Linking Ecological Specialization to Its Macroevolutionary Consequences: An Example with Passerine Nest Type.

A long-standing hypothesis in evolutionary biology is that the evolution of resource specialization can lead to an evolutionary dead end, where specialists have low diversification rates and limited ability to evolve into generalists. In recent years, advances in comparative methods investigating trait-based differences associated with diversification have enabled more robust tests of this idea and have found mixed support. We test the evolutionary dead end hypothesis by estimating net diversification rate differences associated with nest-type specialization among 3224 species of passerine birds. In particular, we test whether the adoption of hole-nesting, a nest-type specialization that decreases predation, results in reduced diversification rates relative to nesting outside of holes. Further, we examine whether evolutionary transitions to the specialist hole-nesting state have been more frequent than transitions out of hole-nesting. Using diversification models that accounted for background rate heterogeneity and different extinction rate scenarios, we found that hole-nesting specialization was not associated with diversification rate differences. Furthermore, contrary to the assumption that specialists rarely evolve into generalists, we found that transitions out of hole-nesting occur more frequently than transitions into hole-nesting. These results suggest that interspecific competition may limit adoption of hole-nesting, but that such competition does not result in limited diversification of hole-nesters. In conjunction with other recent studies using robust comparative methods, our results add to growing evidence that evolutionary dead ends are not a typical outcome of resource specialization. [Cavity nesting; diversification; hidden-state models; passerines; resource specialization.].

Unearthing Modes of Climatic Adaptation in Underground Storage Organs Across Liliales.

Testing adaptive hypotheses about how continuous traits evolve in association with developmentally structured discrete traits, while accounting for the confounding influence of other, hidden, evolutionary forces, remains a challenge in evolutionary biology. For example, geophytes are herbaceous plants-with underground buds-that use underground storage organs (USOs) to survive extended periods of unfavorable conditions. Such plants have evolved multiple times independently across all major vascular plant lineages. Even within closely related lineages, however, geophytes show impressive variation in the morphological modifications and structures (i.e.,"types" of USOs) that allow them to survive underground. Despite the developmental and structural complexity of USOs, the prevailing hypothesis is that they represent convergent evolutionary "solutions" to a common ecological problem, though some recent research has drawn this conclusion into question. We extend existing phylogenetic comparative methods to test for links between the hierarchical discrete morphological traits associated with USOs and adaptation to environmental variables, using a phylogeny of 621 species in Liliales. We found that plants with different USO types do not differ in climatic niche more than expected by chance, with the exception of root morphology, where modified roots are associated with lower temperature seasonality. These findings suggest that root tubers may reflect adaptations to different climatic conditions than those represented by other types of USOs. Thus, the tissue type and developmental origin of the USO structure may influence the way it mediates ecological relationships, which draws into question the appropriateness of ascribing broad ecological patterns uniformly across geophytic taxa. This work provides a new framework for testing adaptive hypotheses and for linking ecological patterns across morphologically varying taxa while accounting for developmental (non-independent) relationships in morphological data. [Climatic niche evolution; geophytes; imperfect correspondence; macroevolution.].

Trait-dependent diversification in angiosperms: Patterns, models and data.

Variation in species richness across the tree of life, accompanied by the incredible variety of ecological and morphological characteristics found in nature, has inspired many studies to link traits with species diversification. Angiosperms are a highly diverse group that has fundamentally shaped life on earth since the Cretaceous, and illustrate how species diversification affects ecosystem functioning. Numerous traits and processes have been linked to differences in species richness within this group, but we know little about their relative importance and how they interact. Here, we synthesised data from 152 studies that used state-dependent speciation and extinction (SSE) models on angiosperm clades. Intrinsic traits related to reproduction and morphology were often linked to diversification but a set of universal drivers did not emerge as traits did not have consistent effects across clades. Importantly, SSE model results were correlated to data set properties - trees that were larger, older or less well-sampled tended to yield trait-dependent outcomes. We compared these properties to recommendations for SSE model use and provide a set of best practices to follow when designing studies and reporting results. Finally, we argue that SSE model inferences should be considered in a larger context incorporating species' ecology, demography and genetics.

Wallacean and Melanesian Islands Promote Higher Rates of Diversification within the Global Passerine Radiation Corvides.

