Ecological and evolutionary components of body size: geographic variation of venomous snakes at the global scale

Biogeographical patterns of animal body size and the environmental and evolutionary mechanisms that may be driving them have been broadly investigated in macroecology, although just barely in ectotherms. We separately studied two snake clades, Viperidae and Elapidae, and used phylogenetic eigenvector regression and ordinary least squares multiple regression methods to perform a global grid-based analysis of the extent at which the patterns of body size (measured for each species as its log₁₀-transformed maximum body length) of these groups are phylogenetically structured or driven by current environment trends. Phylogenetic relatedness explained 20% of the across-species size variation in Viperidae, and 59% of that of Elapidae, which is a more recent clade. Conversely, when we analysed spatial trends in mean body size values (calculated for each grid-cell as the average size of its extant species), an environmental model including temperature, precipitation, primary productivity (as indicated by the global vegetation index) and topography (range in elevation) explained 37.6% of the variation of Viperidae, but only 4.5% of that of Elapidae. These contrasted responses of body size patterns to current environment gradients are discussed, taking into consideration the dissimilar evolutionary histories of these closely-related groups. Additionally, the results obtained emphasize the importance of the need to start adopting deconstructive approaches in macroecology.  © 2009 The Linnean Society of London, Biological Journal of the Linnean Society , 2009, 98 , 94–109.     

Interspecific patterns of species richness, geographic range size, and body size among New World venomous snakes

Many higher taxa exhibit latitudinal gradients in species richness, geographic range size, and body size. However, these variables are often interdependent, such that examinations of univariate or bivariate patterns alone may be misleading. Therefore, I examined latitudinal gradients in, and relationships between, species richness, geographic range size, and body size among 144 species of New World venomous snakes [families Elapidae (coral snakes) and Viperidae (pitvipers)]. Both lineages are monophyletic, collectively span 99° of latitude, and are extremely variable in body size and geographic range sizes. Coral snakes exhibit highest species richness near the equator, while pitviper species richness peaks in Central America. Species – range size distributions were strongly right-skewed for both families. There was little support for Bergmann's rule or Rapoport's rule for snakes of either family, as neither body size nor range size increased significantly with latitude. However, range area and median range latitude were positively correlated above 15° N, indicating a possible "Rapoport effect" at high northern latitudes. Geographic range size was positively associated with body size. Available continental area strongly influenced range size. Comparative (phylogenetically-based) analyses revealed that shared history is a poor predictor of range size variation within clades. Among vipers, trends in geographic range sizes may have been structured more by historical biogeography than by macroecological biotic factors.     

The phylogeny and classification of caenophidian snakes inferred from seven nuclear protein-coding genes

More than 80% of the approximately 3000 living species of snakes are placed in the taxon Caenophidia (advanced snakes), a group that includes the families Acrochordidae, Viperidae, Elapidae, Atractaspididae, and the paraphyletic 'Colubridae'. Previous studies using DNA sequences have involved few nuclear genes (one or two). Several nodes have therefore proven difficult to resolve with statistical significance. Here, we investigated the higher-level relationships of caenophidian snakes with seven nuclear protein-coding genes and obtained a well-supported topology. Accordingly, some adjustments to the current classification of Caenophidia are made to better reflect the relationships of the groups. The phylogeny also indicates that, ancestrally, caenophidian snakes are Asian and nocturnal in origin, although living species occur on nearly all continents and are ecologically diverse.     

Richness patterns, species distributions and the principle of extreme deconstruction

