Macroevolutionary Models Research Articles

Novel isolates expand the physiological diversity of Prochlorococcus and illuminate its macroevolution.

Prochlorococcus is a diverse picocyanobacterial genus and the most abundant phototroph on Earth. Its photosynthetic diversity divides it into high-light (HL)- or low-light (LL)-adapted groups representing broad phylogenetic grades-each composed of several monophyletic clades. Here, we physiologically characterize four new Prochlorococcus strains isolated from below the deep chlorophyll maximum in the North Pacific Ocean. We combine these physiological properties with genomic analyses to explore the evolution of photosynthetic antennae and discuss potential macroevolutionary implications. The isolates belong to deeply branching low-light-adapted clades that have no other cultivated representatives and display some unusual characteristics. For example, despite its otherwise low-light-adapted physiological characteristics, strain MIT1223 has low chl b2 content similar to high-light-adapted strains. Isolate genomes revealed that each strain contains a unique arsenal of pigment biosynthesis and binding alleles that have been horizontally acquired, contributing to the observed physiological diversity. Comparative genomic analysis of all picocyanobacteria reveals that Pcb, the major pigment carrying protein in Prochlorococcus, greatly increased in copy number and diversity per genome along a branch that coincides with the loss of facultative particle attachment. Collectively, these observations support a recently developed macroevolutionary model, in which niche-constructing radiations allowed ancestral lineages of picocyanobacteria to transition from a particle-attached to planktonic lifestyle and broadly colonize the euphotic zone.IMPORTANCEThe marine cyanobacterium, Prochlorococcus, is among the Earth's most abundant organisms, and much of its genetic and physiological diversity remains uncharacterized. Although field studies help reveal the scope of diversity, cultured isolates allow us to link genomic potential to physiological processes, illuminate eco-evolutionary feedbacks, and test theories arising from comparative genomics of wild cells. Here, we report the isolation and characterization of novel low-light (LL)-adapted Prochlorococcus strains that fill in multiple evolutionary gaps. These new strains are the first cultivated representatives of the LLVII and LLVIII paraphyletic grades of Prochlorococcus, which are broadly distributed in the lower regions of the ocean euphotic zone. Each of these grades is a unique, highly diverse section of the Prochlorococcus tree that separates distinct ecological groups: the LLVII grade branches between monophyletic clades that have facultatively particle-associated and constitutively planktonic lifestyles, whereas the LLVIII grade lies along the branch that leads to all high-light (HL)-adapted clades. Characterizing strains and genomes from these grades yields insights into the large-scale evolution of Prochlorococcus. The new LLVII and LLVIII strains are adapted to growth at very low irradiance levels and possess unique light-harvesting gene signatures and pigmentation. The LLVII strains represent the most basal Prochlorococcus group with a major expansion in photosynthetic antenna genes. Furthermore, a strain from the LLVIII grade challenges the paradigm that all LL-adapted Prochlorococcus exhibit high ratios of chl b:a2. These findings provide insights into the photophysiological evolution of Prochlorococcus and redefine what it means to be a low- vs high-light-adapted Prochlorococcus cell.

Why Were Zebras Not Domesticated? A Review of Domesticability Traits and Tests of Their Role in Ungulate Domestications with Macroevolutionary Models.

Since Darwin, many evolutionary and behavioral researchers have considered the role of phenotypic traits that favor the domestication of nonhuman animals. Among such proposed traits are a species' social structure, level of intra- and interspecific agonistic interactions, sociosexual behaviors, parental strategies, reaction to humans, habitat preference, dietary habits, developmental trajectories, and utility to humans. However, little to no comparative phylogenetic evidence exists concerning the importance of these attributes for the domestication of animals. Moreover, rather than considering domestication as a dichotomous event (non-domesticated vs. domesticated), humans and their potential domesticates encountered numerous socioecological challenges/obstacles during the domestication process before reaching the stage of full domestication. The present study explored the influence of adult body mass, gregariousness, dietary breadth, and reaction to humans on the domestication process of ungulates. The phylogenetic comparative model revealed that capture myopathy (CM), as a proxy for reaction to humans, negatively and significantly influenced the domestication process. The present paper also explored the evolution of CM in equine species in response to the presence of large carnivoran predators during the Pleistocene. Ecologies that preserved most of the large carnivoran predators of equine species also featured more equine taxa with CM (e.g., zebras), which were thus less suitable for domestication.

