Evolutionary Changes In Body Size Research Articles

Variability in vertebral numbers does not contribute to sexual size dimorphism, interspecific variability, or phenotypic plasticity in body size in geckos (Squamata: Gekkota: Paroedura).

Body size is a fundamental trait correlated with nearly every aspect of animal life. It is influenced by numerous genetic and non-genetic factors. Despite its central importance, proximate mechanisms of intra- and interspecific variability in body size are still not well understood even in such a largely studied group as reptiles. For our study, we concentrated on the gecko species Paroedura picta. We investigated whether differences in sexual size dimorphism and in final and asymptotic snout-vent length (induced by a range of incubation and rearing temperatures) are correlated with differences in the number of presacral vertebrae. Moreover, we tested whether changes in this number were associated with evolutionary changes in sexual size dimorphism and body size in the genus Paroedura. We found that the variation in the number of presacral vertebrae is very limited both intra- and interspecifically, ranging between 26 and 28 vertebrae with most individuals possessing the modal number of 27. We conclude that changes in the number of vertebrae do not contribute to developmental plasticity or evolutionary changes in body size nor, in contrast to some other squamate lineages, to sexual size dimorphism.

Cooperative interactions within the family enhance the capacity for evolutionary change in body size.

Classical models of evolution seldom predict the rate at which populations evolve in the wild. One explanation is that the social environment affects how traits change in response to natural selection. Here, we determine how social interactions between parents and offspring, and among larvae, influence the response to experimental selection on adult size. Our experiments focus on burying beetles (Nicrophorus vespilloides), whose larvae develop within a carrion nest. Some broods exclusively self-feed on the carrion while others are also fed by their parents. We found populations responded to selection for larger adults but only when parents cared for their offspring. We also found populations responded to selection for smaller adults too, but only by removing parents and causing larval interactions to exert more influence on eventual adult size. Comparative analyses revealed a similar pattern: evolutionary increases in species size within the genus Nicrophorus are associated with the obligate provision of care. Synthesising our results with previous studies, we suggest that cooperative social environments enhance the response to selection whereas excessive conflict can prevent further directional selection.

Bone microstructure and the evolution of growth patterns in Permo-Triassic therocephalians (Amniota, Therapsida) of South Africa.

Therocephalians were a speciose clade of nonmammalian therapsids whose ecological diversity and survivorship of the end-Permian mass extinction offer the potential to investigate the evolution of growth patterns across the clade and their underlying influences on post-extinction body size reductions, or ‘Lilliput effects’. We present a phylogenetic survey of limb bone histology and growth patterns in therocephalians from the Middle Permian through Middle Triassic of the Karoo Basin, South Africa. Histologic sections were prepared from 80 limb bones representing 11 genera of therocephalians. Histologic indicators of skeletal growth, including cortical vascularity (%CV) and mean primary osteon diameters (POD), were evaluated in a phylogenetic framework and assessed for correlations with other biologically significant variables (e.g., size and robusticity). Changes in %CV and POD correlated strongly with evolutionary changes in body size (i.e., smaller-bodied descendants tended to have lower %CV than their larger-bodied ancestors across the tree). Bone wall thickness tended to be high in early therocephalians and lower in the gracile-limbed baurioids, but showed no general correlation with cross-sectional area or degree of vascularity (and, thus, growth). Clade-level patterns, however, deviated from previously studied within-lineage patterns. For example, Moschorhinus, one of few therapsid genera to have survived the extinction boundary, demonstrated higher %CV in the Triassic than in the Permian despite its smaller size in the extinction aftermath. Results support a synergistic model of size reductions for Triassic therocephalians, influenced both by within-lineage heterochronic shifts in survivor taxa (as reported in Moschorhinus and the dicynodont Lystrosaurus) and phylogenetically inferred survival of small-bodied taxa that had evolved short growth durations (e.g., baurioids). These findings mirror the multi-causal Lilliput patterns described in marine faunas, but contrast with skeletochronologic studies that suggest slow, prolonged shell secretion over several years in marine benthos. Applications of phylogenetic comparative methods to new histologic data will continue to improve our understanding of the evolutionary dynamics of growth and body size shifts during mass extinctions and recoveries.