Aim To analyse the global patterns in species richness of Viperidae snakes through the deconstruction of richness into sets of species according to their distribution models, range size, body size and phylogenetic structure, and to test if environmental drivers explaining the geographical ranges of species are similar to those explaining richness patterns, something we called the extreme deconstruction principle. Location Global. Methods We generated a global dataset of 228 terrestrial viperid snakes, which included geographical ranges (mapped at 1° resolution, for a grid with 7331 cells world‐wide), body sizes and phylogenetic relationships among species. We used logistic regression (generalized linear model; GLM) to model species geographical ranges with five environmental predictors. Sets of species richness were also generated for large and small‐bodied species, for basal and derived species and for four classes of geographical range sizes. Richness patterns were also modelled against the five environmental variables through standard ordinary least squares (OLS) multiple regressions. These subsets are replications to test if environmental factors driving species geographical ranges can be directly associated with those explaining richness patterns. Results Around 48% of the total variance in viperid richness was explained by the environmental model, but richness sets revealed different patterns across the world. The similarity between OLS coefficients and the primacy of variables across species geographical range GLMs was equal to 0.645 when analysing all viperid snakes. Thus, in general, when an environmental predictor it is important to model species geographical ranges, this predictor is also important when modelling richness, so that the extreme deconstruction principle holds. However, replicating this correlation using subsets of species within different categories in body size, range size and phylogenetic structure gave more variable results, with correlations between GLM and OLS coefficients varying from –0.46 up to 0.83. Despite this, there is a relatively high correspondence (r = 0.73) between the similarity of GLM‐OLS coefficients and R² values of richness models, indicating that when richness is well explained by the environment, the relative importance of environmental drivers is similar in the richness OLS and its corresponding set of GLMs. Main conclusions The deconstruction of species richness based on macroecological traits revealed that, at least for range size and phylogenetic level, the causes underlying patterns in viperid richness differ for the various sets of species. On the other hand, our analyses of extreme deconstruction using GLM for species geographical range support the idea that, if environmental drivers determine the geographical distribution of species by establishing niche boundaries, it is expected, at least in theory, that the overlap among ranges (i.e. richness) will reveal similar effects of these environmental drivers. Richness patterns may be indeed viewed as macroecological consequences of population‐level processes acting on species geographical ranges.     

Phylogeny of the Colubroidea (Serpentes): new evidence from mitochondrial and nuclear genes

The Colubroidea contains over 85% of all the extant species of snakes and is recognized as monophyletic based on morphological and molecular data. Using DNA sequences (cyt b, c-mos) from 100 species we inferred the phylogeny of colubroids with special reference to the largest family, the Colubridae. Tree inference was obtained using Bayesian, likelihood, and parsimony methods. All analyses produced five major groups, the Pareatidae, Viperidae, Homalopsidae, the Elapidae, and the Colubridae. The specific content of the latter two groups has been altered to accommodate evolutionary history and to yield a more stable taxonomy. We propose an updated classification based on the reallocation of species as indicated by our inferred phylogeny.     

The shadow of forgotten ancestors differently constrains the fate of Alligatoroidea and Crocodyloidea

Aim We tested the hypothesis that the evolutionary fates of two sister groups (Alligatoroidea and Crocodyloidea) are differently constrained by phylogenetic and ecological (functional) factors in the face of climatic change. Location Global. Methods We quantified disparity in skull rostrum shape by means of geometric morphometrics. Mechanical performance of the rostrum was analyzed by applying beam theory calculations to morphological data and experimentally measured bite force. The phylogeny was expressed in the form of principal coordinates, the first ones of which were used as a set of explanatory variables. Extents of species occurrence were computed using species distribution maps. Finally, species maximum skull size were measured and considered as a proxy of maximum body size. We performed variation partitioning analyses in order to compare differential contributions of phylogenetic and ecological factors in Alligatoroidea and Crocodyloidea. Results Alligatoroidea show higher ‘pure’ historical components than Crocodyloidea in explaining both rostrum shape and extent of occurrence (after controlling for body size). On the contrary, geometric variation of skull rostra of Crocodyloidea unequivocally shows a higher ‘pure’ functional component (linked to performance on prey capture) and a higher phylogenetically structured environmental variation than those found in Alligatoroidea. Results obtained for body size variation are consistent with these patterns. In Alligatoroidea, body size variation contains a higher phylogenetic signal than in Crocodyloidea. Main Conclusions Our results suggest that Crocodyloidea and Alligatoroidea may react differently when faced with significant environmental changes. We predict that global climatic changes will have a more important effect on Crocodyloidea than in Alligatoroidea by (1) promoting trait shift, adaptation to the new diet and speciation and (2) modifying the geographical range distribution of species (which may track favourable ecological conditions).     

