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.     

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.     

Gloger's rule in plants: The species and ecosystem levels

Gloger''s rule posits that darker birds are found more often in humid environments than in arid ones, especially in the tropics. Accordingly, desert-inhabiting animals tend to be light-colored. This rule is also true for certain mammalian groups, including humans. Gloger''s rule is manifested at 2 levels: (1) at the species level (different populations of the same species have different pigmentation at different latitudes), and (2) at the species assembly level (different taxa at a certain geography have different pigmentation than other taxa found at different habitats or latitudes). Concerning plants, Gloger''s rule was first proposed to operate in many plant species growing in sand dunes, sandy shores and in deserts, because of being white, whitish, or silver colored, based on white trichomes, because of sand grains and clay particles glued to sticky glandular trichomes, or because of light-colored waxes. Recently, Gloger''s rule was shown to also be true at the intraspecific level in relation to protection of anthers from UV irradiation. While Gloger''s rule is true in certain plant taxa and ecologies, there are others where “anti-Gloger” coloration patterns exist. In some of these the selective agents are known and in others they are not. I present both Gloger and “anti-Gloger” cases and argue that this largely neglected aspect of plant biology deserves much more research attention.     

Darker where cold and wet: Australian birds follow their own version of Gloger's rule

Gloger's rule is usually interpreted as predicting darker coloured animals in warmer and more humid/vegetated regions. The relative importance of temperature and rainfall or vegetation is however unclear, and often only one variable is tested at a time, mainly through proxies. Here, I assess the predictions of Gloger's rule for interspecific achromatic plumage variation (dark to light variation) for an entire avifauna (551 species of Australian landbirds). I tested the effects of climatic variables (temperature and rainfall) and vegetation structure on plumage reflectance at species and assemblage level (100 × 100 km cells), controlling for phylogenetic relatedness and spatial autocorrelation. To assess the robustness of these results I compared observed results with those of a null distribution of effects obtained from repeatedly simulating random plumage reflectance evolution on the phylogeny. At both the species and assemblage level, darker coloured birds were found in wetter and colder regions and in more densely vegetated habitats. Simulations confirm results at the species level and the effect of temperature at the assemblage level, but rainfall and vegetation effects at the assemblage level fall within the distribution of simulated effects and should be interpreted with care. Interspecific colour variation in Australian birds supports Gloger's rule for rainfall/vegetation, but shows the opposite pattern for temperature. Darker colours in wet and vegetated environments are consistent with the role of melanin pigmentation in preventing feather degradation by bacteria, but also with background‐matching for camouflage. Darker plumage might be beneficial in colder regions or detrimental in warmer regions if it affects thermoregulation, a selective force often only assumed to be of importance for ectotherms. The data highlight the need to test the generality of biogeographic rules across levels and at broad scale. Experimental work is needed to confirm the mechanisms linking plumage achromatic variation to climate.     

The dark side of coloration: Ecogeographical evidence supports Gloger's rule in American marsupials

Geographical distribution of color phenotypes and associations with ecological predictors remains poorly understood. An important geographic pattern concerning this topic is Gloger's rule, which predicts the increase of pigmentation in endothermic animals from cold and dry to warm and wet environments. Didelphid marsupials exhibit a variety of color patterns, ranging from light and dark uniform to more complex colorations. However, surprisingly little is known about the adaptive significance of dark coloration in this singular group of mammals. Using a phylogenetic comparative approach, we investigated whether coloration in different body regions of didelphids (i.e., dorsum and face) is associated with variables representing heat and humidity of the environment, as predicted by Gloger's rule. We demonstrated that Gloger's rule explains the interspecific color variation in American marsupials, especially when considering the facial region. Thus, dark coloration was more frequent among didelphid species occupying warm and wet environments than cold and dry environments. We also discuss the selective forces that can potentially explain coat color variation in didelphid marsupials, including camouflage, pathogen resistance, and pleiotropy hypotheses.     