The Changing Face of Evolutionary Thinking

The Changing Face of Evolutionary Thinking

Multiple determinants of whole and regional brain volume among terrestrial carnivorans.

Mammalian brain volumes vary considerably, even after controlling for body size. Although several hypotheses have been proposed to explain this variation, most research in mammals on the evolution of encephalization has focused on primates, leaving the generality of these explanations uncertain. Furthermore, much research still addresses only one hypothesis at a time, despite the demonstrated importance of considering multiple factors simultaneously. We used phylogenetic comparative methods to investigate simultaneously the importance of several factors previously hypothesized to be important in neural evolution among mammalian carnivores, including social complexity, forelimb use, home range size, diet, life history, phylogeny, and recent evolutionary changes in body size. We also tested hypotheses suggesting roles for these variables in determining the relative volume of four brain regions measured using computed tomography. Our data suggest that, in contrast to brain size in primates, carnivoran brain size may lag behind body size over evolutionary time. Moreover, carnivore species that primarily consume vertebrates have the largest brains. Although we found no support for a role of social complexity in overall encephalization, relative cerebrum volume correlated positively with sociality. Finally, our results support negative relationships among different brain regions after accounting for overall endocranial volume, suggesting that increased size of one brain regions is often accompanied by reduced size in other regions rather than overall brain expansion.

EVOLUTION OF BODY SIZE IN THE MAP TURTLES AND SAWBACKS (EMYDIDAE: DEIROCHELYINAE: GRAPTEMYS)

Map turtles and sawbacks (Emydidae: Deirochelyinae: Graptemys) are a diverse group of turtles that are of ecological interest due to their diversity in trophic morphology, particularly in females, and their extreme sexual size dimorphism (with females larger). I used comparative analyses (independent contrasts in correlation analyses and GLM analyses) to examine hypotheses regarding the evolution of body size in the genus. Evolutionary changes in body size of both males and females were positively related to inferred shifts in latitude. Trophic morphology (relative head width, expressed either as a continuous or a discrete variable) was not an additive source of variation in male body size, but was for female body size, primarily due to the large body sizes exhibited by the megacephalic southern clade (G. pulchra, G. ernsti, G. gibbonsi, and G. barbouri). Status as allopatric or sympatric to other species of Graptemys was not an additive source of variation in female body size. These results argue against the hypothesis that character displacement of body size in females was important in the radiation of map turtle and sawback species and instead suggest a functional relationship whereby degree of molluscivory in females covaries with body size. Sexual size dimorphism was found to increase with body size of females, also due primarily to the large females of the megacephalic clade; this result means Graptemys is an exception to Rensch's Rule. In a latitude-corrected analysis of body size evolution in deirochelyine turtles, the exceptional degree of sexual size dimorphism in Graptemys appears to result more from reduction in male size than increase in female size. Decreased male size may indicate relaxed selection for large body size in Graptemys males as a consequence of the fact that they rarely leave the water for terrestrial excursions, because selection for larger male body size in other deirochelyines may be mediated by (a) predation pressure imposed by terrestrial predators, (b) enhancement of overland mobility for mate searching, and (c) the need for resistance to desiccation during overland excursions. Alternatively, male body size reduction in Graptemys may be explained by energetic requirements of searching for mates in the fluvial environment or unknown differences in social structure among deirochelyine turtles.

