Allometric space and allometric disparity: a developmental perspective in the macroevolutionary analysis of morphological disparity

Here, we advance novel uses of allometric spaces--multidimensional spaces specifically defined by allometric coefficients--with the goal of investigating the focal role of development in shaping the evolution of morphological disparity. From their examination, operational measures of allometric disparity can be derived, complementing standard signals of morphological disparity through an intuitive and process-oriented refinement of established analytical protocols used in disparity studies. Allometric spaces thereby become a promising context to reveal different patterns of evolutionary developmental changes and to assess their relative prevalence and importance. Such spaces offer a novel domain of investigation of phenotypic variation and should help in detecting large-scale trends, thus placing various macroevolutionary phenomena in an explicitly developmental context. Ammonoidea (Cephalopoda) at the Lower-Middle Jurassic transition were chosen as a case study to illustrate this methodological approach. We constructed two phenotypic spaces: a static, adult one (adult morphospace) and a dynamic, developmental one (allometric space). Comparative disparity analyses show a strikingly stable occupation in both spaces, despite extensive change in taxonomic composition. In contrast, disparity analyses of subclades reveal clearly distinct morphological and allometric disparity dynamics. Allometric approaches allow developmental insights into morphological diversification otherwise intractable from the analysis of adult morphospace alone.     

BBMV: an R package for the estimation of macroevolutionary landscapes

The distribution of traits along phylogenies bears signatures of how ecological and evolutionary processes have interacted to influence phenotypic evolution, which can be deciphered using macroevolutionary models. BBMV implements a model for the evolution of continuous characters on phylogenies that generalizes existing ones, like Brownian motion and the Ornstein‐Uhlenbeck model. In this model quantitative characters evolve under both random diffusion and a deterministic force that can be of any possible shape and strength. The model can be used to infer evolutionary scenarios that remained inaccessible so far, like directional trends, disruptive selection, and even bounded evolution. With this new tool at hand, researchers will be able to test complex hypothesis‐driven scenarios regarding trait evolution, but they will also have the possibility to estimate the shape of the adaptive landscapes in which traits evolved. Ultimately, this will provide a way to infer how ecological processes have influenced phenotypic evolution over long timescales. The BBMV package is implemented in the R statistical language and is freely available on the CRAN repository < https://CRAN.R‐project.org/package=BBMV >. All source code can also be found on < https://github.com/fcboucher/BBMV >, along with a detailed tutorial.     

Exploring macroevolution using modern and fossil data

Macroevolution, encompassing the deep-time patterns of the origins of modern biodiversity, has been discussed in many contexts. Non-Darwinian models such as macromutations have been proposed as a means of bridging seemingly large gaps in knowledge, or as a means to explain the origin of exquisitely adapted body plans. However, such gaps can be spanned by new fossil finds, and complex, integrated organisms can be shown to have evolved piecemeal. For example, the fossil record between dinosaurs and Archaeopteryx has now filled up with astonishing fossil intermediates that show how the unique plexus of avian adaptations emerged step by step over 60 Myr. New numerical approaches to morphometrics and phylogenetic comparative methods allow palaeontologists and biologists to work together on deep-time questions of evolution, to explore how diversity, morphology and function have changed through time. Patterns are more complex than sometimes expected, with frequent decoupling of species diversity and morphological diversity, pointing to the need for some new generalizations about the processes that lie behind such patterns.     

The influence of size on body shape diversification across Indo‐Pacific shore fishes*

Understanding the causes of body shape variability across the tree of life is one of the central issues surrounding the origins of biodiversity. One potential mechanism driving observed patterns of shape disparity is a strongly conserved relationship between size and shape. Conserved allometry has been shown to account for as much as 80% of shape variation in some vertebrate groups. Here, we quantify the amount of body shape disparity attributable to changes in body size across nearly 800 species of Indo‐Pacific shore fishes using a phylogenetic framework to analyze 17 geometric landmarks positioned to capture general body shape and functionally significant features. In marked contrast to other vertebrate lineages, we find that changes in body size only explain 2.9% of the body shape variation across fishes, ranging from 3% to 50% within our 11 sampled families. We also find a slight but significant trend of decreasing rates of shape evolution with increasing size. Our results suggest that the influence of size on fish shape has largely been overwhelmed by lineage‐specific patterns of diversification that have produced the modern landscape of highly diverse forms that we currently observe in nature.     

