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The development of state‐dependent speciation and extinction (SSE) models. The original binary‐state speciation and extinction model (BiSSE) model (Maddison et al., 2007) is shown at the top of the diagram with all other models depicted below, in the order of their publication. Acronyms are defined as follows: Binary‐State Speciation and Extinction–node enhanced state shift (BiSSE‐ness; Magnuson‐ford & Otto, 2012), Cladogenetic and Anagenetic Models of Chromosome Number Evolution (ChromoSSE; Freyman & Höhna, 2018), Character‐Independent Diversification (CID; Beaulieu & O'Meara, 2016), Cladogenetic State change Speciation and Extinction (ClaSSE; Goldberg and Igić, 2012), Fast, Intuitive State‐dependent Speciation‐Extinction (FiSSE; Rabosky & Goldberg, 2017), Geographic State Speciation and Extinction (GeoSSE; Goldberg et al., 2011), Hidden Geographic State Speciation and Extinction (GeoHiSSE; Caetano et al., 2018), Hidden State Speciation and Extinction (HiSSE; Beaulieu & O'Meara, 2016), Multi‐State Speciation and Extinction (MuSSE; FitzJohn, 2012), Multicharacter Hidden State Speciation and Extinction (Mu‐HiSSE; Nakov et al., 2018), Quantitative State Speciation and Extinction (QuaSSE; FitzJohn, 2010; Verboom et al., 2020) and Several Examined and Concealed States‐dependent Speciation and Extinction (SecSSE; Herrera‐Alsina et al., 2019). Each box shows the name of the model and the associated citation. Models that share similar attributes (e.g. those with hidden states) are colour coded and grouped with boxes. This is not an exhaustive list of SSE models and does not include, for example, models used in epidemiology that allow tips to be sampled at various points in time (Scire et al., 2020).
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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 h...
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A long-standing question in macroevolution is whether diversification is governed by the same processes that structure diversity at ecological scales, particularly competition. This competition has led to the development of a model where diversification rates depend on diversity, analogous to density-dependence in population growth models. Various...
Citations
... In the last decade, hundreds of studies focusing on specific angiosperm clades or the group as a whole have attempted to identify the traits and geographic areas that explain this variation (reviewed in [8] and [9]). Although many of these studies support a correlation between a trait or habitat and variations in speciation and/or extinction rates, a series of criticisms and recent reviews have put in doubt the generality of these results. ...
... Studies using newer extensions that allow for rate heterogeneity across different parts of phylogenetic trees and better null models (e.g. [11]) have found generally lower support for the link between diversification and specific characters [9]. Secondly, studies that combine and discuss results across several clades often find conflicting results. ...
... Secondly, studies that combine and discuss results across several clades often find conflicting results. This suggests that there is no single key innovation that is widely supported as a trigger for speciation and/or extinction across multiple unrelated clades [7,9]. As such, the pursuit for a consistent and universal driver of diversification within angiosperms, has, so far, proved unfruitful. ...
The remarkable diversity of angiosperm species has prompted a search for universal drivers that modulate rates of speciation and extinction across this clade. To date, attempts to explain differences in species diversity have focused on the potential correlation of net diversification rates with particular key traits. However, an often overlooked explanation is that the evolutionary lability, here defined as the rates of trait change, is a better predictor of the diversification dynamics than the observed traits themselves. This hypothesis, first proposed in the context of biome shifts 50 years ago, is based on the idea that the capacity to adapt to environmental changes is the key element defining angiosperm diversification dynamics. Using a phylogenetic dataset of 49 angiosperm clades including 18,617 species we demonstrate that the propensity of change between open, closed, and widespread biomes is significantly correlated with lineage speciation and extinction rates across clades. Additionally, we find that transition rates tend to be faster from open to closed-canopy biomes. This results in ancestral state estimates that favor several deep time origins from open-canopy biomes into closed-canopy biomes, contrary to prevailing ideas in the field. More generally, we suggest a more comprehensive understanding into how biodiversity is generated and maintained is found by focusing on dynamic evolutionary processes rather than singular key traits.
... Finding plausible explanations for unique historical shifts in trait evolution or diversification rates remains an outstanding challenge in biology (Uyeda et al., 2018). Such rate shifts are typically context-dependent, and consequently, diversification in some radiations may arise from causes that do not trigger similar shifts across the tree (e.g., Helmstetter et al., 2023;Queiroz, 2002). Integrating different hypotheses about the drivers of macroevolutionary shifts into statistical models remains a significant barrier to understanding the mechanisms underlying rate heterogeneity across the tree of life. ...
