ASYNCHRONOUS EVOLUTION OF PHYSIOLOGY AND MORPHOLOGY IN ANOLIS LIZARDS

Species‐rich adaptive radiations typically diversify along several distinct ecological axes, each characterized by morphological, physiological, and behavioral adaptations. We test here whether different types of adaptive traits share similar patterns of evolution within a radiation by investigating patterns of evolution of morphological traits associated with microhabitat specialization and of physiological traits associated with thermal biology in Anolis lizards. Previous studies of anoles suggest that close relatives share the same “structural niche” (i.e., use the same types of perches) and are similar in body size and shape, but live in different “climatic niches” (i.e., use habitats with different insolation and temperature profiles). Because morphology is closely tied to structural niche and field active body temperatures are tied to climatic niches in Anolis, we expected phylogenetic analyses to show that morphology is more evolutionarily conservative than thermal physiology. In support of this hypothesis, we find (1) that thermal biology exhibits more divergence among recently diverged Anolis taxa than does morphology; and (2) diversification of thermal biology among all species often follows diversification in morphology. These conclusions are remarkably consistent with predictions made by anole biologists in the 1960s and 1970s.     

Macroecology and macroevolution of body size in Anolis lizards

Body size is one of the most influential traits affecting many ecological and physiological processes across animal and plant taxa. Studies of the environmental factors shaping body size patterns may evaluate either temporal or spatial dimensions. Here, we analyzed body size evolution in the radiation of Anolis lizards across both geographical and temporal dimensions. We used a set of macroecological and macroevolutionary methods to test current and past environmental effects on geographical gradients of body size and its evolutionary rates. First, we test whether a set of current ecological/physiological hypotheses (heat balance, productivity and seasonality) explains spatial body size gradients. Second, we evaluate how tempo (i.e. evolutionary rates) and mode (i.e. evolutionary process) of body size evolution changed through time and the role of paleo-temperatures on rates of body size evolution during the Cenozoic. We did not find a signature of current environmental variables driving spatial body size gradients. By contrast, we found strong support for a correlation between temperature changes (i.e. climate cooling) during the Cenozoic and rates of body size evolution (i.e. body size diversification). We suggest that patterns of body size evolution in Anolis lizards might be influenced by thermoregulatory behavior across clades and regions.     

Does ecological specialization transcend scale? Habitat partitioning among individuals and species of Anolis lizards

Ecological specialization is common across all levels of biological organization, raising the question of whether the evolution of specialization at one scale in a taxon is linked to specialization at other scales. Anolis lizards have diversified repeatedly along axes of habitat use, but it remains unknown if this diversification into habitat use specialists is underlain by individual specialization. From repeated observations of individuals in a population of Anolis sagrei in Florida, we show that the extent of habitat use specialization among individuals is comparable to the extent of specialization in the same traits among ten sympatric Anolis habitat specialist species in Cuba. However, the adaptive correlations between habitat use and morphology commonly seen across species of Anolis were not observed across individuals in the sampled population. Our results therefore suggest that while patterns of ecological specialization can transcend scale, these parallels are the consequence of distinct ecological processes acting at microevolutionary and macroevolutionary scales.     

CONVERGENT EVOLUTION OF SEXUAL DIMORPHISM IN SKULL SHAPE USING DISTINCT DEVELOPMENTAL STRATEGIES

Studies integrating evolutionary and developmental analyses of morphological variation are of growing interest to biologists as they promise to shed fresh light on the mechanisms of morphological diversification. Sexually dimorphic traits tend to be incredibly divergent across taxa. Such diversification must arise through evolutionary modifications to sex differences during development. Nevertheless, few studies of dimorphism have attempted to synthesize evolutionary and developmental perspectives. Using geometric morphometric analysis of head shape for 50 Anolis species, we show that two clades have converged on extreme levels of sexual dimorphism through similar, male‐specific changes in facial morphology. In both clades, males have evolved highly elongate faces whereas females retain faces of more moderate proportion. This convergence is accomplished using distinct developmental mechanisms; one clade evolved extreme dimorphism through the exaggeration of a widely shared, potentially ancestral, developmental strategy whereas the other clade evolved a novel developmental strategy not observed elsewhere in the genus. Together, our analyses indicate that both shared and derived features of development contribute to macroevolutionary patterns of morphological diversity among Anolis lizards.     