The complex island archipelagoes of Wallacea and Melanesia have provided empirical data behind integral theories in evolutionary biology, including allopatric speciation and island biogeography. Yet, questions regarding the relative impact of the layered biogeographic barriers, such as deep-water trenches and isolated island systems, on faunal diversification remain underexplored. One such barrier is Wallace's Line, a significant biogeographic boundary that largely separates Australian and Asian biodiversity. To assess the relative roles of biogeographic barriers-specifically isolated island systems and Wallace's Line-we investigated the tempo and mode of diversification in a diverse avian radiation, Corvides (Crows and Jays, Birds-of-paradise, Vangas, and allies). We combined a genus-level data set of thousands of ultraconserved elements (UCEs) and a species-level, 12-gene Sanger sequence matrix to produce a well-resolved supermatrix tree that we leveraged to explore the group's historical biogeography and the effects of the biogeographic barriers on their macroevolutionary dynamics. The tree is well resolved and differs substantially from what has been used extensively for past comparative analyses within this group. We confirmed that Corvides, and its major constituent clades, arose in Australia and that a burst of dispersals west across Wallace's Line occurred after the uplift of Wallacea during the mid-Miocene. We found that dispersal across this biogeographic barrier was generally rare, though westward dispersals were two times more frequent than eastward dispersals. Wallacea's central position between Sundaland and Sahul no doubt acted as a bridge for island-hopping dispersal out of Australia, across Wallace's Line, to colonize the rest of Earth. In addition, we found that the complex island archipelagoes east of Wallace's Line harbor the highest rates of net diversification and are a substantial source of colonists to continental systems on both sides of this biogeographic barrier. Our results support emerging evidence that island systems, particularly the geologically complex archipelagoes of the Indo-pacific, are drivers of species diversification. [Historical biogeography; island biogeography; Melanesia; molecular phylogenetics; state-dependent diversification and extinction.].

Pulled Diversification Rates, Lineages-Through-Time Plots, and Modern Macroevolutionary Modeling.

Estimating time-dependent rates of speciation and extinction from dated phylogenetic trees of extant species (timetrees), and determining how and why they vary, is key to understanding how ecological and evolutionary processes shape biodiversity. Due to an increasing availability of phylogenetic trees, a growing number of process-based methods relying on the birth-death model have been developed in the last decade to address a variety of questions in macroevolution. However, this methodological progress has regularly been criticized such that one may wonder how reliable the estimations of speciation and extinction rates are. In particular, using lineages-through-time (LTT) plots, a recent study has shown that there are an infinite number of equally likely diversification scenarios that can generate any timetree. This has led to questioning whether or not diversification rates should be estimated at all. Here, we summarize, clarify, and highlight technical considerations on recent findings regarding the capacity of models to disentangle diversification histories. Using simulations, we illustrate the characteristics of newly proposed "pulled rates" and their utility. We recognize that the recent findings are a step forward in understanding the behavior of macroevolutionary modeling, but they in no way suggest we should abandon diversification modeling altogether. On the contrary, the study of macroevolution using phylogenetic trees has never been more exciting and promising than today. We still face important limitations in regard to data availability and methods, but by acknowledging them we can better target our joint efforts as a scientific community. [Birth-death models; extinction; phylogenetics; speciation.].

Interaction among ploidy, breeding system and lineage diversification.

If particular traits consistently affect rates of speciation and extinction, broad macroevolutionary patterns can be interpreted as consequences of selection at high levels of the biological hierarchy. Identifying traits associated with diversification rates is difficult because of the wide variety of characters under consideration and the statistical challenges of testing for associations from comparative phylogenetic data. Ploidy (diploid vs polyploid states) and breeding system (self-incompatible vs self-compatible states) are both thought to be drivers of differential diversification in angiosperms. We fit 29 diversification models to extensive trait and phylogenetic data in Solanaceae and investigate how speciation and extinction rate differences are associated with ploidy, breeding system, and the interaction between these traits. We show that diversification patterns in Solanaceae are better explained by breeding system and an additional unobserved factor, rather than by ploidy. We also find that the most common evolutionary pathway to polyploidy in Solanaceae occurs via direct breakdown of self-incompatibility by whole genome duplication, rather than indirectly via breakdown followed by polyploidization. Comparing multiple stochastic diversification models that include complex trait interactions alongside hidden states enhances our understanding of the macroevolutionary patterns in plant phylogenies.

Rethinking phylogenetic comparative methods.