... See Supplementary Table S3 for parameter estimates from PGLS analyses. lizards and show that species diversification across epochal timescales arises from a series of interacting, context-specific events (e.g., Donoghue & Sanderson, 2015;Garcia-Porta & Ord, 2013;Helmstetter et al., 2023). ...
... Neither arboreality, insularity, nor the evolution of large body sizes impact speciation rates when considering the entire Pleurodonta clade. However, bursts in speciation rates are often observed in some lineages characterized by these traits, indicating that intrinsic features of lineages, idiosyncrasies of the ecological and environmental shifts, and historical contingencies could all explain why a source of ecological opportunity has a certain effect on one part of the phylogeny but not in the other (Burress & Muñoz, 2022;Garcia-Porta & Ord, 2013;Helmstetter et al., 2023;Larouche et al., 2020;Miller et al., 2021). ...
Evolution proceeds unevenly across the tree of life, with some lineages accumulating diversity more rapidly than others. Explaining this disparity is challenging as similar evolutionary triggers often do not result in analogous shifts across the tree, and similar shifts may reflect different evolutionary triggers. We used a combination of approaches to directly consider such context-dependency and untangle the complex network of processes that shape macroevolutionary dynamics, focusing on Pleurodonta, a diverse radiation of lizards. Our approach shows that some lineage-wide signatures are lost when conditioned on sublineages: while viviparity appears to accelerate diversification, its effect size is overestimated by its association with the Andean mountains. Conversely, some signals that erode at broader phylogenetic scales emerge at shallower ones. Mountains, in general, do not affect speciation rates; rather, the occurrence in the Andean mountains specifically promotes diversification. Likewise, the evolution of larger sizes catalyzes diversification rates, but only within certain ecological and geographical settings. We caution that conventional methods of fitting models to entire trees may mistakenly assign diversification heterogeneity to specific factors despite evidence against their plausibility. Our study takes a significant stride toward disentangling confounding factors and identifying plausible sources of ecological opportunities in the diversification of large evolutionary radiations.
... Benton, 2009;Ezard et al., 2011;Drury et al., 2016;Condamine et al., 2019) may be responsible for extant diversity patterns with biological and ecological traits being key features to understanding the diversification history of clades (e.g. Rabosky et al., 2013, Helmstetter et al., 2023Wiens, 2023). Over the last two decades, as phylogenetic data and comparative methods became increasingly available, trait evolution models and trait-dependent diversification have become major topics in macroevolution and macroecology (Maddison et al., 2007;Ng & Smith, 2014;Beaulieu & O'Meara, 2016;Helmstetter et al., 2023;Wiens, 2023). ...
... Rabosky et al., 2013, Helmstetter et al., 2023Wiens, 2023). Over the last two decades, as phylogenetic data and comparative methods became increasingly available, trait evolution models and trait-dependent diversification have become major topics in macroevolution and macroecology (Maddison et al., 2007;Ng & Smith, 2014;Beaulieu & O'Meara, 2016;Helmstetter et al., 2023;Wiens, 2023). Yet, macroevolutionary dynamics remain to be explored across a substantial portion of the tree of life. ...
... The implementation of concealed traits offers alternative models that reduce the risk of wrongly choosing a state-dependent diversification model over alternative ones (Beaulieu & O'Meara, 2016;Herrera-Alsina et al., 2019;Helmstetter et al., 2023). In this sense, SecSSE models may not detect any signal if the examined trait only weakly explains diversification dynamics Downloaded from https://academic.oup.com/evolut/advance-article/doi/10.1093/evolut/qpae070/7673161 by Bibliothèque Universitaire de médecine -Nîmes user on 16 May 2024 A c c e p t e d M a n u s c r i p t (Herrera-Alsina et al., 2019). ...
Estimating how traits evolved and impacted diversification across the tree of life represents a critical topic in ecology and evolution. Although there has been considerable research in comparative biology, large parts of the tree of life remain underexplored. Sharks are an iconic clade of marine vertebrates, and key components of marine ecosystems since the early Mesozoic. However, few studies have addressed how traits evolved or whether they impacted their extant diversity patterns. Our study aimed to fill this gap by reconstructing the largest time-calibrated species-level phylogeny of sharks and compiling an exhaustive database for ecological (diet, habitat) and biological (reproduction, maximum body length) traits. Using state-of-the-art models of evolution and diversification, we outlined the major character shifts and modes of trait evolution across shark species. We found support for sequential models of trait evolution and estimated a small to medium-sized lecithotrophic and coastal-dwelling most recent common ancestor for extant sharks. However, our exhaustive hidden traits analyses do not support trait-dependent diversification for any examined traits, challenging previous works. This suggests that the role of traits in shaping sharks' diversification dynamics might have been previously overestimated and should motivate future macroevolutionary studies to investigate other drivers of diversification in this clade.