Macroevolutionary integration of phenotypes within and across ant worker castes

Phenotypic traits are often integrated into evolutionary modules: sets of organismal parts that evolve together. In social insect colonies, the concepts of integration and modularity apply to sets of traits both within and among functionally and phenotypically differentiated castes. On macroevolutionary timescales, patterns of integration and modularity within and across castes can be clues to the selective and ecological factors shaping their evolution and diversification. We develop a set of hypotheses describing contrasting patterns of worker integration and apply this framework in a broad (246 species) comparative analysis of major and minor worker evolution in the hyperdiverse ant genus Pheidole. Using geometric morphometrics in a phylogenetic framework, we inferred fast and tightly integrated evolution of mesosoma shape between major and minor workers, but slower and more independent evolution of head shape between the two worker castes. Thus, Pheidole workers are evolving as a mixture of intracaste and intercaste integration and rate heterogeneity. The decoupling of homologous traits across worker castes may represent an important process facilitating the rise of social complexity.     

DETERMINISM IN THE DIVERSIFICATION OF HISPANIOLAN TRUNK‐GROUND ANOLES (ANOLIS CYBOTES SPECIES COMPLEX)

The evolutionary processes that produce adaptive radiations are enigmatic. They can only be studied after the fact, once a radiation has occurred and been recognized, rather than while the processes are ongoing. One way to connect pattern to process is to study the processes driving divergence today among populations of species that belong to an adaptive radiation, and compare the results to patterns observed at a deeper, macroevolutionary level. We tested whether evolution is a deterministic process with similar outcomes during different stages of the adaptive radiation of Anolis lizards. Using a clade of terrestrial–scansorial lizards in the genus Anolis, we inferred the adaptive basis of spatial variation among contemporary populations and tested whether axes of phenotypic differentiation among them mirror known axes of diversification at deeper levels of the anole radiation. Nonparallel change associated with genetic divergence explains the vast majority of geographic variation. However, we found phenotypic variation to be adaptive as confirmed by convergence in populations occurring in similar habitats in different mountain ranges. Morphological diversification among populations recurs deterministically along two axes of diversification previously identified in the anole radiation, but the characters involved differ from those involved in adaptation at higher levels of anole phylogeny.     

Microevolutionary patterns in the common caiman predict macroevolutionary trends across extant crocodilians

Both extinct and extant crocodilians have repeatedly diversified in skull shape along a continuum, from narrow‐snouted to broad‐snouted phenotypes. These patterns occur with striking regularity, although it is currently unknown whether these trends also apply to microevolutionary divergence during population differentiation or the early stages of speciation. Assessing patterns of intraspecific variation within a single taxon can potentially provide insight into the processes of macroevolutionary differentiation. For example, high levels of intraspecific variation along a narrow‐broad axis would be consistent with the view that cranial shapes can show predictable patterns of differentiation on relatively short timescales, and potentially scale up to explain broader macroevolutionary patterns. In the present study, we use geometric morphometric methods to characterize intraspecific cranial shape variation among groups within a single, widely distributed clade, Caiman crocodilus. We show that C. crocodilus skulls vary along a narrow/broad‐snouted continuum, with different subspecies strongly clustered at distinct ends of the continuum. We quantitatively compare these microevolutionary trends with patterns of diversity at macroevolutionary scales (among all extant crocodilians). We find that morphological differences among the subspecies of C. crocodilus parallel the patterns of morphological differentiation across extant crocodilians, with the primary axes of morphological diversity being highly correlated across the two scales. We find intraspecific cranial shape variation within C. crocodilus to span variation characterized by more than half of living species. We show the main axis of intraspecific phenotypic variation to align with the principal direction of macroevolutionary diversification in crocodilian cranial shape, suggesting that mechanisms of microevolutionary divergence within species may also explain broader patterns of diversification at higher taxonomic levels.     

