Evolutionary and biogeographical implications of variation in skull morphology of raccoon dogs (Nyctereutes procyonoides,Mammalia: Carnivora)

Morphological characteristics reflect geographical variation resulting from adaptation to varying environmental conditions. Carnivore species distributed over a wide geographical range generally have highly polymorphic morphological variation. The raccoon dog (Nyctereutes procyonoides) has a longitudinal distribution restricted to East Asia and the northern Indochina Peninsula. Its unique geographical range makes it an appropriate model to examine how morphological differences are influenced by geography. To demonstrate morphological evolution of Russian, Chinese, Korean and Japanese raccoon dogs predicted by geographical differences, we tested the island rule and Bergmann's rule. We compared craniodental variation among populations and examined morphological implications for intraspecific taxonomic status. Insular raccoon dogs possessed substantially smaller body size than those from the mainland. Moreover, different island effects among Japanese islands were demonstrated by markedly larger occipital condyle breath in the Hokkaido population. Larger skull size in Russian and Hokkaido raccoon dogs could be explained by Bergmann's rule. Based on previous chromosomal and molecular studies and results of our morphological analyses, we suggest Japanese raccoon dogs are a distinct species from the mainland N. procyonoides.     

Ecological drivers of body size evolution and sexual size dimorphism in short‐horned grasshoppers (Orthoptera: Acrididae)

Sexual size dimorphism (SSD) is widespread and variable in nature. Although female‐biased SSD predominates among insects, the proximate ecological and evolutionary factors promoting this phenomenon remain largely unstudied. Here, we employ modern phylogenetic comparative methods on eight subfamilies of Iberian grasshoppers (85 species) to examine the validity of different models of evolution of body size and SSD and explore how they are shaped by a suite of ecological variables (habitat specialization, substrate use, altitude) and/or constrained by different evolutionary pressures (female fecundity, strength of sexual selection, length of the breeding season). Body size disparity primarily accumulated late in the history of the group and did not follow a Brownian motion pattern, indicating the existence of directional evolution for this trait. We found support for the converse of Rensch's rule (i.e. females are proportionally bigger than males in large species) across all taxa but not within the two most speciose subfamilies (Gomphocerinae and Oedipodinae), which showed an isometric pattern. Our results do not provide support for the fecundity or sexual selection hypotheses, and we did not find evidence for significant effects of habitat use. Contrary to that expected, we found that species with narrower reproductive window are less dimorphic in size than those that exhibit a longer breeding cycle, suggesting that male protandry cannot solely account for the evolution of female‐biased SSD in Orthoptera. Our study highlights the need to consider alternatives to the classical evolutionary hypotheses when trying to explain why in certain insect groups males remain small.     

Ecogeographical patterns of morphological variation in pygmy shrews Sorex minutus (Soricomorpha: Soricinae) within a phylogeographical and continental‐and‐island framework

Ecogeographical patterns of morphological variation were studied in the Eurasian pygmy shrew Sorex minutus aiming to understand the species’ morphological diversity in a continental and island setting, and within the context of previous detailed phylogeographical studies. In total, 568 mandibles and 377 skulls of S. minutus from continental and island populations from Europe and Atlantic islands were examined using a geometric morphometrics approach, and the general relationships of mandible and skull size and shape with geographical and environmental variables were studied. Samples were then pooled into predefined geographical groups to evaluate the morphological differences among them using analyses of variance, aiming to contrast the morphological and genetic relationships based on morphological and genetic distances and ancestral state reconstructions, as well as assess the correlations of morphological, genetic, and geographical distances with Mantel tests. We found significant relationships of mandible size with geographical and environmental variables, fitting the converse Bergmann's rule; however, for skull size, this was less evident. Continental groups of S. minutus could not readily be differentiated from each other by shape. Most island groups of S. minutus were easily discriminated from the continental groups by being larger, indicative of an island effect. Moreover, morphological and genetic distances differed substantially and, again, island groups were distinctive morphologically. Morphological and geographical distances were significantly correlated, although this was not the case for morphological and genetic distances, indicating that morphological variation does not reflect genetic subdivision in S. minutus. Our analyses showed that environmental variables and insularity had important effects on the morphological differentiation of S. minutus.     

