Technical comment on Condamine et al. (2019): a cautionary note for users of linear diversification dependencies

Condamine et al. (2019; 22: 1900–1912) fitted linear and exponential functions of time‐dependent, diversity‐dependent and temperature‐dependent diversification to investigate diversification dynamics of tetrapod families. Here I highlight potential misinterpretations when using linear diversification dependencies and provide some clarifications.     

Community trees: Identifying codiversification in the Páramo dipteran community

Groups of codistributed species that responded in a concerted manner to environmental events are expected to share patterns of evolutionary diversification. However, the identification of such groups has largely been based on qualitative, post hoc analyses. We develop here two methods (posterior predictive simulation [PPS], Kuhner–Felsenstein [K–F] analysis of variance [ANOVA]) for the analysis of codistributed species that, given a group of species with a shared pattern of diversification, allow empiricists to identify those taxa that do not codiversify (i.e., “outlier” species). The identification of outlier species makes it possible to jointly estimate the evolutionary history of co‐diversifying taxa. To evaluate the approaches presented here, we collected data from Páramo dipterans, identified outlier species, and estimated a “community tree” from species that are identified as having codiversified. Our results demonstrate that dipteran communities from different Páramo habitats in the same mountain range are more closely related than communities in other ranges. We also conduct simulation testing to evaluate this approach. Results suggest that our approach provides a useful addition to comparative phylogeographic methods, while identifying aspects of the analysis that require careful interpretation. In particular, both the PPS and K–F ANOVA perform acceptably when there are one or two outlier species, but less so as the number of outliers increases. This is likely a function of the corresponding degradation of the signal of community divergence; without a strong signal from a codiversifying community, there is no dominant pattern from which to detect an outlier species. For this reason, both the magnitude of K–F distance distribution and outside knowledge about the phylogeographic history of each putative member of the community should be considered when interpreting the results.     

The meaning of birth and death (in macroevolutionary birth-death models)

Birth–death models are central to much macroevolutionary theory. The fundamental parameters of these models concern durations. Different species concepts realize different species durations because they represent different ideas of what birth (speciation) and death (extinction) mean. Here, we use Cenozoic macroperforate planktonic foraminifera as a case study to ask: what are the dynamical consequences of changing the definition of birth and death? We show strong evidence for biotic constraints on diversification using evolutionary species, but less with morphospecies. Discussing reasons for this discrepancy, we emphasize that clarity of species concept leads to clarity of meaning when interpreting macroevolutionary birth–death models.     

Can extinction rates be estimated without fossils?

There is considerable interest in the possibility of using molecular phylogenies to estimate extinction rates. The present study aims at assessing the statistical performance of the birth-death model fitting approach to estimate speciation and extinction rates by comparison to the approach considering fossil data. A simulation-based approach was used. The diversification of a large number of lineages was simulated under a wide range of speciation and extinction rate values. The estimators obtained with fossils performed better than those without fossils. In the absence of fossils (e.g. with a molecular phylogeny), the speciation rate was correctly estimated in a wide range of situations; the bias of the corresponding estimator was close to zero for the largest trees. However, this estimator was substantially biased when the simulated extinction rate was high. On the other hand the estimator of extinction rate was biased in a wide range of situations. Surprisingly, this bias was lesser with medium-sized trees. Some recommendations for interpreting results from a diversification analysis are given.     

Rates of morphological evolution are correlated with species richness in salamanders

The tempo and mode of species diversification and phenotypic evolution vary widely across the tree of life, yet the relationship between these processes is poorly known. Previous tests of the relationship between rates of phenotypic evolution and rates of species diversification have assumed that species richness increases continuously through time. If this assumption is violated, simple phylogenetic estimates of net diversification rate may bear no relationship to processes that influence the distribution of species richness among clades. Here, we demonstrate that the variation in species richness among plethodontid salamander clades is unlikely to have resulted from simple time-dependent processes, leading to fundamentally different conclusions about the relationship between rates of phenotypic evolution and species diversification. Morphological evolutionary rates of both size and shape evolution are correlated with clade species richness, but are uncorrelated with simple estimators of net diversification that assume constancy of rates through time. This coupling between species diversification and phenotypic evolution is consistent with the hypothesis that clades with high rates of morphological trait evolution may diversify more than clades with low rates. Our results indicate that assumptions about underlying processes of diversity regulation have important consequences for interpreting macroevolutionary patterns.     

