Integrative Approach Uncovers New Patterns of Ecomorphological Convergence in Slow Arboreal Xenarthrans

Identifying ecomorphological convergence examples is a central focus in evolutionary biology. In xenarthrans, slow arboreality independently arose at least three times, in the two genera of ‘tree sloths’, Bradypus and Choloepus, and the silky anteater, Cyclopes. This specialized locomotor ecology is expectedly reflected by distinctive morpho-functional convergences. Cyclopes, although sharing several ecological features with ‘tree sloths’, do not fully mirror the latter in their outstandingly similar suspensory slow arboreal locomotion. We hypothesized that the morphology of Cyclopes is closer to ‘tree sloths’ than to anteaters, but yet distinct, entailing that slow arboreal xenarthrans evolved through ‘incomplete’ convergence. In a multivariate trait space, slow arboreal xenarthrans are hence expected to depart from their sister taxa evolving toward the same area, but not showing extensive phenotypical overlap, due to the distinct position of Cyclopes. Conversely, a pattern of ‘complete’ convergence (i.e., widely overlapping morphologies) is hypothesized for ‘tree sloths’. Through phylogenetic comparative methods, we quantified humeral and femoral convergence in slow arboreal xenarthrans, including a sample of extant and extinct non-slow arboreal xenarthrans. Through 3D geometric morphometrics, cross-sectional properties (CSP) and trabecular architecture, we integratively quantified external shape, diaphyseal anatomy and internal epiphyseal structure. Several traits converged in slow arboreal xenarthrans, especially those pertaining to CSP. Phylomorphospaces and quantitative convergence analyses substantiated the expected patterns of ‘incomplete’ and ‘complete’ convergence for slow arboreal xenarthrans and ‘tree sloths’, respectively. This work, highlighting previously unidentified convergence patterns, emphasizes the value of an integrative multi-pronged quantitative approach to cope with complex mechanisms underlying ecomorphological convergence.

Multiple evolutionary origins and losses of tooth complexity in squamates

Teeth act as tools for acquiring and processing food, thus holding a prominent role in vertebrate evolution. In mammals, dental-dietary adaptations rely on tooth complexity variations controlled by cusp number and pattern. Complexity increase through cusp addition has dominated the diversification of mammals. However, studies of Mammalia alone cannot reveal patterns of tooth complexity conserved throughout vertebrate evolution. Here, we use morphometric and phylogenetic comparative methods across fossil and extant squamates to show they also repeatedly evolved increasingly complex teeth, but with more flexibility than mammals. Since the Late Jurassic, multiple-cusped teeth evolved over 20 times independently from a single-cusped common ancestor. Squamates frequently lost cusps and evolved varied multiple-cusped morphologies at heterogeneous rates. Tooth complexity evolved in correlation with changes in plant consumption, resulting in several major increases in speciation. Complex teeth played a critical role in vertebrate evolution outside Mammalia, with squamates exemplifying a more labile system of dental-dietary evolution.

The Evolutionary Dynamics of Negative Existentials in Indo-European

Where in earlier work diachronic change is used to explain away exceptions to typologies, linguistic typologists have started to make use of explicit diachronic models as explanations for typological distributions. A topic that lends itself for this approach especially well is that of negation. In this article, we assess the explanatory value of a specific hypothesis, the Negative Existential Cycle (NEC), on the distribution of negative existential strategies (“types”) in 106 Indo-European languages. We use Bayesian phylogenetic comparative methods to infer posterior distributions of transition rates and parameters, thus applying rational methods to construct and evaluate a set of different models under which the attested typological distribution could have evolved. We find that the frequency of diachronic processes that affect negative existentials outside of the NEC cannot be ignored—the unidirectional NEC alone cannot explain the evolution of negative existential strategies in our sample. We show that non-unidirectional evolutionary models, especially those that allow for different and multiple transitions between strategies, provide better fit. In addition, the phylogenetic modeling is impacted by the expected skewed distribution of negative existential strategies in our sample, pointing out the need for densely sampled and family-based typological research.

Evolutionary history of quadrupedal walking gaits shows mammalian release from locomotor constraint

Vertebrates employ an impressive range of strategies for coordinating their limb movements while walking. Although this gait variation has been quantified and hypotheses for its origins tested in select tetrapod lineages, a comprehensive understanding of gait evolution in a macroevolutionary context is currently lacking. We used freely available internet videos to nearly double the number of species with quantitative gait data, and used phylogenetic comparative methods to test key hypotheses about symmetrical gait origin and evolution. We find strong support for an ancestral lateral-sequence diagonal-couplet gait in quadrupedal gnathostomes, and this mode is remarkably conserved throughout tetrapod phylogeny. Evolutionary rate analyses show that mammals overcame this ancestral constraint, resulting in a greater range of phase values than any other tetrapod lineage. Diagonal-sequence diagonal-couplet gaits are significantly associated with arboreality in mammals, though this relationship is not recovered for other tetrapod lineages. Notably, the lateral-sequence lateral-couplet gait, unique to mammals among extant tetrapods, is not associated with any traditional explanations. The complex drivers of gait diversification in mammals remain unclear, but our analyses suggest that their success was due, in part, to release from a locomotor constraint that has probably persisted in other extant tetrapod lineages for over 375 Myr.