Developmental basis of limb length in rodents: evidence for multiple divisions of labor in mechanisms of endochondral bone growth

Mammals are remarkably diverse in limb lengths and proportions, but the number and kind of developmental mechanisms that contribute to length differences between limb bones remain largely unknown. Intra- and interspecific differences in bone length could result from variations in the cellular processes of endochondral bone growth, creating differences in rates of chondrocyte proliferation or hypertrophy, variation in the shape and size of chondrocytes, differences in the number of chondrocytes in precursor populations and throughout growth, or a combination of these mechanisms. To address these questions, this study compared cellular mechanisms of endochondral bone growth in cross-sectional ontogenetic series of the appendicular skeleton of two rodent species: the mouse (Mus musculus) and Mongolian gerbil (Meriones unguiculatus). Results indicate that multiple cellular processes of endochondral bone growth contribute to phenotypic differences in limb bone length. The data also suggest that separate developmental processes contribute to intraspecific length differences in proximal versus distal limb bones, and that these proximo-distal mechanisms are distinct from mechanisms that contribute to interspecific differences in limb bone length related to body size. These developmental "divisions of labor" are hypothesized to be important features of vertebrate limb development that allow (1) morphology in the autopods to evolve independently of the proximal limb skeleton, and (2) adaptive changes in limb proportions related to locomotion to evolve independently of evolutionary changes in body size.

MATERNAL BODY SIZE AS AN EVOLUTIONARY CONSTRAINT ON EGG SIZE IN A BUTTERFLY

Genetic and developmental constraints have often been invoked to explain patterns of existing morphologies. Yet, empirical tests addressing this issue directly are still scarce. We here set out to investigate the importance of maternal body size as an evolutionary constraint on egg size in the tropical butterfly Bicyclus anynana, employing an artificial two-trait selection experiment on simultaneous changes in body and egg size (synergistic and antagonistic selection). Selection on maternal body size and egg size was successful in both the synergistic and the antagonistic selection direction. Yet, responses to selection and realized heritabilities varied across selection regimes: the most extreme values for pupal mass were found in the synergistic selection directions, whereas in the antagonistic selection direction realized heritabilities were low and nonsignificant in three of four cases. In contrast, for egg size the highest values were obtained in the lines selected for low pupal mass. Thus, selection on body size yielded a stronger correlated response in egg size than vice versa, which is likely to bias (i.e., constrain), if weakly, evolutionary change in body size. However, it seems questionable whether this will prevent evolution toward novel phenotypes, given enough time and that natural selection is strong. Correlated responses to selection were overall weak. Egg and larval development times tended to be associated with changes in maternal size, whereas variation in pupal development times weakly tended to follow variation in egg size. Lifetime fecundity was similar across selection regimes, except for females simultaneously selected for large body mass and small egg size, exhibiting increased fecundity. Multiple regressions showed that lifetime fecundity and concomitantly reproductive investment were primarily determined by longevity, as expected for an income breeder, whereas egg size was primarily determined by pupal mass. Evidence for a phenotypic trade-off between egg size and number was weak.

Dissociation of somatic growth from segmentation drives gigantism in snakes

Body size is significantly correlated with number of vertebrae (pleomerism) in multiple vertebrate lineages, indicating that change in number of body segments produced during somitogenesis is an important factor in evolutionary change in body size, but the role of segmentation in the evolution of extreme sizes, including gigantism, has not been examined. We explored the relationship between body size and vertebral count in basal snakes that exhibit gigantism. Boids, pythonids and the typhlopid genera, Typhlops and Rhinotyphlops, possess a positive relationship between body size and vertebral count, confirming the importance of pleomerism; however, giant taxa possessed fewer than expected vertebrae, indicating that a separate process underlies the evolution of gigantism in snakes. The lack of correlation between body size and vertebral number in giant taxa demonstrates dissociation of segment production in early development from somatic growth during maturation, indicating that gigantism is achieved by modifying development at a different stage from that normally selected for changes in body size.

Life history evolution in cichlids 2: directional evolution of the trade-off between egg number and egg size

The negative relationship between offspring number and offspring size provides a classic example of the role of trade-offs in life history theory. However, the evolutionary transitions in egg size and clutch size that have produced this negative relationship are still largely unknown. Since body size may affect both of these traits, it would be helpful to understand how evolutionary changes in body size may have facilitated or constrained shifts in clutch and egg size. By using comparative methods with a database of life histories and a phylogeny of 222 genera of cichlid fishes, we investigated the order of evolutionary transitions in these traits in relation to each other. We found that the ancestral large-bodied cichlids first increased egg size, followed by a decrease in both body size and clutch size resulting in the common current combination of a small-bodied cichlid with a small clutch of large eggs. Furthermore, lineages that deviated from the negative relationship between clutch and egg size underwent different transitions in these traits according to their body size (large bodied genera have moved towards the large clutch/small egg end of the continuum and small bodied genera towards the small clutch/large egg end of the continuum) to reach the negative relationship between clutch size and egg size. Our results show that body size is highly important in shaping the negative relationship between clutch size and egg size.

