genome size despite very different body size, while P. norvegica, of similar body size as C. hyperboreus, had the largest genome sizes ever recorded from copepods. The inter‐ and intraspecific latitudinal body size clines suggest that climate change may have major impact on body size composition of keystone species in marine planktonic food webs.     

Re-establishment of clinal variation in flowering time among introduced populations of purple loosestrife (Lythrum salicaria, Lythraceae)

Range expansion during biological invasion requires that invaders adapt to geographical variation in climate, which should yield latitudinal clines in reproductive phenology. We investigated geographic variation in life history among 25 introduced populations of Lythrum salicaria, a widespread European invader of North American wetlands. We detected a strong latitudinal cline in initiation of flowering and size at flowering, which paralleled that reported among native populations. Plants from higher latitudes flowered earlier and at a smaller size than those from lower latitudes, even when raised in a uniform glasshouse. Early flowering was associated with greatly reduced reproductive output, but this was not associated with latitudinal variation in abundance, and probably did not result from a genetic correlation between time to and size at flowering. As introduction to North America c. 200 years ago, L. salicaria has re-established latitudinal clines in life history, probably as an evolutionary response to climatic selection.     

Different cell size and cell number contribution in two newly established and one ancient body size cline of Drosophila subobscura

Latitudinal genetic clines in body size occur in many ectotherms including Drosophila species. In the wing of D. melanogaster, these clines are generally based on latitudinal variation in cell number. In contrast, differences in wing area that evolve by thermal selection in the laboratory are in general based on cell size. To investigate possible reasons for the different cellular bases of these two types of evolutionary response, we compared the newly established North and South American wing size clines of Drosophila subobscura. The new clines are based on latitudinal variation in cell area in North America and cell number in South America. The ancestral European cline is also based on latitudinal variation in cell number. The difference in the cellular basis of wing size variation in the American clines, which are roughly the same age, together with the similar cellular basis of the new South American cline and the ancient European one, suggest that the antiquity of a cline does not explain its cellular basis. Furthermore, the results indicate that wing size as a whole, rather than its cellular basis, is under selection. The different cellular bases of different size clines are most likely explained either entirely by chance or by different patterns of genetic variance--or its expression--in founding populations.     

Presence of an invasive species reverses latitudinal clines of multiple traits in a native species

Understanding the processes driving formation and maintenance of latitudinal clines has become increasingly important in light of accelerating global change. Many studies have focused on the role of abiotic factors, especially temperature, in generating clines, but biotic factors, including the introduction of non‐native species, may also drive clinal variation. We assessed the impact of invasion by predatory fire ants on latitudinal clines in multiple fitness‐relevant traits—morphology, physiological stress responsiveness, and antipredator behavior—in a native fence lizard. In areas invaded by fire ants, a latitudinal cline in morphology is opposite both the cline found in museum specimens from historical populations across the species’ full latitudinal range and that found in current populations uninvaded by fire ants. Similarly, clines in stress‐relevant hormone response to a stressor and in antipredator behavior differ significantly between the portions of the fence lizard range invaded and uninvaded by fire ants. Changes in these traits within fire ant‐invaded areas are adaptive and together support increased and more effective antipredator behavior that allows escape from attacks by this invasive predator. However, these changes may mismatch lizards to the environments under which they historically evolved. This research shows that novel biotic pressures can alter latitudinal clines in multiple traits within a single species on ecological timescales. As global change intensifies, a greater understanding of novel abiotic and biotic pressures and how affected organisms adapt to them across space and time will be central to predicting and managing our changing environment.     

Climate warming is associated with smaller body size and shorter lifespans in moose near their southern range limit

Despite the importance of body size for individual fitness, population dynamics and community dynamics, the influence of climate change on growth and body size is inadequately understood, particularly for long‐lived vertebrates. Although temporal trends in body size have been documented, it remains unclear whether these changes represent the adverse impact of climate change (environmental stress constraining phenotypes) or its mitigation (via phenotypic plasticity or evolution). Concerns have also been raised about whether climate change is indeed the causal agent of these phenotypic shifts, given the length of time‐series analysed and that studies often do not evaluate – and thereby sufficiently rule out – other potential causes. Here, we evaluate evidence for climate‐related changes in adult body size (indexed by skull size) over a 4–decade period for a population of moose (Alces alces) near the southern limit of their range whilst also considering changes in density, predation, and human activities. In particular, we document: (i) a trend of increasing winter temperatures and concurrent decline in skull size (decline of 19% for males and 13% for females) and (ii) evidence of a negative relationship between skull size and winter temperatures during the first year of life. These patterns could be plausibly interpreted as an adaptive phenotypic response to climate warming given that latitudinal/temperature clines are often accepted as evidence of adaptation to local climate. However, we also observed: (iii) that moose with smaller skulls had shorter lifespans, (iv) a reduction in lifespan over the 4‐decade study period, and (v) a negative relationship between lifespan and winter temperatures during the first year of life. Those observations indicate that this phenotypic change is not an adaptive response to climate change. However, this decline in lifespan was not accompanied by an obvious change in population dynamics, suggesting that climate change may affect population dynamics and life‐histories differently.     