ECOLOGICAL OPPORTUNITY AND THE RATE OF MORPHOLOGICAL EVOLUTION IN THE DIVERSIFICATION OF GREATER ANTILLEAN ANOLES

The pace of phenotypic diversification during adaptive radiation should decrease as ecological opportunity declines. We test this prediction using phylogenetic comparative analyses of a wide range of morphological traits in Greater Antillean Anolis lizards. We find that the rate of diversification along two important axes of Anolis radiation—body size and limb dimensions—decreased as opportunity declined, with opportunity quantified either as time elapsed in the radiation or as the diversity of competing anole lineages inferred to have been present on an island at different times in the past. Most previous studies of the ecological opportunity hypothesis have focused on the rate of species diversification; our results provide a complementary perspective, indicating that the rate of phenotypic diversification declines with decreasing opportunity in an adaptive radiation.     

Evolution of a complex phenotype with biphasic ontogeny: Contribution of development versus function and climatic variation to skull modularity in toads

The theory of morphological integration and modularity predicts that if functional correlations among traits are relevant to mean population fitness, the genetic basis of development will be molded by stabilizing selection to match functional patterns. Yet, how much functional interactions actually shape the fitness landscape is still an open question. We used the anuran skull as a model of a complex phenotype for which we can separate developmental and functional modularity. We hypothesized that functional modularity associated to functional demands of the adult skull would overcome developmental modularity associated to bone origin at the larval phase because metamorphosis would erase the developmental signal. We tested this hypothesis in toad species of the Rhinella granulosa complex using species phenotypic correlation pattern (P‐matrices). Given that the toad species are distributed in very distinct habitats and the skull has important functions related to climatic conditions, we also hypothesized that differences in skull trait covariance pattern are associated to differences in climatic variables among species. Functional and hormonal‐regulated modules are more conspicuous than developmental modules only when size variation is retained on species P‐matrices. Without size variation, there is a clear modularity signal of developmental units, but most species have the functional model as the best supported by empirical data without allometric size variation. Closely related toad species have more similar climatic niches and P‐matrices than distantly related species, suggesting phylogenetic niche conservatism. We infer that the modularity signal due to embryonic origin of bones, which happens early in ontogeny, is blurred by the process of growth that occurs later in ontogeny. We suggest that the species differing in the preferred modularity model have different demands on the orbital functional unit and that species contrasting in climate are subjected to divergent patterns of natural selection associated to neurocranial allometry and T3 hormone regulation.     

Burrowing constrains patterns of skull shape evolution in wrasses

The evolution of behavioral and ecological specialization can have marked effects on the tempo and mode of phenotypic evolution. Head-first burrowing has been shown to exert powerful selective pressures on the head and body shapes of many vertebrate and invertebrate taxa. In wrasses, burrowing behaviors have evolved multiple times independently, and are commonly used in foraging and predator avoidance behaviors. While recent studies have examined the kinematics and body shape morphology associated with this behavior, no study to-date has examined the macroevolutionary implications of burrowing on patterns of phenotypic diversification in this clade. Here, we use three-dimensional geometric morphometrics and phylogenetic comparative methods to study the evolution of skull shape in fossorial wrasses and their relatives. We test for skull shape differences between burrowing and non burrowing wrasses and evaluate hypotheses of shape convergence among the burrowing wrasses. We also quantify rates of skull shape evolution between burrowing and non burrowing wrasses to test for whether burrowing constrains or accelerates rates of skull shape evolution in this clade. We find that while burrowing and non burrowing wrasses exhibit similar degrees of morphological disparity, for burrowing wrasses, it took nearly twice as long to amass this disparity. Furthermore, while the disparities between groups are evenly matched, we find that most burrowing species are confined to a particular region of shape space with most species exhibiting narrower heads than many non-burrowing species. These results suggest head-first burrowing constrains patterns of skull shape diversification in wrasses by potentially restricting the range of phenotypes that can perform this behavior.     

