Patterns Of Body Size Evolution Research Articles

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

AbstractAimThe emergence of large‐scale patterns of animal body size is the central expectation of a wide range of (macro)ecological and evolutionary hypotheses. The drivers shaping these patterns include climate (e.g. Bergmann's rule), resource availability (e.g. ‘resource rule’), biogeographic settings and niche partitioning (e.g. adaptive radiation). However, these hypotheses often make opposing predictions about the trajectories of body size evolution. Therefore, whether underlying drivers of body size evolution can be identified remains an open question. Here, we employ the most comprehensive global dataset of body size in amphibians, to address multiple hypotheses that predict patterns of body size evolution based on climatic factors, ecology and biogeographic settings to identify underlying drivers and their generality across lineages.LocationGlobal.Time PeriodPresent.Major Taxa StudiedAmphibians.MethodsUsing a global dataset spanning 7270 (>87% of) species of Anura, Caudata and Gymnophiona, we employed phylogenetic Bayesian modelling to test the roles of climate, resource availability, insularity, elevation, habitat use and diel activity on body size.ResultsOnly climate and elevation drive body size patterns, and these processes are order‐specific. Seasonality in precipitation and in temperature predict body size clines in anurans, whereas caecilian body size increases with aridity. However, neither of these drivers explained variation in salamander body size. In both anurans and caecilians, size increases with elevational range and with midpoint elevation in caecilians only. No effects of mean temperature, resource abundance, insularity, time of activity or habitat use were found.Main ConclusionsPrecipitation and temperature seasonality are the dominant climatic drivers of body size variation in amphibians overall. Bergmann's rule is consistently rejected, and so are other alternative hypotheses. We suggest that the rationale sustaining existing macroecological rules of body size is unrealistic in amphibians and discuss our findings in the context of the emerging hypothesis that climate change can drive body size shifts.

Strength of the 'island rule' in birds is positively associated with absence of avian predators.

The similar characteristics shared by island environments have been shown to lead to common patterns of adaptations in island species, commonly referred to as the 'insularity syndrome'. A well-known example is the 'island rule', where large species become smaller on islands and small species become larger, leading to well-known cases of dwarfism and gigantism. This pattern was recently verified on a global scale, but the mechanisms underlying it have been poorly investigated. Here, we focused on the role of released pressure from predation and competition experienced by island birds. Using 120 pairs of endemic island species and their mainland sister relatives, we first verified that the island rule was detected in our dataset, and then evaluated the effects of the numbers of raptors and interspecific competitors on the evolution of the insular species' body mass. We found a strong effect of predation on body mass evolution, with a stronger island rule for species occurring on islands with no raptors, while the pattern disappears in their presence. However, we did not find an effect of competition on this pattern. Our study shows the importance of considering ecological interactions for understanding patterns of body size evolution, and the exceptions to those patterns.

Climate shapes patterns of sexual size and shape dimorphism across the native range of the green anole lizard,Anolis carolinensis(Squamata: Dactyloidae)

AbstractGeographical variation in sexual size dimorphism (SSD) can result from the combined effects of environmental and sexual selection. To understand the determinants of SSD across geographical landscapes, we tested for relationships between SSD and climatic variables in the widespread lizard Anolis carolinensis. To distinguish alternative hypotheses for observed patterns of variation in SSD, we also examined sex-specific patterns of body size evolution and asked whether SSD was associated with certain patterns of sexual shape dimorphism. We found strong evidence for Rensch’s rule (an increase in male-biased SSD with average body size) in A. carolinensis and evidence for the reversed version of Bergmann’s rule (an increase in body size towards warmer environments) in males. Across populations, SSD was positively related to temperature; however, female body size was not related to any climatic variable, suggesting that the latitudinal gradient of SSD might be driven by a gradient in the intensity of sexual selection acting on males. Sexual size dimorphism was positively correlated with sexual dimorphism in head shape and negatively correlated with limb length dimorphism, suggesting that sexual selection in males might drive the evolution of SSD and that differences in size and limb shape between sexes might represent alternative strategies to avoid competition for the same resources.

