A review of Gloger's rule,an ecogeographical rule of colour: definitions,interpretations and evidence

Gloger's rule is an ecogeographical rule that links animal colouration with climatic variation. This rule is named after C.W.L. Gloger who was one of the first to summarise the associations between climatic variation and animal colouration, noting in particular that birds and mammals seemed more pigmented in tropical regions. The term ‘Gloger's rule' was coined by B. Rensch in 1929 and included different patterns of variation from those described by Gloger. Rensch defined the rule in two ways: a simple version stating that endothermic animals are predicted to be darker in warmer and humid areas due to the increased deposition of melanin pigments; and a complex version that includes the differential effects of humidity and temperature on both main types of melanin pigments – eu‐ and phaeo‐melanin. The blackish eu‐melanins are predicted to increase with humidity, and decrease only at extreme low temperatures, while the brown‐yellowish phaeomelanins prevail in dry and warm regions and decrease rapidly with lower temperatures. A survey of the literature indicates that there is considerable variation/confusion in the way Gloger's rule is understood (based on 271 studies that define the rule). Whereas the complex version is hardly mentioned, only a quarter of the definitions are consistent with the simple version of Gloger's rule (darker where warm and wet), and most definitions mention only the effects of humidity (darker where wet). A smaller subset of studies define the rule based on other correlated climatic and environmental variables such as vegetation, latitude, altitude, solar radiation, etc., and a few even contradict the original definition (darker where cold). Based on the literature survey, I synthesised the qualitative (N = 124 studies) and quantitative (meta‐analytically, N = 38 studies, 241 effects) evidence testing the simple version of Gloger's rule (I found no tests of the complex version). Both lines of evidence supported the predicted effects of humidity (and closely linked variables) on colour variation, but not the effects of temperature. Moreover, humidity effects are not restricted to birds and mammals, as the data indicate that these effects also apply to insects. This suggests that the simple version of Gloger's rule as originally defined may not be valid, and possibly that the rule should be re‐formulated in terms of humidity effects only. I suggest, however, that more data are needed before such a reformulation, due to potential publication biases. In conclusion, I recommend that authors cite Rensch when referring to Gloger's rule and that they make clear which version they are referring to. Future research should concentrate on rigorously testing the validity and generality of both versions of Gloger's rule and establishing the mechanism(s) responsible for the patterns it describes. Since humidity seems to be the core climatic variable behind Gloger's rule, I suggest that the two most plausible mechanisms are camouflage and protection against parasites/pathogens, the latter possibly through pleiotropic effects on the immune system. Understanding the processes that lead to climatic effects on animal colouration may provide insights into past and future patterns of adaptation to climatic change.     

Disentangling thermal from alternative drivers of reflectance in jewel beetles: A macroecological study

Aim

To predict future colour–climate relationships, it is important to distinguish thermal drivers of reflectance from other evolutionary drivers. We aimed to achieve this by comparing relationships between climate and coloration in ultraviolet–visible (UV–Vis) and near-infrared (NIR) light, separately.

Location

Samples were distributed primarily across Australia and North America, with some from Africa and Asia.

Major taxa studied

Coleoptera: Buprestidae.

Methods

We used jewel beetles as models to identify climatic drivers of reflectance, because jewel beetles have highly diverse coloration and a wide distribution and are often active in hot conditions. Specifically, we tested the association between climate, body size and reflectance using a phylogenetic comparative analysis for three wavebands (UV–Vis, NIR and total).

Results

Reflectance of jewel beetles was more strongly predicted by body size than by climate. NIR reflectance and total reflectance were not associated with climate, but larger beetles had higher NIR reflectance. For UV–Vis reflectance, small beetles were darker in warmer and more humid environments, whereas there was no association with climate for large beetles.

Main conclusions

Our study suggests that variation in reflectance of jewel beetles is not driven by thermal requirements and highlights the importance of considering NIR reflectance when evaluating explanations of the effects of colour on thermoregulation.     

Environmental steepness,tolerance gradient,and ecogeographical rules in glassfrogs (Anura: Centrolenidae)

Spatial variation in biological traits reflects evolutionary and biogeographical processes of the history of clades, and patterns of body size and range size can be suitable to recover such processes. In the present study, we test for latitudinal and altitudinal gradients in both body and range sizes in an entire family of tropical anurans, Centrolenidae. We partition the species latitudinal, and altitudinal distributions into an indirect measure of tolerance, and then test its effect on the body size gradient. We use an assemblage‐based approach to correlate the traits with altitudinal and latitudinal axes, taking into account both phylogenetic and spatial autocorrelation in data. Centrolenids lack any gradient in range size but show a positive cline of both body size and adaptive body enlargement with altitude. This pattern is also positively correlated with an altitudinal gradient of cold tolerance, thus lending support to the heat balance hypothesis as an explanation of the body size cline. By using an entire Neotropical clade of anurans, we add further support for Bergmann's rule in ectotherms, warn for a likely effect of environmental steepness in fashioning the gradient, and offer evidence for an historical scenario (the Oligocene–Eocene Andean uplift) as its likely trigger. © 2013 The Linnean Society of London     