Developmental mechanisms of macroevolutionary change in the tetrapod axis: A case study of Sauropterygia

Understanding how developmental processes change on macroevolutionary timescales to generate body plan disparity is fundamental to the study of vertebrate evolution. Adult morphology of the vertebral column directly reflects the mechanisms that generate vertebral counts (somitogenesis) and their regionalisation (homeotic effects) during embryonic development. Sauropterygians were a group of Mesozoic marine reptiles that exhibited an extremely high disparity of presacral vertebral/somite counts. Using phylogenetic comparative methods, we demonstrate that somitogenesis and homeotic effects evolved in a co‐ordinated way among sauropterygians, contrasting with the wider pattern in tetrapods, in which somitogenetic and homeotic shifts are uncorrelated. Changes in sauropterygian body proportions were primarily enabled by homeotic shifts, with a lesser, but important, contribution from differences in postpatterning growth among somites. High body plan plasticity was present in Triassic sauropterygians and was maintained among their Jurassic and Cretaceous descendants. The extreme disparity in the body plan of plesiosaurian sauropterygians did not result from accelerated rates of evolutionary change in neck length, but instead reflect this ancestral versatility of sauropterygian axial development. Our results highlight variation in modes of axial development among tetrapods, and show that heterogeneous statistical models can uncover novel macroevolutionary patterns for animal body plans and the developmental mechanisms that control them.     

Categorical versus geometric morphometric approaches to characterizing the evolution of morphological disparity in Osteostraci (Vertebrata,stem Gnathostomata)

Morphological variation (disparity) is almost invariably characterized by two non-mutually exclusive approaches: (1) quantitatively, through geometric morphometrics; and (2) in terms of discrete, ‘cladistic’, or categorical characters. Uncertainty over the comparability of these approaches diminishes the potential to obtain nomothetic insights into the evolution of morphological disparity and the few benchmarking studies conducted so far show contrasting results. Here, we apply both approaches to characterizing morphology in the stem-gnathostome clade Osteostraci in order to assess congruence between these alternative methods as well as to explore the evolutionary patterns of the group in terms of temporal disparity and the influence of phylogenetic relationships and habitat on morphospace occupation. Our results suggest that both approaches yield similar results in morphospace occupation and clustering, but also some differences indicating that these metrics may capture different aspects of morphology. Phylomorphospaces reveal convergence towards a generalized ‘horseshoe’-shaped cranial morphology and two strong trends involving major groups of osteostracans (benneviaspidids and thyestiids), which probably reflect adaptations to different lifestyles. Temporal patterns of disparity obtained from categorical and morphometric approaches appear congruent, however, disparity maxima occur at different times in the evolutionary history of the group. The results of our analyses indicate that categorical and continuous data sets may characterize different patterns of morphological disparity and that discrepancies could reflect preservational limitations of morphometric data and differences in the potential of each data type for characterizing more or less inclusive aspects of overall phenotype.     

The complex effects of mass extinctions on morphological disparity

Studies of biodiversity through deep time have been a staple for biologists and paleontologists for over 60 years. Investigations of species richness (diversity) revealed that at least five mass extinctions punctuated the last half billion years, each seeing the rapid demise of a large proportion of contemporary taxa. In contrast to diversity, the response of morphological diversity (disparity) to mass extinctions is unclear. Generally, diversity and disparity are decoupled, such that diversity may decline as morphological disparity increases, and vice versa. Here, we develop simulations to model disparity changes across mass extinctions using continuous traits and birth-death trees. We find no simple null for disparity change following a mass extinction but do observe general patterns. The range of trait values decreases following either random or trait-selective mass extinctions, whereas variance and the density of morphospace occupation only decline following trait-selective events. General trends may differentiate random and trait-selective mass extinctions, but methods struggle to identify trait selectivity. Long-term effects of mass extinction trait selectivity change support for phylogenetic comparative methods away from the simulated Brownian motion toward Ornstein-Uhlenbeck and Early Burst models. We find that morphological change over mass extinction is best studied by quantifying multiple aspects of morphospace occupation.     