Evolution of conspicuous colouration, body size and gregariousness: a comparative analysis of lepidopteran larvae

Protective colouration in animals includes camouflage (i.e., crypsis), that decreases the risk of detection, and conspicuous colouration, which is often used in combination with chemical defences to deter predators from attacking. Experiments have shown that the efficacy of conspicuous colouration increases with increasing size of pattern elements and larger body size. Prey species that have acquired avoidance inducing colouration therefore may be exposed to selection for larger body size, and such colouration may more easily evolve in large than in small prey species. Here we test for a difference in body size between species with different colouration modes and perform a comparative analysis based on phylogenetically independent contrasts to examine if evolutionary shifts in colour pattern have been associated with evolutionary changes in body size, using data for 578 species of moths. Larval body size did not differ between species with signalling and non-signalling larvae, and results from the comparative analysis suggest that these two traits have not evolved in parallel. The lack of association between evolutionary changes in colouration and body size may reflect a confounding influence of lifestyle, because evolutionary shifts from solitary to group-living larvae were associated with decreased larval body length and adult wing span. Because evolutionary changes in larval body size were associated with evolutionary changes in adult wing span the predicted association between colouration and size may have been confounded also by conflicting selection on body size in larvae and adults.

CORRELATED EVOLUTION OF CONSPICUOUS COLORATION AND BODY SIZE IN POISON FROGS (DENDROBATIDAE)

Conspicuous coloration is often used in combination with chemical defenses to deter predators from attacking. Experimental studies have shown that the avoidance inducing effect of conspicuous prey coloration increases with increasing size of pattern elements and with increasing body size. Here we use a comparative approach to test the prediction from these findings, namely that conspicuous coloration will evolve in tandem with body size. In our analysis, we use a previously published mitochondrial DNA-based phylogeny and comparative analysis of independent contrasts to examine if evolutionary shifts in color pattern have been associated with evolutionary changes in body size in aposematic poison frogs (Anura: Dendrobatidae). Information on body size (snout to vent length) and coloration were obtained from the literature. Two different measures of conspicuousness were used, one based on rankings by human observers and the other based on computer analysis of digitized photographs. The results from comparative analyses using either measure of coloration indicated that avoidance inducing coloration and body size have evolved in concert in poison frogs. Results from reconstruction of character change further indicate that the correlated evolution of size and coloration has involved changes in both directions within each of the different clades of the phylogenetic tree. This finding is consistent with the hypothesis that selection imposed by visually guided predators has promoted the evolution of larger body size in species with conspicuous coloration, or enhanced evolution of conspicuous coloration in larger species.

An ecomorphological model of the initial hominid dispersal from Africa.

We use new data on the timing and extent of the early Pleistocene dispersal of Homo erectus to estimate diffusion coefficients of early Homo from Africa. These diffusion coefficients indicate more rapid and efficient dispersals than those calculated for fossil Macaca sp., Theropithecus darti, and Mesopithecus pentelicus. Increases in home range size associated with changes in ecology, hominid body size, and possibly foraging strategy may underlay these differences in dispersal efficiency. Ecological data for extant primates and human foragers indicate a close relationship between body size, home range size, and diet quality. These data predict that evolutionary changes in body size and foraging behavior would have produced a 10-fold increase in the home range size of H. erectus compared with that of the australopithecines. These two independent datasets provide a means of quantifying aspects of the dispersal of early Homo and suggest that rapid rates of dispersal appear to have been promoted by changes in foraging strategy and body size in H. erectus facilitated by changes in ecosystem structure during the Plio-Pleistocene.

