Evolution Of Body Size Research Articles

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.

Developmental strategies underlying gigantism and miniaturization in non-avialan theropod dinosaurs.

In amniotes, the predominant developmental strategy underlying body size evolution is thought to be adjustments to the rate of growth rather than its duration. However, most theoretical and experimental studies supporting this axiom focus on pairwise comparisons and/or lack an explicit phylogenetic framework. We present the first large-scale phylogenetic comparative analysis examining developmental strategies underlying the evolution of body size, focusing on non-avialan theropod dinosaurs. We reconstruct ancestral states of growth rate and body mass in a taxonomically rich dataset, finding that contrary to expectations, changes in the rate and duration of growth played nearly equal roles in the evolution of the vast body size disparity present in non-avialan theropods-and perhaps that of amniotes in general.

Largest-known fossil penguin provides insight into the early evolution of sphenisciform body size and flipper anatomy

AbstractRecent fossil discoveries from New Zealand have revealed a remarkably diverse assemblage of Paleocene stem group penguins. Here, we add to this growing record by describing nine new penguin specimens from the late Paleocene (upper Teurian local stage; 55.5–59.5 Ma) Moeraki Formation of the South Island, New Zealand. The largest specimen is assigned to a new species, Kumimanu fordycei n. sp., which may have been the largest penguin ever to have lived. Allometric regressions based on humerus length and humerus proximal width of extant penguins yield mean estimates of a live body mass in the range of 148.0 kg (95% CI: 132.5 kg–165.3 kg) and 159.7 kg (95% CI: 142.6 kg–178.8 kg), respectively, for Kumimanu fordycei. A second new species, Petradyptes stonehousei n. gen. n. sp., is represented by five specimens and was slightly larger than the extant emperor penguin Aptenodytes forsteri. Two small humeri represent an additional smaller unnamed penguin species. Parsimony and Bayesian phylogenetic analyses recover Kumimanu and Petradyptes crownward of the early Paleocene mainland NZ taxa Waimanu and Muriwaimanu, but stemward of the Chatham Island taxon Kupoupou. These analyses differ, however, in the placement of these two taxa relative to Sequiwaimanu, Crossvallia, and Kaiika. The massive size and placement of Kumimanu fordycei close to the root of the penguin tree provide additional support for a scenario in which penguins reached the upper limit of sphenisciform body size very early in their evolutionary history, while still retaining numerous plesiomorphic features of the flipper.UUID: https://zoobank.org/15b1d5b2-a5a0-4aa5-ba0a-8ef3b8461730

Habitat Drives Body Size Evolution in Mustelidae (Mammalia: Carnivora)

Body size of organisms is often associated with physiological demands and habitat structure. Several theories and models have been proposed to explain body size trends across geographical space and evolutionary time. It is proposed that herbivores are larger due to their more voluminous digestive system, allowing a longer retention time of the digested material. Simultaneously, for carnivores, it is expected that the bigger the prey, the larger the predator. Additionally, some body size trends have been attributed to climatic variation across space and habitat structure. Bergmann’s Rule proposes that larger endotherms inhabit colder areas, once a larger body size promotes better heat retention due to reduced surface/volume ratio. Similarly, aquatic endotherms are larger than expected, due to analogous physiological demands to endotherms living in colder environments. Here we tested whether body size of the Mustelidae clade can be explained by diet, habitat structure or environmental temperature. We performed phylogenetic regressions to assess the relationships between body size and the aforementioned predictors in 53 species of Mustelidae. We found that neither diet nor temperature were related to body size evolution. However, habitat was related to body size, with semi aquatic species being larger. Mechanisms involving thermal inertia, predation pressure, better quality resources close to water and bone density are hypotheses that suggest larger body sizes evolution in semi-aquatic vertebrates. We highlight the importance of considering widely accepted ecological traits for large groups, at lower taxonomic levels, in order to expand our understanding of the maintenance of these standards on different scales.

