Geographic gradients in body size: a clarification of Bergmann's rule

1997 marked the sesquicentenary of the publication by Carl Bergmann of the observation that, in general, large-bodied animal species tend to live further north than their small-bodied relatives. This has been dubbed Bergmann's rule in his honour. However, more than 150 years on, we appear to be little closer to a general understanding of the rule, or even to any consensus as to whether it exists. This is due in large part to confusion about the taxonomic level at which the rule is considered to operate, and to the conflation of pattern and mechanism. In this paper, we attempt to resolve this confusion by highlighting its sources, and by providing a definition of Bergmann's rule that is practical and useful, yet that retains the essential features of its original formulation. We conclude by briefly reviewing the mechanisms proposed to explain Bergmann's rule as we define it.     

Bergmann's idiosyncratic rule: a role for fecundity selection?

The negative relationship between temperature and geographical variation in body size, or Bergmann's rule, is among the most thoroughly studied ecogeographical rules, yet the pattern and process underlying it remain controversial. Bergmann's original observations were of body size clines among endotherms, but in the last 50 years there has been increasing recognition that both Bergmann's rule and its reverse occur in many ectotherm taxa. A new study of syngnathid fish by Wilson (2009 ) in this issue of Molecular Ecology sheds light on intriguing alternative mechanisms that may explain variation in the direction of body size clines across taxa. Wilson shows that Bergmann's rule is found in pipefish of the genus Syngnathus , but not in seahorses of the genus Hippocampus . His results suggest that polygamy in pipefish allows fecundity selection to favour large size at low temperatures, compensating for increases in brooding time.     

Intra- and interspecific morphological variation in the field mouse species Apodemus argenteus and A. speciosus in the Japanese archipelago: the role of insular isolation and biogeographic gradients

Two species of field mice, Apodemus argenteus and A. speciosus, occur in sympatry across the Japanese archipelago. The inter- and intraspecific patterns of morphological differentiation have been evaluated, using a Fourier analysis of the mandible outline. The relative importance of the effect of insular isolation and latitudinal climatic gradient on the size and shape of the two species was assessed by a comparison of the populations from the large island of Honshu and the surrounding small-island populations. The size variation in A. argenteus is correlated with the climatic gradient whilst the shape variation corresponds mainly to a random differentiation of the small-island populations from a Honshu-like basic morphological pattern. A. speciosus displays increased size on small islands, and its shape variation is related to both the climatic gradient and insularity. Finally, the two species are differentiated by both the size and shape of the mandible across the Japanese archipelago, suggesting that interspecific competition between both species is reduced via niche partitioning. Our results emphasize the importance of insular isolation on shape differentiation, but a part of the morphological differentiation is also related to the latitudinal climatic gradient. Isolation on small islands could have favoured such a response to environmental factors by lowering the gene flow that prevents almost any significant differentiation within Honshu populations.     

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.     

Amphipod gigantism dictated by oxygen availability?

A recent study of gigantism in amphipods proposes a novel mechanism which could be used to explain Bergmann's rule, namely differences in environmental O₂ concentration. Consideration of the respiratory biology of this group indicates significant flaws in this proposal. Nonetheless, it is not unreasonable to predict a relationship between ectotherm body size and O₂ partial pressure ( p O₂) in some systems, where the partial pressure gradient is steep, either in time (comparison of Carboniferous and Permian atmospheres) or space (animals inhabiting oceanic O₂ minimum layers, and, particularly in freshwaters, living at high altitude). Animal gigantism can be correlated with periods of very high environmental p O₂ over geological time. Unfortunately, data for present day spatial patterns are scant.     

