ACDC: Analysis of Congruent Diversification Classes

Diversification rates inferred from phylogenies are not identifiable. There are infinitely many combinations of speciation and extinction rate functions that have the exact same likelihood score for a given phylogeny, building a congruence class. The specific shape and characteristics of such congruence classes have not yet been studied. Whether speciation and extinction rate functions within a congruence class share common features is also not known. Instead of striving to make the diversification rates identifiable, we can embrace their inherent non-identifiable nature. We use two different approaches to explore a congruence class: (i) testing of specific alternative hypotheses, and (ii) randomly sampling alternative rate function within the congruence class. Our methods are implemented in the open-source R package ACDC (https://github.com/afmagee/ACDC). ACDC provides a flexible approach to explore the congruence class and provides summaries of rate functions within a congruence class. The summaries can highlight common trends, i.e. increasing, flat or decreasing rates. Although there are infinitely many equally likely diversification rate functions, these can share common features. ACDC can be used to assess if diversification rate patterns are robust despite non-identifiability. In our example, we clearly identify three phases of diversification rate changes that are common among all models in the congruence class. Thus, congruence classes are not necessarily a problem for studying historical patterns of biodiversity from phylogenies.

The rise of grasslands is linked to atmospheric CO2 decline in the late Palaeogene

Grasslands are predicted to experience a major biodiversity change by the year 2100. A better understanding of how grasslands have responded to past environmental changes will help predict the outcome of current and future environmental changes. Here, we explore the relationship between past atmospheric CO2 and temperature fluctuations and the shifts in diversification rate of Poaceae (grasses) and Asteraceae (daisies), two exceptionally species-rich grassland families (~11,000 and ~23,000 species, respectively). To this end, we develop a Bayesian approach that simultaneously estimates diversification rates through time from time-calibrated phylogenies and correlations between environmental variables and diversification rates. Additionally, we present a statistical approach that incorporates the information of the distribution of missing species in the phylogeny. We find strong evidence supporting a simultaneous increase in diversification rates for grasses and daisies after the most significant reduction of atmospheric CO2 in the Cenozoic (~34 Mya). The fluctuations of paleo-temperatures, however, appear not to have had a significant relationship with the diversification of these grassland families. Overall, our results shed new light on our understanding of the origin of grasslands in the context of past environmental changes.

An Evolutionary Study of Carex Subg. Psyllophorae (Cyperaceae) Sheds Light on a Strikingly Disjunct Distribution in the Southern Hemisphere, With Emphasis on Its Patagonian Diversification

Carex subgenus Psyllophorae is an engaging study group due to its early diversification compared to most Carex lineages, and its remarkable disjunct distribution in four continents corresponding to three independent sections: sect. Psyllophorae in Western Palearctic, sect. Schoenoxiphium in Afrotropical region, and sect. Junciformes in South America (SA) and SW Pacific. The latter section is mainly distributed in Patagonia and the Andes, where it is one of the few Carex groups with a significant in situ diversification. We assess the role of historical geo-climatic events in the evolutionary history of the group, particularly intercontinental colonization events and diversification processes, with an emphasis on SA. We performed an integrative study using phylogenetic (four DNA regions), divergence times, diversification rates, biogeographic reconstruction, and bioclimatic niche evolution analyses. The crown age of subg. Psyllophorae (early Miocene) supports this lineage as one of the oldest within Carex. The diversification rate probably decreased over time in the whole subgenus. Geography seems to have played a primary role in the diversification of subg. Psyllophorae. Inferred divergence times imply a diversification scenario away from primary Gondwanan vicariance hypotheses and suggest long-distance dispersal-mediated allopatric diversification. Section Junciformes remained in Northern Patagonia since its divergence until Plio-Pleistocene glaciations. Andean orogeny appears to have acted as a northward corridor, which contrasts with the general pattern of North-to-South migration for temperate-adapted organisms. A striking niche conservatism characterizes the evolution of this section. Colonization of the SW Pacific took place on a single long-distance dispersal event from SA. The little ecological changes involved in the trans-Pacific disjunction imply the preadaptation of the group prior to the colonization of the SW Pacific. The high species number of the section results from simple accumulation of morphological changes (disparification), rather than shifts in ecological niche related to increased diversification rates (radiation).

Fossils Do Not Substantially Improve, and May Even Harm, Estimates of Diversification Rate Heterogeneity

There is a prevailing view that the inclusion of fossil data could remedy identifiability issues related to models of diversification, by drastically reducing the number of congruent models. The fossilized birth-death (FBD) model is an appealing way of directly incorporating fossil information when estimating diversification rates. Here we explore the benefits of including fossils by implementing and then testing two-types of FBD models in more complex likelihood-based models that assume multiple rate classes across the tree. We also assess the impact of severely undersampling, and even not including fossils that represent samples of lineages that also had sampled descendants (i.e., k-type fossils), as well as converting a fossil set to represent stratigraphic ranges. Under various simulation scenarios, including a scenario that exists far outside the set of models we evaluated, including fossils rarely outperforms analyses that exclude them altogether. At best, the inclusion of fossils improves precision but does not influence bias. We also found that severely undercounting the number of k-type fossils produces highly inflated rates of turnover and extinction fraction. Similarly, we found that converting the fossil set to stratigraphic ranges results in turnover rates and extinction fraction estimates that are generally underestimated. While fossils remain essential for understanding diversification through time, in the specific case of understanding diversification given an existing, largely modern tree, they are not especially beneficial.

