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

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

Bergmann's rule in larval ant lions: testing the starvation resistance hypothesis

Abstract.  1. Body size of the ant lion Myrmeleon immaculatus follows Bergmann's rule – an increase in body size towards higher latitudes. The hypothesis that ant lion body size is larger in the north as an adaptation for starvation resistance was tested.
2. In a laboratory experiment testing starvation resistance, survivorship curves differed among 10 ant lion populations for both a starved and a fed treatment.
3. The average number of months survived by each population was correlated positively with latitude for both treatments. Across both treatments and all populations, large individuals survived longer than small individuals; however individuals from high latitudes had higher survivorship, even after factoring out variation due to initial body size.
4. These results suggest that starvation resistance may be an adaptation for coping with reduced prey availability in high latitudes. Starvation resistance may contribute to latitudinal gradients in body size of ant lions and other ectotherms.     

Patterns of within-species body size variation of birds: strong evidence for Bergmann's rule

Aim The aim of this study is to test whether Bergmann's rule, a general intraspecific tendency towards larger body size in cooler areas and at higher latitudes, holds for birds throughout the world. Location This study includes information on species of birds from throughout the world. Methods I gathered data on body size variation from the literature and used two general meta‐analytical procedures to test the validity of Bergmann's rule in birds: a modified vote‐counting approach and calculation of overall effect sizes. Related species may show similar body size trends, thus I performed all analyses using nonphylogenetic and phylogenetic methods. I used tests of phylogenetic signal for each data set to decide which type of statistical analysis (nonphylogenetic or phylogenetic) was more appropriate. Results The majority of species of birds (76 of 100 species) are larger at higher latitudes, and in cooler areas (20 of 22 species). Birds show a grand mean correlation coefficient of +0.32 for body size and latitude, and ?0.81 for body size and temperature, both significant trends. Sedentary species show stronger body size trends in some, but not all, analyses. Neither males nor females consistently have stronger body size trends. Additionally, the strength of body size trends does not vary with latitude or body mass. Conclusions Bergmann's rule holds for birds throughout the world, regardless of whether temperature or latitude (as a proxy) is used. Previous studies have suggested that Bergmann's rule is stronger for sedentary than migratory species, males than females and temperate than tropical taxa. I did not find strong support for any of these as general themes for birds, although few studies of tropical taxa have been conducted. The processes responsible for Bergmann's rule remain somewhat of a black box; however, fasting endurance is probably a more important factor than the traditional hypothesis of heat conservation.     

Multiple selection pressures generate adherence to Bergmann's rule in a Neotropical migratory songbird

Aim Bergmann's rule, the tendency for body size to be positively correlated with latitude, is widely accepted but the mechanisms behind the patterns are still debated. Bergmann's originally conceived mechanism was based on heat conservation; other proposed mechanisms invoke phylogeny, migration distance and resource seasonality. With the goal of examining these mechanisms, we quantified morphological variation across the breeding range of a Neotropical migratory songbird, the cerulean warbler (Dendroica cerulea). Location Deciduous forests of eastern North America. Methods We sampled nine cerulean warbler populations, spanning the species’ breeding range. We captured 156 males using targeted playback and model presentation, and included 127 adult males in our analyses of morphological variation. We used an information‐theoretical approach to identify climatic variables associated with geographical variation in body size. Results Cerulean warbler body size adheres to Bergmann's rule: individuals in northern populations are larger than those in southern populations. Variation in body size is best explained by variation in dry and wet‐bulb temperature and actual evapotranspiration. Main conclusions Adherence to Bergmann's rule by the cerulean warbler appears to be linked to thermodynamics (heat conservation in the north, evaporative cooling in the south) and resource seasonality. Multiple selection pressures can interact to generate a single axis of morphological geographical variation, and even subtle fluctuations in climatic variables can exert significant selection pressures. We suggest that the influence of selection pressures on migrants might be enhanced by migratory connectivity, providing further support for the important role played by this phenomenon in the ecology, evolution and population dynamics of migratory songbirds.     

