Functional adaptation rather than ecogeographical rules determine body-size metrics along a thermal cline with elevation in the Chinese pygmy dormouse (Typhlomys cinereus)

Phenotypic plasticity is crucial for how organisms respond to variation in their environment, affecting their diversity and distribution, especially in the light of rapid environmental change. Ecogeographical rules predict an association between specific adaptive morphological and physiological traits with cooler conditions due to higher latitude, elevation, or climate change. Such ecogeographical effects are often most evident in ancient species due to continuous selective adaptation occurring over long periods of time. Here, we use the suitably ancient Chinese pygmy dormouse (Typhlomys cinereus) to test whether body-size, appendage length and heart size vary in accordance with Bergmann's, Allen's and Hesse's rule, respectively. Based on a sample of 67 adult individuals (female, n = 29; male n = 38) trapped at 37 sites transcending an elevational range from 414 to 1757 m, we tested for trait concordance with Bergmann's rule (body mass, length and SMI), Allen's rule (length of tail, foot, ear, snout), and Hesse's rule (wet and dry heart mass). Effects of elevation (and thus temperature lapse rate; calculated as 0.61 °C per 100 m) on body size, appendage length and heart size, were tested by fitting Standardized Major Axis (SMA) models. We observed substantial heterogeneity in morphometric traits allowing for the detection of ecogeographical clines. However, none conformed with Bergmann's, Allen's (except ear size), or Hesse's rule. However, our results indicate some support for Geist's rule of net primary productivity. We conclude that pervasive functional life-history adaptations in this blind, arboreal, echolocating ancient species exceeded selection for morphological energy efficiency constraints, with the notable exception of reduced ear pinnae size at colder, elevated sites. This is an important consideration for predicting how species, and populations in general, may adapt to human induced rapid environmental change, contrary to expectations of warming driving selection for smaller body-size.     

Morphological variations in a widely distributed Eastern Asian passerine cannot be consistently explained by ecogeographic rules

Ecogeographic rules that describe quantitative relationships between morphologies and climate might help us predict how morphometrics of animals was shaped by local temperature or humidity. Although the ecogeographic rules had been widely tested in animals of Europe and North America, they had not been fully validated for species in regions that are less studied. Here, we investigate the morphometric variation of a widely distributed East Asian passerine, the vinous‐throated parrotbill (Sinosuthora webbiana), to test whether its morphological variation conforms to the prediction of Bergmann''s rule, Allen''s rules, and Gloger''s rule. We at first described the climatic niche of S. webbiana from occurrence records (n = 7838) and specimen records (n = 290). The results of analysis of covariance (ANCOVA) suggested that the plumage coloration of these parrotbills was darker in wetter/warmer environments following Gloger''s rule. However, their appendage size (culmen length, beak volume, tarsi length) was larger in colder environments, the opposite of the predictions of Allen''s rule. Similarly, their body size (wing length) was larger in warmer environments, the opposite of the predictions of Bergmann''s rule. Such disconformity to both Bergmann''s rule and Allen''s rule suggests that the evolution of morphological variations is likely governed by multiple selection forces rather than dominated by thermoregulation. Our results suggest that these ecogeographic rules should be validated prior to forecasting biological responses to climate change especially for species in less‐studied regions.     

The fiddler crab,Minuca pugnax,follows Bergmann's rule

Bergmann's rule predicts that organisms at higher latitudes are larger than ones at lower latitudes. Here, we examine the body size pattern of the Atlantic marsh fiddler crab, Minuca pugnax (formerly Uca pugnax), from salt marshes on the east coast of the United States across 12 degrees of latitude. We found that M. pugnax followed Bergmann's rule and that, on average, crab carapace width increased by 0.5 mm per degree of latitude. Minuca pugnax body size also followed the temperature–size rule with body size inversely related to mean water temperature. Because an organism's size influences its impact on an ecosystem, and M. pugnax is an ecosystem engineer that affects marsh functioning, the larger crabs at higher latitudes may have greater per‐capita impacts on salt marshes than the smaller crabs at lower latitudes.     

