Body size variation among mainland populations of the western rattlesnake (Crotalus viridis)

In general, squamate reptiles follow the converse to Bergmann's rule, attaining smaller sizes in cooler environments, whereas other vertebrate groups follow Bergmann's rule, attaining larger sizes in cooler areas. Intensive studies of body size evolution for species of squamates are necessary to understand the processes responsible for this trend. Here I present data on body size variation among mainland populations of the western rattlesnake, Crotalus viridis. This species consists of two well-differentiated phylogenetic clades, therefore all analyses were performed for the C. viridis group as a whole and separately for each of the two clades within the C. viridis group. Although both phylogenetic and nonphylogenetic analyses were performed, the data did not show phylogenetic conservatism, and therefore the nonphylogenetic results are preferred. I found no significant relationships between mean adult female snout-vent length and any of the physical and climatic variables that were examined for the C. viridis group using simple linear regression analysis. Examined separately, I found that individuals of the western clade, C. oreganus, were smaller in cooler and more seasonal environments, whereas individuals of the eastern clade. C. viridis sensu stricto, were larger in cooler and more seasonal areas. Thus, the observed size trends were in opposite directions for the two clades. Multiple regression analysis revealed that seasonality was a stronger predictor of body size variation than was temperature for both clades. The differences in body size trends between these clades may be due to differences in mortality rates among populations.     

Latitudinal and climatic variation in body size and dorsal scale counts in Sceloporus lizards:a phylogenetic perspective

Squamates often follow an inverse Bergmann's rule, with larger-bodied animals occurring in warmer areas or at lower latitudes. The size of dorsal scales in lizards has also been proposed to vary along climatic gradients, with species in warmer areas exhibiting larger scales, putatively to reduce heat load. We tested for these patterns in the diverse and widespread lizard genus Sceloporus. Among 106 species or populations, body size was associated positively with maximum temperature (consistent with the inverse of Bergmann's rule) and aridity, but did not covary with latitude. Scale size (inferred from the inverse relation with numbers of scales) was positively related to body size. Controlling for body size via multiple regression, scale size was associated negatively with latitude (best predictor), positively with minimum temperature, and negatively with aridity (similar results were obtained using scores from a principal components analysis of latitude and climatic indicators). Thus, lizards with larger scales are not necessarily found in areas with higher temperatures. Univariate analyses indicated phylogenetic signal for body size, scale counts, latitude, and all climate indicators. In all cases, phylogenetic regression models fit the data significantly better than nonphylogenetic models; thus, residuals for log(10) number of dorsal scale rows exhibited phylogenetic signal.     

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.     

The phylogeny of a species-level tendency: species heritability and possible deep origins of Bergmann's rule in tetrapods

One of the most widely recognized generalizations in biology is Bergmann's rule, the observation that, within species of birds and mammals, body size tends to be inversely related to ambient temperature. Recent studies indicate that turtles and salamanders also tend to follow Bergmann's rule, which hints that this species-level tendency originated early in tetrapod history. Furthermore, exceptions to Bergmann's rule are concentrated within squamate reptiles (lizards and snakes), suggesting that the tendency to express a Bergmann's rule cline may be heritable at the species level. We evaluated species-level heritability and early origination of Bergmann's rule by mapping size-latitude relationships for 352 species onto a tetrapod phylogeny. When the largest available dataset is used, Bergmann's rule shows significant phylogenetic signal, indicating species-level heritability. This represents one of the few demonstrations of heritability for an emergent species-level property and the first for an ecogeographic rule. When species are discretely coded as showing either Bergmann's rule or its converse, parsimony reconstructions suggest that: (1) the tendency to follow Bergmann's rule is ancestral for tetrapods, and (2) most extant species that express the rule have retained this tendency from that ancient ancestor. The first inference also generally holds when the discrete data or size-latitude correlation coefficients are analyzed using maximum likelihood, although the results are only statistically significant for some versions of the discrete analyses. The best estimates of ancestral states suggest that the traditional adaptive explanation for Bergmann's rule-conservation of metabolic heat-was not involved in the origin of the trait since that origin predates the evolution of endothermy. A more general thermoregulatory hypothesis could apply to endotherms and some ectotherms, but fails to explain why salamanders have retained Bergmann's rule. Thus, if thermoregulation underlies the origin of a Bergmann's rule tendency, this trait may have been continuously maintained while its cause changed. Alternatively, thermoregulation may not underlie Bergmann's rule in any tetrapod group. The results also suggest that many extinct groups not included in our analyses followed Bergmann's rule.     

