Rule reversal: Ecogeographical patterns of body size variation in the common treeshrew (Mammalia,Scandentia)

There are a number of ecogeographical “rules” that describe patterns of geographical variation among organisms. The island rule predicts that populations of larger mammals on islands evolve smaller mean body size than their mainland counterparts, whereas smaller‐bodied mammals evolve larger size. Bergmann's rule predicts that populations of a species in colder climates (generally at higher latitudes) have larger mean body sizes than conspecifics in warmer climates (at lower latitudes). These two rules are rarely tested together and neither has been rigorously tested in treeshrews, a clade of small‐bodied mammals in their own order (Scandentia) broadly distributed in mainland Southeast Asia and on islands throughout much of the Sunda Shelf. The common treeshrew, Tupaia glis, is an excellent candidate for study and was used to test these two rules simultaneously for the first time in treeshrews. This species is distributed on the Malay Peninsula and several offshore islands east, west, and south of the mainland. Using craniodental dimensions as a proxy for body size, we investigated how island size, distance from the mainland, and maximum sea depth between the mainland and the islands relate to body size of 13 insular T. glis populations while also controlling for latitude and correlation among variables. We found a strong negative effect of latitude on body size in the common treeshrew, indicating the inverse of Bergmann's rule. We did not detect any overall difference in body size between the island and mainland populations. However, there was an effect of island area and maximum sea depth on body size among island populations. Although there is a strong latitudinal effect on body size, neither Bergmann's rule nor the island rule applies to the common treeshrew. The results of our analyses demonstrate the necessity of assessing multiple variables simultaneously in studies of ecogeographical rules.     

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.     

Body proportions of circumpolar peoples as evidenced from skeletal data: Ipiutak and Tigara (Point Hope) versus Kodiak Island Inuit

Given the well‐documented fact that human body proportions covary with climate (presumably due to the action of selection), one would expect that the Ipiutak and Tigara Inuit samples from Point Hope, Alaska, would be characterized by an extremely cold‐adapted body shape. Comparison of the Point Hope Inuit samples to a large (n > 900) sample of European and European‐derived, African and African‐derived, and Native American skeletons (including Koniag Inuit from Kodiak Island, Alaska) confirms that the Point Hope Inuit evince a cold‐adapted body form, but analyses also reveal some unexpected results. For example, one might suspect that the Point Hope samples would show a more cold‐adapted body form than the Koniag, given their more extreme environment, but this is not the case. Additionally, univariate analyses seldom show the Inuit samples to be more cold‐adapted in body shape than Europeans, and multivariate cluster analyses that include a myriad of body shape variables such as femoral head diameter, bi‐iliac breadth, and limb segment lengths fail to effectively separate the Inuit samples from Europeans. In fact, in terms of body shape, the European and the Inuit samples tend to be cold‐adapted and tend to be separated in multivariate space from the more tropically adapted Africans, especially those groups from south of the Sahara. Am J Phys Anthropol, 2010. © 2009 Wiley‐Liss, Inc.     

Reproductive seasonality in captive wild ruminants: implications for biogeographical adaptation,photoperiodic control,and life history