Interrelations of global macroecological patterns in wing and thorax size,sexual size dimorphism,and range size of the Drosophilidae

Support for macroecological rules in insects is mixed, with potential confounding interrelations between patterns rarely studied. We here investigate global patterns in body and wing size, sexual size dimorphism and range size in common fruit flies (Diptera: Drosophilidae) and explore potential interrelations and the predictive power of Allen's, Bergmann's, Rensch's and Rapoport's rules. We found that thorax length (r² = 0.05) and wing size (r² = 0.09) increased with latitude, supporting Bergmann's rule. Contrary to patterns often found in endothermic vertebrates, relative wing size increased towards the poles (r² = 0.12), a pattern against Allen's rule, which we attribute to selection for increased flight capacity in the cold. Sexual size dimorphism decreased with size, evincing Rensch's rule across the family (r² = 0.14). Yet, this pattern was largely driven by the virilis–repleta radiation. Finally, range size did not correlate with latitude, although a positive relationship was present in a subset of the species investigated, providing no convincing evidence for Rapoport's rule. We further found little support for confounding interrelations between body size, wing loading and range size in this taxon. Nevertheless, we demonstrate that studying several traits simultaneously at minimum permits better interpretation in case of multiple, potentially conflicting trends or hypotheses concerning the macroecology of insects.     

Bergmann's Rule rules body size in an ectotherm: heat conservation in a lizard along a 2200‐metre elevational gradient

Bergmann's Rule predicts larger body sizes in colder habitats, increasing organisms' ability to conserve heat. Originally formulated for endotherms, it is controversial whether Bergmann's Rule may be applicable to ectotherms, given that larger ectotherms show diminished capacity for heating up. We predict that Bergmann's Rule will be applicable to ectotherms when the benefits of a higher conservation of heat due to a larger body size overcompensate for decreased capacity to heating up. We test this hypothesis in the lizard Psammodromus algirus, which shows increased body size with elevation in Sierra Nevada (SE Spain). We measured heating and cooling rates of lizards from different elevations (from 300 to 2500 m above sea level) under controlled conditions. We found no significant differences in the heating rate along an elevational gradient. However, the cooling rate diminished with elevation and body size: highland lizards, with larger masses, have a higher thermal inertia for cooling, which allows them to maintain heat for more time and keep a high body temperature despite the lower thermal availability. Consequently, the net gaining of heat increased with elevation and body size. This study highlights that the heat conservation mechanism for explaining Bergmann's Rule works and is applicable to ectotherms, depending on the thermal benefits and costs associated with larger body sizes.     

Phenotypic evolution in high‐elevation populations of western fence lizards (Sceloporus occidentalis) in the Sierra Nevada Mountains

Adaptive divergence in response to variable habitats, climates, and altitude is often accentuated along elevation gradients. We investigate phenotypic evolution in body size and coloration in the western fence lizard (Sceloporus occidentalis Baird & Girard, 1852) across elevation gradients in Yosemite National Park, California, situated in the Sierra Nevada mountains of Western North America. High‐elevation populations occurring above 2100 m a.s.l. are recognized as a separate subspecies (Sceloporus occidentalis taylori Camp, 1916), with a distinctive phenotype characterized by a large body size and extensive blue ventral pigmentation. We sampled S. occidentalis from across elevation gradients in Yosemite National Park, California, and collected phenotypic data (body size and ventral coloration measurements; 410 specimens) and mitochondrial DNA sequence data (complete NADH1 gene; 969 bp, 181 specimens) to infer phylogenetic relationships, and examine the genetic and phenotypic diversity among populations. Populations of S. occidentalis in Yosemite National Park follow Bergmann's rule and exhibit larger body sizes in colder, high‐elevation environments. The high‐elevation subspecies S. o. taylori is not monophyletic, and the mitochondrial DNA genealogy supports a model of convergent phenotypic evolution among high‐elevation populations belonging to different river drainages. The hypothesis that separate populations of S. occidentalis expanded up river drainages after the recession of glaciers is supported by population demographic analyses, and suggest that Bergmann's clines can evolve rapidly along elevation gradients. The distinctive high‐elevation phenotype that is attributable to S. o. taylori has evolved independently several times, and includes adaptive phenotypic changes associated with increases in body size and ventral coloration. © 2010 The Linnean Society of London, Biological Journal of the Linnean Society, 2010, 100 , 630–641.     