Bergmann's rule in the ant lion Myrmeleon immaculatus DeGeer (Neuroptera: Myrmeleontidae): geographic variation in body size and heterozygosity

Aim Geographic variation in body size and heterozygosity were surveyed for discrete populations of the ant lion, Myrmeleon immaculatus DeGeer, collected from the central and northeastern United States. Location Collection sites were located in the central and eastern United States ranging from western Oklahoma to northern New York. Methods We collected 872 M. immaculatus larvae from thirty-four collecting sites. At each site, we randomly sampled ant lion pits and collected between fifteen and fifty-two larvae in total. Larvae were preserved in 95% ETOH for morphological analysis and frozen in a ?80°C freezer for protein electrophoresis. We measured the body size of eighty-five preserved adult M. immaculatus obtained from museum collections using head width as an indicator of body size. Five enzymes [GPI (glucose phosphate isomerase), MDH (malate dehydrogenase), PEP (peptidase), DIA (diaphorase) and SOD (superoxide dismutase)] were used in the heterozygosity analyses. Results Larval and adult body size increased with latitude, but decreased with elevation. Average heterozygosity, measured at five polymorphic loci, also increased significantly with latitude. Minimum temperature variance was the best predictor of body size, whereas precipitation and maximum temperature were the best predictors of heterozygosity. Populations were genetically differentiated from one another and showed a pattern of isolation by distance, as measured by Wright's F_st values and Nei's genetic distances. Main conclusions Sampling artifacts, heat conservation, character displacement, cell-size variation, density-dependent mortality, and differential dispersal probably cannot account for latitudinal variation in ant lion body size. Our results implicate the importance of diurnal photoperiod, which varies with latitude, but not with elevation. Because photoperiod often controls growth, diapause, and metamorphosis, it may be an important determinant of latitudinal clines in body size and life history of insects.     

Energy and interspecific body size patterns of amphibian faunas in Europe and North America: anurans follow Bergmann's rule, urodeles its converse

Aim To describe broad‐scale geographical patterns of body size for European and North American amphibian faunas and to explore possible processes underlying these patterns. Specifically, we propose a heat balance hypothesis, as both heat conservation and heat gain determine the heat balance of ectotherms, and test it along with five other hypotheses that have a possible influence on body size gradients: size dependence, migration ability, primary productivity, seasonality and water availability. Location Western Europe and North America north of Mexico. Methods We processed distribution maps for native amphibian species to estimate the mean body size in 110 × 110 km cells and calculated eight environmental predictors to explore the relationship between environmental gradients and the observed patterns. We used least squares regression modelling and model selection approaches based on information theory to evaluate the relative support for each hypothesis. Results We found consistent body size gradients and similar relationships to environmental variables within each amphibian group in Europe and North America. Annual potential evapotranspiration, a measure of environmental energy, was the strongest predictor of mean body size in both regions. However, the contrasting responses to ambient energy in each group resulted in opposite geographical patterns, i.e. anurans increased in size from high‐ to low‐energy areas in both continents and urodeles showed the opposite pattern. Main conclusions Our results support the heat balance hypothesis, suggesting that the thermoregulatory abilities of anurans would allow them to reach larger sizes in colder climates by optimizing the trade‐off between heating and cooling rates, whereas a lack of such strategies among urodele faunas would explain why these organisms tend to be smaller in cooler areas. These findings may also have implications for the role of climate warming on the global decline of amphibians.     

The island rule and a research agenda for studying ecogeographical patterns

We are currently experiencing a resurgence of interest in ecogeographical rules, which describe general trends in morphology and related traits along geographical gradients. In order to develop a more comprehensive understanding of the generality and underlying causal mechanisms for these patterns, we recommend a new, more integrated research agenda. In particular, we recommend studies that simultaneously consider different clines in morphology, geographical ranges and diversity as intricately related phenomena; all being ecological, evolutionary and biogeographical responses of organisms to selection regimes that vary non-randomly over space and time, and among species with different ecological and evolutionary histories.     

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.     

Bergmann's rule in amphibians: combining demographic and ecological parameters to explain body size variation among populations in the common toad Bufo bufo

Large‐scale patterns of body size variation are described by well‐known generalizations such as Bergmann’s rule; the generality and underlying causes of these patterns have been much debated. Intraspecific extension of this rule was tested in various ectotherms, and evidence was found for both Bergmann and converse Bergmann clines. In this study, we explored spatial patterns of variation in a widespread amphibian, the Common toad (Bufo bufo), along a 2240 km latitudinal gradient across Europe. We tested for covariation of adult body size, age and growth parameters with latitude, altitude, length of activity period and mean temperature during this period using both original and literature data. We selected 13 European populations, representing a latitudinal range from 43 to 63°N and altitudinal range from 15 to 1850 m a.s.l. The length of activity period (12–33 weeks) and T_mean (6.6–15.6°C) significantly decreased as latitude and altitude of these populations increased. Mean body size decreased as latitude increased (not with altitude), and increased with T_mean (not with length of activity period). Mean and minimal adult age increased with latitude and altitude, longevity increased with altitude only. Age increased as length of activity period decreased (not with T_mean). The growth coefficient (0.32–0.92 in males, 0.18–0.74 in females, available for six populations) decreased as altitude increased, and increased as both length of activity period and T_mean increased; latitudinal trend was non‐significant. Our analysis shows that B. bufo clearly exhibited a converse Bergmann cline along latitudinal gradient, but not along altitudinal gradient; the main effect of elevation was on age. The effects of ecological conditions also differed: body size increased with T_mean, while age parameters were related to the length of activity period. This study highlights that, to identify causal factors underlying general ecogeographical rules, we have to take into account different phases of the life cycle, co‐variation among life history traits and ecological factors acting on each of these traits. In amphibians with complex life cycles, lack of appropriate demographical or ecological data may affect our understanding of the variety of observed body size patterns.     