As a result of the process of descent with modification, closely related species tend to be similar to one another in a myriad different ways. In statistical terms, this means that traits measured on one species will not be independent of traits measured on others. Since their introduction in the 1980s, phylogenetic comparative methods (PCMs) have been framed as a solution to this problem. In this article, we argue that this way of thinking about PCMs is deeply misleading. Not only has this sowed widespread confusion in the literature about what PCMs are doing but has led us to develop methods that are susceptible to the very thing we sought to build defenses against-unreplicated evolutionary events. Through three Case Studies, we demonstrate that the susceptibility to singular events is indeed a recurring problem in comparative biology that links several seemingly unrelated controversies. In each Case Study, we propose a potential solution to the problem. While the details of our proposed solutions differ, they share a common theme: unifying hypothesis testing with data-driven approaches (which we term "phylogenetic natural history") to disentangle the impact of singular evolutionary events from that of the factors we are investigating. More broadly, we argue that our field has, at times, been sloppy when weighing evidence in support of causal hypotheses. We suggest that one way to refine our inferences is to re-imagine phylogenies as probabilistic graphical models; adopting this way of thinking will help clarify precisely what we are testing and what evidence supports our claims.

Evolution of floral traits and impact of reproductive mode on diversification in the phlox family (Polemoniaceae).

Pollinator-mediated selection is a major driver of evolution in flowering plants, contributing to the vast diversity of floral features. Despite long-standing interest in floral variation and the evolution of pollination syndromes in Polemoniaceae, the evolution of floral traits and known pollinators has not been investigated in an explicit phylogenetic context. Here we explore macroevolutionary patterns of both pollinator specificity and three floral traits long considered important determinants of pollinator attraction across the most comprehensive species-level phylogenetic tree yet produced for the family. The presence of floral chlorophyll is reconstructed as the ancestral character state of the family, even though the presence of floral anthocyanins is the most prevalent floral pigment in extant taxa. Mean corolla length and width of the opening of the floral tube are correlated, and both appear to vary with pollinator type. The evolution of pollination systems appears labile, with multiple gains and losses of selfing and conflicting implications for patterns of diversification. Explicit testing of diversification models rejects the hypothesis that selfing is an evolutionary dead-end. This study begins to disentangle the individual components that comprise pollination syndromes and lays the foundation for future work on the genetic mechanisms that control each trait.

Evaluating the role of genome downsizing and size thresholds from genome size distributions in angiosperms.

PREMISE OF THE STUDY: Whole-genome duplications (WGDs) can rapidly increase genome size in angiosperms. Yet their mean genome size is not correlated with ploidy. We compared three hypotheses to explain the constancy of genome size means across ploidies. The genome downsizing hypothesis suggests that genome size will decrease by a given percentage after a WGD. The genome size threshold hypothesis assumes that taxa with large genomes or large monoploid numbers will fail to undergo or survive WGDs. Finally, the genome downsizing and threshold hypothesis suggests that both genome downsizing and thresholds affect the relationship between genome size means and ploidy. METHODS: We performed nonparametric bootstrap simulations to compare observed angiosperm genome size means among species or genera against simulated genome sizes under the three different hypotheses. We evaluated the hypotheses using a decision theory approach and estimated the expected percentage of genome downsizing. KEY RESULTS: The threshold hypothesis improves the approximations between mean genome size and simulated genome size. At the species level, the genome downsizing with thresholds hypothesis best explains the genome size means with a 15% genome downsizing percentage. In the genus level simulations, the monoploid number threshold hypothesis best explains the data. CONCLUSIONS: Thresholds of genome size and monoploid number added to genome downsizing at species level simulations explain the observed means of angiosperm genome sizes, and monoploid number is important for determining the genome size mean at the genus level.

Conservation applications of niche modeling: Native and naturalized ferns may compete for limited Hawaiian dryland habitat.

Premise: Competition from naturalized species and habitat loss are common threats to native biodiversity and may act synergistically to increase competition for decreasing habitat availability. We use Hawaiian dryland ferns as a model for the interactions between land-use change and competition from naturalized species in determining habitat availability. Methods: We used fine-resolution climatic variables and carefully curated occurrence data from herbaria and community science repositories to estimate the distributions of Hawaiian dryland ferns. We quantified the degree to which naturalized ferns tend to occupy areas suitable for native species and mapped the remaining available habitat given land-use change. Results: Of all native species, Doryopteris angelica had the lowest percentage of occurrences of naturalized species in its suitable area while D. decora had the highest. However, all Doryopteris spp. had a higher percentage overlap, while Pellaea ternifolia had a lower percentage overlap, than expected by chance. Doryopteris decora and D. decipiens had the lowest proportions (<20%) of suitable area covering native habitat. Discussion: Areas characterized by shared environmental preferences of native and naturalized ferns may decrease due to human development and fallowed agricultural lands. Our study demonstrates the value of place-based application of a recently developed correlative ecological niche modeling approach for conservation risk assessment in a rapidly changing and urbanized island ecosystem.

The rapid radiation of Bomarea (Alstroemeriaceae: Liliales), driven by the rise of the Andes.