Evidence for parallel ecological speciation in scincid lizards of the Eumeces skiltonianus species group (Squamata: Scincidae).

We identify instances of parallel morphological evolution in North American scincid lizards of the Eumeces skiltonianus species group and provide evidence that this system is consistent with a model of ecological speciation. The group consists of three putative species divided among two morphotypes, the small-bodied and striped E. skiltonianus and E. lagunensis versus the large-bodied and typically uniform-colored E. gilberti. Members of the group pass through markedly similar phenotypic stages during early development, but differ with respect to where terminal morphology occurs along the developmental sequence. The morphotypes also differ in habitat preference, with the large-bodied gilberti form generally inhabiting lower elevations and drier environments than the smaller, striped morphs. We inferred the phylogenetic relationships of 53 skiltonianus group populations using mtDNA sequence data from the ND4 protein-coding gene and three flanking tRNAs (900 bp total). Sampling encompassed nearly the entire geographic range of the group, and all currently recognized species and subspecies were included. Our results provide strong evidence for parallel origins of three clades characterized by the gilberti morphotype, two of which are nested within the more geographically widespread E. skiltonianus. Eumeces lagunensis was also nested among populations of E. skiltonianus. Comparative analyses using independent contrasts show that evolutionary changes in body size are correlated with differences in adult color pattern. The independently derived association of gilberti morphology with warm, arid environments suggests that phenotypic divergence is the result of adaptation to contrasting selection regimes. We provide evidence that body size was likely the target of natural selection, and that divergences in color pattern and mate recognition are probable secondary consequences of evolving large body size.

EVIDENCE FOR PARALLEL ECOLOGICAL SPECIATION IN SCINCID LIZARDS OF THE EUMECES SKILTONIANUS SPECIES GROUP (SQUAMATA: SCINCIDAE)

We identify instances of parallel morphological evolution in North American scincid lizards of the Eumeces skiltonianus species group and provide evidence that this system is consistent with a model of ecological speciation. The group consists of three putative species divided among two morphotypes, the small-bodied and striped E. skiltonianus and E. lagunensis versus the large-bodied and typically uniform-colored E. gilberti. Members of the group pass through markedly similar phenotypic stages during early development, but differ with respect to where terminal morphology occurs along the developmental sequence. The morphotypes also differ in habitat preference, with the large-bodied gilberti form generally inhabiting lower elevations and drier environments than the smaller, striped morphs. We inferred the phylogenetic relationships of 53 skiltonianus group populations using mtDNA sequence data from the ND4 protein-coding gene and three flanking tRNAs (900 bp total). Sampling encompassed nearly the entire geographic range of the group, and all currently recognized species and subspecies were included. Our results provide strong evidence for parallel origins of three clades characterized by the gilberti morphotype, two of which are nested within the more geographically widespread E. skiltonianus. Eumeces lagunensis was also nested among populations of E. skiltonianus. Comparative analyses using independent contrasts show that evolutionary changes in body size are correlated with differences in adult color pattern. The independently derived association of gilberti morphology with warm, arid environments suggests that phenotypic divergence is the result of adaptation to contrasting selection regimes. We provide evidence that body size was likely the target of natural selection, and that divergences in color pattern and mate recognition are probable secondary consequences of evolving large body size.

The developmental and physiological basis of body size evolution in an insect.

The evolution of body size is a dominant feature of animal evolution. However, little is known about how the underlying developmental mechanisms that determine size change as body size evolves. Here we report on a case of body size evolution in the tobacco hornworm Manduca sexta that occurred over a period of nearly 30 years. We take advantage of an extensive series of physiological studies performed in the early 1970s that established the parameters that regulate body size in this species and compare their values with those of modern individuals that are descendants of the same colony. We show that three of the five processes that determine adult body size changed during this period, while two remained constant. Changes in these three developmental processes completely account for the observed evolutionary change in body size.