Geographic variation of body size in New World anurans: energy and water in a balance

The validity of Bergmann's rule, perhaps the best known ecogeographical rule, has been questioned for ectothermic species. Here, we explore the interspecific version of the rule documenting body size gradients for anurans across the whole New World and evaluating which environmental variables best explain the observed patterns. We assembled a dataset of body sizes for 2761 anuran species of the Western Hemisphere and conducted assemblage‐based and cross‐species analyses that consider the spatial and phylogenetic structure in the data. In accordance with heat and water‐related explanations for body size clines, we found a consistent association of median body size and potential evapotranspiration across the New World. A relevant role of water availability also emerges, suggesting the joint importance of body size for thermoregulation and hydroregulation in anurans. Anurans do not follow a simple Bergmannian pattern of increasing size towards high latitudes. Consistent with previous regional findings, our Hemisphere‐wide analyses detect that the geographic variation in anuran body sizes is highly dependent on a trade‐off between heat and water balance. The observed size‐climate relationships possibly emerge from the interplay between thermoregulatory abilities and the benefits inherent to reduced surface‐to‐volume ratios in larger species, which decrease the rates of evaporative water loss and favour heat retention. Our results also show how temperature becomes important for species that are directly in contact with the substrate and water, like burrowing and terrestrial anurans, while arboreal species exhibit a body size cline linked with potential evapotranspiration.     

Ecogeographical variation of body size in the newt Triturus carnifex: comparing the hypotheses using an information‐theoretic approach

Aim Ecogeographical variation of body size in vertebrates (e.g. Bergmann's rule) has long been recognized. However, the patterns and causes of intra‐specific ecogeographical variation of body size in ectotherms, and in amphibians in particular, are strongly debated. We identified the relationship between bioclimatic variables and body size predicted a priori by alternative hypotheses (heat balance, endurance, seasonality, starvation resistance, water availability, primary productivity, parental investment) proposed to explain ecogeographical patterns of body size in ectotherms, and we evaluated the relative support of these hypotheses in explaining variation in body size of the Italian crested newt, Triturus carnifex. Location Twenty‐three populations covering the whole range of T. carnifex (Austria, Croatia, Italy and Slovenia). Methods We obtained data on body size (snout–vent length, SVL) of 2639 adult newts from direct measurements and the literature; we obtained high‐resolution environmental data for the sampled localities. We used an information‐theoretic approach to evaluate the support of the data for the different hypotheses. We also integrated information on population genetics in our models. Results We observed strong geographical variation of body size. The best Akaike information criterion (AIC) models showed that populations with larger body size are associated with cold climates and secondarily with high primary productivity. Furthermore, sexual dimorphism increases in cold climates, as the increase in body size was stronger for females. When taking into account population genetics, we did not find support for relationships with the other variables. Main conclusion Our results are consistent with three hypotheses proposed to explain ecogeographical variation in amphibians: heat balance, increased parental investment of females and productivity. Information theory provides the framework for comparing hypotheses rather than looking for patterns. We suggest that evaluating the support for mechanisms can provide better insights than simply assessing whether ecogeographical variation is in agreement with some ‘rule’.     

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.     

Biogeography of body size in terrestrial isopods (Crustacea: Oniscidea)

This study tries to unveil the contribution of climatic shift in shaping the extreme body size diversity in terrestrial isopods (Oniscidea). Trying to explain size variation at an interspecific level, we test five hypotheses: (1) Bergmann's Rule and the temperature‐size rule postulate large size in cold areas; (2) The metabolic cold adaptation theory postulates small animal sizes in cold environments; (3) The primary productivity hypothesis predicts size increase in resource‐rich areas; (4) The aridity resistance hypothesis predicts large size in arid regions; and (5). The acidosis hypothesis predicts smaller size with decreasing soil pH. Globally, Bergmann's rule and the aridity hypothesis are weakly supported. Among families and genera, results are variable and idiosyncratic. Conglobating species sizes provide weak support for the acidosis hypothesis. Overall, size is strongly affected by familial affiliation. Isopod size evolution seems to be mainly affected by phylogenetically constrained life‐history traits.     