Lizards as models to explore the ecological and neuroanatomical correlates of miniaturization

Abstract Extreme body size reductions bring about unorthodox anatomical arrangements and novel ways in which animals interact with the environment. Drawing from studies of vertebrates and invertebrates, we provide a theoretical framework for miniaturization to inform hypotheses using lizards as a study system. Through this approach, we demonstrate the repeated evolution of miniaturization across 11 families and a tendency for miniaturized species to occupy terrestrial microhabitats, possibly driven by physiological constraints. Differences in gross brain morphology between two gecko species demonstrate a proportionally larger telencephalon and smaller olfactory bulbs in the miniaturized species, though more data are needed to generalize this trend. Our study brings into light the potential contributions of miniaturized lizards to explain patterns of body size evolution and its impact on ecology and neuroanatomy. In addition, our findings reveal the need to study the natural history of miniaturized species, particularly in relation to their sensory and physiological ecology.

The island rule explains consistent patterns of body size evolution in terrestrial vertebrates.

Island faunas can be characterized by gigantism in small animals and dwarfism in large animals, but the extent to which this so-called 'island rule' provides a general explanation for evolutionary trajectories on islands remains contentious. Here we use a phylogenetic meta-analysis to assess patterns and drivers of body size evolution across a global sample of paired island-mainland populations of terrestrial vertebrates. We show that 'island rule' effects are widespread in mammals, birds and reptiles, but less evident in amphibians, which mostly tend towards gigantism. We also found that the magnitude of insular dwarfism and gigantism is mediated by climate as well as island size and isolation, with more pronounced effects in smaller, more remote islands for mammals and reptiles. We conclude that the island rule is pervasive across vertebrates, but that the implications for body size evolution are nuanced and depend on an array of context-dependent ecological pressures and environmental conditions.

Physiological constraints on body size distributions in Crocodyliformes.

At least 26 species of crocodylian populate the globe today, but this richness represents a minute fraction of the diversity and disparity of Crocodyliformes. Fossil forms are far more varied, spanning from erect, fully terrestrial species to flippered, fully marine species. To quantify the influence of a marine habitat on the directionality, rate, and variance of evolution of body size in Crocodyliformes and thereby identify underlying selective pressures, we compiled a database of body sizes for 264 fossil and modern species of crocodyliform covering terrestrial, semi-aquatic, and marine habitats. We find increases in body size coupled with increases in strength of selection and decreases in variance following invasions of marine habitats but not of semiaquatic habitats. A model combining constraints from thermoregulation and lung capacity provides a physiological explanation for the larger minimum and average sizes of marine species. It appears that constraints on maximum size are shared across Crocodyliformes, perhaps through factors such as the allometric scaling of feeding rate versus basal metabolism with body size. These findings suggest that broad-scale patterns of body size evolution and the shapes of body size distributions within higher taxa are often determined more by physiological constraints than by ecological interactions or environmental fluctuations.

The multi-peak adaptive landscape of crocodylomorph body size evolution

BackgroundLittle is known about the long-term patterns of body size evolution in Crocodylomorpha, the > 200-million-year-old group that includes living crocodylians and their extinct relatives. Extant crocodylians are mostly large-bodied (3–7 m) predators. However, extinct crocodylomorphs exhibit a wider range of phenotypes, and many of the earliest taxa were much smaller (< 1.2 m). This suggests a pattern of size increase through time that could be caused by multi-lineage evolutionary trends of size increase or by selective extinction of small-bodied species. Here, we characterise patterns of crocodylomorph body size evolution using a model fitting-approach (with cranial measurements serving as proxies). We also estimate body size disparity through time and quantitatively test hypotheses of biotic and abiotic factors as potential drivers of crocodylomorph body size evolution.ResultsCrocodylomorphs reached an early peak in body size disparity during the Late Jurassic, and underwent an essentially continual decline since then. A multi-peak Ornstein-Uhlenbeck model outperforms all other evolutionary models fitted to our data (including both uniform and non-uniform), indicating that the macroevolutionary dynamics of crocodylomorph body size are better described within the concept of an adaptive landscape, with most body size variation emerging after shifts to new macroevolutionary regimes (analogous to adaptive zones). We did not find support for a consistent evolutionary trend towards larger sizes among lineages (i.e., Cope’s rule), or strong correlations of body size with climate. Instead, the intermediate to large body sizes of some crocodylomorphs are better explained by group-specific adaptations. In particular, the evolution of a more aquatic lifestyle (especially marine) correlates with increases in average body size, though not without exceptions.ConclusionsShifts between macroevolutionary regimes provide a better explanation of crocodylomorph body size evolution on large phylogenetic and temporal scales, suggesting a central role for lineage-specific adaptations rather than climatic forcing. Shifts leading to larger body sizes occurred in most aquatic and semi-aquatic groups. This, combined with extinctions of groups occupying smaller body size regimes (particularly during the Late Cretaceous and Cenozoic), gave rise to the upward-shifted body size distribution of extant crocodylomorphs compared to their smaller-bodied terrestrial ancestors.