The Influence of Modularity on Cranial Morphological Disparity in Carnivora and Primates (Mammalia)

Background

Although variation provides the raw material for natural selection and evolution, few empirical data exist about the factors controlling morphological variation. Because developmental constraints on variation are expected to act by influencing trait correlations, studies of modularity offer promising approaches that quantify and summarize patterns of trait relationships. Modules, highly-correlated and semi-autonomous sets of traits, are observed at many levels of biological organization, from genes to colonies. The evolutionary significance of modularity is considerable, with potential effects including constraining the variation of individual traits, circumventing pleiotropy and canalization, and facilitating the transformation of functional structures. Despite these important consequences, there has been little empirical study of how modularity influences morphological evolution on a macroevolutionary scale. Here, we conduct the first morphometric analysis of modularity and disparity in two clades of placental mammals, Primates and Carnivora, and test if trait integration within modules constrains or facilitates morphological evolution.

Principal Findings

We used both randomization methods and direct comparisons of landmark variance to compare disparity in the six cranial modules identified in previous studies. The cranial base, a highly-integrated module, showed significantly low disparity in Primates and low landmark variance in both Primates and Carnivora. The vault, zygomatic-pterygoid and orbit modules, characterized by low trait integration, displayed significantly high disparity within Carnivora. 14 of 24 results from analyses of disparity show no significant relationship between module integration and morphological disparity. Of the ten significant or marginally significant results, eight support the hypothesis that integration within modules constrains morphological evolution in the placental skull. Only the molar module, a highly-integrated and functionally important module, showed significantly high disparity in Carnivora, in support of the facilitation hypothesis.

Conclusions

This analysis of within-module disparity suggested that strong integration of traits had little influence on morphological evolution over large time scales. However, where significant results were found, the primary effect of strong integration of traits was to constrain morphological variation. Thus, within Primates and Carnivora, there was some support for the hypothesis that integration of traits within cranial modules limits morphological evolution, presumably by limiting the variation of individual traits.     

Tests of the contribution of acclimation to geographic variation in water loss rates of the West Indian lizard <Emphasis Type="Italic">Anolis cristatellus</Emphasis>

Phenotypic plasticity can contribute to the process of adaptive radiation by facilitating population persistence in novel environments. West Indian Anolis lizards provide a classic example of an adaptive radiation, in which divergence has occurred along two primary ecological axes: structural microhabitat and climate. Adaptive plasticity in limb morphology is hypothesized to have facilitated divergence along the structural niche axis in Anolis, but very little work has explored plasticity in physiological traits. Here, we experimentally ask whether Puerto Rican Anolis cristatellus from mesic and xeric habitats differ in desiccation rates, and whether these lizards exhibit an acclimation response to changes in relative humidity. We first present microclimatic data collected at lizard perch sites that demonstrate that abiotic conditions experienced by lizards differ between mesic and xeric habitat types. In Experiment 1, we measured desiccation rates of lizards from both habitats maintained under identical laboratory conditions. This experiment demonstrated that desiccation rates differ between populations; xeric lizards lose water more slowly than mesic lizards. In Experiment 2, lizards from each habitat were either maintained under the conditions of Experiment 1, or under extremely low relative humidity. Desiccation rates did not differ between lizards from the same habitat maintained under different treatments and xeric lizards maintained lower desiccation rates than mesic lizards within each treatment. Our results demonstrate that A. cristatellus does not exhibit an acclimation response to abrupt changes of hydric conditions, and suggest that tropical Anolis lizards might be unable to exhibit physiological plasticity in desiccation rates in response to varying climatic conditions.     

Does nasal echolocation influence the modularity of the mammal skull?

In vertebrates, changes in cranial modularity can evolve rapidly in response to selection. However, mammals have apparently maintained their pattern of cranial integration throughout their evolutionary history and across tremendous morphological and ecological diversity. Here, we use phylogenetic, geometric morphometric and comparative analyses to test the hypothesis that the modularity of the mammalian skull has been remodelled in rhinolophid bats due to the novel and critical function of the nasal cavity in echolocation. We predicted that nasal echolocation has resulted in the evolution of a third cranial module, the ‘nasal dome’, in addition to the braincase and rostrum modules, which are conserved across mammals. We also test for similarities in the evolution of skull shape in relation to habitat across rhinolophids. We find that, despite broad variation in the shape of the nasal dome, the integration of the rhinolophid skull is highly consistent with conserved patterns of modularity found in other mammals. Across their broad geographical distribution, cranial shape in rhinolophids follows two major divisions that could reflect adaptations to dietary and environmental differences in African versus South Asian distributions. Our results highlight the potential of a relatively simple modular template to generate broad morphological and functional variation in mammals.     