Amphibians do not follow Bergmann's rule

The tendency for organisms to be larger in cooler climates (Bergmann's rule) is widely observed in endotherms, and has been reputed to apply to some ectotherms including amphibians. However, recent reports provide conflicting support for the pattern, questioning whether Bergmann's clines are generally present in amphibians. In this study, we measured 96,996 adult Plethodon from 3974 populations to test for the presence of Bergmann's clines in these salamanders. Only three Plethodon species exhibited a significant negative correlation between body size and temperature consistent with Bergmann's rule, whereas 37 of 40 species did not display a pattern consistent with this prediction. Further, a phylogenetic comparative analysis found no relationship between body size and temperature among species. A meta-analysis combining our data with the available data for other amphibian species revealed no support for Bergmann's rule at the genus (Plethodon), order (Caudata), or class (Amphibia) levels. Our findings strongly suggest that negative thermal body size clines are not common in amphibians, and we conclude that Bergmann's rule is not generally applicable to these taxa. Thus, evolutionary explanations of Bergmann's clines in other tetrapods need not account for unique life-history attributes of amphibians.     

The importance of phylogenetic scale in tests of Bergmann's and Rapoport's rules: lessons from a clade of South American lizards

We tested for the occurrence of Bergmann's rule, the pattern of increasing body size with latitude, and Rapoport's rule, the positive relationship between geographical range size and latitude, in 34 lineages of Liolaemus lizards that occupy arid regions of the Andean foothills. We tested the climatic-variability hypothesis (CVH) by examining the relationship between thermal tolerance breadth and distribution. Each of these analyses was performed varying the level of phylogenetic inclusiveness. Bergmann's rule and the CVH were supported, but Rapoport's rule was not. More variance in the data for Bergmann's rule and the CVH was explained using species belonging to the L. boulengeri series rather than all species, and inclusion of multiple outgroups tended to obscure these macroecological patterns. Evidence for Bergmann's rule and the predicted patterns from the CVH remained after application of phylogenetic comparative methods, indicating a greater role of ecological processes rather than phylogeny in shaping the current species distributions of these lizards.     

Bergmann and converse bergmann latitudinal clines in arthropods: two ends of a continuum?

Two seemingly opposite evolutionary patterns of clinal variationin body size and associated life history traits exist in nature.According to Bergmann's rule, body size increases with latitude,a temperature effect. According to the converse Bergmann rule,body size decreases with latitude, a season length effect. Athird pattern causally related to the latter is countergradientvariation, whereby populations of a given species compensateseasonal limitations at higher latitudes by evolving fastergrowth and larger body sizes compared to their low latitudeconspecifics. We discuss these patterns and argue that theyare not mutually exclusive because they are driven by differentenvironmental causes and proximate mechanisms; they thereforecan act in conjunction, resulting in any intermediate pattern.Alternatively, Bergmann and converse Bergmann clines can beinterpreted as over- and undercompensating countergradient variation,respectively. We illustrate this with data for the wide-spreadyellow dung fly, Scathophaga stercoraria (Diptera: Scathophagidae),which in Europe shows a Bergmann cline for size and a converseBergmann cline (i.e., countergradient variation) for developmenttime. A literature review of the available evidence on arthropodlatitudinal clines further shows a patterned continuum of responses.Converse Bergmann clines due to end-of-season time limitationsare more common in larger species with longer development times.Our study thus provides a synthesis to the controversy aboutthe importance of Bergmann's rule and the converse Bergmannrule in nature.     

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.     

Carnivores, biases and Bergmann's rule

Studies of Bergmann's rule may encompass a non-random subsample of extant homeotherms. We examined patterns of correlation between skull length and geographical latitude in 44 species of carnivores in order to test the validity of Bergmann's rule in the Carnivora. Results were then compared to those of other studies. Significant positive correlation between skull length and latitude was found in 50% of carnivore species, while significant negative correlation was found in only 11% of species. These results indicate that the occurrence of Bergmann's rule in the Carnivora is less frequent than earlier published data suggest. Publication bias is not detected in published data. Therefore, previous studies of geographical size variation might be biased in favour of species known to follow Bergmann's rule.  © 2004 The Linnean Society of London, Biological Journal of the Linnean Society , 2004, 81 , 579–588.     