Bergmann's and Rensch's rules and the spur‐thighed tortoise (Testudo graeca)

Body size is an ecologically important variable in animals. The geographical size variation of most snakes and some lizards counters Bergmann's rule in that, among related taxa, the larger ones live at warmer latitudes. However, exceptions notwithstanding, and despite being ectothermic, turtles as a group tend to obey Bergmann's rule. We examined this idea in Testudo graeca, ranging from Morocco to Romania and to Iran with disputed systematics, both at the global scale (using literature) and within the focal area of Israel (using museum specimens). Both globally and locally, carapace length correlated with latitude, in accordance with Bergmann's rule. The scant data on reproduction fully support the hypothesis that Bergmann's rule enables larger clutches where the climate would limit repeated clutches. The sexual size dimorphism (SSD) was approached using two methodologies: (1) ‘conventional’, using globally literature data and locally museum samples and (2) ‘innovated’, using photographs of copulating tortoises from Israel and Turkey. By each methodology, SSD emerged as being male biased in the larger‐bodied populations and female biased in the smaller‐bodied populations, obeying Rensch's rule. Some observations support the hypothesis that the evolution of large males serves intermale combating. Finally, Rensch's rule was found to apply separately within Anatolia and within the Levant, possibly indicating that these populations are separate.     

Bergmann's rule does not apply to geometrid moths along an elevational gradient in an Andean montane rain forest

Aim Bergmann's rule generally predicts larger animal body sizes with colder climates. We tested whether Bergmann's rule at the interspecific level applies to moths (Lepidoptera: Geometridae) along an extended elevational gradient in the Ecuadorian Andes. Location Moths were sampled at 22 sites in the province Zamora‐Chinchipe in southern Ecuador in forest habitats ranging from 1040 m to 2677 m above sea level. Methods Wingspans of 2282 male geometrid moths representing 953 species were measured and analysed at the level of the family Geometridae, as well as for the subfamily Ennominae with the tribes Boarmiini and Ourapterygini, and the subfamily Larentiinae with the genera Eois, Eupithecia and Psaliodes. Results Bergmann's rule was not supported since the average wingspan of geometrid moths was negatively correlated with altitude (r = ?0.59, P < 0.005). The relationship between body size and altitude in Geometridae appears to be spurious because species of the subfamily Larentiinae are significantly smaller than species of the subfamily Ennominae and simultaneously increase in their proportion along the gradient. A significant decrease of wingspan was also found in the ennomine tribe Ourapterygini, but no consistent body size patterns were found in the other six taxa studied. In most taxa, body size variation increases with altitude, suggesting that factors acting to constrain body size might be weaker at high elevations. Main conclusions The results are in accordance with previous studies that could not detect consistent body size patterns in insects at the interspecific level along climatic gradients.     

Patterns of size variation in bees at a continental scale: does Bergmann's rule apply?

Body size latitudinal clines have been widley explained by the Bergmann's rule in homeothermic vertebrates. However, there is no general consensus in poikilotherms organisms in particular in insects that represent the large majority of wildlife. Among them, bees are a highly diverse pollinators group with high economic and ecological value. Nevertheless, no comprehensive studies of species assemblages at a phylogenetically larger scale have been carried out even if they could identify the traits and the ecological conditions that generate different patterns of latitudinal size variation. We aimed to test Bergmann's rule for wild bees by assessing relationships between body size and latitude at continental and community levels. We tested our hypotheses for bees showing different life history traits (i.e. sociality and nesting behaviour). We used 142 008 distribution records of 615 bee species at 50 × 50 km (CGRS) grids across the West Palearctic. We then applied generalized least squares fitted linear model (GLS) to assess the relationship between latitude and mean body size of bees, taking into account spatial autocorrelation. For all bee species grouped, mean body size increased with higher latitudes, and so followed Bergmann's rule. However, considering bee genera separately, four genera were consistent with Bergmann's rule, while three showed a converse trend, and three showed no significant cline. All life history traits used here (i.e. solitary, social and parasitic behaviour; ground and stem nesting behaviour) displayed a Bergmann's cline. In general there is a main trend for larger bees in colder habitats, which is likely to be related to their thermoregulatory abilities and partial endothermy, even if a ‘season length effect’ (i.e. shorter foraging season) is a potential driver of the converse Bergmann's cline particularly in bumblebees.     