A major shift in diversification rate helps explain macroevolutionary patterns in primate species diversity

Primates represent one of the most species rich, wide ranging, and ecologically diverse clades of mammals. What major macroevolutionary factors have driven their diversification and contributed to the modern distribution of primate species remains widely debated. We employed phylogenetic comparative methods to examine the role of clade age and evolutionary rate heterogeneity in the modern distribution of species diversity of Primates. Primate diversification has accelerated since its origin, with decreased extinction leading to a shift to even higher evolutionary rates in the most species rich family (Cercopithecidae). Older primate clades tended to be more diverse, however a shift in evolutionary rate was necessary to adequately explain the imbalance in species diversity. Species richness was also poorly explained by geographic distribution, especially once clade age and evolutionary rate shifts were accounted for, and may relate instead to other ecological factors. The global distribution of primate species diversity appears to have been strongly impacted by heterogeneity in evolutionary rates.     

Do different disparity proxies converge on a common signal? Insights from the cranial morphometrics and evolutionary history of Pterosauria (Diapsida: Archosauria)

Disparity, or morphological diversity, is often quantified by evolutionary biologists investigating the macroevolutionary history of clades over geological timescales. Disparity is typically quantified using proxies for morphology, such as measurements, discrete anatomical characters, or geometric morphometrics. If different proxies produce differing results, then the accurate quantification of disparity in deep time may be problematic. However, despite this, few studies have attempted to examine disparity of a single clade using multiple morphological proxies. Here, as a case study for this question, we examine the disparity of the volant Mesozoic fossil reptile clade Pterosauria, an intensively studied group that achieved substantial morphological, ecological and taxonomic diversity during their 145+ million-year evolutionary history. We characterize broadscale patterns of cranial morphological disparity for pterosaurs for the first time using landmark-based geometric morphometrics and make comparisons to calculations of pterosaur disparity based on alternative metrics. Landmark-based disparity calculations suggest that monofenestratan pterosaurs were more diverse cranially than basal non-monofenestratan pterosaurs (at least when the aberrant anurognathids are excluded), and that peak cranial disparity may have occurred in the Early Cretaceous, relatively late in pterosaur evolution. Significantly, our cranial disparity results are broadly congruent with those based on whole skeleton discrete character and limb proportion data sets, indicating that these divergent approaches document a consistent pattern of pterosaur morphological evolution. Therefore, pterosaurs provide an exemplar case demonstrating that different proxies for morphological form can converge on the same disparity signal, which is encouraging because often only one such proxy is available for extinct clades represented by fossils. Furthermore, mapping phylogeny into cranial morphospace demonstrates that pterosaur cranial morphology is significantly correlated with, and potentially constrained by, phylogenetic relationships.     

Understanding the effect of competition during evolutionary radiations: an integrated model of phenotypic and species diversification

Competition can drive macroevolutionary change, for example during adaptive radiations. However, we still lack a clear understanding of how it shapes diversification processes and patterns. To better understand the macroevolutionary consequences of competition, as well as the signal left on phylogenetic data, we developed a model linking trait evolution and species diversification in an ecological context. We find four main results: first, competition spurs trait diversity but not necessarily species richness; second, competition produces slowdowns in species diversification even in the absence of explicit ecological limits, but not in phenotypic diversification even in the presence of such limits; third, early burst patterns do not provide a reliable way of testing for adaptive radiations; and fourth, looking for phylogenetic signal in trait data and support for phenotypic models incorporating competition is a better alternative. Our results clarify the macroevolutionary consequences of competition and could help design more powerful tests of adaptive radiations in nature.     