... Traditionally, the individual factors influencing diversification have been studied through two major models: the Court Jester model, postulating a paramount role of extrinsic abiotic factors (geomorphology, biogeography, and abiotic climatic niche evolution), and the Red Queen model, proposing biotic factors (intrinsic traits, species interactions) as main drivers of diversification (Barnosky 2001;Benton 2009). Although substantial support has been found for both models (Court Jester: i.e., Kong et al. 2022;McCullough et al. 2022;Red Queen: i.e., Quental and Marshall 2013;Fernández-Mazuecos et al. 2019;García-Girón et al. 2020;Fraser et al. 2021;Pérez-Escobar et al. 2022), both approaches fall short in that they attribute strong individual effects to the respective a-/biotic factor under study, without exploring the potential for multiple interacting and potentially temporally staggered effects on diversification dynamics (Fig. 1, Wiens 2011; Aguilée et al. 2018;Uyeda et al. 2018;Helmstetter et al. 2023). Testing for the relative contribution of these factors is challenging because a thorough analysis requires the availability of various data types such as a well-sampled, time-calibrated molecular phylogeny, occurrence information, abiotic climatic data, and trait/natural history information ( Supplementary Fig. S1), which are difficult to collect for large, widespread clades occurring in remote areas. ...
... The need for such inclusive, multifactor diversification assessments has been recognized broadly across the scientific community (Condamine et al. 2018;Uyeda et al. 2018), yet, the implementation of satisfying approaches has been slow. Authors have, to date, mostly used separate models to assess the effects of either an abiotic or biotic factor on diversification (i.e., through state-dependent speciation and extinction (SSE) models, Helmstetter et al. 2023), and even when incorporating both into a study, they were usually retained in separate modeling approaches (Lagomarsino et al. 2016;Condamine et al. 2018;Testo et al. 2019). Likelihood frameworks for the comparison of some models (i.e., time-and environment-dependent birth-death models, Condamine et al. 2018), and promising approaches for modeling the reciprocal effects of continuous (i.e., climatic niche) and discrete (i.e., fruit type) character evolution (Boyko et al. 2023;Tribble et al. 2023) have been proposed. ...
... sampled), and time calibration (few fossils), that are, unfortunately, inherent to many evolutionary studies. Low sampling fractions, small clade sizes, and uncertainty around divergence time estimates may all increase the likelihood of detecting significant effects of single factors on diversification dynamics (Helmstetter et al. 2023), and this might hold equally true when assessing the effects of multiple factors. To evaluate whether these data-inherent features also impact our results, we have 1) randomly subsampled our dataset to 50% (70 spp., reducing the sampling fraction to ca. 23%) and 2) run our analyses across two different phylogenetic hypotheses (Dellinger et al. 2019b;Reginato et al. 2022) which differ in calibration techniques and age estimates. ...
Why and how organismal lineages radiate is commonly studied through either assessing abiotic factors (biogeography, geomorphological processes, and climate) or biotic factors (traits and interactions). Despite increasing awareness that both abiotic and biotic processes may have important joint effects on diversification dynamics, few attempts have been made to quantify the relative importance and timing of these factors, and their potentially interlinked direct and indirect effects, on lineage diversification. We here combine assessments of historical biogeography, geomorphology, climatic niche, vegetative, and floral trait evolution to test whether these factors jointly, or in isolation, explain diversification dynamics of a Neotropical plant clade (Merianieae, Melastomataceae). After estimating ancestral areas and the changes in niche and trait disparity over time, we employ Phylogenetic Path Analyses as a synthesis tool to test eleven hypotheses on the individual direct and indirect effects of these factors on diversification rates. We find strongest support for interlinked effects of colonization of the uplifting Andes during the mid-Miocene and rapid abiotic climatic niche evolution in explaining a burst in diversification rate in Merianieae. Within Andean habitats, later increases in floral disparity allowed for the exploitation of wider pollination niches (i.e., shifts from bee to vertebrate pollinators), but did not affect diversification rates. Our approach of including both vegetative and floral trait evolution, rare in assessments of plant diversification in general, highlights that the evolution of woody habit and larger flowers preceded the colonization of the Andes, but was likely critical in enabling the rapid radiation in montane environments. Overall, and in concert with the idea that ecological opportunity is a key element of evolutionary radiations, our results suggest that a combination of rapid niche evolution and trait shifts was critical for the exploitation of newly available niche space in the Andes in the mid-Miocene. Further, our results emphasize the importance of incorporating both abiotic and biotic factors into the same analytical framework if we aim to quantify the relative and interlinked effects of these processes on diversification.