A new diminutive fossil ziphiid from the deep-sea floor off northern Chile and some remarks on the body size evolution and palaeobiogeography of the beaked whales

A new diminutive fossil ziphiid from the deep-sea floor off northern Chile and some remarks on the body size evolution and palaeobiogeography of the beaked whales

Divergent life histories between wild and commercially-sourced Cotesia flavipes (Hymenoptera: Braconidae) parasitizing four species of Diatraea (Lepidoptera: Crambidae)

Moths of the genus Diatraea Guilding (Lepidoptera: Crambidae) are stalk-boring pests of sugarcane throughout the neotropics. In Colombia, the economically important species are D. busckella, D. indigenella, D. saccharalis, and D. tabernella. Augmentative releases of the gregarious endoparasitoid Cotesia flavipes (Cameron) are one tactic used to manage this pest complex. We compared the laboratory performance of two C. flavipes populations, one field-collected, and one commercially-sourced, on all four host species, hypothesizing lower performance of the commercial population on host species other than D. saccharalis due to continuous rearing on this species. Parasitism success did not vary with parasitoid source, but varied among host species, being highest in D. indigenella and lowest in D. tabernella, with other species intermediate. Sex ratio was female-biased, averaging 0.635, and did not vary with parasitoid source or host species. Wild wasps developed more slowly than commercial wasps on all hosts, being slowest on D. tabernella, whereas commercial wasps were slowest on D. busckella. Both parasitoid populations produced their largest broods in D. indigenella, but commercial wasps produced smaller broods than wild wasps in D. busckella and D. tabernella, and substantially lower weight gain of host larvae post-parasitism, suggesting impaired host regulation ability. In all host species, wild wasps produced larger female progeny, based on wing area, than commercial wasps. When all metrics of parasitoid performance (fitness) were combined into a single index of host suitability, D. indigenella was the most suitable host for both parasitoid populations. Both parasitoid sources had similar performance on D. saccharalis, the host used to rear the commercial population, whereas wild wasps performed better on all other Diatraea species. The inadvertant consequences of artificial selection in mass-reared cultures of gregarious endoparasitoids are discussed, specifically the evolution of faster development and smaller body size.

Functional and sex-specific dynamics of ectoparasite size evolution in marine isopod–fish interactions: Harrison’s rule and increasing variance

Harrison's rule, a pattern predicting that the body size of parasites correlates positively with the size of their hosts, is well-supported. However, its interaction with highly distinct "guilds" of closely related parasites warrants further exploration. The increasing variance hypothesis predicts that the variance in parasite size should also increase with the size of their hosts. Though untested, in parasite taxa with differential sex-dependent pressures on body size, this relationship should also be divergent across sexes due to differential size-fecundity relationships. We compiled global data on sequentially hermaphroditic isopods (Isopoda: Cymothoidae) parasitic on fish from published literature. With a data set comprising of 204 marine cymothoid species and their hosts, we used Bayesian hierarchical models to primarily test (1) Harrison's rule and its scaling across three functionally distinct guilds (mouth, gill, external); (2) the increasing variance hypothesis and sex-specific patterns. Our results revealed a strong positive association between parasite and host body sizes, but with uniform scaling across guilds. Host size exerted divergent, sex-specific effects on the relative intraspecific variation in parasite size, where this association was positive in males and absent in females. Here, we show that Harrison's rule is independent of guild, suggesting body size evolution across all cymothoids is equally underpinned by the size of their hosts. The sex-specificity of the increasing variance hypothesis can be explained by female fecundity being tightly bound to body size, whereas the dependency of reproductive success on size is inherently more relaxed in males.

Evolutionary loss of complexity in animal signals: cause and consequence.

We identified hypotheses for the cause and consequences of the loss of complexity in animal signals and tested these using a genus of visually communicating lizards, the Southeast Asian Draco lizards. Males of some species have lost the headbob component from their display, which is otherwise central to the communication of this genus. These males instead display a large, colorful dewlap to defend territories and attract mates. This dewlap initially evolved to augment the headbob component of the display, but has become the exclusive system of communication. We tested whether the loss of headbobs was caused by relaxed selection, habitat-dependent constraints, or size-specific energetic constraints on display movement. We then examined whether the consequences of this loss have been mitigated by increased signaling effort or complexity in the color of the dewlap. It appears the increased cost of display movement resulting from the evolution of large body size might have contributed to the loss of headbobs and has been somewhat compensated for by the evolution of greater complexity in dewlap color. However, this evolutionary shift is unlikely to have maintained the complexity previously present in the communication system, resulting in an apparent detrimental loss of information potential.

Way to big cats: Directional selection in body size evolution in living felids

Way to big cats: Directional selection in body size evolution in living felids

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.

Modeling the Evolution of Rates of Continuous Trait Evolution.