Conserved and variable segments of the snake phospholipase A2 amino acid domain]

Homologous amino acid sequences of phospholipases A2 of snakes belonging to families Elapidae, Viperidae and Colubridae were considered in order to study the location of conservative and variable regions. To identify significant conservative and variable regions a comparison between two groups of aligned sequences of snake phospholipases A2 was successfully applied. The phospholipases A2 sequences were divided into two groups (taxons) according to the phylogenetic tree reconstructed from the pair distance matrix. Results of the comparison were plotted to facilitate the identification of significant conservative and variable regions. It was shown, that the results of the comparison between two phylogenetic groups of snake phospholipases A2 didn't depend much on the number of each group representatives, and the location of conservative and variable regions didn't significantly change if one of the groups was represented by the single sequence. It should be mentioned, that the more the phylogenetic difference between groups of phospholipases A2 the more was the number of significant conservative and variable regions. The knowledge of the number and location of conservative and variable regions and their dependence on phylogenetic relations between the compared taxons can be used to predict the synthetic peptide structure to obtain antibodies of various specificity. These antibodies may have either a wide range of cross-reactivity against all of phospholipases A2 or a limited range of cross-reactivity against phospholipases A2 of one taxon.     

Phylogenetic comparative analysis supports aposematic colouration–body size association in millipede assassins (Hemiptera: Reduviidae: Ectrichodiinae)

The diversity of colour patterns and its importance in interactions with the environment make colouration in animals an intriguing research focus. Aposematic colouration is positively correlated with body size in certain groups of animals, suggesting that warning colours are more effective or that crypsis is harder to achieve in larger animals. Surprisingly, this relationship has not been recovered in studies investigating insects, which may have been confounded by a focus on aposematic taxa that are also gregarious. Millipede assassin bugs (Hemiptera: Reduviidae: Ectrichodiinae) comprise species with cryptic and aposematic colour patterns across a range of body sizes, are typically solitary as adults and are thus an excellent model for investigating a possible association between colouration and body size. Here, we use a comprehensive phylogeny for Ectrichodiinae, ancestral state reconstruction of colouration, and phylogenetic comparative methods to test for a colouration–body size association. The ancestor of Ectrichodiinae is reconstructed as cryptically coloured, with multiple subsequent transitions between aposematic and cryptic colouration. Aposematic colouration is positively associated with male body length and supports the hypothesis that selection on Ectrichodiinae body size may influence evolutionary transitions between aposematic and cryptic colouration or alternatively that selection for aposematic colouration influences body size evolution.     

Lachesis muta (Viperidae) cDNAs reveal diverging pit viper molecules and scaffolds typical of cobra (Elapidae) venoms: implications for snake toxin repertoire evolution

Efforts to describe toxins from the two major families of venomous snakes (Viperidae and Elapidae) usually reveal proteins belonging to few structural types, particular of each family. Here we carried on an effort to determine uncommon cDNAs that represent possible new toxins from Lachesis muta (Viperidae). In addition to nine classes of typical toxins, atypical molecules never observed in the hundreds of Viperidae snakes studied so far are highly expressed: a diverging C-type lectin that is related to Viperidae toxins but appears to be independently originated; an ohanin-like toxin, which would be the third member of the most recently described class of Elapidae toxins, related to human butyrophilin and B30.2 proteins; and a 3FTx-like toxin, a new member of the widely studied three-finger family of proteins, which includes major Elapidae neurotoxins and CD59 antigen. The presence of these common and uncommon molecules suggests that the repertoire of toxins could be more conserved between families than has been considered, and their features indicate a dynamic process of venom evolution through molecular mechanisms, such as multiple recruitments of important scaffolds and domain exchange between paralogs, always keeping a minimalist nature in most toxin structures in opposition to their nontoxin counterparts.     