Conformity to Bergmann's rule in birds depends on nest design and migration

Ecogeographical rules attempt to explain large‐scale spatial patterns in biological traits. One of the most enduring examples is Bergmann''s rule, which states that species should be larger in colder climates due to the thermoregulatory advantages of larger body size. Support for Bergmann''s rule, however, is not consistent across taxonomic groups, raising questions about what factors may moderate its effect. Behavior may play a crucial, yet so far underexplored, role in mediating the extent to which species are subject to environmental selection pressures in colder climates. Here, we tested the hypothesis that nest design and migration influence conformity to Bergmann''s rule in a phylogenetic comparative analysis of the birds of the Western Palearctic, a group encompassing dramatic variation in both climate and body mass. We predicted that migratory species and those with more protected nest designs would conform less to the rule than sedentary species and those with more exposed nests. We find that sedentary, but not short‐ or long‐distance migrating, species are larger in colder climates. Among sedentary species, conformity to Bergmann''s rule depends, further, on nest design: Species with open nests, in which parents and offspring are most exposed to adverse climatic conditions during breeding, conform most strongly to the rule. Our findings suggest that enclosed nests and migration enable small birds to breed in colder environments than their body size would otherwise allow. Therefore, we conclude that behavior can substantially modify species’ responses to environmental selection pressures.     

Adaptation of Pelage Color and Pigment Variations in Israeli Subterranean Blind Mole Rats,Spalax Ehrenbergi

Background

Concealing coloration in rodents is well established. However, only a few studies examined how soil color, pelage color, hair-melanin content, and genetics (i.e., the causal chain) synergize to configure it. This study investigates the causal chain of dorsal coloration in Israeli subterranean blind mole rats, Spalax ehrenbergi.

Methods

We examined pelage coloration of 128 adult animals from 11 populations belonging to four species of Spalax ehrenbergi superspecies (Spalax galili, Spalax golani, Spalax carmeli, and Spalax judaei) and the corresponding coloration of soil samples from the collection sites using a digital colorimeter. Additionally, we quantified hair-melanin contents of 67 animals using HPLC and sequenced the MC1R gene in 68 individuals from all four mole rat species.

Results

Due to high variability of soil colors, the correlation between soil and pelage color coordinates was weak and significant only between soil hue and pelage lightness. Multiple stepwise forward regression revealed that soil lightness was significantly associated with all pelage color variables. Pelage color lightness among the four species increased with the higher southward aridity in accordance to Gloger''s rule (darker in humid habitats and lighter in arid habitats). Darker and lighter pelage colors are associated with darker basalt and terra rossa, and lighter rendzina soils, respectively. Despite soil lightness varying significantly, pelage lightness and eumelanin converged among populations living in similar soil types. Partial sequencing of the MC1R gene identified three allelic variants, two of which were predominant in northern species (S. galili and S. golani), and the third was exclusive to southern species (S. carmeli and S. judaei), which might have caused the differences found in pheomelanin/eumelanin ratio.

Conclusion/Significance

Darker dorsal pelage in darker basalt and terra rossa soils in the north and lighter pelage in rendzina and loess soils in the south reflect the combined results of crypsis and thermoregulatory function following Gloger''s rule.     

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.     

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.     

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.     

What drives the evolution of body size in ectotherms? A global analysis across the amphibian tree of life

Aim

The emergence of large-scale patterns of animal body size is the central expectation of a wide range of (macro)ecological and evolutionary hypotheses. The drivers shaping these patterns include climate (e.g. Bergmann's rule), resource availability (e.g. ‘resource rule’), biogeographic settings and niche partitioning (e.g. adaptive radiation). However, these hypotheses often make opposing predictions about the trajectories of body size evolution. Therefore, whether underlying drivers of body size evolution can be identified remains an open question. Here, we employ the most comprehensive global dataset of body size in amphibians, to address multiple hypotheses that predict patterns of body size evolution based on climatic factors, ecology and biogeographic settings to identify underlying drivers and their generality across lineages.

Location

Global.

Time Period

Present.

Major Taxa Studied

Amphibians.

Methods

Using a global dataset spanning 7270 (>87% of) species of Anura, Caudata and Gymnophiona, we employed phylogenetic Bayesian modelling to test the roles of climate, resource availability, insularity, elevation, habitat use and diel activity on body size.

Results

Only climate and elevation drive body size patterns, and these processes are order-specific. Seasonality in precipitation and in temperature predict body size clines in anurans, whereas caecilian body size increases with aridity. However, neither of these drivers explained variation in salamander body size. In both anurans and caecilians, size increases with elevational range and with midpoint elevation in caecilians only. No effects of mean temperature, resource abundance, insularity, time of activity or habitat use were found.

Main Conclusions

Precipitation and temperature seasonality are the dominant climatic drivers of body size variation in amphibians overall. Bergmann's rule is consistently rejected, and so are other alternative hypotheses. We suggest that the rationale sustaining existing macroecological rules of body size is unrealistic in amphibians and discuss our findings in the context of the emerging hypothesis that climate change can drive body size shifts.     