Seasonal variations in body melanism and size of the wolf spider Pardosa astrigera (Araneae: Lycosidae)

Variations in species morphology and life‐history traits strongly correlate with geographic and climatic characteristics. Most studies on morphological variations in animals focus on ectotherms distributed on a large geographic scale across latitudinal and/or altitudinal gradient. However, the morphological variations of spiders living in the same habitats across different seasons have not been reported. In this study, we used the wolf spider, Pardosa astrigera, as a model to determine seasonal differences in adult body size, melanism, fecundity, and egg diameter both in the overwintering and the first generation for 2010 and 2016. The results showed that in 2010, both females and males of the overwintering generation were significantly darker than the first generation. Moreover, the overwintering females were markedly larger and produced more and bigger eggs than the first generation in both 2010 and 2016. Considering the overwintering P. astrigera experiencing low temperature and/or desiccation stress, these results suggest that substantially darker and larger body of the overwintering generation is adaptive to adverse conditions.     

Unveiling the environmental drivers of intraspecific body size variation in terrestrial vertebrates

Aim

Whether intraspecific spatial patterns in body size are generalizable across species remains contentious, as well as the mechanisms underlying these patterns. Here we test several hypotheses explaining within-species body size variation in terrestrial vertebrates including the heat balance, seasonality, resource availability and water conservation hypotheses for ectotherms, and the heat conservation, heat dissipation, starvation resistance and resource availability hypotheses for endotherms.

Location

Global.

Time period

1970–2016.

Major taxa studied

Amphibians, reptiles, birds and mammals.

Methods

We collected 235,905 body size records for 2,229 species (amphibians = 36; reptiles = 81; birds = 1,545; mammals = 567) and performed a phylogenetic meta-analysis of intraspecific correlations between body size and environmental variables. We further tested whether correlations differ between migratory and non-migratory bird and mammal species, and between thermoregulating and thermoconforming ectotherms.

Results

For bird species, smaller intraspecific body size was associated with higher mean and maximum temperatures and lower resource seasonality. Size–environment relationships followed a similar pattern in resident and migratory birds, but the effect of resource availability on body size was slightly positive only for non-migratory birds. For mammals, we found that intraspecific body size was smaller with lower resource availability and seasonality, with this pattern being more evident in sedentary than migratory species. No clear size–environment relationships were found for reptiles and amphibians.

Main conclusions

Within-species body size variation across endotherms is explained by disparate underlying mechanisms for birds and mammals. Heat conservation (Bergmann's rule) and heat dissipation are the dominant processes explaining biogeographic intraspecific body size variation in birds, whereas in mammals, body size clines are mostly explained by the starvation resistance and resource availability hypotheses. Our findings contribute to a better understanding of the mechanisms behind species adaptations to the environment across their geographic distributions.     

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.     

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.     

Length of activity season drives geographic variation in body size of a widely distributed lizard

Understanding the factors that drive geographic variation in life history is an important challenge in evolutionary ecology. Here, we analyze what predicts geographic variation in life‐history traits of the common lizard, Zootoca vivipara, which has the globally largest distribution range of all terrestrial reptile species. Variation in body size was predicted by differences in the length of activity season, while we found no effects of environmental temperature per se. Females experiencing relatively short activity season mature at a larger size and remain larger on average than females in populations with relatively long activity seasons. Interpopulation variation in fecundity was largely explained by mean body size of females and reproductive mode, with viviparous populations having larger clutch size than oviparous populations. Finally, body size‐fecundity relationship differs between viviparous and oviparous populations, with relatively lower reproductive investment for a given body size in oviparous populations. While the phylogenetic signal was weak overall, the patterns of variation showed spatial effects, perhaps reflecting genetic divergence or geographic variation in additional biotic and abiotic factors. Our findings emphasize that time constraints imposed by the environment rather than ambient temperature play a major role in shaping life histories in the common lizard. This might be attributed to the fact that lizards can attain their preferred body temperature via behavioral thermoregulation across different thermal environments. Length of activity season, defining the maximum time available for lizards to maintain optimal performance, is thus the main environmental factor constraining growth rate and annual rates of mortality. Our results suggest that this factor may partly explain variation in the extent to which different taxa follow ecogeographic rules.     