Genome size in arthropods; different roles of phylogeny,habitat and life history in insects and crustaceans

Despite the major role of genome size for physiology, ecology, and evolution, there is still mixed evidence with regard to proximate and ultimate drivers. The main causes of large genome size are proliferation of noncoding elements and/or duplication events. The relative role and interplay between these proximate causes and the evolutionary patterns shaped by phylogeny, life history traits or environment are largely unknown for the arthropods. Genome size shows a tremendous variability in this group, and it has a major impact on a range of fitness‐related parameters such as growth, metabolism, life history traits, and for many species also body size. In this study, we compared genome size in two major arthropod groups, insects and crustaceans, and related this to phylogenetic patterns and parameters affecting ambient temperature (latitude, depth, or altitude), insect developmental mode, as well as crustacean body size and habitat, for species where data were available. For the insects, the genome size is clearly phylogeny‐dependent, reflecting primarily their life history and mode of development, while for crustaceans there was a weaker association between genome size and phylogeny, suggesting life cycle strategies and habitat as more important determinants. Maximum observed latitude and depth, and their combined effect, showed positive, and possibly phylogenetic independent, correlations with genome size for crustaceans. This study illustrate the striking difference in genome sizes both between and within these two major groups of arthropods, and that while living in the cold with low developmental rates may promote large genomes in marine crustaceans, there is a multitude of proximate and ultimate drivers of genome size.     

Rapid prey‐induced shift in body size in an isolated snake population (Notechis scutatus,Elapidae)

Abstract Geographic divergence in phenotypic traits between long‐isolated populations likely has a genetic basis, but can phenotypic plasticity generate such divergence rapidly in the initial stages of isolation? Australian tiger snakes (Notechis scutatus, Elapidae) provide a classic model system for the evolution of body size: mean adult sizes are relatively invariant in mainland populations, but many offshore islands have dwarf or giant populations. Previous work has shown a genetic basis to this divergence in long‐isolated islands (>10 000 years), but what of the initial stages of this process? Human translocation of mainland snakes to Carnac Island 90 years ago gives us a unique opportunity to assess the proximate reasons for the giant size of Carnac Island animals compared with mainland conspecifics. Our data suggest a major role for phenotypic plasticity. Feeding trials on captive snakes from both island and mainland populations showed a strong link between food intake and growth rates, similar in the two populations. Snakes given abundant food grew much larger than we have ever recorded in the wild, demonstrating that observed mean body sizes are driven by food availability rather than genetic limits to growth. In combination with earlier work showing genetic divergence in growth rates in snakes from long‐isolated islands, our data suggest that geographical divergence in mean adult body sizes in this system initially is driven by a rapid shift due to phenotypic plasticity, with the divergence later canalized by a gradual accumulation of genetic differentiation.     

The geography of body size – challenges of the interspecific approach

Recent compilations of large-scale data bases on the geographical distributions and body sizes of animals, coupled with developments in spatial statistics, have led to renewed interest in the geographical distribution of animal body sizes and the interspecific version of Bergmann's rule. Standard practice seems to be an examination of mean body sizes within higher taxa on gridded maps, with little regard to species richness or phylogeny. However, because the frequency distribution of body sizes is typically highly skewed, average size within grid cells may differ significantly between species-rich and species-poor cells even when the median and modal sizes remain constant. Species richness influences body size patterns because species are not added to communities at random in relation to their size: areas of low diversity are characterized by a higher range of body sizes than is expected by chance. Finally, a consideration of phylogenetic structure within taxa is necessary to elucidate whether patterns in the geography of size result from turnover between or within intermediate taxonomic levels. We suggest that the highest and lowest quantiles of body size distribution be mapped in order to expose possible physiological or ecological limitations on body size.     

Modeling body size evolution in Felidae under alternative phylogenetic hypotheses

The use of phylogenetic comparative methods in ecological research has advanced during the last twenty years, mainly due to accurate phylogenetic reconstructions based on molecular data and computational and statistical advances. We used phylogenetic correlograms and phylogenetic eigenvector regression (PVR) to model body size evolution in 35 worldwide Felidae (Mammalia, Carnivora) species using two alternative phylogenies and published body size data. The purpose was not to contrast the phylogenetic hypotheses but to evaluate how analyses of body size evolution patterns can be affected by the phylogeny used for comparative analyses (CA). Both phylogenies produced a strong phylogenetic pattern, with closely related species having similar body sizes and the similarity decreasing with increasing distances in time. The PVR explained 65% to 67% of body size variation and all Moran's I values for the PVR residuals were non-significant, indicating that both these models explained phylogenetic structures in trait variation. Even though our results did not suggest that any phylogeny can be used for CA with the same power, or that "good" phylogenies are unnecessary for the correct interpretation of the evolutionary dynamics of ecological, biogeographical, physiological or behavioral patterns, it does suggest that developments in CA can, and indeed should, proceed without waiting for perfect and fully resolved phylogenies.     