Exploring the Macroevolutionary Signature of Asymmetric Inheritance at Speciation.

Popular comparative phylogenetic models such as Brownian Motion, Ornstein-Ulhenbeck, and their extensions, assume that, at speciation, a trait value is inherited identically by two descendant species. This assumption contrasts with models of speciation at a micro-evolutionary scale where descendants' phenotypic distributions are sub-samples of the ancestral distribution. Different speciation mechanisms can lead to a displacement of the ancestral phenotypic mean among descendants and an asymmetric inheritance of the ancestral phenotypic variance. In contrast, even macro-evolutionary models that account for intraspecific variance assume symmetrically conserved inheritance of ancestral phenotypic distribution at speciation. Here we develop an Asymmetric Brownian Motion model (ABM) that relaxes the assumption of symmetric and conserved inheritance of the ancestral distribution at the time of speciation. The ABM jointly models the evolution of both intra- and inter-specific phenotypic variation. It also infers the mode of phenotypic inheritance at speciation, which can range from a symmetric and conserved inheritance, where descendants inherit the ancestral distribution, to an asymmetric and displaced inheritance, where descendants inherit divergent phenotypic means and variances. To demonstrate this model, we analyze the evolution of beak morphology in Darwin finches, finding evidence of displacement at speciation. The ABM model helps to bridge micro- and macro-evolutionary models of trait evolution by providing a more robust framework for testing the effects of ecological speciation, character displacement, and niche partitioning on trait evolution at the macro-evolutionary scale.

The Fractional MacroEvolution Model: a simple quantitative scaling macroevolution model

AbstractScaling fluctuation analyses of marine animal diversity and extinction and origination rates based on the Paleobiology Database occurrence data have opened new perspectives on macroevolution, supporting the hypothesis that the environment (climate proxies) and life (extinction and origination rates) are scaling over the “megaclimate” biogeological regime (from ≈1 Myr to at least 400 Myr). In the emerging picture, biodiversity is a scaling “crossover” phenomenon being dominated by the environment at short timescales and by life at long timescales with a crossover at ≈40 Myr. These findings provide the empirical basis for constructing the Fractional MacroEvolution Model (FMEM), a simple stochastic model combining destabilizing and stabilizing tendencies in macroevolutionary dynamics, driven by two scaling processes: temperature and turnover rates.Macroevolution models are typically deterministic (albeit sometimes perturbed by random noises) and are based on integer-ordered differential equations. In contrast, the FMEM is stochastic and based on fractional-ordered equations. Stochastic models are natural for systems with large numbers of degrees of freedom, and fractional equations naturally give rise to scaling processes.The basic FMEM drivers are fractional Brownian motions (temperature, T) and fractional Gaussian noises (turnover rates, E+) and the responses (solutions), are fractionally integrated fractional relaxation noises (diversity [D], extinction [E], origination [O], and E− = O − E). We discuss the impulse response (itself representing the model response to a bolide impact) and derive the model's full statistical properties. By numerically solving the model, we verified the mathematical analysis and compared both uniformly and irregularly sampled model outputs with paleobiology series.

A late burst of colour evolution in a radiation of songbirds (Passeriformes: Parulidae) suggests secondary contact drives signal divergence.

Evolutionary radiations provide important insights into species diversification, which is especially true of adaptive radiations. New World wood warblers (Parulidae) are a family of small, insectivorous, forest-dwelling passerine birds, often considered an exemplar of adaptive radiation due to their rapid diversification followed by a slowdown. However, they deviate from the expectations of an adaptive radiation scenario due to the lack of conspicuous morphological and ecological differentiation. We fitted several macroevolutionary models to trait data in 105 species of wood warblers. We tested whether morphological traits underwent an early burst of evolution (suggesting adaptation to new ecological niches in adaptive radiations) and whether song and colour underwent a diversity-dependent acceleration of trait evolutionary rate (consistent with reproductive interference driving signal evolution). Morphology and song evolved gradually under stabilizing selection, suggesting niche conservatism, with morphology possibly acting as a constraint on song evolution. In contrast, many feather colour traits underwent a diversity-dependent burst of evolution occurring late in the clade's history. We suggest that a two-step process has led to the remarkable diversification of wood warblers. First, their early diversification probably proceeded by allopatric speciation. Second, feather colour divergence likely occurred during secondary contact after range expansion. This diversification of signalling traits might have facilitated species coexistence, in combination with behavioural niche partitioning. Wood warblers seem to present characteristics of both adaptive and non-adaptive radiations.