Geological events such as mountain uplift affect how, when, and where species diversify, but measuring those effects is a longstanding challenge. Andean orogeny impacted the evolution of regional biota by creating barriers to gene flow, opening new habitats, and changing local climate. B⁢o⁢m⁢a⁢r⁢e⁢a (Alstroemeriaceae) are tropical plants with (often) small, isolated ranges; in total, B⁢o⁢m⁢a⁢r⁢e⁢a species occur from central Mexico to central Chile. This genus appears to have evolved rapidly and quite recently, and rapid radiations are often challenging to resolve with traditional phylogenetic inference. In this study, we apply phylogenomics-with hundreds of loci, gene-tree-based data curation, and a multispecies-coalescent approach-to infer the phylogeny of B⁢o⁢m⁢a⁢r⁢e⁢a. We use this phylogeny to untangle the potential drivers of diversification and biogeographic history. In particular, we test if Andean orogeny contributed to the diversification of B⁢o⁢m⁢a⁢r⁢e⁢a. We find that B⁢o⁢m⁢a⁢r⁢e⁢a originated in the central Andes during the mid-Miocene, then spread north, following the trajectory of mountain uplift. Furthermore, Andean lineages diversified faster than non-Andean relatives. B⁢o⁢m⁢a⁢r⁢e⁢a thus demonstrates that-at least in some cases-geological change rather than environmental stability has driven high species diversity in a tropical biodiversity hotspot. These results also demonstrate the utility (and danger) of genome-scale data for making macroevolutionary inferences.

Dramatic difference in rate of chromosome number evolution among sundew (Drosera L., Droseraceae) lineages.

Chromosome number change is a driver of speciation in eukaryotic organisms. Carnivorous sundews in the plant genus Drosera L. exhibit single chromosome number variation both among and within species, especially in the Australian Drosera subg. Ergaleium D.C., potentially linked to atypical centromeres that span much of the length of the chromosomes. We critically reviewed the literature on chromosome counts in Drosera, verified the taxonomy and quality of the original counts, and reconstructed dated phylogenies. We used the BiChrom model to test whether rates of single chromosome number increase and decrease, and chromosome number doubling differed between D. subg. Ergaleium and the other subgenera and between self-compatible and self-incompatible lineages. The best model for chromosome evolution among subgenera had equal rates of chromosome number doubling but higher rates of single chromosome number change in D. subg. Ergaleium than in the other subgenera. Contrary to expectation, self-incompatible lineages had a significantly higher rate of single chromosome loss than self-compatible lineages. We found no evidence for an association between differences in single chromosome number changes and diploidization after polyploidy or centromere type. This study presents an exemplar for critically examining published cytological data and rigorously testing factors that may impact the rates of chromosome number evolution.

Using ChromEvol to Determine the Mode of Chromosomal Evolution.

The ChromEvol software was the first to implement a likelihood-based approach, using probabilistic models that depict the pattern of chromosome number change along a specified phylogeny. The initial models have been completed and expanded during the last years. New parameters that model polyploid chromosome evolution have been implemented in ChromEvol v.2. In recent years, new and more complex models have been developed. The BiChrom model is able to implement two distinct chromosome models for the two possible trait states of a binary character of interest. ChromoSSE jointly implements chromosome evolution, speciation, and extinction. In the near future, we will be able to study chromosome evolution with increasingly complex models.

Opposing effects of plant traits on diversification.

Species diversity can vary dramatically across lineages due to differences in speciation and extinction rates. Here, we explore the effects of several plant traits on diversification, finding that most traits have opposing effects on diversification. For example, outcrossing may increase the efficacy of selection and adaptation but also decrease mate availability, two processes with contrasting effects on lineage persistence. Such opposing trait effects can manifest as differences in diversification rates that depend on ecological context, spatiotemporal scale, and associations with other traits. The complexity of pathways linking traits to diversification suggests that the mechanistic underpinnings behind their correlations may be difficult to interpret with any certainty, and context dependence means that the effects of specific traits on diversification are likely to differ across multiple lineages and timescales. This calls for taxonomically and context-controlled approaches to studies that correlate traits and diversification.

Interactions between breeding system and ploidy affect niche breadth in Solanum.