Rates of phenotypic evolution vary markedly across the tree of life, from the accelerated evolution apparent in adaptive radiations to the remarkable evolutionary stasis exhibited by so-called "living fossils". Such rate variation has important consequences for large-scale evolutionary dynamics, generating vast disparities in phenotypic diversity across space, time, and taxa. Despite this, most methods for estimating trait evolution rates assume rates vary deterministically with respect to some variable of interest or change infrequently during a clade's history. These assumptions may cause underfitting of trait evolution models and mislead hypothesis testing. Here, we develop a new trait evolution model that allows rates to vary gradually and stochastically across a clade. Further, we extend this model to accommodate generally decreasing or increasing rates over time, allowing for flexible modeling of "early/late bursts" of trait evolution. We implement a Bayesian method, termed "evolving rates" (evorates for short), to efficiently fit this model to comparative data. Through simulation, we demonstrate that evorates can reliably infer both how and in which lineages trait evolution rates varied during a clade's history. We apply this method to body size evolution in cetaceans, recovering substantial support for an overall slowdown in body size evolution over time with recent bursts among some oceanic dolphins and relative stasis among beaked whales of the genus Mesoplodon. These results unify and expand on previous research, demonstrating the empirical utility of evorates.

Quaternary megafauna extinctions altered body size distribution in tortoises.

The late Quaternary is characterized by the extinction of many terrestrial megafauna, which included tortoises (Family: Testudinidae). However, limited information is available on how extinction shaped the phenotype of surviving taxa. Here, based on a global dataset of straight carapace length, we investigate the temporal variation, spatial distribution and evolution of tortoise body size over the past 23 million years, thereby capturing the effects of Quaternary extinctions in this clade. We found a significant change in body size distribution characterized by a reduction of both mean body size and maximum body size of extant tortoises relative to fossil taxa. This reduction of body size occurred earlier in mainland (Early Pleistocene 2.588-0.781 Ma) than in island tortoises (Late Pleistocene/Holocene 0.126-0 Ma). Despite contrasting body size patterns between fossil and extant taxa on a spatial scale, tortoise body size showed limited variation over time until this decline. Body size is a fundamental functional trait determining many aspects of species ecologies, with large tortoises playing key roles as ecosystem engineers. As such, the transition from larger sized to smaller sized classes indicated by our findings likely resulted in the homogenization of tortoises' ecological functions and diminished the role of tortoises in structuring the vegetation community.

More and bigger lizards reside on islands with more resources

AbstractWhile global patterns in body size evolution in island vertebrates have been described extensively, the ecological processes that generate these patterns are not well understood. Here we used variation among lizard populations occupying an archipelago to test hypotheses about body size evolution. We examined 35 populations of Aegean wall lizards (Podarcis erhardii, Lacertidae), a species widely distributed across the Balkan mainland and hundreds of Aegean islands. We evaluated measures of resource availability (island area and seabird density), intraspecific competition (lizard abundance) and predation risk (presence of rats, carnivorous mammals, vipers, and birds of prey) as possible factors affecting lizard body size. Lizard body size increased with island size overall, as well as with seabird colony density, suggesting a role for increased food resources and especially seabird subsidies in the evolution of body size. Lizards were larger where lizard population density was higher, suggesting a possible role for intraspecific competition in the evolution of body size. In our sample, rats, carnivorous mammals, and vipers did not have obvious effects on lizard body size, and lizards were smaller on islands with resident birds of prey. Males were larger than females on average, yet sexual dimorphism did not vary consistently with measures of resource availability and competition. Overall, our results suggest that local resource levels predict population density and body size in these lizards, and that nesting seabirds in particular can substantially affect lizard body size.

On the estimation of body mass in temnospondyls: a case study using the large‐bodied Eryops and Paracyclotosaurus

AbstractTemnospondyli are a morphologically varied and ecologically diverse clade of tetrapods that survived for over 200 million years. The body mass of temnospondyls is a key variable in inferring their ecological, physiological and biomechanical attributes. However, estimating the body mass of these extinct creatures has proven difficult because the group has no extant descendants. Here we apply a wide range of body mass estimation techniques developed for tetrapods to the iconic temnospondyls Paracyclotosaurus davidi and Eryops megacephalus. These same methods are also applied to a collection of extant organisms that serve as ecological and morphological analogues. These include the giant salamanders Andrias japonicus and Andrias davidianus, the tiger salamander Ambystoma tigrinum, the California newt Taricha torosa and the saltwater crocodile, Crocodylus porosus. We find that several methods can provide accurate mass estimations across this range of living taxa, suggesting their suitability for estimating the body masses of temnospondyls. Based on this, we estimate the mass of Paracyclotosaurus to have been between 159 and 365 kg, and that of Eryops between 102 and 222 kg. These findings provide a basis for examining body size evolution in this clade across their entire temporal span.