Connecting proximate mechanisms and evolutionary patterns: pituitary gland size and mammalian life history

At the proximate level, hormones are known to play a critical role in influencing the life history of mammals, including humans. The pituitary gland is directly responsible for producing several hormones, including those related to growth and reproduction. Although we have a basic understanding of how hormones affect life history characteristics, we still have little knowledge of this relationship in an evolutionary context. We used data from 129 mammal species representing 14 orders to investigate the relationship between pituitary gland size and life history variation. Because pituitary gland size should be related to hormone production and action, we predicted that species with relatively large pituitaries should be associated with fast life histories, especially increased foetal and post‐natal growth rates. Phylogenetic analyses revealed that total pituitary size and the size of the anterior lobe of the pituitary significantly predicted a life history axis that was correlated with several traits including body mass, and foetal and post‐natal growth rates. Additional models directly examining the association between relative pituitary size and growth rates produced concordant results. We also found that relative pituitary size variation across mammals was best explained by an Ornstein–Uhlenbeck model of evolution, suggesting an important role of stabilizing selection. Our results support the idea that the size of the pituitary is linked to life history variation through evolutionary time. This pattern is likely due to mediating hormone levels but additional work is needed. We suggest that future investigations incorporating endocrine gland size may be critical for understanding life history evolution.     

Distinct evolutionary patterns of morphometric sperm traits in passerine birds

The striking diversity of sperm shape across the animal kingdom is still poorly understood. Postcopulatory sexual selection is an important factor driving the evolution of sperm size and shape. Interestingly, morphometric sperm traits, such as the length of the head, midpiece and flagellum, exhibit a strong positive phenotypic correlation across species. Here we used recently developed comparative methods to investigate how such phenotypic correlations between morphometric sperm traits may evolve. We compare allometric relationships and evolutionary trajectories of three morphometric sperm traits (length of head, midpiece and flagellum) in passerine birds. We show that these traits exhibit strong phenotypic correlations but that allometry varies across families. In addition, the evolutionary trajectories of the midpiece and flagellum are similar while the trajectory for head length differs. We discuss our findings in the light of three scenarios accounting for correlated trait evolution: (i) genetic correlation; (ii) concerted response to selection acting simultaneously on different traits; and (iii) phenotypic correlation between traits driven by mechanistic constraints owing to selection on sperm performance. Our results suggest that concerted response to selection is the most likely explanation for the phenotypic correlation between morphometric sperm traits.     

A phylogenetic analysis of macroevolutionary patterns in fermentative yeasts

When novel sources of ecological opportunity are available, physiological innovations can trigger adaptive radiations. This could be the case of yeasts (Saccharomycotina), in which an evolutionary novelty is represented by the capacity to exploit simple sugars from fruits (fermentation). During adaptive radiations, diversification and morphological evolution are predicted to slow‐down after early bursts of diversification. Here, we performed the first comparative phylogenetic analysis in yeasts, testing the “early burst” prediction on species diversification and also on traits of putative ecological relevance (cell‐size and fermentation versatility). We found that speciation rates are constant during the time‐range we considered (ca., 150 millions of years). Phylogenetic signal of both traits was significant (but lower for cell‐size), suggesting that lineages resemble each other in trait‐values. Disparity analysis suggested accelerated evolution (diversification in trait values above Brownian Motion expectations) in cell‐size. We also found a significant phylogenetic regression between cell‐size and fermentation versatility (R² = 0.10), which suggests correlated evolution between both traits. Overall, our results do not support the early burst prediction both in species and traits, but suggest a number of interesting evolutionary patterns, that warrant further exploration. For instance, we show that the Whole Genomic Duplication that affected a whole clade of yeasts, does not seems to have a statistically detectable phenotypic effect at our level of analysis. In this regard, further studies of fermentation under common‐garden conditions combined with comparative analyses are warranted.     