Understanding the factors driving ecological and evolutionary interactions of economically important plant species is important for agricultural sustainability. The geography of crop wild relatives, including wild potatoes (Solanum section Petota), have received attention; however, such information has not been analysed in combination with phylogenetic histories, genomic composition and reproductive systems to identify potential species for use in breeding for abiotic stress tolerance. We used a combination of ordinary least-squares (OLS) and phylogenetic generalized least-squares (PGLM) analyses to identify the discrete climate classes that make up the climate niche that wild potato species inhabit in the context of breeding system and ploidy. Self-incompatible diploid or self-compatible polyploid species significantly increase the number of discrete climate classes within a climate niche inhabited. This result was sustained when correcting for phylogenetic non-independence in the linear model. Our results support the idea that specific breeding system and ploidy combinations increase niche breadth through the decoupling of geographical range and niche diversity, and therefore, these species may be of particular interest for crop adaptation to a changing climate.

EyeChrom and CCDBcurator: Visualizing chromosome count data from plants.

PREMISE OF THE STUDY: Chromosome count data are available for hundreds of plant species and can be explored in text-only format at the Chromosome Counts Database (http://ccdb.tau.ac.il). CCDBcurator and EyeChrom are an R package and a web application, respectively, that first curate and then visualize these data graphically, so that intra- and interspecific variation of chromosome numbers can be easily summarized and displayed for a given genus. METHODS AND RESULTS: We developed R code to clean, summarize, and display in several formats the chromosome count data for a selected genus or set of species present in the Chromosome Counts Database. These data and figures can be exported for use in analyses, publications, or teaching. CONCLUSIONS: Chromosome count data are critical for a number of evolutionary studies in plant biology, and their importance is underscored by the increasing appreciation of the prevalence of polyploidy in land plants. CCDBcurator and EyeChrom provide a fast, easy, and reproducible means of cleaning, curating, and then visualizing the chromosome count data currently available for plants.

chromploid: An R package for chromosome number evolution across the plant tree of life.

PREMISE OF THE STUDY: Polyploidy has profound evolutionary consequences for land plants. Despite the availability of large phylogenetic and chromosomal data sets, estimating the rates of polyploidy and chromosomal evolution across the tree of life remains a challenging, computationally complex problem. We introduce the R package chromploid, which allows scientists to perform inference of chromosomal evolution rates across large phylogenetic trees. METHODS AND RESULTS: chromploid is an open-source package in the R environment that calculates the likelihood function of models of chromosome evolution. Models of discrete character evolution can be customized using chromploid. We demonstrate the performance of the BiChroM model, testing for associations between rates of chromosome doubling (as a proxy for polyploidy) and a binary phenotypic character, within chromploid using simulations and empirical data from Solanum. In simulations, estimated chromosome-doubling rates were unbiased and the variance decreased with larger trees, but distinguishing small differences in rates of chromosome doubling, even from large data sets, remains challenging. In the Solanum data set, a custom model of chromosome number evolution demonstrated higher rates of chromosome doubling in herbaceous species compared to woody. CONCLUSIONS: chromploid enables researchers to perform robust likelihood-based inferences using complex models of chromosome number evolution across large phylogenies.

Testing the association of phenotypes with polyploidy: An example using herbaceous and woody eudicots.

Although numerous studies have surveyed the frequency with which different plant characters are associated with polyploidy, few statistical tools are available to identify the factors that potentially facilitate polyploidy. We describe a new probabilistic model, BiChroM, designed to associate the frequency of polyploidy and chromosomal change with a binary phenotypic character in a phylogeny. BiChroM provides a robust statistical framework for testing differences in rates of polyploidy associated with phenotypic characters along a phylogeny while simultaneously allowing for evolutionary transitions between character states. We used BiChroM to test whether polyploidy is more frequent in woody or herbaceous plants, based on tree with 4711 eudicot species. Although polyploidy occurs in woody species, rates of chromosome doubling were over six times higher in herbaceous species. Rates of single chromosome increases or decreases were also far higher in herbaceous than woody species. Simulation experiments indicate that BiChroM performs well with little to no bias and relatively little variance at a wide range of tree depths when trees have at least 500 taxa. Thus, BiChroM provides a first step toward a rigorous statistical framework for assessing the traits that facilitate polyploidy.

Vertebrate blood cell volume increases with temperature: implications for aerobic activity.

Aerobic activity levels increase with body temperature across vertebrates. Differences in these levels, from highly active to sedentary, are reflected in their ecology and behavior. Yet, the changes in the cardiovascular system that allow for greater oxygen supply at higher temperatures, and thus greater aerobic activity, remain unclear. Here we show that the total volume of red blood cells in the body increases exponentially with temperature across vertebrates, after controlling for effects of body size and taxonomy. These changes are accompanied by increases in relative heart mass, an indicator of aerobic activity. The results point to one way vertebrates may increase oxygen supply to meet the demands of greater activity at higher temperatures.