Long‐distance call evolution in the Felidae: effects of body weight,habitat, and phylogeny

Long‐distance calls used for mate attraction and territorial spacing are distinctive signals in the felid vocal repertoire. Their evolution is subject to natural and sexual selection, as well as various constraints. Body size is an important morphological constraint, with the scaling of the spectral characteristics of a species' vocalizations with its body size being established for several vertebrate groups. Alternatively, the structure of long‐distance calls may have been optimized for transmission in species' habitats (acoustic adaptation hypothesis). The present study assessed whether the mean dominant frequency of long‐distance calls in the Felidae (approximately 70% of all species incorporated) is influenced by the species' body size and/or conforms to the acoustic adaptation hypothesis. After controlling for phylogenetic relationships, we found a significant correlation between mean dominant frequency of a taxon's long‐distance calls and conditions for sound transmission in its habitat type (‘open/heterogeneous’ versus ‘dense’), although no significant influence of body size. Taxa living in more open habitat types have long‐distance calls with significantly lower mean dominant frequencies than those living in dense habitats. The result obtained in the present analysis is fairly robust against random removal of single or few taxa from the data, and also against the use of different branch‐length transformation models in phylogenetic regression. © 2010 The Linnean Society of London, Biological Journal of the Linnean Society, 2010, 101 , 487–500.     

Evolutionary change in seed size among some legume species: The effects of phylogeny

The importance of phylogenetic effects in controlling seed size variation at the macroevolutionary levels was examined using species of a well-defined, monophyletic family, the Leguminosae. A nested ANOVA was used to separate variance components at the various taxonomic levels such as subfamily, genus, and subgenus. Statistical significance was found at most of the taxonomic levels examined, which suggests that phylogeny as shown by the accepted taxonomy of the family, exerted a substantial influence over seed size variation. Thus, there appears to be a characteristic mean seed size for each genus and subgenus. The overall positive correlation between plant height and seed size was interpreted as a scaling of seed size to plant height. When the effect of plant height was controlled, the amount of variance changed to some extent across taxonomic levels, though resulting in no change in statistical significance at various taxonomic levels. This results indicate that phylogenetic effects in seed size variation among congeneric or consubgeneric groupings were largely independent of allometric effects. The patterns of variance components and intraclass correlation coefficients for seed size differed to some extent among subfamilies. The difference in those patterns among taxa will reflect evolutionary change more closely with larger sample sizes. A simple inverse relationship between seed size and number per fruit among related legume species was difficult to generalize. This was perhaps due to phylogenetic constraints on seed size and/or seed number (or ovule number). These results demonstrate that phylogeny and plant height affect seed size variation among related species.     

The importance of phylogenetic scale in tests of Bergmann's and Rapoport's rules: lessons from a clade of South American lizards

We tested for the occurrence of Bergmann's rule, the pattern of increasing body size with latitude, and Rapoport's rule, the positive relationship between geographical range size and latitude, in 34 lineages of Liolaemus lizards that occupy arid regions of the Andean foothills. We tested the climatic-variability hypothesis (CVH) by examining the relationship between thermal tolerance breadth and distribution. Each of these analyses was performed varying the level of phylogenetic inclusiveness. Bergmann's rule and the CVH were supported, but Rapoport's rule was not. More variance in the data for Bergmann's rule and the CVH was explained using species belonging to the L. boulengeri series rather than all species, and inclusion of multiple outgroups tended to obscure these macroecological patterns. Evidence for Bergmann's rule and the predicted patterns from the CVH remained after application of phylogenetic comparative methods, indicating a greater role of ecological processes rather than phylogeny in shaping the current species distributions of these lizards.     