Spatial patterns in the size of Chinese lizards are driven by multiple factors

BackgroundFor almost two centuries, ecologists have examined geographical patterns in the evolution of body size and the associated determinants. During that time, one of the most common patterns to have emerged is the increase in body size with increasing latitude (referred to as Bergmann''s rule). Typically, this pattern is explained in terms of an evolutionary response that serves to minimize heat loss in colder climates, mostly in endotherms. In contrast, however, this rule rarely explains geographical patterns in the evolution of body size among ectotherms (e.g., reptiles).LocationChina.AimIn this study, we assembled a dataset comprising the maximum sizes of 211 lizard species in China and examined the geographical patterns in body size evolution and its determinants. Specifically, we assessed the relationship between body size and climate among all lizard species and within four major groups at both assemblage and interspecific levels.ResultsAlthough we found that the body size of Chinese lizards was larger in warmer regions, we established that at the assemblage level, size was correlated with multiple climatic factors, and that body size–climate correlations differed within the four major groups. Phylogenetic analysis at the species level revealed that no single climatic factor was associated with body size, with the exception of agamids, for which size was found to be positively correlated with temperature.Main conclusionsGeographical patterns in Chinese lizard body size are driven by multiple factors, and overall patterns are probably influenced by those of the major groups. We suggest that our analyses at two different levels may have contributed to the inconsistent results obtained in this study. Further studies investigating the effects of altitude and ecological factors are needed to gain a more comprehensive understanding of the evolution of ectotherm body size.     

Range margin populations show high climate adaptation lags in European trees

How populations of long‐living species respond to climate change depends on phenotypic plasticity and local adaptation processes. Marginal populations are expected to have lags in adaptation (i.e. differences between the climatic optimum that maximizes population fitness and the local climate) because they receive pre‐adapted alleles from core populations preventing them from reaching a local optimum in their climatically marginal habitat. Yet, whether adaptation lags in marginal populations are a common feature across phylogenetically and ecologically different species and how lags can change with climate change remain unexplored. To test for range‐wide patterns of phenotypic variation and adaptation lags of populations to climate, we (a) built model ensembles of tree height accounting for the climate of population origin and the climate of the site for 706 populations monitored in 97 common garden experiments covering the range of six European forest tree species; (b) estimated populations' adaptation lags as the differences between the climatic optimum that maximizes tree height and the climate of the origin of each population; (c) identified adaptation lag patterns for populations coming from the warm/dry and cold/wet margins and from the distribution core of each species range. We found that (a) phenotypic variation is driven by either temperature or precipitation; (b) adaptation lags are consistently higher in climatic margin populations (cold/warm, dry/wet) than in core populations; (c) predictions for future warmer climates suggest adaptation lags would decrease in cold margin populations, slightly increasing tree height, while adaptation lags would increase in core and warm margin populations, sharply decreasing tree height. Our results suggest that warm margin populations are the most vulnerable to climate change, but understanding how these populations can cope with future climates depend on whether other fitness‐related traits could show similar adaptation lag patterns.     

Age and annual growth rate cause spatial variation in body size in Phrynocephalus przewalskii (Agamid)

Whether or not biogeographic rules dealing with spatial patterns of animal body sizes are valid for ectotherms is controversial. As the ectotherms grow all their lives, we explored the role of age and annual growth rate in body size variation in Phrynocephalus przewalskii in northern China. Morphological data were collected from 11 populations across a broad geographic gradient. Correlations between age, sex, climatic factors, and body size were analyzed using generalized linear model (GLM) and generalized linear mixed model (GLMM). GLM analysis indicated that the general body size of both sexes and the appendage size of females increased significantly with increasing temperature; however, the coefficient of determination was very small. GLMM analysis indicated that body size only correlated with age, whereas appendage size was affected by age, temperature, rainfall, and sunshine. Annual growth rates were positively correlated with temperature. We concluded that body size variation was mainly caused by age structure and plasticity of the growth rate in P. przewalskii and did not follow Bergmann''s rule; however, females followed Allen''s rule. Future studies to investigate the effect of energy restriction are needed to further understand the relationship between growth rate and body size. We also suggest that further studies on thermal advantage and sexual selection may be helpful to understand appendage size variation in P. przewalskii.     