The evolution of cranial form and function in theropod dinosaurs: insights from geometric morphometrics

Theropod dinosaurs, an iconic clade of fossil species including Tyrannosaurus and Velociraptor, developed a great diversity of body size, skull form and feeding habits over their 160+ million year evolutionary history. Here, we utilize geometric morphometrics to study broad patterns in theropod skull shape variation and compare the distribution of taxa in cranial morphospace (form) to both phylogeny and quantitative metrics of biting behaviour (function). We find that theropod skulls primarily differ in relative anteroposterior length and snout depth and to a lesser extent in orbit size and depth of the cheek region, and oviraptorosaurs deviate most strongly from the "typical" and ancestral theropod morphologies. Noncarnivorous taxa generally fall out in distinct regions of morphospace and exhibit greater overall disparity than carnivorous taxa, whereas large-bodied carnivores independently converge on the same region of morphospace. The distribution of taxa in morphospace is strongly correlated with phylogeny but only weakly correlated with functional biting behaviour. These results imply that phylogeny, not biting function, was the major determinant of theropod skull shape.     

Evolutionary processes and its environmental correlates in the cranial morphology of western chipmunks (Tamias)

The importance of the environment in shaping phenotypic evolution lies at the core of evolutionary biology. Chipmunks of the genus Tamias (subgenus Neotamias) are part of a very recent radiation, occupying a wide range of environments with marked niche partitioning among species. One open question is if and how those differences in environments affected phenotypic evolution in this lineage. Herein we examine the relative importance of genetic drift versus natural selection in the origin of cranial diversity exhibited by clade members. We also explore the degree to which variation in potential selective agents (environmental variables) are correlated with the patterns of morphological variation presented. We found that genetic drift cannot explain morphological diversification in the group, thus supporting the potential role of natural selection as the predominant evolutionary force during Neotamias cranial diversification, although the strength of selection varied greatly among species. This morphological diversification, in turn, was correlated with environmental conditions, suggesting a possible causal relationship. These results underscore that extant Neotamias represent a radiation in which aspects of the environment might have acted as the selective force driving species’ divergence.     

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.     

Geographic range velocity and its association with phylogeny and life history traits in North American woody plants

The geographic ranges of taxa change in response to environmental conditions. Yet whether rates of range movement (biotic velocities) are phylogenetically conserved is not well known. Phylogenetic conservatism of biotic velocities could reflect similarities among related lineages in climatic tolerances and dispersal‐associated traits. We assess whether late Quaternary biotic velocities were phylogenetically conserved and whether they correlate with climatic tolerances and dispersal‐associated traits. We used phylogenetic regression and nonparametric correlation to evaluate associations between biotic velocities, dispersal‐associated traits, and climatic tolerances for 28 woody plant genera and subgenera in North America. The velocities with which woody plant taxa shifted their core geographic range limits were positively correlated from time step to time step between 16 and 7 ka. The strength of this correlation weakened after 7 ka as the pace of climate change slowed. Dispersal‐associated traits and climatic tolerances were not associated with biotic velocities. Although the biotic velocities of some genera were consistently fast and others consistently slow, biotic velocities were not phylogenetically conserved. The rapid late Quaternary range shifts of plants lacking traits that facilitate frequent long‐distance dispersal has long been noted (i.e., Reid's Paradox). Our results are consistent with this paradox and show that it remains robust when phylogenetic information is taken into account. The lack of association between biotic velocities, dispersal‐associated traits, and climatic tolerances may reflect several, nonmutually exclusive processes, including rare long‐distance dispersal, biotic interactions, and cryptic refugia. Because late Quaternary biotic velocities were decoupled from dispersal‐associated traits, trait data for genera and subgenera cannot be used to predict longer‐term (millennial‐scale) floristic responses to climate change.     