Diversity and evolutionary origins of fungi associated with seeds of a neotropical pioneer tree: a case study for analysing fungal environmental samples

Fungi associated with seeds of tropical trees pervasively affect seed survival and germination, and thus are an important, but understudied, component of forest ecology. Here, we examine the diversity and evolutionary origins of fungi isolated from seeds of an important pioneer tree (Cecropia insignis, Cecropiaceae) following burial in soil for five months in a tropical moist forest in Panama. Our approach, which relied on molecular sequence data because most isolates did not sporulate in culture, provides an opportunity to evaluate several methods currently used to analyse environmental samples of fungi. First, intra- and interspecific divergence were estimated for the nu-rITS and 5.8S gene for four genera of Ascomycota that are commonly recovered from seeds. Using these values we estimated species boundaries for 527 isolates, showing that seed-associated fungi are highly diverse, horizontally transmitted, and genotypically congruent with some foliar endophytes from the same site. We then examined methods for inferring the taxonomic placement and phylogenetic relationships of these fungi, evaluating the effects of manual versus automated alignment, model selection, and inference methods, as well as the quality of BLAST-based identification using GenBank. We found that common methods such as neighbor-joining and Bayesian inference differ in their sensitivity to alignment methods; analyses of particular fungal genera differ in their sensitivity to alignments; and numerous and sometimes intricate disparities exist between BLAST-based versus phylogeny-based identification methods. Lastly, we used our most robust methods to infer phylogenetic relationships of seed-associated fungi in four focal genera, and reconstructed ancestral states to generate preliminary hypotheses regarding the evolutionary origins of this guild. Our results illustrate the dynamic evolutionary relationships among endophytic fungi, pathogens, and seed-associated fungi, and the apparent evolutionary distinctiveness of saprotrophs. Our study also elucidates the diversity, taxonomy, and ecology of an important group of plant-associated fungi and highlights some of the advantages and challenges inherent in the use of ITS data for environmental sampling of fungi.     

Determinants of local abundance in a major radiation of Australian passerines (Aves: Meliphagoidea)

Aim  To identify the factors that contribute to variation in abundance (population density), and to investigate whether habitat breadth and diet breadth predict macroecological patterns in a suborder of passerine birds (Meliphagoidea).
Location  Australia (including Tasmania).
Methods  Mean abundance data were collated from site surveys of bird abundance (the Australian Bird Count); range size and latitudinal position data from published distribution maps; and body mass and diet breadth information from published accounts. A diversity index of habitats used (habitat breadth) was calculated from the bird census data. We used bivariate correlation and multiple regression techniques, employing two phylogenetic comparative methods: phylogenetic generalized least squares and independent contrasts.
Results  Body mass and latitude were the only strong predictors of abundance, with larger-bodied and lower-latitude species existing at lower densities. Together, however, body mass and latitude explained only 11.1% of the variation in mean abundance. Range size and habitat breadth were positively correlated, as were diet breadth and body mass. However, neither range size, nor habitat breadth and diet breadth, explained patterns in abundance either directly or indirectly.
Main conclusions  Levels of abundance (population density) in meliphagoid birds are most closely linked to body mass and latitudinal position, but not range size. As with many other macroecological analyses, we find little evidence for aspects of niche breadth having an effect on patterns of abundance. We hypothesize that evolutionary age may also have a determining effect on why species tend to be rarer (less abundant) in the tropics.     

The evolution of pyrrolizidine alkaloid diversity among and within Jacobaea species

Plants produce many secondary metabolites showing considerable inter- and intraspecific diversity of concentration and composition as a strategy to cope with environmental stresses. The evolution of plant defenses against herbivores and pathogens can be unraveled by understanding the mechanisms underlying chemical diversity. Pyrrolizidine alkaloids are a class of secondary metabolites with high diversity. We performed a qualitative and quantitative analysis of 80 pyrrolizidine alkaloids with liquid chromatography-tandem mass spectrometry of leaves from 17 Jacobaea species including one to three populations per species with 4–10 individuals per population grown under controlled conditions in a climate chamber. We observed large inter- and intraspecific variation in pyrrolizidine alkaloid concentration and composition, which were both species-specific. Furthermore, we sequenced 11 plastid and three nuclear regions to reconstruct the phylogeny of the 17 Jacobaea species. Ancestral state reconstruction at the species level showed mainly random distributions of individual pyrrolizidine alkaloids. We found little evidence for phylogenetic signals, as nine out of 80 pyrrolizidine alkaloids showed a significant phylogenetic signal for Pagel's λ statistics only, whereas no significance was detected for Blomberg's K measure. We speculate that this high pyrrolizidine alkaloid diversity is the result of the upregulation and downregulation of specific pyrrolizidine alkaloids depending on ecological needs rather than gains and losses of particular pyrrolizidine alkaloid biosynthesis genes during evolution.     