Ecotypic variation in the context of global climate change: revisiting the rules

Patterns of ecotypic variation constitute some of the few 'rules' known to modern biology. Here, we examine several well-known ecogeographical rules, especially those pertaining to body size in contemporary, historical and fossil taxa. We review the evidence showing that rules of geographical variation in response to variation in the local environment can also apply to morphological changes through time in response to climate change. These rules hold at various time scales, ranging from contemporary to geological time scales. Patterns of body size variation in response to climate change at the individual species level may also be detected at the community level. The patterns underlying ecotypic variation are complex and highly context-dependent, reducing the 'predictive-power' of ecogeographical rules. This is especially true when considering the increasing impact of human activities on the environment. Nonetheless, ecogeographical rules may help interpret the likely influences of anthropogenic climate change on ecosystems. Global climate change has already influenced the body size of several contemporary species, and will likely have an even greater impact on animal communities in the future. For this reason, we highlight and emphasise the importance of museum specimens and the continued need for documenting the earth's biological diversity.     

Beyond latitude: Temperature,productivity and thermal niche conservatism drive global body size variation in Odonata

Aim

So far, latitudinal body size clines have been discussed primarily in the context of thermoregulation, sensu Bergmann. However, body size patterns are ambiguous in ectotherms, and this heterogeneity remains poorly understood. We tested whether Bergmann's rule and the resource availability rule, which states that energetic requirements determine species body size, apply to damselflies and dragonflies (Odonata). Furthermore, we hypothesized that the contrasting effects of thermoregulation and resource availability (e.g., productivity) can obscure the overall gradient in body size variation.

Location

Global.

Time period

Contemporary.

Major taxa studied

Odonata.

Methods

Using data for 43% of all odonate species described so far, we tested our hypotheses in phylogenetically and spatially comparative analyses at assemblage and species levels. For the distribution data, we integrated expert range maps and ecoregional ranges based on all available occurrence records. To distinguish between long-term and evolutionarily recent responses of environmental drivers in body size, we constructed a phylogenetically informed classification of all odonate species and decomposed the body size into its phylogenetic and specific components for our subset of species.

Results

We documented a weak positive relationship between body length and latitude but found strong and contrasting effects for temperature between dragonflies and damselflies and consistent positive effects for productivity that explained 35–57% of body size variation. Moreover, we showed a strong phylogenetic signal in sized-based thermoregulation that shaped the distribution of dragonflies, but not of damselflies.

Main conclusions

We concluded that temperature, productivity and conservatism in size-based thermoregulation synergistically determine the distribution of ectotherms, while the taxon-specific importance of these factors can lead to contrasting and weak latitude–size relationships. Our results reinforce the importance of body size as a determinant of species distributions and responses to climate change.     

Clinal variation in the morph ratio of Black Sparrowhawks Accipiter melanoleucus in South Africa and its correlation with environmental variables

The morph ratio distribution in polymorphic species often varies clinally, with a gradual change in morph ratios across the distributional range of the species. In polymorphic bird populations, clinal variation is rarely quantified. We describe a cline in the morph ratios of Black Sparrowhawks across South Africa, which is principally driven by a higher ratio of dark morph birds in the newly colonized southwest of the country. Across the 1400 km of our cline, the probability of a bird being a dark morph declined from over 80% close to the Cape Peninsula to under 20% in the northeast. Higher frequencies of dark morphs were associated with a higher proportion of rainfall falling during the winter breeding months. Further investigation revealed relationships between the proportion of dark morphs and altitude, amount of rainfall during the breeding months, and an interaction between this variable and temperature. These results provide some support for the suggestion that the higher frequency of dark morphs in the southwest is an adaptive response, rather than the result of a founder effect or genetic drift. These findings also suggest that, in theory, polymorphic species may be better adapted to cope with the challenges of climate change or may be able to expand their ranges more quickly into novel climatic areas, since selection pressure can act on a pre‐existing trait that may be beneficial in new conditions.     