Global patterns of body size evolution are driven by precipitation in legless amphibians

Body size shapes ecological interactions across and within species, ultimately influencing the evolution of large‐scale biodiversity patterns. Therefore, macroecological studies of body size provide a link between spatial variation in selection regimes and the evolution of animal assemblages through space. Multiple hypotheses have been formulated to explain the evolution of spatial gradients of animal body size, predominantly driven by thermal (Bergmann's rule), humidity (‘water conservation hypothesis’) and resource constraints (‘resource rule’, ‘seasonality rule’) on physiological homeostasis. However, while integrative tests of all four hypotheses combined are needed, the focus of such empirical efforts needs to move beyond the traditional endotherm–ectotherm dichotomy, to instead interrogate the role that variation in lifestyles within major lineages (e.g. classes) play in creating neglected scenarios of selection via analyses of largely overlooked environment–body size interactions. Here, we test all four rules above using a global database spanning 99% of modern species of an entire Order of legless, predominantly underground‐dwelling amphibians (Gymnophiona, or caecilians). We found a consistent effect of increasing precipitation (and resource abundance) on body size reductions (supporting the water conservation hypothesis), while Bergmann's, the seasonality and resource rules are rejected. We argue that subterranean lifestyles minimize the effects of aboveground selection agents, making humidity a dominant selection pressure – aridity promotes larger body sizes that reduce risk of evaporative dehydration, while smaller sizes occur in wetter environments where dehydration constraints are relaxed. We discuss the links between these principles with the physiological constraints that may have influenced the tropically‐restricted global radiation of caecilians.

Global patterns of body size evolution in squamate reptiles are not driven by climate

AbstractAimVariation in body size across animal species underlies most ecological and evolutionary processes shaping local‐ and large‐scale patterns of biodiversity. For well over a century, climatic factors have been regarded as primary sources of natural selection on animal body size, and hypotheses such as Bergmann's rule (the increase of body size with decreasing temperature) have dominated discussions. However, evidence for consistent climatic effects, especially among ectotherms, remains equivocal. Here, we test a range of key hypotheses on climate‐driven size evolution in squamate reptiles across several spatial and phylogenetic scales.LocationGlobal.Time periodExtant.Major taxa studiedSquamates (lizards and snakes).MethodsWe quantified the role of temperature, precipitation, seasonality and net primary productivity as drivers of body mass across ca. 95% of extant squamate species (9,733 spp.). We ran spatial autoregressive models of phylogenetically corrected median mass per equal‐area grid cell. We ran models globally, across separate continents and for major squamate clades independently. We also performed species‐level analyses using phylogenetic generalized least square models and linear regressions of independent contrasts of sister species.ResultsOur analyses failed to identify consistent spatial patterns in body size as a function of our climatic predictors. Nearly all continent‐ and family‐level models differed from one another, and species‐level models had low explanatory power.Main conclusionsThe global distribution of body mass among living squamates varies independently from the variation in multiple components of climate. Our study, the largest in spatial and taxonomic scale conducted to date, reveals that there is little support for a universal, consistent mechanism of climate‐driven size evolution within squamates.