Do New World pitvipers “scale‐down” at high elevations? Macroecological patterns of scale characters and body size

Bergmann's rule describes the macroecological pattern of increasing body size in response to higher latitudes and elevations. This pattern is extensively documented in endothermic vertebrates, within and among species; however, studies involving ectotherms are less common and suggest no consistent pattern for amphibians and reptiles. Moreover, adaptive traits, such as epidermal features like scales, have not been widely examined in conjunction with Bergmann's rule, even though these traits affect physiological processes, such as thermoregulation, which are hypothesized as underlying mechanisms for the pattern. Here, we investigate how scale characters correlate with elevation among 122 New World pitviper species, representing 15 genera. We found a contra‐Bergmann's pattern, where body size is smaller at higher elevations. This pattern was mainly driven by the presence of small‐bodied clades at high elevations and large‐bodied clades at low elevations, emphasizing the importance of taxonomic scope in studying macroecological patterns. Within a subset of speciose clades, we found that only Crotalus demonstrated a significant negative relationship between body size and elevation, perhaps because of its wide elevational range. In addition, we found a positive correlation between scale counts and body size but no independent effect of elevation on scale numbers. Our study increases our knowledge of Bergmann's rule in reptiles by specifically examining characters of squamation and suggests a need to reexamine macroecological patterns for this group.     

Rule reversal: Ecogeographical patterns of body size variation in the common treeshrew (Mammalia,Scandentia)

There are a number of ecogeographical “rules” that describe patterns of geographical variation among organisms. The island rule predicts that populations of larger mammals on islands evolve smaller mean body size than their mainland counterparts, whereas smaller‐bodied mammals evolve larger size. Bergmann's rule predicts that populations of a species in colder climates (generally at higher latitudes) have larger mean body sizes than conspecifics in warmer climates (at lower latitudes). These two rules are rarely tested together and neither has been rigorously tested in treeshrews, a clade of small‐bodied mammals in their own order (Scandentia) broadly distributed in mainland Southeast Asia and on islands throughout much of the Sunda Shelf. The common treeshrew, Tupaia glis, is an excellent candidate for study and was used to test these two rules simultaneously for the first time in treeshrews. This species is distributed on the Malay Peninsula and several offshore islands east, west, and south of the mainland. Using craniodental dimensions as a proxy for body size, we investigated how island size, distance from the mainland, and maximum sea depth between the mainland and the islands relate to body size of 13 insular T. glis populations while also controlling for latitude and correlation among variables. We found a strong negative effect of latitude on body size in the common treeshrew, indicating the inverse of Bergmann's rule. We did not detect any overall difference in body size between the island and mainland populations. However, there was an effect of island area and maximum sea depth on body size among island populations. Although there is a strong latitudinal effect on body size, neither Bergmann's rule nor the island rule applies to the common treeshrew. The results of our analyses demonstrate the necessity of assessing multiple variables simultaneously in studies of ecogeographical rules.     

Latitudinal variation in sexual dimorphism in life‐history traits of a freshwater fish

Sexual dimorphism is common across the animal kingdom, but the contribution of environmental factors shaping differences between the sexes remains controversial. In ectotherms, life‐history traits are known to correlate with latitude, but sex‐specific responses are not well understood. We analyzed life‐history trait variation between the sexes of European perch (Perca fluviatilis L.), a common freshwater fish displaying larger female size, by employing a wide latitudinal gradient. We expected to find sex‐dependent latitudinal variation in life‐history variables: length at age, length increment, and size at maturity, with females showing consistently higher values than males at all latitudes. We further anticipated that this gender difference would progressively decrease with the increasingly harsh environmental conditions toward higher latitude. We hypothesized that growth and length increment would decrease and size/age at maturity would increase at higher latitudes. Our results confirmed female‐biased sexual size dimorphism at all latitudes and the magnitude of sexual dimorphism diminished with increase in latitude. Growth of both sexes decreased with increase in latitude, and the female latitudinal clines were steeper than those of males. Hence, we challenge two predominant ecological rules (Rensch's and Bergmann's rules) that describe common large‐scale patterns of body size variation. Our data demonstrate that these two rules are not universally applicable in ectotherms or female‐biased species. Our study highlights the importance of sex‐specific differences in life‐history traits along a latitudinal gradient, with evident implications for a wide range of studies from individual to ecosystems level.     