Macroevolutionary constraints on global microbial diversity.

Biologists have long sought to quantify the number of species on Earth. Often missing from these efforts is the contribution of microorganisms, the smallest but most abundant form of life on the planet. Despite recent large-scale sampling efforts, estimates of global microbial diversity span many orders of magnitude. It is important to consider how speciation and extinction over the last 4 billion years constrain inventories of biodiversity. We parameterized macroevolutionary models based on birth-death processes that assume constant and universal speciation and extinction rates. The models reveal that richness beyond 1012 species is feasible and in agreement with empirical predictions. Additional simulations suggest that mass extinction events do not place hard limits on modern-day microbial diversity. Together, our study provides independent support for a massive global-scale microbiome while shedding light on the upper limits of life on Earth.

Digest: Complex dynamics of speciation and implications for macroevolutionary models.

What kinds of reproductive barriers are important for maintaining species integrity, and how are species boundaries preserved in the face of gene flow? Ivey et al. (2023) find little evidence for reproductive barriers and uncover a history of introgression between two incipient species of monkeyflower. These findings contribute to a growing body of work that calls for a reconsideration of how speciation dynamics are modeled at the macroevolutionary level.

Towards a global perspective for Salvia L.: Phylogeny, diversification and floral evolution.

Salvia is the most species-rich genus in Lamiaceae, encompassing approximately 1000 species distributed all over the world. We sought a new evolutionary perspective for Salvia by employing macroevolutionary analyses to address the tempo and mode of diversification. To study the association of floral traits with speciation and extinction, we modelled and explored the evolution of corolla length and the lever-mechanism pollination system across our Salvia phylogeny. We reconstructed a multigene phylogeny for 366 species of Salvia in the broad sense including all major recognized lineages and 50 species from Iran, a region previously overlooked in studies of the genus. Our comprehensive sampling of Iranian species of Salvia provides higher phylogenetic resolution for southwestern Asian species than obtained in previous studies. Our phylogenetic data in combination with divergence time estimates were used to examine the evolution of corolla length, woody versus herbaceous habit, and presence versus absence of a lever mechanism. We investigated the timing and dependence of Salvia diversification related to corolla length evolution through a disparity test and BAMM analysis. A HiSSE model was used to evaluate the dependency of diversification on the lever-mechanism pollination system in Salvia. A medium corolla length (15-18 mm) was reconstructed as the ancestral state for Salvia with multiple shifts to shorter and longer corollas. Macroevolutionary model analyses indicate that corolla length disparity is high throughout Salvia evolution, significantly different from expectations under a Brownian motion model during the last 28 million years of evolution. Our analyses show evidence of a higher diversification rate of corolla length for some Andean species of Salvia compared to other members of the genus. Based on our tests of diversification models, we reject the hypothesis of a direct effect of the lever mechanism on Salvia diversification. Therefore, we suggest caution in considering the lever-mechanism pollination system as one of the main drivers of speciation in Salvia.

A novel phylogenetic comparative method for evaluating the strength of branch-specific directional selection.

Phylogenetic comparative methods (PCMs) have played a central role in studying the evolution of phenotypic traits. However, when a trait experienced directional selection, previous PCMs have faced a dilemma between mathematically tractable but restrictive models (i.e., simple Gaussian process models) and flexible but intractable approaches (i.e., a simulation-based process model of phenotype evolution built on population genetics frameworks). This paper proposes a novel Gaussian process macroevolutionary model, called the "branch-specific directional selection (BSDS)," for evaluating the strength of directional selection to reconcile these two approaches. This model is based on a second-order approximation of a previous simulation-based process model but has a closed-form likelihood function. This can also be extended to incorporate intraspecies variations and to linear mixed models, which are necessary for meta-analysis. We conduct numerical experiments to validate the proposed method and apply it to the brain volume of Hominidae species. The results show that the proposed methods yield statistically more reliable inferences and computational time is about hundred thousand times faster than the previous simulation-based methods. Further extensions of the BSDS model are expected to provide a clearer picture of the connection of microevolutionary processes and macroevolutionary patterns.