Adaptive phenotypic and genomic divergence in the common chaffinch (Fringilla coelebs) following niche expansion within a small oceanic island

According to models of ecological speciation, adaptation to adjacent, contrasting habitat types can lead to population divergence given strong enough environment-driven selection to counteract the homogenizing effect of gene flow. We tested this hypothesis in the common chaffinch (Fringilla coelebs) on the small island of La Palma, Canary Islands, where it occupies two markedly different habitats. Isotopic (δ¹³C, δ¹⁵N) analysis of feathers indicated that birds in the two habitats differed in ecosystem and/or diet, and analysis of phenotypic traits revealed significant differences in morphology and plumage colouration that are consistent with ecomorphological and ecogeographical predictions respectively. A genome-wide survey of single-nucleotide polymorphism revealed marked neutral structure that was consistent with geography and isolation by distance, suggesting low dispersal. In contrast, loci putatively under selection identified through genome-wide association and genotype-environment association analyses, revealed a marked adaptive divergence between birds in both habitats. Loci associated with phenotypic and environmental differences among habitats were distributed across the genome, as expected for polygenic traits involved in local adaptation. Our results suggest a strong role for habitat-driven local adaptation in population divergence in the chaffinches of La Palma, a process that appears to be facilitated by a strong reduction in effective dispersal distances despite the birds' high dispersal capacity.     

Environment and morphology in Australian Aborigines: a re-analysis of the Birdsell database

Pursuant to his major research interest in the cultural ecology of hunter-gatherers, Birdsell collected an unparalleled body of phenotypic data on Aboriginal Australians during the mid twentieth century. Birdsell did not explicitly relate the geographic patterning in his data to Australia's climatic variation, instead arguing that the observable differences between groups reflect multiple origins of Australian Aborigines. In this article, bivariate correlation and multivariate analyses demonstrate statistically significant associations between climatic variables and the body build of Australians that are consistent with the theoretical expectations of Bergmann's and Allen's rules. While Australian Aborigines in comparison to Eurasian and New World populations can be generally described as long-headed, linear in build, and characterized by elongated distal limbs, the variation in this morphological pattern across the continent evidently reflects biological adaptation to local Holocene climates. These results add to a growing body of evidence for the role of environmental selection in the development of modern human variation.     

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.     

Geographic variation in body size and its relationship with environmental gradients in the Oriental Garden Lizard,Calotes versicolor

Patterns of geographic variation in body size are predicted to evolve as adaptations to local environmental gradients. However, many of these clinal patterns in body size, such as Bergmann's rule, are controversial and require further investigation into ectotherms such as reptiles on a regional scale. To examine the environmental variables (temperature, precipitation, topography and primary productivity) that shaped patterns of geographic variation in body size in the reptile Calotes versicolor, we sampled 180 adult specimens (91 males and 89 females) at 40 locations across the species range in China. The MANOVA results suggest significant sexual size dimorphism in C. versicolor (F_23,124 = 11.32, p < .001). Our results showed that C. versicolor failed to fit the Bergmann's rule. We found that the most important predictors of variation in body size of C. versicolor differed for males and females, but mechanisms related to heat balance and water availability hypotheses were involved in both sexes. Temperature seasonality, precipitation of the driest month, precipitation seasonality, and precipitation of the driest quarter were the most important predictors of variation in body size in males, whereas mean precipitation of the warmest quarter, mean temperature of the wettest quarter, precipitation seasonality, and precipitation of the wettest month were most important for body size variation in females. The discrepancy between patterns of association between the sexes suggested that different selection pressures may be acting in males and females.     

Population level differences in adult body mass emerge in infancy and early childhood: Evidence from a global sample of low and lower‐income countries

Many studies have linked measures of adult body shape and mass in ancient and contemporary populations to ecogeographical variables such as temperature and latitude. These results tend to support Bergmann's rule, which posits that bodies will be relatively less slender for their height in colder climates and more slender in warmer climates. Less well explored is the ontogeny of these population‐level differences. Here we use data on infants and children from 46 low and lower income countries to test whether children's weight for height is associated with measures of temperature and latitude. We also test the hypothesis that children living in areas with greater pathogen prevalence will be lighter for their height because of life history trade‐offs between investment in immune function and growth. Finally, we test whether population specific adult body mass predicts infant and child body mass, and whether this is independent of ecogeographical variables. Our results show that maximum monthly temperature explains 17% of children's weight for height while adult population‐level body mass explains ～44% (Table 5 ). The measures of pathogen prevalence explain little of the variation in children's body shape (8%; P > 0.05). Our results suggest that population differences are consistent with Bergmann's rule but parental body shape explains more variance. Moreover, these population‐level differences arise early in development, suggesting that any possible environmental influences occur in utero and/or result from epigenetic or population genetic differences. Am J Phys Anthropol 154:232–238, 2014. © 2014 Wiley Periodicals, Inc.     