Ecological and evolutionary trends of body size in Pristimantis frogs, the world's most diverse vertebrate genus

Body size is a key organismal trait. However, the environmental and evolutionary factors that drive body size patterns at the interspecific level remain unclear. Here, we explored these relationships between phenotype-environment using neotropical frogs of Pristimantis, the world’s most diverse vertebrate genus. We analyzed: (a) whether this group follows the Rensch’s rule, a trend of sexual size dimorphism (SSD) to increase with size when males are the larger sex; (b) whether environmental constraints have influenced body size variation; and (c) how the rates of body size evolution have varied over time. Analyses were based on two information sources, the first one including body sizes of ~ 85% (495 species) of known species in the genus, and a second one incorporating molecular phylogenetic information for 257 species. Our results showed that all Pristimantis species exhibited marked SSD but did not follow Rensch’s rule. We found that the models that best explained body size in males, females, and SSD contained environmental variations in temperature, precipitation, and elevation as predictors. In turn, body size has evolved toward an optimum, with a decelerating rate of evolution differentiated between the large Pristimantis clades.

Slow and steady wins the race: Diversification rate is independent from body size and lifestyle in Malagasy skinks (Squamata: Scincidae: Scincinae)

Most of the unique and diverse vertebrate fauna that inhabits Madagascar derives from in situ diversification from colonisers that reached this continental island through overseas dispersal. The endemic Malagasy Scincinae lizards are amongst the most species-rich squamate groups on the island. They colonised all bioclimatic zones and display many ecomorphological adaptations to a fossorial (burrowing) lifestyle. Here we propose a new phylogenetic hypothesis for their diversification based on the largest taxon sampling so far compiled for this group. We estimated divergence times and investigated several aspects of their diversification (diversification rate, body size and fossorial lifestyle evolution, and biogeography). We found that diversification rate was constant throughout most of the evolutionary history of the group, but decreased over the last 6–4 million years and independently from body size and fossorial lifestyle evolution. Fossoriality has evolved from fully quadrupedal ancestors at least five times independently, which demonstrates that even complex morphological syndromes – in this case involving traits such as limb regression, body elongation, modification of cephalic scalation, depigmentation, and eyes and ear-opening regression – can evolve repeatedly and independently given enough time and eco-evolutionary advantages. Initial diversification of the group likely occurred in forests, and the divergence of sand-swimmer genera around 20 Ma appears linked to a period of aridification. Our results show that the large phenotypic variability of Malagasy Scincinae has not influenced diversification rate and that their rich species diversity results from a constant accumulation of lineages through time. By compiling large geographic and trait-related datasets together with the computation of a new time tree for the group, our study contributes important insights on the diversification of Malagasy vertebrates.

Mammalian body size evolution was shaped by habitat transitions as an indirect effect of climate change

AbstractAimBody size evolution has long been hypothesized to have been driven by factors linked to climate change, but the specific mechanisms are difficult to disentangle due to the wide range of functional traits that covary with body size. In this study, we investigated the impact of regional habitat changes as a potential indirect effect of climate change on body size evolution.LocationEurope and North America.Time periodThe Neogene (~23–2 million years ago).Major taxaFive orders of terrestrial mammals: Artiodactyla, Carnivora, Perissodactyla, Proboscidea and Primates.MethodsWe compared the two continental faunas, which have exceptional fossil records of terrestrial mammals and underwent different processes of habitat transition during the Neogene. Using Bayesian multilevel regression models, we assessed the variation in the temporal dynamics of body size diversity among ecographic groups, defined by their continent of occurrence and dietary preference.ResultsModel comparisons unanimously supported a combined effect of diet and continent on all metrics of body size frequency distributions, rejecting the shared energetic advantage of larger bodies in colder climates as a dominant mechanism of body size evolution. Rather, the diet‐specific dynamics on each continent pinpointed an indirect effect of climate change – change in habitat availability, and thus the resource landscape as a key driver of mammalian evolution.Main conclusionsOur study highlights dietary preference as a mechanistic link between mammalian evolution and habitat transition mediating an indirect climate‐change effect and demonstrates the complexity of climatic influence on biodiversity. Our findings suggest that the intensified habitat modification today likely poses a bigger threat than climate change in itself to living mammals, and perhaps all endotherms.