Patterns of within-species body size variation of birds: strong evidence for Bergmann's rule

Aim The aim of this study is to test whether Bergmann's rule, a general intraspecific tendency towards larger body size in cooler areas and at higher latitudes, holds for birds throughout the world. Location This study includes information on species of birds from throughout the world. Methods I gathered data on body size variation from the literature and used two general meta‐analytical procedures to test the validity of Bergmann's rule in birds: a modified vote‐counting approach and calculation of overall effect sizes. Related species may show similar body size trends, thus I performed all analyses using nonphylogenetic and phylogenetic methods. I used tests of phylogenetic signal for each data set to decide which type of statistical analysis (nonphylogenetic or phylogenetic) was more appropriate. Results The majority of species of birds (76 of 100 species) are larger at higher latitudes, and in cooler areas (20 of 22 species). Birds show a grand mean correlation coefficient of +0.32 for body size and latitude, and ?0.81 for body size and temperature, both significant trends. Sedentary species show stronger body size trends in some, but not all, analyses. Neither males nor females consistently have stronger body size trends. Additionally, the strength of body size trends does not vary with latitude or body mass. Conclusions Bergmann's rule holds for birds throughout the world, regardless of whether temperature or latitude (as a proxy) is used. Previous studies have suggested that Bergmann's rule is stronger for sedentary than migratory species, males than females and temperate than tropical taxa. I did not find strong support for any of these as general themes for birds, although few studies of tropical taxa have been conducted. The processes responsible for Bergmann's rule remain somewhat of a black box; however, fasting endurance is probably a more important factor than the traditional hypothesis of heat conservation.     

A global assessment of Bergmann's rule in mammals and birds

Bergmann's rule states that endotherms have a large body size in high latitudes and cold climates. However, previous empirical studies have reported mixed evidence on the relationships between body size and latitude, raising the question of why some clades of endotherms follow Bergmann's rule, whereas others do not. Here, we synthesized the interspecific relationships between body size and latitude among 16,187 endothermic species (5422 mammals and 10,765 birds) using Bayesian phylogenetic generalized linear mixed models to examine the strength and magnitude of Bergmann's rule. We further assessed the effect of biological and ecological factors (i.e., body mass categories, dietary guild, winter activity, habitat openness, and climate zone) on the variations in the body mass–latitude relationships by adding an interaction term in the models. Our results revealed a generally weak but significant adherence to Bergmann's rule among all endotherms at the global scale. Despite taxonomic variation in the strength of Bergmann's rule, the body mass of species within most animal orders showed an increasing trend toward high latitudes. Generally, large-bodied, temperate species, non-hibernating mammals, and migratory and open-habitat birds tend to conform to Bergmann's rule more than their relatives do. Our results suggest that whether Bergmann's rule applies to a particular taxon is mediated by not only geographic and biological features, but also potential alternate strategies that species might have for thermoregulation. Future studies could explore the potential of integrating comprehensive trait data into phylogenetic comparative analysis to re-assess the classic ecogeographic rules on a global scale.     

Body size explains interspecific variation in size–latitude relationships in geographically widespread beetle species

1. In most birds and mammals, larger individuals of the same species tend to be found at higher latitudes, but in insects, body size–latitude relationships are highly variable. 2. Recent studies have shown that larger‐bodied insect species are more likely to decrease in size when reared at increased temperature, compared with smaller‐sized species. These findings have led to the prediction that a positive relationship between body size and latitude should be more prevalent in larger‐bodied insect species. 3. This study measured the body size of > 4000 beetle specimens (12 species) collected throughout North America. Some beetle species increased in size with latitude, while others decreased. Importantly, mean species body size explained c. 30% of the interspecific variation in the size–latitude response. 4. As predicted, larger‐bodied beetle species were more likely to show a positive relationship between body size and latitude (Bergmann's rule), and smaller‐bodied species were more likely to show a negative body size–latitude relationship (inverse Bergmann's rule). 5. These body size–latitude patterns suggest that size‐specific responses to temperature may underlie global latitudinal distributions of body size in Coleoptera, as well as other insects.     