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

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

Climate‐driven elevational variation in range sizes of vascular plants in the central Himalayas: A supporting case for Rapoport's rule

A fundamental yet controversial topic in biogeography is how and why species range sizes vary along spatial gradients. To advance our understanding of these questions and to provide insights into biological conservation, we assessed elevational variations in the range sizes of vascular plants with different life forms and biogeographical affinities and explored the main drivers underlying these variations in the longest valley in China''s Himalayas, the Gyirong Valley. Elevational range sizes of vascular plants were documented in 96 sampling plots along an elevational gradient ranging from 1,800 to 5,400 m above sea level. We assessed the elevational variations in range size by averaging the range sizes of all recorded species within each sampling plot. We then related the range size to climate, disturbance, and the mid‐domain effect and explored the relative importance of these factors in explaining the range size variations using the Random Forest model. A total of 545 vascular plants were recorded in the sampling plots along the elevational gradient. Of these, 158, 387, 337, and 112 were woody, herbaceous, temperate, and tropical species, respectively. The range size of each group of vascular plants exhibited uniform increasing trends along the elevational gradient, which was consistent with the prediction of Rapoport''s rule. Climate was the main driver of the increasing trends of vascular plant range sizes in the Gyirong Valley. The climate variability hypothesis and mean climate condition hypothesis could both explain the elevation–range size relationships. Our results reinforce the previous notion that Rapoport''s rule applies to regions where the influence of climate is the most pronounced, and call for close attention to the impact of climate change to prevent species range contraction and even extinction due to global warming.     

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.     

Geographic variation in body size: the effects of ambient temperature and precipitation

Latitudinal trends in body size have been explained as a response to temperature- or water-related factors, which are predictors of primary production. We used the first principal component calculated from three body parameters (weight, body length and the greatest length of the skull) of a sample of mammals from Israel and Sinai to determine those species that vary in size geographically, and whether such variation is related to annual rainfall, average minimum January temperature and average maximum August temperature. We used a conservative approach to discern the effects of precipitation and temperature by applying sequential regression. Variable priorities were assigned according to their bivariate correlation with body size, except for rainfall and its interactions that entered into the model last. Eleven species (Acomys cahirinus, Apodemus mystacinus, Canis lupus, Crocidura suaveolens, Gerbillus dasyurus, Hyaena hyaena, Lepus capensis, Meles meles, Meriones tristrami, Rousettus aegyptius and Vulpes vulpes) of the 17 species examined varied in size geographically. In five of them, rainfall was positively related to body size, while in one species it was negatively related to it. Contrary to the prediction of Bergmann’s rule, mean minimum January temperature was positively related to body size in five species and negatively related to body size in two species (C. suaveolens and G. dasyurus). As predicted by Bergmann’s rule, maximum June temperature was negatively related to body size in three species, and positively so in one (L. capensis). Primary production, particularly in desert and semi-desert areas, is determined mainly by precipitation. The above results indicate that, in our sample, primary production has an important effect on body size of several species of mammals. This is evident from the considerable proportion of the variability in body size explained by rain. However, low ambient temperatures may slow down and even inhibit photosynthesis. Hence, the observed positive relationships between average minimum January temperature and body size in four of the six species influenced by rain further support this conclusion.     

Environmental correlates of body size influence range size and extinction risk: A global study in rodents

Aim

Species-level traits, such as body and range sizes, are important correlates of extinction risk. However, both are often related and are driven by environmental factors. Here, we elucidated links between environmental factors, body size, range size and susceptibility to extinction, across the whole order of rodents.

Location

Global.

Time period

Current.

Major taxa studied

Rodents (order Rodentia).

Methods

We compiled an unprecedentedly large database of rodent morphology, phylogeny, range size, conservation status, global climate and normalized difference vegetation index (NDVI), comprising >86% of all described species. Using phylogenetic regressions, we initially explored the environmental factors driving body size. Next, we modelled the relationship between body size and range size. From this relationship, we computed and mapped (at the assemblage level) an index of relative range size, corresponding to the deviation from the expected range size of each species, given its body size. Finally, we tested whether relative range was correlated with the risk of extinction of the species derived from an assessment by the International Union for Conservation of Nature.

Results

We found that, contrary to the expectations of Bergmann's rule, the body size of rodents was mostly influenced by variation in NDVI (rather than latitude/temperature). Body size, in turn, imposed a constraint on species range size, as evidenced by a triangular relationship that was segmented at the lower bound. The relative species range size derived from this relationship highlighted four geographical regions where rodents with small relative range were concentrated globally. We demonstrated that lower relative range size was associated with increased risk of extinction.

Main conclusions

Species that, given their body size, are distributed across ranges that are smaller than expected have elevated extinction risk. Therefore, investigating the relationships between environmental drivers, body size and range size might help to detect species that could become threatened in the near future.