Many ruminant species show seasonal patterns of reproduction. Causes for this are widely debated, and include adaptations to seasonal availability of resources (with cues either from body condition in more tropical, or from photoperiodism in higher latitude habitats) and/or defence strategies against predators. Conclusions so far are limited to datasets with less than 30 species. Here, we use a dataset on 110 wild ruminant species kept in captivity in temperate‐zone zoos to describe their reproductive patterns quantitatively [determining the birth peak breadth (BPB) as the number of days in which 80% of all births occur]; then we link this pattern to various biological characteristics [latitude of origin, mother‐young‐relationship (hider/follower), proportion of grass in the natural diet (grazer/browser), sexual size dimorphism/mating system], and compare it with reports for free‐ranging animals. When comparing taxonomic subgroups, variance in BPB is highly correlated to the minimum, but not the maximum BPB, suggesting that a high BPB (i.e. an aseasonal reproductive pattern) is the plesiomorphic character in ruminants. Globally, latitude of natural origin is highly correlated to the BPB observed in captivity, supporting an overruling impact of photoperiodism on ruminant reproduction. Feeding type has no additional influence; the hider/follower dichotomy, associated with the anti‐predator strategy of ‘swamping’, has additional influence in the subset of African species only. Sexual size dimorphism and mating system are marginally associated with the BPB, potentially indicating a facilitation of polygamy under seasonal conditions. The difference in the calculated Julian date of conception between captive populations and that reported for free‐ranging ones corresponds to the one expected if absolute day length was the main trigger in highly seasonal species: calculated day length at the time of conception between free‐ranging and captive populations followed a y = x relationship. Only 11 species (all originating from lower latitudes) were considered to change their reproductive pattern distinctively between the wild and captivity, with 10 becoming less seasonal (but not aseasonal) in human care, indicating that seasonality observed in the wild was partly resource‐associated. Only one species (Antidorcas marsupialis) became more seasonal in captivity, presumably because resource availability in the wild overrules the innate photoperiodic response. Reproductive seasonality explains additional variance in the body mass–gestation period relationship, with more seasonal species having shorter gestation periods for their body size. We conclude that photoperiodism, and in particular absolute day length, are genetically fixed triggers for reproduction that may be malleable to some extent by body condition, and that plasticity in gestation length is an important facilitator that may partly explain the success of ruminant radiation to high latitudes. Evidence for an anti‐predator strategy involving seasonal reproduction is limited to African species. Reproductive seasonality following rainfall patterns may not be an adaptation to give birth in periods of high resource availability but an adaptation to allow conception only at times of good body condition.     

Parabolic variation in sexual selection intensity across the range of a cold‐water pipefish: implications for susceptibility to climate change

While an understanding of evolutionary processes in shifting environments is vital in the context of rapid ecological change, one of the most potent selective forces, sexual selection, remains curiously unexplored. Variation in sexual selection across a species range, especially across a gradient of temperature regimes, has the potential to provide a window into the possible impacts of climate change on the evolution of mating patterns. Here, we investigated some of the links between temperature and indicators of sexual selection, using a cold‐water pipefish as model. We found that populations differed with respect to body size, length of the breeding season, fecundity, and sexual dimorphism across a wide latitudinal gradient. We encountered two types of latitudinal patterns, either linear, when related to body size, or parabolic in shape when considering variables related to sexual selection intensity, such as sexual dimorphism and reproductive investment. Our results suggest that sexual selection intensity increases toward both edges of the distribution and that the large differences in temperature likely play a significant role. Shorter breeding seasons in the north and reduced periods for gamete production in the south certainly have the potential to alter mating systems, breeding synchrony, and mate monopolization rates. As latitude and water temperature are tightly coupled across the European coasts, the observed patterns in traits related to sexual selection can lead to predictions regarding how sexual selection should change in response to climate change. Based on data from extant populations, we can predict that as the worm pipefish moves northward, a wave of decreasing selection intensity will likely replace the strong sexual selection at the northern range margin. In contrast, the southern populations will be followed by heightened sexual selection, which may exacerbate the problem of local extinction at this retreating boundary.     

Helminths of red foxes (Vulpes vulpes) and raccoon dogs (Nyctereutes procyonoides) in Lithuania

Red foxes and raccoon dogs are hosts for a wide range of parasites including important zoonotic helminths. The raccoon dog has recently invaded into Europe from the east. The contribution of this exotic species to the epidemiology of parasitic diseases, particularly parasitic zoonoses is unknown. The helminth fauna and the abundance of helminth infections were determined in 310 carcasses of hunted red foxes and 99 of raccoon dogs from Lithuania. Both species were highly infected with Alaria alata (94·8% and 96·5% respectively) and Trichinella spp. (46·6% and 29·3%). High and significantly different prevalences in foxes and raccoon dogs were found for Eucoleus aerophilus (97·1% and 30·2% respectively), Crenosoma vulpis (53·8% and 15·1%), Capillaria plica (93·3% and 11·3%), C. putorii (29·4% and 51·5%), Toxocara canis (40·5% and 17·6%) and Uncinaria stenocephala (76·9% and 98·8%). The prevalences of the rodent-transmitted cestodes Echinococcus multilocularis, Taenia polyacantha, T. crassiceps and Mesocestoides spp. were significantly higher in foxes than in raccoon dogs. The abundances of E. multilocularis, Mesocestoides, Taenia, C. plica and E. aerophilus were higher in foxes than those in raccoon dogs. A. alata, U. stenocephala, C. putorii and Echinostomatidae had higher abundances in raccoon dogs. The difference in prevalence and abundance of helminths in both animals may reflect differences in host ecology and susceptibility. The data are consistent with red foxes playing a more important role than raccoon dogs in the transmission of E. multilocularis in Lithuania.     