... In agreement with the blind alley hypothesis, lower diversification rates are often reported in selfing lineages (e.g., Ferrer and Good 2012). Methods have been developed to estimate how traits influence rates of diversification, speciation, and extinction (state-dependent speciation and extinction [SSE] models; Table 2; Maddison et al. 2007;Helmstetter et al. 2023). In the plant family Solanaceae, self-incompatibility (i.e., obligate outcrossing; SI) has been lost multiple times, leading to self-compatible (i.e., potential selfers; SC) lineages. ...
Surprisingly little attention has been given to the impact of selfing on speciation, even though selfing reduces gene flow between populations and affects other key population genetics parameters. Here we review recent theoretical work and compile empirical data from crossing experiments and genomic and phylogenetic studies to assess the effect of mating systems on the speciation process. In accordance with theoretical predictions, we find that accumulation of hybrid incompatibilities seems to be accelerated in selfers, but there is so far limited empirical support for a predicted bias toward underdominant loci. Phylogenetic evidence is scarce and contradictory, including studies suggesting that selfing either promotes or hampers speciation rate. Further studies are therefore required, which in addition to measures of reproductive barrier strength and selfing rate should routinely include estimates of demographic history and genetic divergence as a proxy for divergence time.
... Moreover, the SSE framework has faced criticism for having a high type I error rate in situations with an inadequate number of tips (Davis et al., 2013) and in the absence of state-dependent diversification (Rabosky and Goldberg, 2015). While acknowledging the inherent biases in the materials and methods we adopted, the results can still hold value with careful demonstration (Beaulieu and O'Meara, 2016;Helmstetter et al., 2023). These challenges are not unique to our study and are shared by many similar investigations (e.g., Weeks et al., 2014;Givnish et al., 2016;Xiang et al., 2016;Castro-Insua et al., 2018). ...
Tropical forests harbor the richest biodiversity among terrestrial ecosystems, but few studies have addressed the underlying processes of species diversification in these ecosystems. We use the pantropical flowering plant family Annonaceae as a study system to investigate how climate and biogeographic events contribute to diversification. A super-matrix phylogeny comprising 835 taxa (34% of Annonaceae species) based on eight chloroplast regions was used in this study. We show that global temperature may better explain the recent rapid diversification in Annonaceae than time and constant models. Accelerated accumulation of niche divergence (around 15 Ma) lags behind the increase of diversification rate (around 25 Ma), reflecting a heterogeneous transition to recent diversity increases. Biogeographic events are related to only two of the five diversification rate shifts detected. Shifts in niche evolution nevertheless appear to be associated with increasingly seasonal environments. Our results do not support the direct correlation of any particular climatic niche shifts or historical biogeographical event with shifts in diversification rate. Instead, we suggest that Annonaceae diversification can lead to later niche divergence as a result of increasing interspecific competition arising from species accumulation. Shifts in niche evolution appear to be associated with increasingly seasonal environments. Our results highlight the complexity of diversification in taxa with long evolutionary histories.
... Although the results from trait-dependent diversification rates analysis indicated that there were no significant differences in diversification rate between epiphytic and terrestrial species (Table S3), changing life form may have improved environmental adaptability and allowed Cymbidium species to occupy new inches. Trait-dependent diversification is detected less often when phylogenetic trees have fewer tips or younger root ages (Helmstetter et al., 2023), and methodological biases associated with our small datasets could have lead to ambiguous evolutionary histories. Within the orchid family, the adaptive evolution of traits does not necessarily accelerate the diversification rate. ...
... Whether style-length polymorphism was associated with different speciation rates or extinction rates in R1 and R2 cannot be known with our current knowledge of phylogenetics and distribution of style-length polymorphism across all angiosperm species 87 . At the genus level there is mixed phylogenetic evidence about the role of heterostyly in diversification rates 76,88,89 , see also ref. 90, which is congruent with the apparent context and/or lineagedependent role of floral traits on angiosperms diversification rates 91 . We found that style-length polymorphism is evolutionary correlated with various floral traits related to pollination precision and intermediate levels of specialisation for animal pollination, notably actinomorphic flowers with fused perianth parts (a proxy for a floral tube), few stamens fused to the perianth, and few carpels, and with a long-tongued insect pollination system. ...