Lizard scales in an adaptive radiation: variation in scale number follows climatic and structural habitat diversity in Anolis lizards

Lizard scales vary in size, shape and texture among and within species. The overall function of scales in squamates is attributed to protection against abrasion, solar radiation and water loss. We quantified scale number of Anolis lizards across a large sample of species (142 species) and examined whether this variation was related either to structural or to climatic habitat diversity. We found that species in dry environments have fewer, larger scales than species in humid environments. This is consistent with the hypothesis that scales reduce evaporative water loss through the skin. In addition, scale number varied among groups of ecomorphs and was correlated with aspects of the structural microhabitat (i.e. perch height and perch diameter). This was unexpected because ecomorph groups are based on morphological features related to locomotion in different structural microhabitats. Body scales are not likely to play an important role in locomotion in Anolis lizards. The observed variation may relate to other features of the ecomorph niche and more work is needed to understand the putative adaptive basis of these patterns. © 2014 The Linnean Society of London, Biological Journal of the Linnean Society, 2014, 113 , 570–579.     

Tempo and mode of performance evolution across multiple independent origins of adhesive toe pads in lizards

Understanding macroevolutionary dynamics of trait evolution is an important endeavor in evolutionary biology. Ecological opportunity can liberate a trait as it diversifies through trait space, while genetic and selective constraints can limit diversification. While many studies have examined the dynamics of morphological traits, diverse morphological traits may yield the same or similar performance and as performance is often more proximately the target of selection, examining only morphology may give an incomplete understanding of evolutionary dynamics. Here, we ask whether convergent evolution of pad‐bearing lizards has followed similar evolutionary dynamics, or whether independent origins are accompanied by unique constraints and selective pressures over macroevolutionary time. We hypothesized that geckos and anoles each have unique evolutionary tempos and modes. Using performance data from 59 species, we modified Brownian motion (BM) and Ornstein–Uhlenbeck (OU) models to account for repeated origins estimated using Bayesian ancestral state reconstructions. We discovered that adhesive performance in geckos evolved in a fashion consistent with Brownian motion with a trend, whereas anoles evolved in bounded performance space consistent with more constrained evolution (an Ornstein–Uhlenbeck model). Our results suggest that convergent phenotypes can have quite distinctive evolutionary patterns, likely as a result of idiosyncratic constraints or ecological opportunities.     

Host specificity shapes population structure of pinworm parasites in Caribbean reptiles

Host specificity is one of the potential factors affecting parasite diversification because gene flow may be facilitated or constrained by the number of host species that a parasite can exploit. We test this hypothesis using a costructure approach, comparing two sympatric pinworm parasites that differ in host specificity – Parapharyngodon cubensis and Spauligodon anolis – on the Puerto Rican Bank and St. Croix in the Caribbean. Spauligodon anolis specializes on Anolis lizards, whereas P. cubensis parasitizes Anolis lizards as well as many other species of lizards and snakes. We collected lizards from across the Puerto Rican Bank and St. Croix, sampled them for S. anolis and P. cubensis and generated nuclear and mitochondrial sequence data from the parasites. We used these data to show that P. cubensis is comprised of multiple cryptic species that exhibit limited population structure relative to S. anolis, which is consistent with our prediction based on their host specificity. We also provide evidence that the distribution of P. cubensis species is maintained by competitive exclusion, and in contrast to previous theoretical work, the parasites with the greatest number of host species also reach the highest prevalence rates. Overall, our results are consistent with the hypothesis that host specificity shapes parasite diversification, and suggest that even moderate differences in host specificity may contribute to substantial differences in diversification.     