A test of ecological and sexual selection hypotheses for geographical variation in coloration and morphology of golden-crowned kinglets (Regulus satrapa)

Aim To date, studies on geographical variation have extensively investigated Bergmann’s rule, yet Gloger’s rule remains infrequently tested, and climatic predictors of variation in carotenoid coloration have not yet been studied. In addition, hypotheses based on sexual selection, which predict that sexual dimorphism should vary with population density and climatic conditions, have received little attention. Our goals were to characterize geographical variation in the coloration and morphology of golden‐crowned kinglets, Regulus satrapa (Passeriformes, Regulidae), and to investigate possible ecological and sexual selection correlates of this variation. Location The entire species range of golden‐crowned kinglets, comprising North and Central America. Methods We collected data from 511 museum specimens, dating from 1847 to 2006, encompassing all five subspecies of golden‐crowned kinglets. We used reflectance spectrometry to quantify crown and mantle coloration, and measured wing‐chord and tarsus length to approximate body size. We obtained geographical and climatic data from online databases, and population density estimates from the literature. Results There were significant subspecific and gender differences in crown coloration and morphology: male kinglets were generally larger and more colourful. Our data revealed mixed support for Bergmann’s rule: tarsus length decreased with increasing latitude, while patterns of variation in wing‐chord and tarsus length showed conflicting results with temperature. Mantle coloration exhibited an opposite trend to that predicted by Gloger’s rule: upper parts became lighter with increasing relative humidity. Crown coloration was negatively correlated with actual evapotranspiration, suggesting that levels of primary productivity are not directly linked to carotenoid abundance. Sexual dimorphism and dichromatism generally increased with greater population density, lower latitudes and elevations, and warmer temperatures, supporting a previously observed pattern of variation in sexual dimorphism. Main conclusions Geographical variation in golden‐crowned kinglets yielded mixed support for Bergmann’s rule and contradicted Gloger’s rule, suggesting that other mechanisms may be operating. Allen’s rule is likely to be a stronger factor influencing tarsus length. Differences in the degree of sexual dimorphism and dichromatism in varying climatic conditions suggest that the intensity of sexual selection differs between habitats. Further studies on geographical variation in sexual dimorphism in various taxa may reveal a previously unrecognized ecogeographical rule.     

Transcriptomic analysis of skin pigmentation variation in the Virginia opossum (Didelphis virginiana)

Skin pigmentation and coat pigmentation are two of the best‐studied examples of traits under natural selection given their quantifiable fitness interactions with the environment (e.g., camouflage) and signalling with other organisms (e.g., warning coloration). Previous morphological studies have found that skin pigmentation variation in the Virginia opossum (Didelphis virginiana) is associated with variation in precipitation and temperatures across its distribution range following Gloger's rule (lighter pigmentation in temperate environments). To investigate the molecular mechanism associated with skin pigmentation variation, we used RNA‐Seq and quantified gene expression of wild opossums from tropical and temperate populations. Using differential expression analysis and a co‐expression network approach, we found that expression variation in genes with melanocytic and immune functions is significantly associated with the degree of skin pigmentation variation and may be underlying this phenotypic difference. We also found evidence suggesting that the Wnt/β‐catenin signalling pathway might be regulating the depigmentation observed in temperate populations. Based on our study results, we present several alternative hypotheses that may explain Gloger's rule pattern of skin pigmentation variation in opossum, including changes in pathogen diversity supporting a pathogen‐resistant hypothesis, thermal stress associated with temperate environments, and pleiotropic and epistatic interactions between melanocytic and immune genes.     

Interspecific pairwise relationships among body size, clutch size and latitude: deconstructing a macroecological triangle in birds

Aim Ecogeographical ‘rules’, large‐scale patterns in ecological variables across geographical space, can provide important insights into the mechanisms of evolution and ecological assembly. However, interactions between rules could obscure both the observation of large‐scale patterns and their interpretation. Here, we examine a system of three variables interrelated by ecogeographical rules – the latitudinal increase in body size within closely related homeotherms (Bergmann’s rule), the negative allometry of clutch size (Calder’s rule) and the latitudinal increase in clutch size (Lack’s rule) – in a global dataset of birds. Location Global. Methods We used linear regressions and meta‐analysis techniques to quantify the three rules across clades and through the taxonomic hierarchy. Path analysis was used to quantify interactions between rules at multiple taxonomic levels, as a function of both phylogenetic inheritance of traits and indirect feedbacks between the three rules. Independent contrasts analyses were performed on four clades with available phylogenies, and the taxonomic partitioning of variation in each trait was quantified. Results Standardizing across all clades, Lack’s and Bergmann’s rules were supported at all taxonomic levels, with Calder’s rule being supported at the order level. Lack’s rule was consistently stronger and more often detected than the other two rules. Path analysis showed that the indirect effects often outweighed the direct effects of Calder’s rule at the genus level and Bergmann’s rule at the order level. Strong interactions between Calder’s and Bergmann’s rules led to a trade‐off between the rules depending on taxonomic resolution. Main conclusions We found strong interactions between Bergmann’s, Lack’s and Calder’s rules in birds, and these interactions varied in strength and direction over the taxonomic hierarchy and among avian clades. Ecogeographical rules may be masked by feedbacks from other, correlated variables, even when the underlying selective mechanism is operating. The apparently conflicting pairwise relationships among clutch size, body size and latitude illustrate the difficulty of interpreting individual pairwise correlations without recognition of interdependence with other variables.     