Since the insights by Charles Darwin, heterostyly, a floral polymorphism with morphs bearing stigmas and anthers at reciprocal heights, has become a model system for the study of natural selection. Based on his archetypal heterostylous flower, including regular symmetry, few stamens and a tube, Darwin hypothesised that heterostyly evolved to promote outcrossing through efficient pollen transfer between morphs involving different areas of a pollinator’s body, thus proposing his seminal pollination-precision hypothesis. Here we update the number of heterostylous and other style-length polymorphic taxa to 247 genera belonging to 34 families, notably expanding known cases by 20%. Using phylogenetic and comparative analyses across the angiosperms, we show numerous independent origins of style-length polymorphism associated with actinomorphic, tubular flowers with a low number of sex organs, stamens fused to the corolla, and pollination by long-tongued insects. These associations provide support for the Darwinian pollination-precision hypothesis as a basis for convergent evolution of heterostyly across angiosperms.
... These studies suggest a contextual importance of, for example, innovations in floral morphology and reproduction efficiency that facilitated interactions with pollinators and seed dispersers (Kay et al., 2006a;Sauquet et al., 2017); coevolution with animals (especially pollinators and herbivores; (Xiao et al., 2021); new photosynthetic capabilities (Benton et al., 2022); whole genome duplication (WGD) events (Tank et al., 2015;Clark and Donoghue, 2018); or geographic distribution patterns (Vamosi and Vamosi, 2011). However, significant gaps in our understanding of angiosperm evolution remain; it has been particularly difficult to find universal drivers of increased DR that can explain SR patterns in angiosperms, because traits do not seem to have a consistent effect across clades (Doyle and Donoghue, 1986;Friis et al., 2006;Crepet and Niklas, 2009;Vamosi and Vamosi, 2010;Sauquet and Magalloń, 2018;Soltis et al., 2019;Hernańdez-Hernańdez and Wiens, 2020;Helmstetter et al., 2023). ...
... However, much progress has been made to include them in the Tree of life (To), and ongoing efforts to sequence under-represented taxa in the angiosperm tree, such as the oneKB initiative (Leebens-Mack et al., 2019), make the study of depauperons feasible. Another reason why there has been less attention to depauperons lies in the difficulties to assess whether plant families have unusually low SR due to the complexity of diversification rate models, the existence of broad shifts in the inferred DR over evolutionary time, and the wide variation in the estimated crown and stem age of taxa across studies that employ different markers, statistical methods, and fossil data Benton et al., 2022;Helmstetter et al., 2023). In this study, we aimed to account for these limitations by (1) estimating the age of significant shifts in the DR rate of angiosperm families using Bayesian methods in each of five large phylogenetic studies and then dividing the data into geological intervals within which DRs could be expected to be uniform and then (2) employing the Distribution of nine traits across families with poor, predicted, or high species richness based on strict consensus. ...
Introduction
The phenomenal expansion of angiosperms has prompted many investigations into the factors driving their diversification, but there remain significant gaps in our understanding of flowering plant species diversity.
Methods
Using the crown age of families from five studies, we used a maximum likelihood approach to classify families as having poor, predicted or high species richness (SR) using strict consensus criteria. Using these categories, we looked for associations between family SR and i) the presence of an inferred familial ancestral polyploidization event, ii) 23 life history and floral traits compiled from previously published datasets and papers, and iii) sexual system (dioecy) or genetically determined self-incompatibility (SI) mating system using an updated version of our own database and iv) geographic distribution using a new database describing the global distribution of plant species/families across realms and biomes and inferred range.
Results
We find that more than a third of angiosperm families (65%) had predicted SR, a large proportion (30.2%) were species poor, while few (4.8%) had high SR. Families with poor SR were less likely to have undergone an ancestral polyploidization event, exhibited deficits in diverse traits, and were more likely to have unknown breeding systems and to be found in only one or few biomes and realms, especially the Afrotropics or Australasia. On the other hand, families with high SR were more likely to have animal mediated pollination or dispersal, are enriched for epiphytes and taxa with an annual life history, and were more likely to harbour sporophytic SI systems. Mapping the global distribution of georeferenced taxa by their family DR, we find evidence of regions dominated by taxa from lineages with high vs low SR.
Discussion
These results are discussed within the context of the literature describing “depauperons” and the factors contributing to low and high biodiversity in angiosperm clades.
... [3][4][5] Neutral processes of lineage splitting and extinction can account for some variation in interclade diversity. [6][7][8] But because many phylogenies are more uneven than predicted by these neutral processes, [9][10][11][12][13] non-random macro-evolutionary processes are still frequently invoked (reviewed in ref. 14 ) as the cause of this additional variation. By accelerating speciation rates or by reducing extinction rates, the evolution of phenotypic ''key innovations'' may increase diversification beyond the background rates of neutral processes. ...
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.