Geometric morphometric analyses provide evidence for the adaptive character of the Tanganyikan cichlid fish radiations

The cichlids of East Africa are renowned as one of the most spectacular examples of adaptive radiation. They provide a unique opportunity to investigate the relationships between ecology, morphological diversity, and phylogeny in producing such remarkable diversity. Nevertheless, the parameters of the adaptive radiations of these fish have not been satisfactorily quantified yet. Lake Tanganyika possesses all of the major lineages of East African cichlid fish, so by using geometric morphometrics and comparative analyses of ecology and morphology, in an explicitly phylogenetic context, we quantify the role of ecology in driving adaptive speciation. We used geometric morphometric methods to describe the body shape of over 1000 specimens of East African cichlid fish, with a focus on the Lake Tanganyika species assemblage, which is composed of more than 200 endemic species. The main differences in shape concern the length of the whole body and the relative sizes of the head and caudal peduncle. We investigated the influence of phylogeny on similarity of shape using both distance-based and variance partitioning methods, finding that phylogenetic inertia exerts little influence on overall body shape. Therefore, we quantified the relative effect of major ecological traits on shape using phylogenetic generalized least squares and disparity analyses. These analyses conclude that body shape is most strongly predicted by feeding preferences (i.e., trophic niches) and the water depths at which species occur. Furthermore, the morphological disparity within tribes indicates that even though the morphological diversification associated with explosive speciation has happened in only a few tribes of the Tanganyikan assemblage, the potential to evolve diverse morphologies exists in all tribes. Quantitative data support the existence of extensive parallelism in several independent adaptive radiations in Lake Tanganyika. Notably, Tanganyikan mouthbrooders belonging to the C-lineage and the substrate spawning Lamprologini have evolved a multitude of different shapes from elongated and Lamprologus-like hypothetical ancestors. Together, these data demonstrate strong support for the adaptive character of East African cichlid radiations.     

Morphological evolution of the lizard skull: a geometric morphometrics survey

Patterns of diversity among lizard skulls were studied from a morphological, phylogenetic, and functional perspective. A sample of 1,030 lizard skulls from 441 species in 17 families was used to create a lizard skull morphospace. This morphospace was combined with a phylogeny of lizard families to summarize general trends in the evolution of the lizard skull. A basal morphological split between the Iguania and Scleroglossa was observed. Iguanians are characterized by a short, high skull, with large areas of attachment for the external adductor musculature, relative to their sister group. The families of the Iguania appear to possess more intrafamilial morphological diversity than families of the Scleroglossa, but rarefaction of the data reveals this to be an artifact caused by the greater number of species represented in Iguanian families. Iguanian families also appear more dissimilar to one another than families of the Scleroglossa. Permutation tests indicate that this pattern is real and not due to the smaller number of families in the Iguanidae. Parallel and convergent evolution is observed among lizards with similar diets: ant and termite specialists, carnivores, and herbivores. However, these patterns are superimposed over the more general phylogenetic pattern of lizard skull diversity. This study has three central conclusions. Different clades of lizards show different patterns of disparity and divergence in patterns of morphospace occupation. Phylogeny imposes a primary signal upon which a secondary ecological signal is imprinted. Evolutionary patterns in skull metrics, taken with functional landmarks, allow testing of trends and the development of new hypotheses concerning both shape and biomechanics.     

Diversification of body shape in Sebastes rockfishes of the north‐east Pacific

Body shape variation is integrally related to many aspects of fish ecology, including locomotion and foraging, and can indicate the functional diversity of fish assemblages. Few studies have thoroughly characterized body shape in a diverse marine fish clade, or investigated both temporal and spatial patterns of variation in body shape disparity. Here, I use digital photographs to measure geometric body shape in 66 species of north‐east Pacific rockfish (Sebastes spp.), including a correction for error introduced by arching of specimens. Different components of interspecific shape variation show associations with fish size, depth habitat, trophic niche and phylogenetic relationships. Overall, the accumulation of body shape disparity appears to have been near‐constant over time, and shows little variation across the latitudinal range of rockfish.