Age and body size of Salamandrella keyserlingii (Caudata: Hynobiidae): a difference in altitudes, latitudes, and temperatures

The debate surrounding Bergmann??s rule, in which the body size of animals is predicted to be larger in cooler environments, is still open concerning ectotherms. Our goal was to test this rule in the broadest ranging amphibian species Salamandrella keyserlingii. We determined age and body size in a cooler region (Darhadyn, Mongolia: mean yearly air temperature?=??C8.31 °C) using skeletochronology, and compared their differences in altitude, latitude, and temperature with those of a warmer area (Kushiro, Japan: 7.98 °C). In Darhadyn, both sexes reached sexual maturity at 5?C6?years of age (growth coefficient: male?=?0.585, female?=?0.266), 2?C3?years later than those in Kushiro (male?=?1.341, female?=?1.129). Mean body size was smaller in Darhadyn (53.08?mm) than in Kushiro (57.63?mm) for males despite their constant metamorphic size around 30?mm. We also analyzed data available from published studies for 27 populations within the geographic range of this species from 43 to 69°N across a 2,900-km long latitudinal gradient. The analysis indicated an intraspecific tendency to decrease body size with increased latitude from 43 to 57°N, to increase size from 57 to 69°N, and to decrease body size with decreased temperature from 8 to ?C7?°C and increase size from ?C7 to ?C15?°C. This pattern does not follow the intraspecific extension of Bergmann??s rule and may follow the converse of Terentjev??s optimum rule??a rule formulated to be an inverted-U shaped curve between increased latitude (or decreased temperature) and increased body size.     

The converse to Bergmann's rule in bumblebees,a phylogenetic approach

Two patterns commonly emerge when animal body size is analyzed as a function of latitudinal distribution. First, body size increases with latitude, a temperature effect known as Bergmann's rule, and second, the converse to Bergmann's rule, a pattern in which body size decreases with latitude. However, other geographic patterns can emerge when the mechanisms that generate Bergmann's and the converse to Bergmann's clines operate together. Here, we use phylogenetic comparative analysis in order to control for phylogenetic inertia, and we show that bumblebees exhibit the converse to Bergmann's rule. Bumblebee taxa are distributed worldwide in temperate and tropical regions. The largest species are found in places with high water availability during the driest time of the year. Nonetheless, large body size is constrained by extreme temperatures. Bumblebees’ body size could be related to a higher extent to the size of food rewards to be harvested than to the energetic advantages of thermoregulation. Moreover, we found that the body size of eusocial and cuckoo species responded in the same way to environmental variables, suggesting that they have not diverged due to different selective pressures.     

Fecundity selection predicts Bergmann's rule in syngnathid fishes

The study of latitudinal increases in organismal body size (Bergmann's rule) predates even Darwin's evolutionary theory. While research has long concentrated on identifying general evolutionary explanations for this phenomenon, recent work suggests that different factors operating on local evolutionary timescales may be the cause of this widespread trend. Bergmann's rule explains body size variation in a diversity of warm-blooded organisms and there is increasing evidence that Bergmann's rule is also widespread in ectotherms. Bergmann's rule acts differentially in species of the Syngnathidae, a family of teleost fishes noted for extreme adaptations for male parental care. While variation in body size of polygamous Syngnathus pipefish is consistent with Bergmann's rule, body size is uncorrelated with latitude in monogamous Hippocampus seahorses. A study of populations of Syngnathus leptorhynchus along a natural latitudinal and thermal gradient indicates that increases in body size with latitude maintain the potential reproductive rate of males despite significant decreases in ambient temperatures. Polygyny is necessary in order to maximize male reproductive success in S. leptorhynchus , suggesting a possible a link between fecundity selection and Bergmann's rule in this species.     

Seeing the forest for the trees: partitioning ecological and phylogenetic components of Bergmann's rule in European Carnivora

Comparative methods have commonly been applied in macroecological research. However, few methods exist to map and analyze phylogenetic variation in geographical space. Here we develop a general analytical framework to partition the phylogenetic and ecological structures of macroecological patterns in geographic space. As an example, we apply the framework to evaluate interspecific patterns of body size geographic variation (Bergmann's rule) in European Carnivora. We model the components of variance attributable to ecological and phylogenetic effects, and to the shared influence of both factors. Spatial patterns in the ecological component are stronger than those in the original body size data. More importantly, the magnitude of intraspecific body size patterns (as measured by the correlation coefficient between body size and latitude) is significantly correlated with the ecological component across species, providing a unified interpretation for Bergmann's rule at multiple levels of biological hierarchy. This approach provides a better understanding of patterns in macroecological traits and allows improved understanding of their underlying ecological and evolutionary mechanisms.     