Neural circuit function redundancy in brain disorders

Redundancy is a ubiquitous property of the nervous system. This means that vastly different configurations of cellular and synaptic components can enable the same neural circuit functions. However, until recently, very little brain disorder research has considered the implications of this characteristic when designing experiments or interpreting data. Here, we first summarise the evidence for redundancy in healthy brains, explaining redundancy and three related sub-concepts: sloppiness, dependencies and multiple solutions. We then lay out key implications for brain disorder research, covering recent examples of redundancy effects in experimental studies on psychiatric disorders. Finally, we give predictions for future experiments based on these concepts.     

Diversification rates of the “Old Endemic” murine rodents of Luzon Island,Philippines are inconsistent with incumbency effects and ecological opportunity

Diversity‐dependent cladogenesis occurs when a colonizing lineage exhibits increasing interspecific competition as it ecologically diversifies. Repeated colonization of a region by closely related taxa may cause similar effects as species within each lineage compete with one another. This may be particularly relevant for secondary colonists, which could experience limited diversification due to competition with earlier, incumbent colonists over evolutionary time. We tested the hypothesis that an incumbent lineage may diminish the diversification of secondary colonists in two speciose clades of Philippine “Old Endemic” murine rodents—Phloeomyini and Chrotomyini—on the relatively old oceanic island of Luzon. Although phylogenetic analyses confirm the independent, noncontemporaneous colonization of Luzon by the ancestors of these two clades, we found no support for arrested diversification in either. Rather, it appears that diversification of both clades resulted from constant‐rate processes that were either uniform or favored the secondary colonists (Chrotomyini), depending on the method used. Our results suggest that ecological incumbency has not played an important role in determining lineage diversification among Luzon murines, despite sympatric occurrence by constituent species within each lineage, and a substantial head start for the primary colonists.     

Detecting Trait-Dependent Diversification Under Diversification Slowdowns

Testing whether a certain biological trait significantly affects clade diversification is central to macroevolutionary research. To this end, many scientists use constant-rate estimators (CR estimators) of diversification. However, it has never been examined whether these estimators report meaningful relationships between traits and diversification even when the diversification itself decelerates over time. In this study, I simulate trait-driven diversification concurrently with diversification slowdowns. Then, I test whether CR estimators manage to uncover the simulated relationships. Results suggest that CR estimators are robust against violation of rate constancy and successfully detect trait-dependent diversification in spite of diversification declines. Interestingly, correct results were recovered whether clade age correlated with clade diversity or not. Further comparison of CR estimators with QuaSSE suggested that QuaSSE performs better under constant diversification, but tends to report spuriously significant outcomes when diversification decelerates (=elevated Type I error). Given that diversification slowdowns have been recently reported for a wide range of taxa, these findings may be of particular relevance for future diversification studies.     

Interpreting the γ Statistic in Phylogenetic Diversification Rate Studies: A Rate Decrease Does Not Necessarily Indicate an Early Burst

Background

Phylogenetic hypotheses are increasingly being used to elucidate historical patterns of diversification rate-variation. Hypothesis testing is often conducted by comparing the observed vector of branching times to a null, pure-birth expectation. A popular method for inferring a decrease in speciation rate, which might suggest an early burst of diversification followed by a decrease in diversification rate is the γ statistic.

Methodology

Using simulations under varying conditions, I examine the sensitivity of γ to the distribution of the most recent branching times. Using an exploratory data analysis tool for lineages through time plots, tree deviation, I identified trees with a significant γ statistic that do not appear to have the characteristic early accumulation of lineages consistent with an early, rapid rate of cladogenesis. I further investigated the sensitivity of the γ statistic to recent diversification by examining the consequences of failing to simulate the full time interval following the most recent cladogenic event. The power of γ to detect rate decrease at varying times was assessed for simulated trees with an initial high rate of diversification followed by a relatively low rate.

Conclusions

The γ statistic is extraordinarily sensitive to recent diversification rates, and does not necessarily detect early bursts of diversification. This was true for trees of various sizes and completeness of taxon sampling. The γ statistic had greater power to detect recent diversification rate decreases compared to early bursts of diversification. Caution should be exercised when interpreting the γ statistic as an indication of early, rapid diversification.     