Bergmann's rule in nonavian reptiles: turtles follow it,lizards and snakes reverse it

Abstract Bergmann's rule is currently defined as a within-species tendency for increasing body size with increasing latitude or decreasing environmental temperature. This well-known ecogeographic pattern has been considered a general trend for all animals, yet support for Bergmann's rule has only been demonstrated for mammals and birds. Here we evaluate Bergmann's rule in two groups of reptiles: chelonians (turtles) and squamates (lizards and snakes). We perform both nonphylogenetic and phylogenetic analyses and show that chelonians follow Bergmann's rule (19 of 23 species increase in size with latitude; 14 of 15 species decrease in size with temperature), whereas squamates follow the converse to Bergmann's rule (61 of 83 species decrease in size with latitude; 40 of 56 species increase in size with temperature). Size patterns of chelonians are significant using both nonphylogenetic and phylogenetic methods, whereas only the nonphylogenetic analyses are significant for squamates. These trends are consistent among major groups of chelonians and squamates for which data are available. This is the first study to document the converse to Bergmann's rule in any major animal group as well as the first to show Bergmann's rule in a major group of ectotherms. The traditional explanation for Bergmann's rule is that larger endothermic individuals conserve heat better in cooler areas. However, our finding that at least one ectothermic group also follows Bergmann's rule suggests that additional factors may be important. Several alternative processes, such as selection for rapid heat gain in cooler areas, may be responsible for the converse to Bergmann's rule in squamates.     

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.     

Variation at high latitudes: the geography of body size and cranial morphology of the muskox, Ovibos moschatus

Abstract Aim Bergmann's rule, one of the most studied and controversial ecogeographical generalizations, has rarely been tested with observations from high latitudes. We tested the rule using cranial measurements of the muskox [Ovibos moschatus (Zimmerman)], a homeotherm with an extremely northern distribution. We also used these data to describe geographical patterns in the species' dental architecture, an extension of the framework developed from interspecific comparisons. Location Specimens were compiled from arctic Canada, Alaska and Greenland, a latitudinal range of 60° N?83° N. Methods Body size was estimated from principal components analysis (PCA) of five cranial characters from 128 specimens. Mean scores on the first principal component from each locality were regressed against latitude and mean temperature to identify geographical variation in body size; scores on the second principal component were regressed against latitude to assess patterns in dental architecture. Regression analyses of the individual characters were performed as a complement to PCA. Results No latitudinal or climatic trend in body size was observed in either sex. On the other hand, for males, significant latitudinal variation was found for the second PCA axis (r = ?0.434), and the feature which loaded most heavily on it, maxillary tooth row length (r = 0.429). For females, this dental structure also tended to increase with latitude (r = 0.423), but the trend was only marginally significant (P=0.12), perhaps owing to a smaller sample size. Main conclusions The geographically invariant body size of muskoxen failed to support current hypotheses of size variation. Behavioural and physiological adaptations may exempt the muskox from selective pressures underlying these hypotheses. We interpret latitudinal variation in dental architecture as a reflection of a cline in diet, dominated by graminoids at the expense of willows at higher latitudes. This intraspecific geographical trend is a recapitulation of the interspecific framework for large mammalian herbivores.     

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.     

Climatological correlates for body size of five species of Australian mammals

Size variation of body and skull of five species of Australian mammals (echidna, Tachyglossus aculeatus ; brush-tail possum, Trichosurus vulpecula ; eastern grey kangaroo, Macropus giganteus ; western grey kangaroo, M. fuliginosus ; red kangaroo, M. rufus ), is related to climatic factors. All five species show trends in body size that conform with Bergmann's rule, individuals from colder environments being larger than those from warmer areas. The western and eastern grey kangaroos also conform with Allen's rule, the relative size of their extremities being large in warmer areas. In four of the five species (not the red kangaroo) body size is also correlated with indices of biomass productivity. However, since biomass productivity and ambient temperature are related to some extent, it is difficult to separate the effects of these factors.     

Against Bergmann's rule: fly sperm size increases with temperature

A long-standing school textbook biological rule, Bergmann's rule, asserts that animals (and their constituent parts) grow bigger when it is colder. This seems to hold for many warm-blooded animals, as well as for egg, cell and body size of most cold-blooded animals. A unifying mechanism producing this pattern has not been found. We here provide the first experimental evidence that the size of an important type of cell, namely sperm, increases (rather than decreases) with temperature in a cold-blooded animal, the yellow dung fly. By pointing to an exception, our work either questions the generality of one prominent category of explanation of Bergmann's rule, that of a physiological constraint, or alternatively suggests that sperm differ fundamentally in their physiology from other cells.