The influence of spatial resolution on macroecological patterns of range size variation: a case study using parrots (Aves: Psittaciformes) of the world

Aim To assess the extent to which the resolution at which geographical range sizes are measured influences macroecological patterns in this variable. Location Global. Methods Data on the geographical ranges of parrot species were digitized, and a Geographic Information System used to produce nine range size estimates for each species using different degrees of spatial resolution. The inter‐correlation of these estimates was then compared, together with their patterns of covariation with population size, body mass and migratory behaviour (across species and controlling for phylogeny), their pattern of phylogenetic correlation, and the frequency distributions of the different measures. Results Strong correlations exist among all nine range size measures across species, albeit that measures of similar spatial resolution are more strongly correlated. All measures show similar patterns of covariation with population size, body mass and migratory behaviour, and similar patterns of phylogenetic correlation. The skewness of frequency distributions increases towards zero as the resolution of the range size measure declines. Main conclusions The results of macroecological analyses are little affected by the resolution with which geographical range sizes are calculated, at least for the parrots of the world. Previously published studies based on crude measures of range size would be unlikely to have produced markedly different conclusions had they used more refined range size metrics.     

Phylogenetics of advanced snakes (Caenophidia) based on four mitochondrial genes

Phylogenetic relationships among advanced snakes (Acrochordus + Colubroidea = Caenophidia) and the position of the genus Acrochordus relative to colubroid taxa are contentious. These concerns were investigated by phylogenetic analysis of fragments from four mitochondrial genes representing 62 caenophidian genera and 5 noncaenophidian taxa. Four methods of phylogeny reconstruction were applied: matrix representation with parsimony (MRP) supertree consensus, maximum parsimony, maximum likelihood, and Bayesian analysis. Because of incomplete sampling, extensive missing data were inherent in this study. Analyses of individual genes retrieved roughly the same clades, but branching order varied greatly between gene trees, and nodal support was poor. Trees generated from combined data sets using maximum parsimony, maximum likelihood, and Bayesian analysis had medium to low nodal support but were largely congruent with each other and with MRP supertrees. Conclusions about caenophidian relationships were based on these combined analyses. The Xenoderminae, Viperidae, Pareatinae, Psammophiinae, Pseudoxyrophiinae, Homalopsinae, Natricinae, Xenodontinae, and Colubrinae (redefined) emerged as monophyletic, whereas Lamprophiinae, Atractaspididae, and Elapidae were not in one or more topologies. A clade comprising Acrochordus and Xenoderminae branched closest to the root, and when Acrochordus was assessed in relation to a colubroid subsample and all five noncaenophidians, it remained associated with the Colubroidea. Thus, Acrochordus + Xenoderminae appears to be the sister group to the Colubroidea, and Xenoderminae should be excluded from Colubroidea. Within Colubroidea, Viperidae was the most basal clade. Other relationships appearing in all final topologies were (1) a clade comprising Psammophiinae, Lamprophiinae, Atractaspididae, Pseudoxyrophiinae, and Elapidae, within which the latter four taxa formed a subclade, and (2) a clade comprising Colubrinae, Natricinae, and Xenodontinae, within which the latter two taxa formed a subclade. Pareatinae and Homalopsinae were the most unstable clades.     

Conservative and variable regions of homologous snake phospholipases A2 sequences: Prediction of the taxonspecific peptides structure

Homologous amino acid sequences of phospholipases A₂ (PLA₂) of snakes belonging to the families Elapidae, Viperidae, and Colubridae were considered in order to study the conservative and variable regions location. The PLA₂ sequences were divided into two groups (taxons) according to the phylogenetic tree reconstructed from the pair similarity matrix. Results of the intergroup comparison were plotted to facilitate the identification of significant conservative and variable regions. It was shown that the results of the comparison between two phylogenetic groups of snake PLA₂ did not much depend on the number of each group representatives and did not markedly change if one of the groups was represented by the single sequence. The knowledge of the number and location of conservative and variable regions and their dependence on the phylogenetic relations between compared taxa may be used to predict a synthetic peptide structure to obtain specific antibodies against PLA₂ of one of these taxons. Such prediction is possible if there is a specific region conservative for one taxon but variable for two of them.     