SYNDROME‐DRIVEN DIVERSIFICATION IN A MEDITERRANEAN ECOSYSTEM

Phylogenetic methods to detect lineage diversification have been traditionally used within a particular taxonomic clade, but rarely applied to detect local diversification. For understanding in situ diversification triggered by novel conditions it is necessary to focus on the time slice where such conditions occur. These new conditions may differentially affect the diversification rate of lineages with different morpho‐functional syndromes. A prominent example of these processes occurs in the Mediterranean Basin, where climate arising along the Tertiary/Quaternary transition acted as an environmental filter. In this context, lineages with different syndromes (sclerophyllous and nonsclerophyllous) are hypothesized to have different local diversification rates after the rise of the Mediterranean conditions. We used macroevolutionary methods of time‐dependent diversification on a calibrated local phylogeny accommodating topological and chronological uncertainty to test syndrome‐driven diversification in Mediterranean shrublands from the eastern Iberian Peninsula. We found phylogenetic evidence of higher speciation associated with the nonsclerophyllous syndrome, although extinction rates were similar between syndromes. Consequently a syndrome‐driven local diversification has occurred in shrublands under Mediterranean conditions. The results provide an example of how the integration of the environmental filter in a dated phylogeny may recreate the local history of lineages and help to explain assembly processes in Mediterranean ecosystems.     

Diversity Dynamics in Nymphalidae Butterflies: Effect of Phylogenetic Uncertainty on Diversification Rate Shift Estimates

The species rich butterfly family Nymphalidae has been used to study evolutionary interactions between plants and insects. Theories of insect-hostplant dynamics predict accelerated diversification due to key innovations. In evolutionary biology, analysis of maximum credibility trees in the software MEDUSA (modelling evolutionary diversity using stepwise AIC) is a popular method for estimation of shifts in diversification rates. We investigated whether phylogenetic uncertainty can produce different results by extending the method across a random sample of trees from the posterior distribution of a Bayesian run. Using the MultiMEDUSA approach, we found that phylogenetic uncertainty greatly affects diversification rate estimates. Different trees produced diversification rates ranging from high values to almost zero for the same clade, and both significant rate increase and decrease in some clades. Only four out of 18 significant shifts found on the maximum clade credibility tree were consistent across most of the sampled trees. Among these, we found accelerated diversification for Ithomiini butterflies. We used the binary speciation and extinction model (BiSSE) and found that a hostplant shift to Solanaceae is correlated with increased net diversification rates in Ithomiini, congruent with the diffuse cospeciation hypothesis. Our results show that taking phylogenetic uncertainty into account when estimating net diversification rate shifts is of great importance, as very different results can be obtained when using the maximum clade credibility tree and other trees from the posterior distribution.     

Ecobat: An online resource to facilitate transparent,evidence‐based interpretation of bat activity data

Acoustic surveys of bats are one of the techniques most commonly used by ecological practitioners. The results are used in Ecological Impact Assessments to assess the likely impacts of future developments on species that are widely protected in law, and to monitor developments’ postconstruction. However, there is no standardized methodology for analyzing or interpreting these data, which can make the assessment of the ecological value of a site very subjective. Comparisons of sites and projects are therefore difficult for ecologists and decision‐makers, for example, when trying to identify the best location for a new road based on relative bat activity levels along alternative routes. Here, we present a new web‐based, data‐driven tool, Ecobat, which addresses the need for a more robust way of interpreting ecological data. Ecobat offers users an easy, standardized, and objective method for analyzing bat activity data. It allows ecological practitioners to compare bat activity data at regional and national scales and to generate a numerical indicator of the relative importance of a night's worth of bat activity. The tool is free and open‐source; because the underlying algorithms are already developed, it could easily be expanded to new geographical regions and species. Data donation is required to ensure the robustness of the analyses; we use a positive feedback mechanism to encourage ecological practitioners to share data by providing in return high quality, contextualized data analysis, and graphical visualizations for direct use in ecological reports.     