Variation in body size and sexual size dimorphism in the most widely ranging lizard: testing the effects of reproductive mode and climate

Reproductive mode, ancestry, and climate are hypothesized to determine body size variation in reptiles but their effects have rarely been estimated simultaneously, especially at the intraspecific level. The common lizard (Zootoca vivipara) occupies almost the entire Northern Eurasia and includes viviparous and oviparous lineages, thus representing an excellent model for such studies. Using body length data for >10,000 individuals from 72 geographically distinct populations over the species' range, we analyzed how sex‐specific adult body size and sexual size dimorphism (SSD) is associated with reproductive mode, lineage identity, and several climatic variables. Variation in male size was low and poorly explained by our predictors. In contrast, female size and SSD varied considerably, demonstrating significant effects of reproductive mode and particularly seasonality. Populations of the western oviparous lineage (northern Spain, south‐western France) exhibited a smaller female size and less female‐biased SSD than those of the western viviparous (France to Eastern Europe) and the eastern viviparous (Eastern Europe to Far East) lineages; this pattern persisted even after controlling for climatic effects. The phenotypic response to seasonality was complex: across the lineages, as well as within the eastern viviparous lineage, female size and SSD increase with increasing seasonality, whereas the western viviparous lineage followed the opposing trends. Altogether, viviparous populations seem to follow a saw‐tooth geographic cline, which might reflect the nonmonotonic relationship of body size at maturity in females with the length of activity season. This relationship is predicted to arise in perennial ectotherms as a response to environmental constraints caused by seasonality of growth and reproduction. The SSD allometry followed the converse of Rensch's rule, a rare pattern for amniotes. Our results provide the first evidence of opposing body size—climate relationships in intraspecific units.     

Higher temperatures during development reduce body size in the zebra finch in the laboratory and in the wild

The most commonly documented morphological response across many taxa to climatic variation across their range follows Bergmann's rule, which predicts larger body size in colder climates. In observational data from wild zebra finches breeding across a range of temperatures in the spring and summer, we show that this relationship appears to be driven by the negative effect of high temperatures during development. This idea was then experimentally tested on zebra finches breeding in temperature‐controlled climates in the laboratory. These experiments confirmed that those individualso produced in a hot environment (30 °C) were smaller than those produced in cool conditions (18 °C). Our results suggest a proximate causal link between temperature and body size and suggest that a hotter climate during breeding periods could drive significant changes in morphology within and between populations. This effect could account for much of the variation in body size that drives the well‐observed patterns first described by Bergmann and that is still largely attributed to selection on adult body size during cold winters. The climate‐dependent developmental plasticity that we have demonstrated is an important component in understanding how endotherms may be affected by climate change.     

Geographical variation in morphology and its environmental correlates in a widespread North American lizard,Anolis carolinensis (Squamata: Dactyloidae)

The green anole, Anolis carolinensis, has long been an important model organism for studies of physiology and behaviour, and recently became the first reptile to have its genome sequenced. With a large and environmentally heterogeneous distribution, especially in relation to well‐studied Antillean relatives, A. carolinensis is also emerging as an important organism for novel studies of geographical differentiation and adaptation. In the present study, we quantify the degree of morphological variation in this species and test for environmental correlates of this variation. We also examine adherence to Bergmann's and Allen's rule, two eco‐geographical principles that have been well studied over large species ranges. We sampled from 14 populations across the distribution of the species in North America and measured 28 distinct morphological traits. We also collected a suite of environmental variables for each site, including those related to temperature, precipitation, and vegetation. Ultimately, we found a large degree of geographical variation in morphology, with head traits contributing the most to differences among populations. Morphological variation was correlated with variation in temperature, precipitation, and latitude across sites. We found no support for reverse Bergmann's rule typical of squamates, although we did find a trend of reverse Allen's rule. Ultimately, the present study provides a novel look at A. carolinensis and establishes it as a strong candidate for further studies of variation and adaptation over a large range.     

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.