Testing the stages model in the adaptive radiation of cichlid fishes in East African Lake Tanganyika

Adaptive radiation (AR) is a key process in the origin of organismal diversity. However, the evolution of trait disparity in connection with ecological specialization is still poorly understood. Available models for vertebrate ARs predict that diversification occurs in the form of temporal stages driven by different selective forces. Here, we investigate the AR of cichlid fishes in East African Lake Tanganyika and use macroevolutionary model fitting to evaluate whether diversification happened in temporal stages. Six trait complexes, for which we also provide evidence of their adaptiveness, are analysed with comparative methods: body shape, pharyngeal jaw shape, gill raker traits, gut length, brain weight and body coloration. Overall, we do not find strong evidence for the ‘stages model’ of AR. However, our results suggest that trophic traits diversify earlier than traits implicated in macrohabitat adaptation and that sexual communication traits (i.e. coloration) diversify late in the radiation.     

Macroevolution of arboreality in salamanders

Evolutionary theory predicts that selection in distinct microhabitats generates correlations between morphological and ecological traits, and may increase both phenotypic and taxonomic diversity. However, some microhabitats exert unique selective pressures that act as a restraining force on macroevolutionary patterns of diversification. In this study, we use phylogenetic comparative methods to investigate the evolutionary outcomes of inhabiting the arboreal microhabitat in salamanders. We find that arboreality has independently evolved at least five times in Caudata and has arisen primarily from terrestrial ancestors. However, the rate of transition from arboreality back to terrestriality is 24 times higher than the converse. This suggests that macroevolutionary trends in microhabitat use tend toward terrestriality over arboreality, which influences the extent to which use of the arboreal microhabitat proliferates. Morphologically, we find no evidence for an arboreal phenotype in overall body proportions or in foot shape, as variation in both traits overlaps broadly with species that utilize different microhabitats. However, both body shape and foot shape display reduced rates of phenotypic evolution in arboreal taxa, and evidence of morphological convergence among arboreal lineages is observed. Taken together, these patterns suggest that arboreality has played a unique role in the evolution of this family, providing neither an evolutionary opportunity, nor an evolutionary dead end.     

Branching patterns in phylogenies cannot distinguish diversity‐dependent diversification from time‐dependent diversification

One of the primary goals of macroevolutionary biology has been to explain general trends in long‐term diversity patterns, including whether such patterns correspond to an upscaling of processes occurring at lower scales. Reconstructed phylogenies often show decelerated lineage accumulation over time. This pattern has often been interpreted as the result of diversity‐dependent (DD) diversification, where the accumulation of species causes diversification to decrease through niche filling. However, other processes can also produce such a slowdown, including time dependence without diversity dependence. To test whether phylogenetic branching patterns can be used to distinguish these two mechanisms, we formulated a time‐dependent, but diversity‐independent model that matches the expected diversity through time of a DD model. We simulated phylogenies under each model and studied how well likelihood methods could recover the true diversification mode. Standard model selection criteria always recovered diversity dependence, even when it was not present. We correct for this bias by using a bootstrap method and find that neither model is decisively supported. This implies that the branching pattern of reconstructed trees contains insufficient information to detect the presence or absence of diversity dependence. We advocate that tests encompassing additional data, for example, traits or range distributions, are needed to evaluate how diversity drives macroevolutionary trends.     

SIZE VARIATION,GROWTH STRATEGIES,AND THE EVOLUTION OF MODULARITY IN THE MAMMALIAN SKULL

Allometry is a major determinant of within‐population patterns of association among traits and, therefore, a major component of morphological integration studies. Even so, the influence of size variation over evolutionary change has been largely unappreciated. Here, we explore the interplay between allometric size variation, modularity, and life‐history strategies in the skull from representatives of 35 mammalian families. We start by removing size variation from within‐species data and analyzing its influence on integration magnitudes, modularity patterns, and responses to selection. We also carry out a simulation in which we artificially alter the influence of size variation in within‐taxa matrices. Finally, we explore the relationship between size variation and different growth strategies. We demonstrate that a large portion of the evolution of modularity in the mammalian skull is associated to the evolution of growth strategies. Lineages with highly altricial neonates have adult variation patterns dominated by size variation, leading to high correlations among traits regardless of any underlying modular process and impacting directly their potential to respond to selection. Greater influence of size variation is associated to larger intermodule correlations, less individualized modules, and less flexible responses to natural selection.