Climate and host‐plant associations shaped the evolution of ceutorhynch weevils throughout the Cenozoic

Using molecular phylogenetic data and methods we inferred divergence times and diversification patterns for the weevil subfamily Ceutorhynchinae in the context of host‐plant associations and global climate over evolutionary time. We detected four major diversification shifts that correlate with both host shifts and major climate events. Ceutorhynchinae experienced an increase in diversification rate at ～53 Ma, during the Early Eocene Climate Optimum, coincident with a host shift to Lamiaceae. A second major diversification phase occurred at the end of the Eocene (～34 Ma). This contrasts with the overall deterioration in climate equability at the Eocene‐Oligocene boundary, but tracks the diversification of important host plant clades in temperate (higher) latitudes, leading to increased diversification rates in the weevil clades infesting temperate hosts. A third major phase of diversification is correlated with the rising temperatures of the Late Oligocene Warming Event (～26.5 Ma); diversification rates then declined shortly after the Middle Miocene Climate Transition (～14.9 Ma). Our results indicate that biotic and abiotic factors together explain the evolution of Ceutorhynchinae better than each of these drivers viewed in isolation.     

A practical guide to MaxEnt for modeling species’ distributions: what it does,and why inputs and settings matter

The MaxEnt software package is one of the most popular tools for species distribution and environmental niche modeling, with over 1000 published applications since 2006. Its popularity is likely for two reasons: 1) MaxEnt typically outperforms other methods based on predictive accuracy and 2) the software is particularly easy to use. MaxEnt users must make a number of decisions about how they should select their input data and choose from a wide variety of settings in the software package to build models from these data. The underlying basis for making these decisions is unclear in many studies, and default settings are apparently chosen, even though alternative settings are often more appropriate. In this paper, we provide a detailed explanation of how MaxEnt works and a prospectus on modeling options to enable users to make informed decisions when preparing data, choosing settings and interpreting output. We explain how the choice of background samples reflects prior assumptions, how nonlinear functions of environmental variables (features) are created and selected, how to account for environmentally biased sampling, the interpretation of the various types of model output and the challenges for model evaluation. We demonstrate MaxEnt’s calculations using both simplified simulated data and occurrence data from South Africa on species of the flowering plant family Proteaceae. Throughout, we show how MaxEnt’s outputs vary in response to different settings to highlight the need for making biologically motivated modeling decisions.     

C~3:Consensus Cancer Driver Gene Caller

Next-generation sequencing has allowed identification of millions of somatic mutations in human cancer cells.A key challenge in interpreting cancer genomes is to distinguish drivers of cancer development among available genetic mutations.To address this issue,we present the first webbased application,consensus cancer driver gene caller(C~3),to identify the consensus driver genes using six different complementary strategies,i.e.,frequency-based,machine learning-based,functional bias-based,clustering-based,statistics model-based,and network-based strategies.This application allows users to specify customized operations when calling driver genes,and provides solid statistical evaluations and interpretable visualizations on the integration results.C~3 is implemented in Python and is freely available for public use at http://drivergene.rwebox.com/c~3.     

Patterns of dental emergence in early anthropoid primates from the Fayum Depression,Egypt

Abstract

Paleontological field work in the Fayum Depression of Egypt has produced a remarkable diversity of fossil anthropoids, and this, combined with advances in genetic analyses of living anthropoids, has led to establishment of a temporal and phylogenetic framework for anthropoids that is achieving some degree of consensus. Less well understood are the evolutionary mechanisms and selective factors behind the origin and early diversification of anthropoids. One area that has remained under explored is investigation into the life history patterns of early anthropoids, a major omission given that understanding patterns of growth and development is essential for interpreting the paleobiology of fossil species. Here we detail dental emergence sequences for five species in four families of early anthropoid primates from the Fayum, and use these data to test Schultz’s Rule concerning the timing of emergence of molars versus premolars in mammals. Two important results are generated: (1) only one species had a dental eruption sequence identical to that observed among crown catarrhine primates; and (2) in all cases, the permanent canine was the last post-incisor dental element to fully erupt, a finding that may be significant for interpreting early anthropoid behavioral strategies.     