A variable-rate quantitative trait evolution model using penalized-likelihood

In recent years it has become increasingly popular to use phylogenetic comparative methods to investigate heterogeneity in the rate or process of quantitative trait evolution across the branches or clades of a phylogenetic tree. Here, I present a new method for modeling variability in the rate of evolution of a continuously-valued character trait on a reconstructed phylogeny. The underlying model of evolution is stochastic diffusion (Brownian motion), but in which the instantaneous diffusion rate (σ2) also evolves by Brownian motion on a logarithmic scale. Unfortunately, it’s not possible to simultaneously estimate the rates of evolution along each edge of the tree and the rate of evolution of σ2 itself using Maximum Likelihood. As such, I propose a penalized-likelihood method in which the penalty term is equal to the log-transformed probability density of the rates under a Brownian model, multiplied by a ‘smoothing’ coefficient, λ, selected by the user. λ determines the magnitude of penalty that’s applied to rate variation between edges. Lower values of λ penalize rate variation relatively little; whereas larger λ values result in minimal rate variation among edges of the tree in the fitted model, eventually converging on a single value of σ2 for all of the branches of the tree. In addition to presenting this model here, I have also implemented it as part of my phytools R package in the function multirateBM. Using different values of the penalty coefficient, λ, I fit the model to simulated data with: Brownian rate variation among edges (the model assumption); uncorrelated rate variation; rate changes that occur in discrete places on the tree; and no rate variation at all among the branches of the phylogeny. I then compare the estimated values of σ2 to their known true values. In addition, I use the method to analyze a simple empirical dataset of body mass evolution in mammals. Finally, I discuss the relationship between the method of this article and other models from the phylogenetic comparative methods and finance literature, as well as some applications and limitations of the approach.

A Phylogeny-Informed Analysis of the Global Coral-Symbiodiniaceae Interaction Network Reveals that Traits Correlated with Thermal Bleaching Are Specific to Symbiont Transmission Mode

ABSTRACT The complex network of associations between corals and their dinoflagellates (family Symbiodiniaceae) are the basis of coral reef ecosystems but are sensitive to increasing global temperatures. Coral-symbiont interactions are restricted by ecological and evolutionary determinants that constrain partner choice and influence holobiont response to environmental stress; however, little is known about how these processes shape thermal resilience of the holobiont. Here, we built a network of global coral-Symbiodiniaceae associations, mapped species traits (e.g., symbiont transmission mode and biogeography) and phylogenetic relationships of both partners onto the network, and assigned thermotolerance to both host and symbiont nodes. Using network analysis and phylogenetic comparative methods, we determined the contribution of species traits to thermal resilience of the holobiont, while accounting for evolutionary patterns among species. We found that the network shows nonrandom interactions among species, which are shaped by evolutionary history, symbiont transmission mode (horizontally transmitted [HT] or vertically transmitted [VT] corals) and biogeography. Coral phylogeny, but not Symbiodiniaceae phylogeny, symbiont transmission mode, or biogeography, was a good predictor of thermal resilience. Closely related corals have similar Symbiodiniaceae interaction patterns and bleaching susceptibilities. Nevertheless, the association patterns that explain increased host thermal resilience are not generalizable across the entire network but are instead unique to HT and VT corals. Under nonstress conditions, thermally resilient VT coral species associate with thermotolerant phylotypes and limit their number of unique symbionts and overall symbiont thermotolerance diversity, while thermally resilient HT coral species associate with a few host-specific symbiont phylotypes. IMPORTANCE Recent advances have revealed a complex network of interactions between coral and Symbiodiniaceae. Specifically, nonrandom association patterns, which are determined in part by restrictions imposed by symbiont transmission mode, increase the sensitivity of the overall network to thermal stress. However, little is known about the extent to which coral-Symbiodiniaceae network resistance to thermal stress is shaped by host and symbiont species phylogenetic relationships and host and symbiont species traits, such as symbiont transmission mode. We built a frequency-weighted global coral-Symbiodiniaceae network and used network analysis and phylogenetic comparative methods to show that evolutionary relatedness, but not transmission mode, predicts thermal resilience of the coral-Symbiodiniaceae holobiont. Consequently, thermal stress events could result in nonrandom pruning of susceptible lineages and loss of taxonomic diversity with catastrophic effects on community resilience to future events. Our results show that inclusion of the contribution of evolutionary and ecological processes will further our understanding of the fate of coral assemblages under climate change.

A Phylogenetic Independent Contrast Method under the Ornstein-Uhlenbeck Model and its Applications in Correlated Evolution

Phylogenetic comparative methods are essential in studying the evolution of traits across a phylogeny. Felsenstein's phylogenetic independent contrast (PIC) method and the generalized least squares (GLS) regression were often utilized to study whether evolutionary changes between traits were correlated. However, a neutral Brownian model is assumed in the PIC method, which impacts the performance of the PIC method when the trait is subject to adaptation. In recent years, the Ornstein-Uhlenbeck (OU) model has attracted increasing attention in studying the evolution of traits with stabilizing selection. In this study, we extended Felsenstein's PIC method under the OU model, which we termed OU-PIC. We simulated trait evolution under the OU model on phylogenetic trees with 8, 10, and 55 species. Compared to the PIC method, the OU-PIC method with correct stabilizing selection parameters achieved an appropriate type I error rate, the highest test power, and the lowest mean squared error. We presented a concise proof of the intrinsic connection between the OU-PIC and the generalized least squares (GLS) regression method in evaluating correlated evolution under the OU model. The OU-PIC method has a broad range of applications when trait evolution could be sufficiently modeled by the OU process. Compared with other phylogenetic comparative methods, OU-PIC avoids the inverse of the covariance matrix and would facilitate the analysis of correlated evolution on large phylogenies.