A hierarchical pattern of limiting factors helps explain variation in home range size

Home range size characterizes the interplay between an organism and its environment. Determinants of home range size can be intrinsic or extrinsic to the individual but all factors relate along a hierarchical pattern according to spatial and temporal scale. Determinants of home range size at species and population levels result from relatively slow processes, such as evolutionary changes in body size or global changes in climate. Range determinants at the lower level of individuals, however, can change at a relatively fast rate as they result from more rapid processes, such as the seasonal production of food or annual changes in predation rates. Not only do higher scales constrain those below but also lower level processes combine to affect higher scales. Further, correlates of home range size can differ among scales. To incorporate the possible findings of different patterns at different temporal and spatial scales we recommend using a comparative approach to complement controlled manipulative experiments.

TESTING FOR UNEQUAL AMOUNTS OF EVOLUTION IN A CONTINUOUS CHARACTER ON DIFFERENT BRANCHES OF A PHYLOGENETIC TREE USING LINEAR AND SQUARED-CHANGE PARSIMONY: AN EXAMPLE USING LESSER ANTILLEAN ANOLIS LIZARDS.

Although a large body of work investigating tests of correlated evolution of two continuous characters exists, hypotheses such as character displacement are really tests of whether substantial evolutionary change has occurred on a particular branch or branches of the phylogenetic tree. In this study, we present a methodology for testing such a hypothesis using ancestral character state reconstruction and simulation. Furthermore, we suggest how to investigate the robustness of the hypothesis test by varying the reconstruction methods or simulation parameters. As a case study, we tested a hypothesis of character displacement in body size of Caribbean Anolis lizards. We compared squared-change, weighted squared-change, and linear parsimony reconstruction methods, gradual Brownian motion and speciational models of evolution, and several resolution methods for linear parsimony. We used ancestor reconstruction methods to infer the amount of body size evolution, and tested whether evolutionary change in body size was greater on branches of the phylogenetic tree in which a transition from occupying a single-species island to a two-species island occurred. Simulations were used to generate null distributions of reconstructed body size change. The hypothesis of character displacement was tested using Wilcoxon Rank-Sums. When tested against simulated null distributions, all of the reconstruction methods resulted in more significant P-values than when standard statistical tables were used. These results confirm that P-values for tests using ancestor reconstruction methods should be assessed via simulation rather than from standard statistical tables. Linear parsimony can produce an infinite number of most parsimonious reconstructions in continuous characters. We present an example of assessing the robustness of our statistical test by exploring the sample space of possible resolutions. We compare ACCTRAN and DELTRAN resolutions of ambiguous character reconstructions in linear parsimony to the most and least conservative resolutions for our particular hypothesis.

Small Clutch Sizes as a Possible Adaptation against Ectoparasitism: A Comparative Analysis

Clutch size is expected to decrease with an increased rate of ectoparasite infestation. In order to test this hypothesis, I carried out comparative analyses using Australian and North American passerines. The allometry method showed a trend for passerine families which have higher degrees of ectoparasitism to also have smaller clutches. In the North American sample, however, the trend was confirmed for mite prevalence but was not for fly relative density. I also analyzed both samples using a method of independent comparisons. Results for Australian passerines suggest that an evolutionary change of clutch size in one direction is associated with an evolutionary change of relative density of ectoparasites in the opposite direction, after controlling for the effects of evolutionary changes in body size. The method of independent comparisons produced non-significant results for the North American sample. The hypothesis was also supported by a direct comparison of Australian and North American passerine families: Australian passerines lay smaller clutches than their North American counterparts and are infested more with contagious ectoparasites.

Genetics of Growth Predict Patterns of Brain-Size Evolution

Experimental evidence is presented supporting a developmental model that explains the genetic basis for brain and body size associations. Evolutionary change in body size causes correlated change in brain size because some genes affect both traits. The commonly observed correlation between brain and body size results from genetic variation in growth determinants affecting both traits simultaneously during fetal and early postnatal growth. Later growth reduces brain-body correlation because of changes in the underlying causal components of growth in each trait. Brain-body size evolution shows a different pattern at higher taxonomic levels from that seen within and between closely related species because body-size evolution among higher taxa occurs primarily by change in early portions of growth, which share more genetic growth determinants with brain size.