Is Rapoport's rule a recent phenomenon? A deep time perspective on potential causal mechanisms

Macroecology strives to identify ecological patterns on broad spatial and temporal scales. One such pattern, Rapoport''s rule, describes the tendency of species'' latitudinal ranges to increase with increasing latitude. Several mechanisms have been proposed to explain this rule. Some invoke climate, either through glaciation driving differential extinction of northern species or through increased seasonal variability at higher latitudes causing higher thermal tolerances and subsequently larger ranges. Alternatively, continental tapering or higher interspecific competition at lower latitudes may be responsible. Assessing the incidence of Rapoport''s rule through deep time can help to distinguish between competing explanations. Using fossil occurrence data from the Palaeobiology Database, we test these hypotheses by evaluating mammalian compliance with the rule throughout the Caenozoic of North America. Adherence to Rapoport''s rule primarily coincides with periods of intense cooling and increased seasonality, suggesting that extinctions caused by changing climate may have played an important role in erecting the latitudinal gradients in range sizes seen today.     

Smaller beaks for colder winters: Thermoregulation drives beak size evolution in Australasian songbirds

Birds’ beaks play a key role in foraging, and most research on their size and shape has focused on this function. Recent findings suggest that beaks may also be important for thermoregulation, and this may drive morphological evolution as predicted by Allen's rule. However, the role of thermoregulation in the evolution of beak size across species remains largely unexplored. In particular, it remains unclear whether the need for retaining heat in the winter or dissipating heat in the summer plays the greater role in selection for beak size. Comparative studies are needed to evaluate the relative importance of these functions in beak size evolution. We addressed this question in a clade of birds exhibiting wide variation in their climatic niche: the Australasian honeyeaters and allies (Meliphagoidea). Across 158 species, we compared species’ climatic conditions extracted from their ranges to beak size measurements in a combined spatial‐phylogenetic framework. We found that winter minimum temperature was positively correlated with beak size, while summer maximum temperature was not. This suggests that while diet and foraging behavior may drive evolutionary changes in beak shape, changes in beak size can also be explained by the beak's role in thermoregulation, and winter heat retention in particular.     

What makes a long tail short? Testing Allen's rule in the toque macaques of Sri Lanka

Allen's rule (1877) predicts ecogeographical anatomical variation in appendage proportions as a function of body temperature regulation. This phenomenon has been tested in a variety of animal species. In macaques, relative tail length (RTL) is one of the most frequently measured appendages to test Allen's rule. These studies have relied on museum specimens or the invasive and time-consuming capturing of free-ranging individuals. To augment sample size and lessen these logistical limitations, we designed and validated a novel noninvasive technique using digitalized photographs processed using LibreCAD, an open-source 2D-computer-aided design (CAD) application. This was used to generate pixelated measurements to calculate an RTL equivalent, the Tail to Trunk Index (TTI) = (tail [tail base to anterior tip] pixel count/trunk [neck to tail base] pixel count). The TTI of 259 adult free-ranging toque macaques (Macaca sinica) from 36 locations between 7 and 2,087 m above sea level (m.a.s.l.) was used in the analysis. Samples were collected from all three putative subspecies (M. s. sinica, aurifrons, and opisthomelas), at locations representing all altitudinal climatic zones where they are naturally distributed. These data were used to test whether toque macaque tail length variation across elevation follows Allen's rule, predicting that RTL decreases with increasing elevation and lower temperature. Our results strongly supported this prediction. There was also a statistically significant, negative correlation between elevation and annual average temperature. The best predictor for the TTI index was elevation. Significant subspecies differences in RTL are linked in part to their ecological and altitudinal niche separation, but overall the variation is seen as the species' adaptation to climate. The method developed for the quick morphometric assessment of relative body proportions, applicable for use on unhabituated free-ranging animals, widens the range of materials available for research studying morphological characteristics and their evolution in primates.