The evolution and maintenance of delayed implantation in the mustelidae (mammalia: carnivora)

Diapause, the temporary cessation of development at an early life-history stage, is widespread among animals and plants. The range of taxa exhibiting various forms of diapause indicates its enormous ecological significance and highlights its value as a model for examining life-history trait evolution. However, despite the impact of diapause on species ecology, there is little understanding of its adaptive value in many groups. Furthermore, the relative roles of phylogeny and ecology in determining the contemporary expression of the trait remain unresolved. Delayed implantation (DI) is a type of diapause found in several orders of mammals. It is particularly prevalent in the Mustelidae, with mustelids making up more than half of all mammals known to exhibit DI. This taxon is thus ideal for examining life-history predictors of DI and investigating the mode of evolution. Both maximum likelihood and maximum parsimony methods of ancestral state reconstruction indicated DI to be plesiomorphic in the mustelids, although multiple state changes are required to explain its contemporary distribution. After controlling for phylogeny, species with and without DI could be discriminated using just three variables: longevity, maximum latitude of the geographical distribution, and a term describing maternal investment. Our analyses supported the hypothesis that DI is more prevalent in seasonal climates. We also showed that longer-lived species are more likely to exhibit DI, suggesting a time cost to the trait. We found no correlate for the highly variable duration of DI, which remains unexplained. Although ecological factors can predict the distribution of DI in modern mustelids, phylogenetic constraint is likely to play an important role.     

神农架海拔梯度上的植物种域分布特征及Rapoport法则检验

根据Rapoport法则, 动物、植物物种的纬度或海拔分布宽度存在着从高纬度或高海拔地区向低纬度或低海拔地区逐渐变窄的现象。本文基于物种的海拔分布数据, 分析了神农架维管束植物及不同种域宽度组的物种丰富度海拔格局; 采用已有的4种方法和本文改进的种域分组中点法, 分析了海拔梯度上种域宽度与种域中点的关系, 并检验其是否符合Rapoport法则。结果表明, 神农架地区维管植物丰富度的海拔梯度分布格局呈单峰型, 峰值在1,000–1,500 m; 不同种域组的物种丰富度分布具有类似的单峰格局, 但随着种域宽度减小, 其物种丰富度的峰值逐渐偏向低海拔。对于神农架的物种海拔分布数据, Stevens方法、Pagel方法和逐种方法的结果都支持Rapoport法则, 而中点法的结果主要反映中域效应的影响, 种域分组中点法可有效控制中域效应的影响, 但不支持Rapoport法则。上述结果表明, 对于Rapoport法则的检验亟待研究方法的改进; 而种域的海拔格局及其形成机制, 还需要更多案例的比较研究, 才能形成普遍性的认识。     

The evolution of embryo size in angiosperms and other seed plants: implications for the evolution of seed dormancy

Abstract.— Seed dormancy plays an important role in germination ecology and seed plant evolution. Morphological seed dormancy is caused by an underdeveloped embryo that must mature prior to germination. It has been suggested that the presence of an underdeveloped embryo is plesiomorphic among seed plants and that parallel directional change in embryo morphology has occurred separately in gymnosperms and in angiosperms. We test these hypotheses using original data on embryo morphology of key basal taxa, a published dataset, and the generalized least squares (GLS) method of ancestral character state reconstruction. Reconstructions for embryo to seed ratio (E:S) using family means for 179 families showed that E:S has increased between the ancestral angiosperm and almost all extant angiosperm taxa. Species in the rosid clade have particularly large embryos relative to the angiosperm ancestor. Results for the gymnosperms show a similar but smaller increase. There were no statistically significant differences in E:S between basal taxa and any derived group due to extremely large standard errors produced by GLS models. However, differences between reconstructed values for the angiosperm ancestor and more highly nested nodes are large and these results are robust to topological and branch-length manipulations. Our analysis supports the idea that the underdeveloped embryo is primitive among seed plants and that there has been a directional change in E:S within both angiosperms and gymnosperms. Our analysis suggests that dormancy enforced by an underdeveloped embryo is plesiomorphic among angiosperms and that nondormancy and other dormancy types probably evolved within the angiosperms. The shift in E:S was likely a heterochronic change, and has important implications for the life history of seed plants.