Space versus phylogeny: disentangling phylogenetic and spatial signals in comparative data

Variation in traits across species or populations is the outcome of both environmental and historical factors. Trait variation is therefore a function of both the phylogenetic and spatial context of species. Here we introduce a method that, within a single framework, estimates the relative roles of spatial and phylogenetic variations in comparative data. The approach requires traits measured across phylogenetic units, e.g. species, the spatial occurrences of those units and a phylogeny connecting them. The method modifies the expected variance of phylogenetically independent contrasts to include both spatial and phylogenetic effects. We illustrate this approach by analysing cross-species variation in body mass, geographical range size and species-typical environmental temperature in three orders of mammals (carnivores, artiodactyls and primates). These species attributes contain highly disparate levels of phylogenetic and spatial signals, with the strongest phylogenetic autocorrelation in body size and spatial dependence in environmental temperatures and geographical range size showing mixed effects. The proposed method successfully captures these differences and in its simplest form estimates a single parameter that quantifies the relative effects of space and phylogeny. We discuss how the method may be extended to explore a range of models of evolution and spatial dependence.     

Trade‐offs in the evolution of bumblebee colony and body size: a comparative analysis

Trade‐offs between life‐history traits – such as fecundity and survival – have been demonstrated in several studies. In eusocial insects, the number of organisms and their body sizes can affect the fitness of the colony. Large‐than‐average body sizes as well as more individuals can improve a colony's thermoregulation, foraging efficiency, and fecundity. However, in bumblebees, large colonies and large body sizes depend largely on high temperatures and a large amount of food resources. Bumblebee taxa can be found in temperate and tropical regions of the world and differ markedly in their colony sizes and body sizes. Variation in colony size and body size may be explained by the costs and benefits associated with the evolutionary history of each species in a particular environment. In this study, we explored the effect of temperature and precipitation (the latter was used as an indirect indicator of food availability) on the colony and body size of twenty‐one bumblebee taxa. A comparative analysis controlling for phylogenetic effects as well as for the body size of queens, workers, and males in bumblebee taxa from temperate and tropical regions indicated that both temperature and precipitation affect colony and body size. We found a negative association between colony size and the rainiest trimester, and a positive association between the colony size and the warmest month of the year. In addition, male bumblebees tend to evolve larger body sizes in places where the rain occurs mostly in the summer and the overall temperature is warmer. Moreover, we found a negative relationship between colony size and body sizes of queens, workers, and males, suggesting potential trade‐offs in the evolution of bumblebee colony and body size.     

An interspecific test of Bergmann's rule reveals inconsistent body size patterns across several lineages of water beetles (Coleoptera: Dytiscidae)

1. Bergmann's rule sensu lato, the ecogeographic pattern relating animals' body size with environmental temperature (or latitude), has been shown to be inconsistent among insect taxa. Body size clines remain largely unexplored in aquatic insects, which may show contrasting patterns to those found in terrestrial groups because of the physiological or mechanical constraints of the aquatic environment. 2. Bergmann's rule was tested using data on body size, phylogeny and distribution for 93 species belonging to four lineages of dytiscid water beetles. The relationship between size and latitude was explored at two taxonomic resolutions – within each independent lineage, and for the whole dataset – employing phylogenetic generalised least‐squares to control for phylogenetic inertia. The potential influence of habitat preference (lotic versus lentic) on body size clines was also considered. 3. Within‐lineage analyses showed negative relationships (i.e. converse Bergmann's rule), but only in two lineages (specifically in those that included both lotic and lentic species). By contrast, no relationship was found between body size and latitude for the whole dataset. 4. These results suggest that there may be no universal interspecific trends in latitudinal variation of body size in aquatic insects, even among closely related groups, and show the need to account for phylogenetic inertia. Furthermore, habitat preferences should be considered when exploring latitudinal clines in body size in aquatic taxa at the interspecific level.