Processing multiple non-adjacent dependencies: evidence from sequence learning

Processing non-adjacent dependencies is considered to be one of the hallmarks of human language. Assuming that sequence-learning tasks provide a useful way to tap natural-language-processing mechanisms, we cross-modally combined serial reaction time and artificial-grammar learning paradigms to investigate the processing of multiple nested (A(1)A(2)A(3)B(3)B(2)B(1)) and crossed dependencies (A(1)A(2)A(3)B(1)B(2)B(3)), containing either three or two dependencies. Both reaction times and prediction errors highlighted problems with processing the middle dependency in nested structures (A(1)A(2)A(3)B(3)_B(1)), reminiscent of the 'missing-verb effect' observed in English and French, but not with crossed structures (A(1)A(2)A(3)B(1)_B(3)). Prior linguistic experience did not play a major role: native speakers of German and Dutch-which permit nested and crossed dependencies, respectively-showed a similar pattern of results for sequences with three dependencies. As for sequences with two dependencies, reaction times and prediction errors were similar for both nested and crossed dependencies. The results suggest that constraints on the processing of multiple non-adjacent dependencies are determined by the specific ordering of the non-adjacent dependencies (i.e. nested or crossed), as well as the number of non-adjacent dependencies to be resolved (i.e. two or three). Furthermore, these constraints may not be specific to language but instead derive from limitations on structured sequence learning.     

Genomic insight into “sky island” species diversification in a mountainous biodiversity hotspot

“Sky island” species diversification contributes greatly to mountainous biodiversity. However, the underlying genomic divergence and the inferred drivers remain largely unknown. In this study, we examined the diversification history of five diploid species with three exclusively endemic to the sky islands (mountains) of the Himalaya–Hengduan Mountains biodiversity hotspot. All of them together comprise a clade of the genus Eutrema (Brassicaceae). We resequenced genomes of multiple individuals of the found populations for each species. We recovered the inconsistent phylogenetic relationships between plastome and nuclear‐genome trees for one species. Based on nuclear population genomic data, we detected high genetic divergence between five species with limited gene flow. Four species seemed to diverge mainly through geographical isolation, whereas one arose through hybrid origin. The origins of the sampled five species were dated to within the late Miocene when mountains were uplifted and climates oscillated. All species decreased their population sizes since the inferred origin of each species initially, but only two of them expanded after the Last Glacial Maximum. Together, these findings suggest that geographic isolation plays an important role in driving the sky island species diversification of the sampled species in addition to the occasional gene flow that might have led to the hybrid origin of some sky island species, similar to the species diversification of sea islands.     

Patterns of host plant utilization and diversification in the brush‐footed butterflies

Herbivorous insects represent one of the most successful animal radiations known. They occupy a wide range of niches, feed on a great variety of plants, and are species rich; yet the factors that influence their diversification are poorly understood. Host breadth is often cited as a major factor influencing diversification, and, according to the Oscillation Hypothesis, shifts from generalist to specialist feeding states increase the diversification rate for a clade. We explored the relationship between host breadth and diversification within the Nymphalidae (Lepidoptera) and explicitly tested predictions of the Oscillation Hypothesis. We found strong evidence of diversification rate heterogeneity, but no difference in host breadth between clades with a higher diversification rate compared to their sisters. We also found some clades exhibited phylogenetic nonindependence in host breadth and these clades had lower host plant turnover than expected by chance, suggesting host breadth is evolutionarily constrained. Finally, we found that transitions among host breadth categories varied, but the likelihood of reductions in host breadth was greater than that of increases. Our results indicate host breadth is decoupled from diversification rate within the Nymphalidae, and that constraints on diet breadth might play an important role in the evolution of herbivorous insects.     

PREDATOR‐DRIVEN TRAIT DIVERSIFICATION IN A DRAGONFLY GENUS: COVARIATION IN BEHAVIORAL AND MORPHOLOGICAL ANTIPREDATOR DEFENSE

Proof for predation as an agent shaping evolutionary trait diversification is accumulating, however, our understanding how multiple antipredator traits covary due to phenotypic differentiation is still scarce. Species of the dragonfly genus Leucorrhinia underwent shifts from lakes with fish as top predators to fishless lakes with large dragonfly predators. This move to fishless lakes was accompanied by a partial loss and reduction of larval spines. Here, we show that Leucorrhinia also reduced burst swimming speed and its associated energy fuelling machinery, arginine kinase activity, when invading fishless lakes. This results in patterns of positive phylogenetic trait covariation between behavioral and morphological antipredator defense (trait cospecialization) and between behavioral antipredator defense and physiological machinery (trait codependence). Across species patterns of trait covariation between spine status, burst swimming speed and arginine kinase activity also matched findings within the phenotypically plastic L. dubia. Our results highlight the importance of predation as a factor affecting patterns of multiple trait covariation during phenotypic diversification.