How Important Is Budding Speciation for Comparative Studies?

The acknowledgment of evolutionary dependence among species has fundamentally changed how we ask biological questions. Phylogenetic models became the standard approach for studies with 3 or more lineages, in particular those using extant species. Most phylogenetic comparative methods (PCMs) translate relatedness into covariance, meaning that evolutionary changes before lineages split should be interpreted together whereas after the split lineages are expected to change independently. This clever realization has shaped decades of research. Here, we discuss one element of the comparative method often ignored or assumed as unimportant: if nodes of a phylogeny represent the dissolution of the ancestral lineage into two new ones or if the ancestral lineage can survive speciation events (i.e., budding). Budding speciation is often reported in paleontological studies, due to the nature of the evidence for budding in the fossil record, but it is surprisingly absent in comparative methods. Here, we show that many PCMs assume that divergence happens as a symmetric split, even if these methods do not explicitly mention this assumption. We discuss the properties of trait evolution models for continuous and discrete traits and their adequacy under a scenario of budding speciation. We discuss the effects of budding speciation under a series of plausible evolutionary scenarios and show when and how these can influence our estimates. We also propose that long-lived lineages that have survived through a series of budding speciation events and given birth to multiple new lineages can produce evolutionary patterns that challenge our intuition about the most parsimonious history of trait changes in a clade. We hope our discussion can help bridge comparative approaches in paleontology and neontology as well as foster awareness about the assumptions we make when we use phylogenetic trees.

Ehrlich and Raven escape and radiate coevolution hypothesis at different levels of organization: Past and future perspectives.

The classic paper by Ehrlich and Raven on coevolution will soon be 60 years old. Although they were not the first to develop the idea of coevolution, their thought-provoking paper certainly popularized this idea and inspired several generations of scientists interested in coevolution. Here, we describe some of their main contributions, quantitatively measure the impact of their seminal paper on different fields of research, and discuss how ideas related to their original paper might push the study of coevolution forward. To guide our discussion, we explore their original hypothesis into three research fields that are associated with distinct scales/levels of organization: (1) the genetic mechanisms underlying coevolutionary interactions; (2) the potential association between coevolutionary diversification and the organization of ecological networks; and (3) the micro- and macroevolutionary mechanisms and expected patterns under their hypothesis. By doing so, we discuss potentially overlooked aspects and future directions for the study of coevolutionary dynamics and diversification.

Macroevolutionary stability predicts interaction patterns of species in seed dispersal networks.

Assessing deep-time mechanisms affecting the assembly of ecological networks is key to understanding biodiversity changes on broader time scales. We combined analyses of diversification rates with interaction network descriptors from 468 bird species belonging to 29 seed dispersal networks to show that bird species that contribute most to the network structure of plant-frugivore interactions belong to lineages that show higher macroevolutionary stability. This association is stronger in warmer, wetter, less seasonal environments. We infer that the macroevolutionary sorting mechanism acts through the regional pool of species by sorting species on the basis of the available relative differences in diversification rates, rather than absolute rates. Our results illustrate how the interplay between interaction patterns and diversification dynamics may shape the organization and long-term dynamics of ecological networks.

Evolutionary trade-offs between male secondary sexual traits revealed by a phylogeny of the hyperdiverse tribe Eumaeini (Lepidoptera: Lycaenidae).

Male butterflies in the hyperdiverse tribe Eumaeini possess an unusually complex and diverse repertoire of secondary sexual characteristics involved in pheromone production and dissemination. Maintaining multiple sexually selected traits is likely to be metabolically costly, potentially resulting in trade-offs in the evolution of male signals. However, a phylogenetic framework to test hypotheses regarding the evolution and maintenance of male sexual traits in Eumaeini has been lacking. Here, we infer a comprehensive, time-calibrated phylogeny from 379 loci for 187 species representing 91% of the 87 described genera. Eumaeini is a monophyletic group that originated in the late Oligocene and underwent rapid radiation in the Neotropics. We examined specimens of 818 of the 1096 described species (75%) and found that secondary sexual traits are present in males of 91% of the surveyed species. Scent pads and scent patches on the wings and brush organs associated with the genitalia were probably present in the common ancestor of Eumaeini and are widespread throughout the tribe. Brush organs and scent pads are negatively correlated across the phylogeny, exhibiting a trade-off in which lineages with brush organs are unlikely to regain scent pads and vice versa. In contrast, scent patches seem to facilitate the evolution of scent pads, although they are readily lost once scent pads have evolved. Our results illustrate the complex interplay between natural and sexual selection in the origin and maintenance of multiple male secondary sexual characteristics and highlight the potential role of sexual selection spurring diversification in this lineage.

Re-evaluation of the "law of constant extinction" for ruminants at different taxonomical scales.

The "law of constant extinction," proposed by Van Valen, states that long and short-lived taxa have equal chances of going extinct. This pattern of age-independent extinction was originally inferred using the fossil record of several different taxa and relied on survivorship curves built from the literal reading of the fossil record. Van Valen's seminal work was mostly done at higher taxonomic levels, hence its prevalence at the species level could not be directly inferred. The surprisingly few subsequent studies done at the species level have challenged the prevalence of age-independent extinction, but those have, for the most part, failed to explicitly incorporate inherent biases of the fossil record. Using a recent Bayesian framework that accounts for several of those biases, including the fact that very short-living lineages might never make to the record itself, we showed that Ruminantia species present age-dependent extinction, where extinction probability decreases with species age. An analysis at the genus level suggested age-independent extinction but further examination suggested that the pattern might be more complex than previously reported by Van Valen. Our results indicate that different taxonomic levels may present different extinction regimes, which could justify the development of new macroevolutionary theory and methods.