Alaria alata (Digenea: Diplostomidae) from Korean Raccoon Dog,Nyctereutes procyonoides koreensis,in Korea

We report a species of diplostomid fluke recovered from 3 carcasses of wild Korean raccoon dog, Nyctereutes procyonoides koreensis, in Korea. A total of 107 diplostomid flukes were recovered from the small intestines of Korean raccoon dogs, which were obtained from the Gangwon Wildlife Medical Rescue Center. Worms fixed with 10% neutral formalin were subjected to microscopic observation and those fixed in 70% ethanol were used for molecular genomic analysis. The worm was divided into 2 separate parts, forebody and hindbody, with a total length of 3,020–4,090 (3,855) μm and a width of 1,210–1,770 (1,562) μm. The boat-shaped forebody has a pair of characteristic tentacular appendage, 2 suckers, holdfast organ, and vitelline follicles. The oval to cylindrical hindbody has reproductive organs. The ovary was round or elliptical and located in the anterior of the testes. Two large testes were slightly segmented and tandemly arranged, occupying almost half of hindbody. The short uterus contained a relatively small number of unembryonated eggs sized 130–140×85–96 μm. The partial sequence of 18S rRNA of this fluke was consistent with Alaria alata. Based on the morphological and molecular characteristics, the diplostomid flukes recovered from the small intestine of Korean raccoon dogs were identified as A. alata (Digenea: Diplostomidae).     

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.     

Cope's rule and the evolution of body size in Pinnipedimorpha (Mammalia: Carnivora)

Cope's rule describes the evolutionary trend for animal lineages to increase in body size over time. In this study, we tested the validity of Cope's rule for a marine mammal clade, the Pinnipedimorpha, which includes the extinct Desmatophocidae, and extant Phocidae (earless seals), Otariidae (fur seals and sea lions), and Odobenidae (walruses). We tested for the presence of Cope's rule by compiling a large dataset of body size data for extant and fossil pinnipeds and then examined how body size evolved through time. We found that there was a positive relationship between geologic age and body size. However, this trend is the result of differences between early assemblages of small-bodied pinnipeds (Oligocene to early Miocene) and later assemblages (middle Miocene to Pliocene) for which species exhibited greater size diversity. No significant differences were found between the number of increases or decreases in body size within Pinnipedimorpha or within specific pinniped clades. This suggests that the pinniped body size increase was driven by passive diversification into vacant niche space, with the common ancestor of Pinnipedimorpha occurring near the minimum adult body size possible for a marine mammal. Based upon the above results, the evolutionary history of pinnipeds does not follow Cope's rule.     

Hematology and serum biochemistry in debilitated, free-ranging raccoon dogs (Nyctereutes procyonoides) infested with sarcoptic mange

Frequent outbreaks of Sarcoptes scabiei infestation in raccoon dogs (Nyctereutes procyonoides) have been reported in Japan. Although many raccoon dogs are brought to Kanazawa Zoological Garden (Yokohama, Kanagawa, Japan) because of S. scabiei infestation and debilitation, some of them die of asthenia. The clinical status of severely debilitated raccoon dogs must be determined to save their lives. In this study, we compared hematological and serum biochemical values between severely debilitated and nondebilitated raccoon dogs infested with S. scabiei. The total protein, albumin, glucose, and calcium values of debilitated raccoon dogs were significantly lower than those of nondebilitated raccoon dogs. On the other hand, debilitated raccoon dogs had significantly higher aspartate aminotransferase, total bilirubin, blood urea nitrogen, sodium, chloride, and phosphorus values than did nondebilitated raccoon dogs. The increase in the blood urea nitrogen value was particularly dramatic. The present study revealed that debilitated raccoon dogs infested with S. scabiei exhibited abnormal hematological values compared with nondebilitated raccoon dogs infested with S. scabiei. Clinically, the raccoon dogs developed malnutrition and sepsis if the mange infestation was untreated. Moreover, dehydration associated with appetite loss may have resulted in insufficient renal perfusion. These findings suggest that chronic S. scabiei infestations debilitated the raccoon dogs and resulted in physiological changes that were detected with hematological and serum biochemical tests.     