The Shape of Phylogenies Under Phase-Type Distributed Times to Speciation and Extinction

Phylogenetic trees describe relationships between extant species, but beyond that their shape and their relative branch lengths can provide information on broader evolutionary processes of speciation and extinction. However, currently many of the most widely used macro-evolutionary models make predictions about the shapes of phylogenetic trees that differ considerably from what is observed in empirical phylogenies. Here, we propose a flexible and biologically plausible macroevolutionary model for phylogenetic trees where times to speciation or extinction events are drawn from a Coxian phase-type (PH) distribution. First, we show that different choices of parameters in our model lead to a range of tree balances as measured by Aldous’ beta statistic. In particular, we demonstrate that it is possible to find parameters that correspond well to empirical tree balance. Next, we provide a natural extension of the beta statistic to sets of trees. This extension produces less biased estimates of beta compared to using the median beta values from individual trees. Furthermore, we derive a likelihood expression for the probability of observing an edge-weighted tree under a model with speciation but no extinction. Finally, we illustrate the application of our model by performing both absolute and relative goodness-of-fit tests for two large empirical phylogenies (squamates and angiosperms) that compare models with Coxian PH distributed times to speciation with models that assume exponential or Weibull distributed waiting times. In our numerical analysis, we found that, in most cases, models assuming a Coxian PH distribution provided the best fit.

Bird lineages colonizing urban habitats have diversified at high rates across deep time.

AimUrbanization exposes species to novel ecological conditions. Some species thrive in urban areas, whereas many others are excluded from these human‐made environments. Previous analyses suggest that the ability to cope with rapid environmental change is associated with long‐term patterns of diversification, but whether the suite of traits associated with the ability to colonize urban environments is linked to this process remains poorly understood.LocationWorld.Time periodCurrent.Major taxa studiedPasserine birds.MethodsWe applied macroevolutionary models to a large dataset of passerine birds to compare the evolutionary history of urban‐tolerant species with that of urban‐avoidant species. Specifically, we examined models of state‐dependent speciation and extinction to assess the macroevolution of urban tolerance as a binary trait, in addition to models of quantitative trait‐dependent diversification based on relative urban abundance. We also ran simulation‐based model assessments to explore potential sources of bias.ResultsWe provide evidence that historically, species with traits promoting urban colonization have undergone faster diversification than urban‐avoidant species, indicating that urbanization favours clades with a historical tendency towards rapid speciation or reduced extinction. In addition, we find that past transitions towards states that currently impede urban colonization by passerines have been more frequent than in the opposite direction. Furthermore, we find a portion of urban‐avoidant passerines to be recent and to undergo fast diversification. All highly supported models give this result consistently.Main conclusionsUrbanization is mainly associated with the loss of lineages that are inherently more vulnerable to extinction over deep time, whereas cities tend to be colonized by less vulnerable lineages, for which urbanization might be neutral or positive in terms of longer‐term diversification. Urban avoidance is associated with high rates of recent diversification for some clades occurring in regions with relatively intact natural ecosystems and low current levels of urbanization.

Computational Modeling of Gluteus Medius Muscle Moment Arm in Caviomorph Rodents Reveals Ecomorphological Specializations.

Vertebrate musculoskeletal locomotion is realized through lever-arm systems. The instantaneous muscle moment arm (IMMA), which is expected to be under selective pressure and thus of interest for ecomorphological studies, is a key aspect of these systems. The IMMA changes with joint motion. It’s length change is technically difficult to acquire and has not been compared in a larger phylogenetic ecomorphological framework, yet. Usually, proxies such as osteological in-levers are used instead. We used 18 species of the ecologically diverse clade of caviomorph rodents to test whether its diversity is reflected in the IMMA of the hip extensor M. gluteus medius. A large IMMA is beneficial for torque generation; a small IMMA facilitates fast joint excursion. We expected large IMMAs in scansorial species, small IMMAs in fossorial species, and somewhat intermediate IMMAs in cursorial species, depending on the relative importance of acceleration and joint angular velocity. We modeled the IMMA over the entire range of possible hip extensions and applied macroevolutionary model comparison to selected joint poses. We also obtained the osteological in-lever of the M. gluteus medius to compare it to the IMMA. At little hip extension, the IMMA was largest on average in scansorial species, while the other two lifestyles were similar. We interpret this as an emphasized need for increased hip joint torque when climbing on inclines, especially in a crouched posture. Cursorial species might benefit from fast joint excursion, but their similarity with the fossorial species is difficult to interpret and could hint at ecological similarities. At larger extension angles, cursorial species displayed the second-largest IMMAs after scansorial species. The larger IMMA optimum results in powerful hip extension which coincides with forward acceleration at late stance beneficial for climbing, jumping, and escaping predators. This might be less relevant for a fossorial lifestyle. The results of the in-lever only matched the IMMA results of larger hip extension angles, suggesting that the modeling of the IMMA provides more nuanced insights into adaptations of musculoskeletal lever-arm systems than this osteological proxy.