Geographic variation in body size and sexual size dimorphism of a seed-feeding beetle

Body size of many animals varies with latitude: body size is either larger at higher latitudes (Bergmann's rule) or smaller at higher latitudes (converse Bergmann's rule). However, the causes underlying these patterns are poorly understood. Also, studies rarely explore how sexual size dimorphism varies with latitude. Here we investigate geographic variation in body size and sexual size dimorphism of the seed-feeding beetle Stator limbatus, collected from 95 locations along a 38 degrees range in latitude. We examine 14 variables to test whether clines in environmental factors are adequate to explain geographic patterns of body size. We found that body size and sexual size dimorphism of S. limbatus varied considerably with latitude; beetles were smaller but more dimorphic at lower latitudes. Body size was not correlated with a gradient in mean temperature, contrary to the commonly accepted hypothesis that clines are produced by latitudinal gradients in temperature. Instead, we found that three factors were adequate to explain the cline in body size: clinal variation in host plant seed size, moisture (humidity), and seasonality (variance in humidity, precipitation, and temperature). We also found that the cline in sexual size dimorphism was partially explainable by a gradient in moisture, though moisture alone was not sufficient to explain the cline. Other ecological or environmental variables must necessarily contribute to differences in selection on male versus female body size. The main implications of our study are that the sexes differ in the magnitude of clinal variation in body size, creating latitudinal variation in sexual size dimorphism, and that clines in body size of seed beetles are likely influenced by variation in host seed size, water availability, and seasonality.     

A test of Allen's rule in ectotherms: the case of two south American Melanopline Grasshoppers (Orthoptera: Acrididae) with partially overlapping geographic ranges

We studied the geographic variation of three morphometric characters in relation to body size in two South American grasshoppers (Acrididae), Dichroplus vittatus Bruner and D. pratensis Bruner to test Allen's rule in these ectotherms. Since both species follow the converse to Bergmann's rule owing to latitudinal and/or altitudinal variation in time available for growth and reproduction, geographic variation in body size proportions of protruding parts may obey to differential allometric growth in different geographic areas. Alternatively, it could reflect true Allenian variation related to thermoregulation. Body proportions were studied by correlation/regression analyses with geographic and climatic variables. In D. pratensis, body proportions increased with latitude and decreased with altitude. These results probably obey to the effects of water balance and seasonality on final body size, and on the allometric growth of the three studied characters not being related to thermoregulation. In D. vittatus, a generally non-significant trend towards the decrease of the mean proportions of all three characters with increasing latitude was observed. Nevertheless, also in this species, it is probable that the environmental gradient responds to seasonality factors (although not to water balance) that affect the length of growing season and, in consequence, body size and its allometric relationships. We conclude that the regularities in the geographic distribution of body proportions of D. pratensis and D. vittatus do not follow Allen's rule in the sense of thermoregulation, and result from variables that determine growing season length and the allometric growth of different body parts.     

The effect of island area on body size in a primate species from the Sunda Shelf Islands

Aim  We examine the effect of island area on body dimensions in a single species of primate endemic to Southeast Asia, the long-tailed macaque ( Macaca fascicularis ). In addition, we test Allen's rule and a within-species or intraspecific equivalent of Bergmann's rule (i.e. Rensch's rule) to evaluate body size and shape evolution in this sample of insular macaques.
Location  The Sunda Shelf islands of Southeast Asia.
Methods  Body size measurements of insular macaques gathered from the literature were analysed relative to island area, latitude, maximum altitude, isolation from the mainland and other islands, and various climatic variables using linear regression.
Results  We found no statistically significant relationship between island area and body length or head length in our sample of insular long-tailed macaques. Tail length correlated negatively with island area. Head length and body length exhibited increases corresponding to increasing latitude, a finding seemingly consistent with the expression of Bergmann's rule within a single species. These variables, however, were not correlated with temperature, indicating that Bergmann's rule is not in effect. Tail length was not correlated with either temperature or increasing latitude, contrary to that predicted by Allen's rule.
Main conclusions  The island rule dictating that body size will covary with island area does not apply to this particular species of primate. Our study is consistent with results presented in the literature by demonstrating that skull and body length in insular long-tailed macaques do not, strictly speaking, conform to Rensch's rule. Unlike previous studies, however, our findings suggest that tail-length variation in insular macaques does not support Allen's rule.     