Wing trait–inversion associations in Drosophila subobscura can be generalized within continents,but may change through time

Clinal variation is one of the most emblematic examples of the action of natural selection at a wide geographical range. In Drosophila subobscura, parallel clines in body size and inversions, but not in wing shape, were found in Europe and South and North America. Previous work has shown that a bottleneck effect might be largely responsible for differences in wing trait–inversion association between one European and one South American population. One question still unaddressed is whether the associations found before are present across other populations of the European and South American clines. Another open question is whether evolutionary dynamics in a new environment can lead to relevant changes in wing traits–inversion association. To analyse geographical variation in these associations, we characterized three recently laboratory founded D. subobscura populations from both the European and South American latitudinal clines. To address temporal variation, we also characterized the association at a later generation in the European populations. We found that wing size and shape associations can be generalized across populations of the same continent, but may change through time for wing size. The observed temporal changes are probably due to changes in the genetic content of inversions, derived from adaptation to the new, laboratory environment. Finally, we show that it is not possible to predict clinal variation from intrapopulation associations. All in all this suggests that, at least in the present, wing traits–inversion associations are not responsible for the maintenance of the latitudinal clines in wing shape and size.     

Shifting clinal patterns of stress resistance traits in Drosophila ananassae

Drosophila ananassae, a desiccation and cold sensitive species, is abundant along the latitudinal gradient of the Indian subcontinent. Analysis of seasonally varying wild-caught flies showed two independent patterns of melanisation: (1) narrow to broad melanic stripes on three anterior abdominal segments only; (2) a novel body color pattern (dark vs. light background). We investigated the degree to which these two melanisation systems vary; first with latitude and secondly among seasons. There is a shallow latitudinal cline for percent striped melanisation as well as for frequency of body color alleles during the rainy season. The frequencies of body color alleles vary significantly across seasons in the northern populations i.e. the light allele occur abundantly (>0.94) during the rainy season while the frequency of the dark allele increases (0.22–0.35) during the dry season causing steeper clines during the dry season. By contrast, the low variations in abdominal stripes showed non-significant changes and the cline was similar across seasons. Furthermore, both types of melanisation patterns showed no plasticity with respect to temperature. The present study also investigated clines related to desiccation, heat and cold stress in D. ananassae females across seasons (rainy and dry) from nine latitudinal populations. The clines for stress related traits changes to steeper and non-linear during the dry season. Thus, latitudinal populations of D. ananassae differ in slope values of clines for stress related traits across seasons. This study reports seasonal changes in latitudinal clines of stress resistance traits as seen in a changing frequency of body color alleles of D. ananassae in northern locality, while in southern localities it remains constant. This is presumably the result of only minor seasonal changes in humidity and temperature in the South, whereas in the North seasonal climatic variability is much higher.     

Are latitudinal clines in body size adaptive?

Body size of animals often increases with increasing latitude. These latitudinal clines in body size have interested biologists for over 150 years. However, the mechanisms that generate these clines in size are still unclear, though latitudinal gradients in temperature appear to play an important role. More importantly, many studies that examine latitudinal clines in body size and the mechanisms responsible for these clines use phenotypic data, confounding genetic (adaptive) and non‐genetic (plasticity) sources of variation. Yet, most of these studies make adaptive conclusions based on phenotypic measures of size. Here I show the dangers of making adaptive inferences from phenotypic measures of size. In addition, I use a specific form of plasticity in body size of ectotherms, called the temperature–size rule, to illustrate how confusion about genetic and non‐genetic contributions to phenotypic variation has hampered progress in understanding the evolution of latitudinal clines in size. Field‐based measurements of body size can no doubt be influenced by plasticity, but demonstrating that latitudinal clines have a genetic basis is necessary to show that these patterns are adaptive.     

Bumblebees moving up: shifts in elevation ranges in the Pyrenees over 115 years

In a warming climate, species are expected to shift their geographical ranges to higher elevations and latitudes, and if interacting species shift at different rates, networks may be disrupted. To quantify the effects of ongoing climate change, repeating historical biodiversity surveys is necessary. In this study, we compare the distribution of a plant–pollinator community between two surveys 115 years apart (1889 and 2005–06), reporting distribution patterns and changes observed for bumblebee species and bumblebee-visited plants in the Gavarnie-Gèdre commune in the Pyrenees, located in southwest Europe at the French–Spanish border. The region has warmed significantly over this period, alongside shifts in agricultural land use and forest. The composition of the bumblebee community shows relative stability, but we observed clear shifts to higher elevations for bumblebees (averaging 129 m) and plants (229 m) and provide preliminary evidence that some bumblebee species shift with the plants they visit. We also observe that some species have been able to occupy the same climate range in both periods by shifting elevation range. The results suggest the need for long-term monitoring to determine the role and impact of the different drivers of global change, especially in montane habitats where the impacts of climate changes are anticipated to be more extreme.