Are chromosome number and genome size associated with habit and environmental niche variables? Insights from the Neotropical orchids.

The entangled relationship of chromosome number and genome size with species distribution has been the subject of study for almost a century, but remains an open question due to previous ecological and phylogenetic knowledge constraints. To better address this subject, we used the clade Maxillariinae, a widely distributed and karyotypically known orchid group, as a model system to infer such relationships in a robust methodological framework. Based on the literature and new data, we gathered the chromosome number and genome size for 93 and 64 species, respectively. We built a phylogenetic hypothesis and assessed the best macroevolutionary model for both genomic traits. Additionally, we collected together ecological data (preferences for bioclimatic variables, elevation and habit) used as explanatory variables in multivariate phylogenetic models explaining genomic traits. Finally, the impact of polyploidy was estimated by running the analyses with and without polyploids in the sample. The association between genomic and ecological data varied depending on whether polyploids were considered or not. Without polyploids, chromosome number failed to present consistent associations with ecological variables. With polyploids, there was a tendency to waive epiphytism and colonize new habitats outside humid forests. The genome size showed association with ecological variables: without polyploids, genome increase was associated with flexible habits, with higher elevation and with drier summers; with polyploids, genome size increase was associated with colonizing drier environments. The chromosome number and genome size variations, essential but neglected traits in the ecological niche, are shaped in the Maxillariinae by both neutral and adaptive evolution. Both genomic traits are partially correlated to bioclimatic variables and elevation, even when controlling for phylogenetic constraints. While polyploidy was associated with shifts in the environmental niche, the genome size emerges as a central trait in orchid evolution by the association between small genome size and epiphytism, a key innovation to Neotropical orchid diversification.

Evolvability in the fossil record

AbstractThe concept of evolvability—the capacity of a population to produce and maintain evolutionarily relevant variation—has become increasingly prominent in evolutionary biology. Paleontology has a long history of investigating questions of evolvability, but paleontological thinking has tended to neglect recent discussions, because many tools used in the current evolvability literature are challenging to apply to the fossil record. The fundamental difficulty is how to disentangle whether the causes of evolutionary patterns arise from variational properties of traits or lineages rather than being due to selection and ecological success. Despite these obstacles, the fossil record offers unique and growing sources of data that capture evolutionary patterns of sustained duration and significance otherwise inaccessible to evolutionary biologists. Additionally, there exist a variety of strategic possibilities for combining prominent neontological approaches to evolvability with those from paleontology. We illustrate three of these possibilities with quantitative genetics, evolutionary developmental biology, and phylogenetic models of macroevolution. In conclusion, we provide a methodological schema that focuses on the conceptualization, measurement, and testing of hypotheses to motivate and provide guidance for future empirical and theoretical studies of evolvability in the fossil record.

Biogeography of curimatid fishes reveals multiple lowland-upland river transitions and differential diversification in the Neotropics (Teleostei, Curimatidae).

The Neotropics harbors a megadiverse ichthyofauna comprising over 6300 species with approximately 80% in just three taxonomic orders within the clade Characiphysi. This highly diverse group has evolved in tropical South America over tens to hundreds of millions of years influenced mostly by re‐arrangements of river drainages in lowland and upland systems. In this study, we investigate patterns of spatial diversification in Neotropical freshwater fishes in the family Curimatidae, a species‐rich clade of the order Characiformes. Specifically, we examined ancestral areas, dispersal events, and shifts in species richness using spatially explicit biogeographic and macroevolutionary models to determine whether lowlands–uplands serve as museums or cradles of diversification for curimatids. We used fossil information to estimate divergence times in BEAST, multiple time‐stratified models of geographic range evolution in BioGeoBEARS, and alternative models of geographic state‐dependent speciation and extinction in GeoHiSSE. Our results suggest that the most recent common ancestor of curimatids originated in the Late Cretaceous likely in lowland paleodrainages of northwestern South America. Dispersals from lowland to upland river basins of the Brazilian and Guiana shields occurred repeatedly across independently evolving lineages in the Cenozoic. Colonization of upland drainages was often coupled with increased rates of net diversification in species‐rich genera such as Cyphocharax and Steindachnerina. Our findings demonstrate that colonization of novel aquatic environments at higher elevations is associated with an increased rate of diversification, although this pattern is clade‐dependent and driven mostly by allopatric speciation. Curimatids reinforce an emerging perspective that Amazonian lowlands act as a museum by accumulating species along time, whereas the transitions to uplands stimulate higher net diversification rates and lineage diversification.