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.     

Intraspecific variation in the skull morphology of the black caiman Melanosuchus niger (Alligatoridae,Caimaninae)

Melanosuchus niger is a caimanine alligatorid widely distributed in the northern region of South America. This species has been the focus of several ecological, genetic and morphological studies. However, morphological studies have generally been limited to examination of interspecific variation among extant species of South American crocodylians. Here, we present the first study of intraspecific variation in the skull of M. niger using a two‐dimensional geometric morphometric approach. The crania of 52 sexed individuals varying in size were analysed to quantify shape variation and to assign observed shape changes to different types of intraspecific variation, that is, ontogenetic variation and sexual dimorphism. Most of the variation in this species is ontogenetic variation in snout length, skull depth, orbit size and the width of the postorbital region. These changes are correlated with bite force performance and probably dietary changes. However, a comparison with previous functional studies reveals that functional adaptations during ontogeny seem to be primarily restricted to the postrostral region, whereas rostral shape changes are more related to dietary shifts. Furthermore, the skulls of M. niger exhibit a sexual dimorphism, which is primarily size‐related. The presence of non‐size‐related sexual dimorphism has to be tested in future examinations.     

Euryhelmis squamula (Digenea: Heterophyidae) Recovered from Korean Raccoon Dog,Nyctereutes procyonoides koreensis,in Korea

In this study, we intended to describe an unrecorded species of heterophyid trematode recovered from the small intestine of a Korean raccoon dog, Nyctereutes procyonoides koreensis, in Korea. A total of 13 small flukes were collected from a deceased Korean raccoon dog which was found in Chuncheon-si, Gangwon-do, Korea in May 2017. The trematode body were covered with many small spines, rectangular, broader than long, 807–1,103 μm long and 1,270–1,550 μm wide. Oral sucker in the anterior end slightly smaller than acetabulum. Pharynx muscular and well developed. Esophagus relatively long and sigmoid. Acetabulum small and located at median in anterior 2/5 portion. Ceca bifurcated at the anterior of genital pore and acetabulum and terminated at testis level. Testes larger, deeply lobed and located at the near of posterior end of body. Ovary small, triangular and located at the slight left of median and the anterior of left testis. Vitelline follicles dendritic and extend from the middle level of esophagus to the posterior portion of body. Eggs embryonated, operculated, small and 33–35×15–16 μm in size. Based on the morphological characteristics, the small heterophyid flukes recovered from the small intestines of Korean raccoon dog, N. procyonoides koreensis, were identified as Euryhelmis squamula (Digenea: Heterophyidae). Accordingly, this species of heterophyid flukes is to be a new trematode fauna in Korea by this study.     

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.     

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.     

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.     

Overwintering strategy of wild free-ranging and enclosure-housed Japanese raccoon dogs (<Emphasis Type="Italic">Nyctereutes procyonoides albus</Emphasis>)

The raccoon dog, Nyctereutes procyonoides, is a canid with a passive overwintering strategy in northern Europe. However, the behaviour and physiology of the Japanese subspecies, N. p. albus, which has fewer chromosomes than the other subspecies, remain unknown. We measured body temperature, body composition and blood biochemistry of wild free-ranging and fasted enclosure-housed N. p. albus during boreal winter in Hokkaido, Japan. Body temperature of N. p. albus decreased from 38°C in autumn to 35.9–36.7°C while maintaining a circadian rhythm in late February (n = 3). A transient 18–36% decrease in resting heart rate occurred when body temperature was low (n = 2). Despite a 33–45% decrease in body weight due to winter fasting, circulating glucose, total protein and triglyceride levels were maintained (n = 4). Serum urea nitrogen dropped by 43–45% from autumn to spring, suggesting protein conservation during fasting. The overwintering survival strategy of N. p. albus in central Hokkaido is based upon large changes in seasonal activity patterns, winter denning and communal housing without the large decrease in body temperature that is characteristic of subarctic animals exhibiting hibernation or torpor. Naoya Kitao, Daisuke Fukui and Peter G. Osborne contributed equally to this work