Dichroplus vittatus (Orthoptera: Acrididae) follows the converse to Bergmann's rule although male morphological variability increases with latitude

Geographic body size variation was analysed in males and females of 19 populations of the South American grasshopper Dichroplus vittatus Bruner spanning 20 degrees of latitude and 2700 m of altitude. Using mean and maximum body length of each sex and factors obtained from principal components analyses of six morphometric linear characters it was shown that D. vittatus followed the converse to Bergmann's rule latitudinally but not altitudinally where no significant trends were observed. For males, variability of body size increased with latitude but not with altitude. Both types of trends were significantly correlated with mean annual temperature and minimum annual temperature (positive correlations), and two estimators of seasonality, the coefficients of variation of mean annual temperature (negative) and mean annual precipitation (positive). Some allometric relationships also showed geographic variation. It is suggested that the observed decrease in size with latitude together with the increase in morphological variability is a consequence of a number of factors: the shortening of the growing season southwards; the increasing seasonality and climatic unpredictability; and the fact that the species exhibits protandry which contributes to smaller and more variable size in males and smaller but more constant body size in females.     

An Intercontinental Analysis of Climate-Driven Body Size Clines in Reptiles: No Support for Patterns, No Signals of Processes

Climatic gradients impose clinal selection on animal ecological and physiological performance, often promoting geographic body size clines. Bergmann’s rule predicts that body size increases with decreasing environmental temperatures given the need to retain body-heat through adjustments of body-mass-to-surface-area ratio. This prediction generally holds for endotherms, but remains controversial for ectotherms. An alternative interpretation, the ‘resource rule’, suggests that food abundance, primary productivity and precipitation (which, unlike temperature, do not necessarily correlate with geography), drive body size clines. We investigate geographic variation in body size within 65 species of lizards and snakes (squamates) based on an intercontinental dataset (6,500+ specimens belonging to 56 Israeli species, and multiple populations of nine Liolaemus species from Argentina and Chile). Bergmann’s rule is only rarely supported by our data (in four species, 6 %), whereas six species (9 %) follow its converse (hence, it is unsupported in 94 % of cases). Similarly, size increases with resource abundance in only 12 species (18 %). Therefore, although neither of the rules is supported, factors suggested by the resource rule are better predictors of body size than temperature. Surprisingly, we show that some measures of the extent of a species’ climatic envelope do not affect the likelihood of it showing a size-climate relationship. We conclude that negative size-temperature associations are an exception rather than a generality among squamates.     

Body size clines in sceloporus lizards: proximate mechanisms and demographic constraints

Although most species of animals examined to date exhibit Bergmann'sclines in body size, squamates tend to exhibit opposing patterns.Squamates might exhibit reversed Bergmann's clines because theytend to behaviorally regulate their body temperature effectively;the outcome of this thermoregulation is that warmer environmentsenable longer daily and annual durations of activity than coolerenvironments. Lizards of the genus Sceloporus provide an opportunityto understand the factors that give rise to contrasting thermalclines in body size because S. undulatus exhibits a standardBergmann's cline whereas S. graciosus exhibits a reverse Bergmann'scline. Interestingly, rapid growth by individuals of both speciesinvolves adjustments of physiological processes that enablemore efficient use of food. Patterns of adult body size arelikely the evolutionary consequence of variation in juvenilesurvivorship among populations. In S. undulatus, delayed maturationat a relatively large body size is exhibited in cooler environmentswhere juveniles experience higher survivorship, resulting ina Bergmann's cline. In S. graciosus, high juvenile survivorshipis not consistently found in cooler environments, resultingin no cline or a reversed Bergmann's cline, i.e., geographicpatterns in body size aren't necessarily produced by naturalselection. Thus, discerning the mechanistic links between thethermal physiology of an organism and environment-specific ratesof mortality will be critical to understanding the evolutionof body size in relation to environmental temperature.