Phylogenomic and Macroevolutionary Evidence for an Explosive Radiation of a Plant Genus in the Miocene.

Mountain systems harbor a substantial fraction of global biodiversity and, thus, provide excellent opportunities to study rapid diversification and to understand the historical processes underlying the assembly of biodiversity hotspots. The rich biodiversity in mountains is widely regarded as having arisen under the influence of geological and climatic processes as well as the complex interactions among them. However, the relative contribution of geology and climate in driving species radiation is seldom explored. Here, we studied the evolutionary radiation of Oreocharis (Gesneriaceae), which has diversified extensively throughout East Asia, especially within the Hengduan Mountains (HDM), using transcriptomic data and a time calibrated phylogeny for 88% (111/126) of all species of the genus. In particular, we applied phylogenetic reconstructions to evaluate the extent of incomplete lineage sorting accompanying the early and rapid radiation in the genus. We then fit macroevolutionary models to explore its spatial and diversification dynamics in Oreocharis and applied explicit birth–death models to investigate the effects of past environmental changes on its diversification. Evidence from 574 orthologous loci suggest that Oreocharis underwent an impressive early burst of speciation starting ca. 12 Ma in the Miocene, followed by a drastic decline in speciation toward the present. Although we found no evidence for a shift in diversification rate across the phylogeny of Oreocharis, we showed a difference in diversification dynamics between the HDM and non-HDM lineages, with higher diversification rates in the HDM. The diversification dynamic of Oreocharis is most likely positively associated with temperature-dependent speciation and dependency on the Asian monsoons. We suggest that the warm and humid climate of the mid-Miocene was probably the primary driver of the rapid diversification in Oreocharis, while mountain building of the HDM might have indirectly affected species diversification of the HDM lineage. This study highlights the importance of past climatic changes, combined with mountain building, in creating strong environmental heterogeneity and driving diversification of mountain plants, and suggests that the biodiversity in the HDM cannot directly be attributed to mountain uplift, contrary to many recent speculations.[East Asian monsoons; environmental heterogeneity; Hengduan Mountains; incomplete lineage sorting; Oreocharis; past climate change; rapid diversification; transcriptome.]

Unifying Phylogenetic Birth-Death Models in Epidemiology and Macroevolution.

Birth–death stochastic processes are the foundations of many phylogenetic models and are widely used to make inferences about epidemiological and macroevolutionary dynamics. There are a large number of birth–death model variants that have been developed; these impose different assumptions about the temporal dynamics of the parameters and about the sampling process. As each of these variants was individually derived, it has been difficult to understand the relationships between them as well as their precise biological and mathematical assumptions. Without a common mathematical foundation, deriving new models is nontrivial. Here, we unify these models into a single framework, prove that many previously developed epidemiological and macroevolutionary models are all special cases of a more general model, and illustrate the connections between these variants. This unification includes both models where the process is the same for all lineages and those in which it varies across types. We also outline a straightforward procedure for deriving likelihood functions for arbitrarily complex birth–death(-sampling) models that will hopefully allow researchers to explore a wider array of scenarios than was previously possible. By rederiving existing single-type birth–death sampling models, we clarify and synthesize the range of explicit and implicit assumptions made by these models. [Birth–death processes; epidemiology; macroevolution; phylogenetics; statistical inference.]

Ecological Limits on the Decoupling of Prey Capture and Processing in Fishes.