Macroevolutionary pattern of Saussurea (Asteraceae) provides insights into the drivers of radiating diversification

Evolutionary radiations have intrigued biologists for more than a century, yet our understanding of the drivers of radiating diversification is still limited. We investigate the roles of environmental and species-intrinsic factors in driving the rapid radiation of Saussurea (Asteraceae) by deploying a number of palaeoenvironment-, diversity- and trait-dependent models, as well as ecological distribution data. We show that three main clades of Saussurea began to diversify in the Miocene almost simultaneously, with increasing diversification rates (DRs) negatively dependent on palaeotemperature but not dependent on species diversity. Our trait-dependent models detect some adaptive morphological innovations associated with DR shifts, while indicating additional unobserved traits are also likely driving diversification. Accounting for ecological niche data, we further reveal that accelerations in DRs are correlated with niche breadth and the size of species' range. Our results point out a macroevolutionary scenario where both adaptive morphological evolution and ecological opportunities provided by palaeoenvironmental fluctuations triggered an exceptionally radiating diversification. Our study highlights the importance of integrating phylogenomic, morphological, ecological and model-based approaches to illustrate evolutionary dynamics of lineages in biodiversity hotspots.

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

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 criticised 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 (Louca and Pennell, 2020) 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 modelling, but they in no way suggest we should abandon diversification modelling 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.

The rise of grasslands is linked to atmospheric CO2 decline in the late Palaeogene

Grasslands are predicted to experience a major biodiversity change by the year 2100 in part due to recent and projected increases in atmospheric CO2 concentration. A better understanding of how grasslands have responded to past environmental changes will help predict the outcome of current and future environmental changes. Here, we explore the relationship between past atmospheric CO2 and temperature fluctuations and the shifts in diversification rate of grasses (Poaceae) and daisies (Asteraceae), two exceptionally species-rich grassland families (≈ 11,000 and ≈ 23,000 species, respectively). To this end, we developed a novel Bayesian approach that simultaneously estimates diversification-rates through time from time-calibrated phylogenies and correlations between environmental variables and diversification rates. Additionally, we developed a new statistical approach that incorporates the information of the distribution of missing species in the phylogeny. We found strong evidence supporting a simultaneous increase in diversification rates for daisies and grasses after the most significant reduction of atmospheric CO2 in the Cenozoic (≈ 34 Mya). The fluctuations of paleo-temperatures, however, appear not to have had a significant relationship with the diversification of these grassland families. Overall, our results shed new light on our understanding of the origin of grasslands in the context of past environmental changes.

The Evolution of Nest Site Specialization and its Macroevolutionary Consequences in Passerine Birds

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. However, 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. Here we test the evolutionary dead end hypothesis by estimating net diversification rate differences associated with nest site specialization among 3,224 species of passerine birds. In particular, we test whether the adoption of hole-nesting, a nest site 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.

Radiating pain: venom has contributed to the diversification of the largest radiations of vertebrate and invertebrate animals

Background Understanding drivers of animal biodiversity has been a longstanding aim in evolutionary biology. Insects and fishes represent the largest lineages of invertebrates and vertebrates respectively, and consequently many ideas have been proposed to explain this diversity. Natural enemy interactions are often important in diversification dynamics, and key traits that mediate such interactions may therefore have an important role in explaining organismal diversity. Venom is one such trait which is intricately bound in antagonistic coevolution and has recently been shown to be associated with increased diversification rates in tetrapods. Despite ~ 10% of fish families and ~ 16% of insect families containing venomous species, the role that venom may play in these two superradiations remains unknown. Results In this paper we take a broad family-level phylogenetic perspective and show that variation in diversification rates are the main cause of variations in species richness in both insects and fishes, and that venomous families have diversification rates twice as high as non-venomous families. Furthermore, we estimate that venom was present in ~ 10% and ~ 14% of the evolutionary history of fishes and insects respectively. Conclusions Consequently, we provide evidence that venom has played a role in generating the remarkable diversity in the largest vertebrate and invertebrate radiations.

Multicellularity and sex helped shape the Tree of Life

Across the Tree of Life, there are dramatic differences in species numbers among groups. However, the factors that explain the differences among the deepest branches have remained unknown. We tested whether multicellularity and sexual reproduction might explain these patterns, since the most species-rich groups share these traits. We found that groups with multicellularity and sexual reproduction have accelerated rates of species proliferation (diversification), and that multicellularity has a stronger effect than sexual reproduction. Patterns of species richness among clades are then strongly related to these differences in diversification rates. Taken together, these results help explain patterns of biodiversity among groups of organisms at the very broadest scales. They may also help explain the mysterious preponderance of sexual reproduction among species (the ‘paradox of sex’) by showing that organisms with sexual reproduction proliferate more rapidly.