Inconsistent patterns of body size evolution in co‐occurring island reptiles

AbstractAimAnimal body sizes are often remarkably variable across islands, but despite much research we still have a poor understanding of both the patterns and the drivers of body size evolution. Theory predicts that interspecific competition and predation pressures are relaxed on small, remote islands, and that these conditions promote body size evolution. We studied body size variation across multiple insular populations of 16 reptile species co‐occurring in the same archipelago and tested which island characteristics primarily drive body size evolution, the nature of the common patterns, and whether co‐occurring species respond in a similar manner to insular conditions.LocationAegean Sea islands.Time period1984–2016.Major taxa studiedReptiles.MethodsWe combined fieldwork, museum measurements and a comprehensive literature survey to collect data on nearly 10,000 individuals, representing eight lizard and eight snake species across 273 islands. We also quantified a large array of predictors to assess directly the effects of island area, isolation (both spatial and temporal), predation and interspecific competition on body size evolution. We used linear models and meta‐analyses to determine which predictors are informative for all reptiles, for lizards and snakes separately, and for each species.ResultsBody size varies with different predictors across the species we studied, and patterns differ within families and between lizards and snakes. Each predictor influenced body size in at least one species, but no general trend was recovered. As a group, lizards are hardly affected by any of the predictors we tested, whereas snake size generally increases with area and with competitor and predator richness, and decreases with isolation.Main conclusionsNo factor emerges as a predominant driver of Aegean reptile sizes. This contradicts theories of general body size evolutionary trajectories on islands. We conclude that overarching generalizations oversimplify patterns and processes of reptile body size evolution on islands. Instead, species’ autecology and island particularities interact to drive the course of size evolution.

Phenotypic Variation and Sexual Size Dimorphism in Dichroplus elongatus (Orthoptera: Acrididae).

Patterns of body size evolution are of particular interest because body size can affect virtually all the physiological and life history traits of an organism. Sexual size dimorphism (SSD), a difference in body size between males and females, is a widespread phenomenon in insects. Much of the variation in SSD is genetically based and likely due to differential selection acting on males and females. The importance of environmental variables and evolutionary processes affecting phenotypeic variation in both sexes may be useful to gain insights into insect ecology and evolution. Dichroplus elongatus Giglio-Tos is a South American grasshopper widely distributed throughout Argentina, Uruguay, most of Chile, and southern Brazil. In this study, we analyzed 122 adult females of D. elongatus collected in eight natural populations from central-east Argentina. Females show large body size variation among the analyzed populations and this variation exhibits a strong relationship with fecundity. Our results have shown that larger females were more fecund than smaller ones. We found that ovariole number varied along a latitudinal gradient, with higher ovariole numbers in populations from warmer locations. A considerable female-biased SSD was detected. SSD for three analyzed morphometric traits scaled isometrically. However, SSD for thorax length displayed a considerable variation across the studied area, indicating a larger relative increase in female size than in male size in warmer environmental conditions.

Body Size Reductions in Nonmammalian Eutheriodont Therapsids (Synapsida) during the End-Permian Mass Extinction

The extent to which mass extinctions influence body size evolution in major tetrapod clades is inadequately understood. For example, the ‘Lilliput effect,’ a common feature of mass extinctions, describes a temporary decrease in body sizes of survivor taxa in post-extinction faunas. However, its signature on existing patterns of body size evolution in tetrapods and the persistence of its impacts during post-extinction recoveries are virtually unknown, and rarely compared in both geologic and phylogenetic contexts. Here, I evaluate temporal and phylogenetic distributions of body size in Permo-Triassic therocephalian and cynodont therapsids (eutheriodonts) using a museum collections-based approach and time series model fitting on a regional stratigraphic sequence from the Karoo Basin, South Africa. I further employed rank order correlation tests on global age and clade rank data from an expanded phylogenetic dataset, and performed evolutionary model testing using Brownian (passive diffusion) models. Results support significant size reductions in the immediate aftermath of the end-Permian mass extinction (ca. 252.3 Ma) consistent with some definitions of Lilliput effects. However, this temporal succession reflects a pattern that was underscored largely by Brownian processes and constructive selectivity. Results also support two recent contentions about body size evolution and mass extinctions: 1) active, directional evolution in size traits is rare over macroevolutionary time scales and 2) geologically brief size reductions may be accomplished by the ecological removal of large-bodied species without rapid originations of new small-bodied clades or shifts from long-term evolutionary patterns.