Knitting patterns of biodiversity,range size and body size in aquatic beetle faunas: significant relationships but slightly divergent drivers

1. Ecogeographical rules refer to recurring patterns in nature, including the latitudinal diversity gradient (LDG), Rapoport's rule and Bergmann's rule, amongst others. In the present study, the existence of these rules was examined for diving beetles (Coleoptera: Dytiscidae), a family of aquatic predatory beetles. 2. Assemblage‐level data were analysed for diving beetles, focusing on species richness, local contribution to beta diversity (LCBD), mean range size and mean body size across the biogeographical provinces of Northern Europe. First, each of these variables was correlated with latitude, and then variation in each variable was modelled using actual environmental variables in boosted regression tree analysis. 3. Species richness was found to decrease with latitude, LCBD increased with latitude, mean range size did not show a significant relationship with latitude, and mean body size decreased with latitude. The latter finding was in contrast to Bergmann's rule. The actual environmental variables best predicting variation in these four response variables varied among the models, although they generally included temperature‐related and land use variables as the most influential ones. 4. The results obtained in the present study suggest that diving beetles conformed to the LDG, did not follow Rapoport's rule, and showed a reversed latitudinal gradient in the context of Bergmann's rule. In addition, species‐poor provinces harboured ecologically most unique faunas, suggesting that species richness and LCBD are complementary measures of biodiversity. 5. Even though general support was not found for most of the ecogeographical rules examined, the findings of the present study are interesting because they suggest that aquatic ectothermic invertebrates may show patterns different from those originally described for terrestrial endothermic vertebrates.     

Patterns of diversity, altitudinal range and body size among freshwater fishes in the Yangtze River basin, China

Aim To document patterns in diversity, altitudinal range and body size of freshwater fishes along an elevational gradient in the Yangtze River basin. Location The Yangtze River basin, China. Methods We used published data to compile the distribution, altitudinal range and body size of freshwater fishes. Correlation, regression, clustering and graphical analyses were used to explore patterns in diversity, altitudinal range and body size of freshwater fishes in 100‐m elevation zones from 0 to 5200 m. Results Species richness patterns across the elevational gradient for total, non‐endemic and endemic fishes were different. The ratio of endemics to total richness peaked at mid elevation. Land area on a 500‐m interval scale explained a significant amount of the variation in species richness. Species density displayed two peaks at mid‐elevation zones. The cluster analysis revealed five distinct assemblages across the elevation gradient. The relationship between elevational range size and the midpoint of the elevational range revealed a triangular distribution. The frequency distribution of log maximum standard length data displayed an atypical right‐skewed pattern. Intermediate body sizes occurred across the greatest range of elevation while small and large body sizes possessed only small elevational amplitudes. The size‐elevation relationship between the two major families revealed a very strong pattern of body size constraint among the Cobitidae with no corresponding elevational constraint and a lot of body size and elevational diversification among the Cyprinidae. Main conclusion The data failed to support either Rapoport's rule or Bergmann's rule.     

When Bergmann's rule fails: evidences of environmental selection pressures shaping phenotypic diversification in a widespread seabird

Organisms tend to exhibit phenotypes that can be shaped by climate, commonly demonstrating clinal variations along latitudinal gradients. In vertebrates, air temperature plays a major role in shaping body size in both ectothermic and endothermic animals. However, additional small‐scale environmental factors can also act as selection pressures in the marine ecosystem (e.g. primary productivity), evidencing multi‐scale processes acting on marine organisms. In this study, we tested Bergmann's rule in a widely distributed seabird, the brown booby Sula leucogaster, in addition to evaluating the relationship of sea surface temperature and chlorophyll α with phenotypes. We used traits from a morphometric dataset (culmen, wing chord, and tarsus length) and body mass of 276 brown boobies distributed on six breeding sites along a latitudinal gradient in the South Atlantic Ocean (0–27°S). We found significant differentiation among colonies, but phenotypic similarities were observed between colonies located at the extremes of the latitudinal gradient. As the colony nearest to the Equator, Saint Peter and Saint Paul archipelago, had the largest and heaviest individuals, the model containing only air temperature explained < 5% of the allometric variation, providing no substantial support for Bergmann's rule. However, when we added the interaction of chlorophyll α and sea surface temperature the deviance explained rose to over 80%. Primary productivity and sea surface temperature do not follow a latitudinal gradient in the ocean and, therefore, the role of small‐scale oceanographic processes in shaping body size and the importance of considering additional environmental variables when testing Bergmann's rule in marine organisms are evident.