Ray-finned fishes have two jaw systems, the oral and pharyngeal jaws, which perform functions associated with prey capture and processing, respectively. The structural independence of the jaw systems is recognized as having broad implications for the functional and ecological diversity of the radiation. Cichlids (and a few other lineages) possess a modified pharyngeal jaw system that enhances prey processing versatility and capacity. This innovation, pharyngognathy, is hypothesized to have freed the oral jaws to diversify in terms of prey capture. We test the relative role of prey capture properties (e.g., evasiveness) and prey processing (e.g., crushing) in driving divergent selection in the oral and pharyngeal jaws using a macroevolutionary model fitting framework. Evolutionary outcomes were asymmetric. All transitions between different properties of prey capture had a corresponding transition in properties of prey processing. In contrast, fewer than half the transitions in the properties of prey processing had a corresponding prey capture transition. This discrepancy was further highlighted by multi-peak models that reflect the opposing function of each jaw system, which fit better than null models for oral jaw traits, but not pharyngeal jaw traits. These results suggest that pharyngeal jaw function can change independently from the function of the oral jaws, but not vice versa. This finding highlights the possibility of ecological limits to the evolutionary decoupling of jaw systems. The independent actions of prey capture and processing may be decoupled, but their respective functional demands (and evolution) are not. Therefore, prey likely impose some degree of coordinated evolution between acquisition and processing functional morphology, even in decoupled jaw systems.

Geographic and subsequent biotic isolations led to a diversity anomaly of section Heterotropa (genus Asarum: Aristolochiaceae) in insular versus continental regions of the Sino‐Japanese Floristic Region

AbstractAimThe Sino‐Japanese Floristic Region has extremely high species diversity with respect to temperate plants; however, the reasons for this diversity are poorly understood because most studies have only considered geographic isolation caused by climatic oscillations. In some plant groups, high floral trait diversity and uneven species diversity between insular systems and the continental area suggest other factors may have important roles too. The primary purpose of this study is to reveal how abiotic and biotic factors have shaped the species diversity anomaly of Heterotropa between the insular systems and the continental area.LocationThe Sino‐Japanese Floristic Region.TaxonSection Heterotropa (genus Asarum; Aristolochiaceae).MethodsUsing ddRAD‐seq and chloroplast genome data, we built a time‐calibrated phylogenetic tree including 79 species. We estimated the patterns of floral traits (flowering time and floral size) evolution using macroevolutionary modelling, and tested the correlation of speciation rate with the trait evolution rates. Finally, we estimated the isolation factors of all taxa pairs and sister‐taxa pairs based on distribution range and floral traits.ResultsPhylogenetic analysis indicated that Heterotropa was diverged into two clades (continental clade and insular clade) in the Miocene, and the major subclades corresponded to geographic entities. Most rate shifts accelerating floral trait's evolution occurred during the Pleistocene period. Evolution rate of floral traits showed positive correlation with the speciation rate. Large proportion of taxa in the insular clade are distributed allopatrically. Several sister pairs showed floral trait divergence with geographic overlap.Main ConclusionsThe diversification of Heterotropa appears to have been triggered by geographic and climatic events, and subsequent repeated floral trait evolution with and without geographic isolation. Furthermore, the high species diversity in the insular systems would have been formed by the repeated range fragmentations and contractions. Our study demonstrates the importance of multidimensional studies to understand the diversification process of temperate plants in the Sino‐Japanese Floristic Region.

Insights from macroevolutionary modelling and ancestral state reconstruction into the radiation and historical dietary ecology of Lemuriformes (Primates, Mammalia)

BackgroundLemurs once rivalled the diversity of rest of the primate order despite thier confinement to the island of Madagascar. We test the adaptive radiation model of Malagasy lemur diversity using a novel combination of phylogenetic comparative methods and geometric methods for quantifying tooth shape.ResultsWe apply macroevolutionary model fitting approaches and disparity through time analysis to dental topography metrics associated with dietary adaptation, an aspect of mammalian ecology which appears to be closely related to diversification in many clades. Metrics were also reconstructed at internal nodes of the lemur tree and these reconstructions were combined to generate dietary classification probabilities at internal nodes using discriminant function analysis. We used these reconstructions to calculate rates of transition toward folivory per million-year intervals. Finally, lower second molar shape was reconstructed at internal nodes by modelling the change in shape of 3D meshes using squared change parsimony along the branches of the lemur tree. Our analyses of dental topography metrics do not recover an early burst in rates of change or a pattern of early partitioning of subclade disparity. However, rates of change in adaptations for folivory were highest during the Oligocene, an interval of possible forest expansion on the island.ConclusionsThere was no clear phylogenetic signal of bursts of morphological evolution early in lemur history. Reconstruction of the molar morphologies corresponding to the ancestral nodes of the lemur tree suggest that this may have been driven by a shift toward defended plant resources, however. This suggests a response to the ecological opportunity offered by expanding forests, but not necessarily a classic adaptive radiation initiated by dispersal to Madagascar.