Chapter 17: Gigantism, Dwarfism, and Cope's Rule: “Nothing in Evolution Makes Sense without a Phylogeny”

Body size is of fundamental importance in understanding macroevolutionary patterns, both for extant taxa and for those with a fossil record. In this paper we describe four different kinds of body-size evolution: autapomorphic giantism, autapomorphic nanism, phyletic giantism, and phyletic nanism. The terms giantism and nanism are preferred here rather than the frequently, although incorrectly used equivalents, gigantism and dwarfism, respectively. We assert that without a known phylogeny, it is difficult or impossible to differentiate these four different kinds of body-size evolution. Case examples are presented for two groups: varanid lizards (family Varanidae) and fossil horses (family Equidae).Previous hypotheses of body-size evolution within the Varanidae suggested that there were several cladogenic events in which some groups and isolated species became large. The most recent phylogeny of Varanidae based on mtDNA suggests otherwise. Mapping the known total body lengths onto the phylogeny indicates that varanids were already getting large early in their evolutionary history, with the crown group, Odatria, becoming secondarily small on mainland Australia. Although hypothesized as a giant island varanid, the komodo dragon (Varanus komodoensis) is discovered to be nested within a clade in which the basalmost taxon (V. salvadorii), also endemic to an island, reaches body lengths similar to those of the komodo dragon. Review of the Varanidae suggests that caution should be taken when characterizing taxa as island giants/dwarfs without first reviewing a phylogeny.Fossil horses (family Equidae) are frequently cited in the literature, as well as depicted in museums, as prime examples of Cope's rule, i.e., a gradual trend toward body-size increase over time. Several recent parsimony analyses have resolved many of the phylogenetic interrelationships of North American fossil horses and have elucidated their patterns of body-size evolution. In light of these new analyses, there is no evidence for Cope's rule in fossil horses. In fact, the evolution of large body size occurred multiple times in fossil horses and exemplifies autapomorphic giantism. Body-size decrease, oftentimes considered the exception to Cope's rule, is actually widespread within multiple clades of fossil horses and is characterized by both autapomorphic and phyletic nanism.The result of our analysis suggests that studies of body-size evolution must be intimately tied to a phylogeny before distinct patterns, if any, can be discerned. Cope's rule is not applicable to the two case examples presented herein, calling into question the most frequently cited mode of body size evolution.

Body size of insular carnivores: little support for the island rule.

Large mammals are thought to evolve to be smaller on islands, whereas small mammals grow larger. A negative correlation between relative size of island individuals and body mass is termed the "island rule." Several mechanisms--mainly competitive release, resource limitation, dispersal ability, and lighter predation pressure on islands, as well as a general physiological advantage of modal size--have been advanced to explain this pattern. We measured skulls and teeth of terrestrial members of the order Carnivora in order to analyze patterns of body size evolution between insular populations and their near mainland conspecifics. No correlations were found between the size ratios of insular/mainland carnivore species and body mass. Only little support for the island rule is found when individual populations rather than species are considered. Our data are at odds with those advanced in support of theories of optimal body size. Carnivore size is subjected to a host of selective pressures that do not vary uniformly from place to place. Mass alone cannot account for the patterns in body size of insular carnivores.

Brachyptery and Phyletic Size Increase in Carabidae (Coleoptera)

Phyletic body size increase is surveyed across taxa of Carabidae for which cladistic hypotheses of phylogenetic relationships are available. Patterns of body size evolution are assessed by regression analysis of body length on cladogram position for species-level taxa. Phyletic size increase is significantly more frequent in taxa containing brachypterous species than in taxa comprising exclusively macropterous species. Brachyptery and increase in body size occur principally in groups inhabiting stable, favorable habitats. Macropterous taxa characteristically inhabit less stable environments and do not exhibit phyletic size increase. Brachyptery may permit evolution of larger body size by removing the need for maintaining a thoracic flight apparatus. For island lineages, the historical constraint of small ancestral size of the colonizing species serves as one explanation for the observed patterns of size increase.