Size-dependent Scaling of Stingless Bee Flight Metabolism Reveals an Energetic Benefit to Small Body Size.

Understanding the effect of body size on flight costs is critical for development of models of aerodynamics and animal energetics. Prior scaling studies that have shown that flight costs scale hypometrically have focused primarily on larger (> 100 mg) insects and birds, but most flying species are smaller. We studied the flight physiology of thirteen stingless bee species over a large range of body sizes (1-115 mg). Metabolic rate during hovering scaled hypermetrically (scaling slope=2.11). Larger bees had warm thoraxes while small bees were nearly ecothermic; however, even controlling for body temperature variation, flight metabolic rate scaled hypermetrically across this clade. Despite having a lower mass-specific metabolic rate during flight, smaller bees could carry the same proportional load. Wingbeat frequency did not vary with body size, in contrast to most studies that find wingbeat frequency increases as body size decreases. Smaller stingless bees have greater relative forewing surface area which may help them reduce the energy requirements needed to fly. Further, we hypothesize that the relatively larger heads of smaller species may change their body pitch in flight. Synthesizing across all flying insects, we demonstrate that the scaling of flight metabolic rate changes from hypermetric to hypometric at approximately 58 mg body mass with hypermetic scaling below (slope=1.2) and hypometric scaling (slope=0.67) above 58 mg in body mass. The reduced cost of flight likely provides selective advantages for the evolution of small body size in insects. The biphasic scaling of flight metabolic rates and wingbeat frequencies in insects supports the hypothesis that the scaling of metabolic rate is closely related to the power requirements of locomotion and cycle frequencies.

Density dependent environments can select for extremes of body size

Body size variation is an enigma. We do not understand why species achieve the sizes they do, and this means we also do not understand the circumstances under which gigantism or dwarfism is selected. We develop size-structured integral projection models to explore evolution of body size and life history speed. We make few assumptions and keep models simple: all functions remain constant across models except for the one that describes development of body size with age. We set sexual maturity to occur when size attains 80% of the asymptotic size, which is typical of a large mammal, and allow negative density dependence to only affect either reproduction or juvenile survival. Fitness -- the quantity that is maximized by adaptive evolution -- is carrying capacity in our models, and we are consequently interested in how it changes with size at sexual maturity, and how this association varies with development rate. The simple models generate complex dynamics while providing insight into the circumstances when extremes of body size evolve. The direction of selection leading to either gigantism or dwarfism crucially depends on the proportion of the population that is sexually mature, which in turn depends on how the development function determines the survivorship schedule. The developmental trajectories consequently interact with size-specific survival or reproductive rates to determine the best life history and the optimal body size emerges from that interaction. These dynamics result in trade-offs between different components of the life history, with the form of the trade-off that emerges depending upon where in the life history density dependence operates most strongly. Empirical application of the approach we develop has potential to help explain the enigma of body size variation across the tree of life.

The oldest semi-aquatic beaver in the world and a new hypothesis for the evolution of locomotion in Castoridae.

The North American rodent fossil record includes hundreds of species representing both an incredible taxonomic diversity and great ecological disparity. Although it is during the Oligocene that taxonomic diversity first peaks, it is not until the Miocene, almost 10 Myr later, that many ecologies, particularly locomotory ecologies, are recorded. Here, I present a new Oligocene-aged species of beaver from Montana, Microtheriomys articulaquaticus sp. nov., which represents the oldest semi-aquatic rodent in North America and the oldest amphibious beaver in the world, pushing the advent of semi-aquatic ecology in beavers by 7 Myr. I also provide morphological data supporting a terrestrial ecology for the sister taxon to Castoridae. Together with existing data, these findings lead to a new hypothesis for the evolutionary ecology of castorids whereby swimming was exapted from burrowing during the Oligocene. This evolution of semi-aquatic locomotion may have taken place in North America instead of Eurasia. It started in small beavers with gigantism achieved only much later. Indeed, body size evolution in castoroids follows a directional drift. Beavers obey Cope's rule, a selection for larger size over time that appears associated with semi-aquatic ecology and may well explain their low modern diversity.