Exploring the drivers of population structure across desert snakes can help to link micro and macroevolution.

To understand the underlying mechanisms generating population genetic divergence and structure is a critical step towards understanding how biodiversity evolves at both micro- and macroevolutionary scales. At the population-level, geographic isolation as well as adaptation to local environmental conditions can generate different patterns of spatial genetic variation among populations. Specific organismal traits as well as the characteristics of the environment might influence the process under which populations become spatially structured. In a From the Cover article in this issue of Molecular Ecology, Myers et al. (2019) present an integrative approach to investigate if the Cochise filter barrier (CFB), lying between the Sonoran and Chihuahuan Deserts, and the surrounding river networks were relevant in driving the population structure of 13 snake species. While local environmental conditions seem to predominantly contribute to lineage divergence, traditionally studied vicariant barriers seem to have played a minor role in shaping population structure across the studied species. This study brings insights into how population-level processes could contribute to the formation of incipient species, which ultimately might affect the speciation rates measured at macroevolutionary scales. Hence, Myers et al. (2019) not only represents an integrative study aiming to understand the drivers of population genetic divergence, but also a potentially important contribution to our ongoing challenge in linking micro- and macroevolution.

How Well Can We Estimate Diversity Dynamics for Clades in Diversity Decline?

The fossil record shows that the vast majority of all species that ever existed are extinct and that most lineages go through an expansion and decline in diversity. However, macroevolutionary analyses based upon molecular phylogenies have difficulty inferring extinction dynamics, raising questions about whether the neontological record can contribute to an understanding of the decline phenomenon. Two recently developed diversification methods for molecular phylogenies (RPANDA and BAMM) incorporate models that theoretically have the capacity to capture decline dynamics by allowing extinction to be higher than speciation. However, the performance of these frameworks over a wide range of decline scenarios has not been studied. Here, we investigate the behavior of these methods under decline scenarios caused by decreasing speciation and increasing extinction through time on simulated trees at fixed intervals over diversity trajectories with expansion and decline phases. We also compared method performance over a comprehensive data set of 214 empirical trees. Our results show that both methods perform equally well when varying speciation rates control decline. When decline was only caused by an increase in extinction rates both methods wrongly assign the variation in net diversification to a drop in speciation, even though the positive gamma values of those trees would suggest otherwise. We also found a tendency for RPANDA to favor increasing extinction and BAMM to favor decreasing speciation as the most common cause of decline in empirical trees. Overall our results shed light on the limitations of both methods, encouraging researchers to carefully interpret the results from diversification studies.

Diversification dynamics of mammalian clades during the K-Pg mass extinction.

The Cretaceous/Palaeogene (K-Pg) episode is an iconic mass extinction, in which the diversity of numerous clades abruptly declined. However, the responses of individual clades to mass extinctions may be more idiosyncratic than previously understood. Here, we examine the diversification dynamics of the three major mammalian clades in North America across the K-Pg. Our results show that these clades responded in dramatically contrasting ways to the K-Pg event. Metatherians underwent a sudden rise in extinction rates shortly after the K-Pg, whereas declining origination rates first halted diversification and later drove the loss of diversity in multituberculates. Eutherians experienced high taxonomic turnover near the boundary, with peaks in both origination and extinction rates. These findings indicate that the effects of geological episodes on diversity are context dependent and that mass extinctions can affect the diversification of clades by independently altering the extinction regime, the origination regime or both.

Estimating Age-Dependent Extinction: Contrasting Evidence from Fossils and Phylogenies.

The estimation of diversification rates is one of the most vividly debated topics in modern systematics, with considerable controversy surrounding the power of phylogenetic and fossil-based approaches in estimating extinction. Van Valen's seminal work from 1973 proposed the "Law of constant extinction," which states that the probability of extinction of taxa is not dependent on their age. This assumption of age-independent extinction has prevailed for decades with its assessment based on survivorship curves, which, however, do not directly account for the incompleteness of the fossil record, and have rarely been applied at the species level. Here, we present a Bayesian framework to estimate extinction rates from the fossil record accounting for age-dependent extinction (ADE). Our approach, unlike previous implementations, explicitly models unobserved species and accounts for the effects of fossil preservation on the observed longevity of sampled lineages. We assess the performance and robustness of our method through extensive simulations and apply it to a fossil data set of terrestrial Carnivora spanning the past 40 myr. We find strong evidence of ADE, as we detect the extinction rate to be highest in young species and declining with increasing species age. For comparison, we apply a recently developed analogous ADE model to a dated phylogeny of extant Carnivora. Although the phylogeny-based analysis also infers ADE, it indicates that the extinction rate, instead, increases with increasing taxon age. The estimated mean species longevity also differs substantially, with the fossil-based analyses estimating 2.0 myr, in contrast to 9.8 myr derived from the phylogeny-based inference. Scrutinizing these discrepancies, we find that both fossil and phylogeny-based ADE models are prone to high error rates when speciation and extinction rates increase or decrease through time. However, analyses of simulated and empirical data show that fossil-based inferences are more robust. This study shows that an accurate estimation of ADE from incomplete fossil data is possible when the effects of preservation are jointly modeled, thus allowing for a reassessment of Van Valen's model as a general rule in macroevolution.

Interactions within and between clades shaped the diversification of terrestrial carnivores.

A longstanding debate in evolutionary biology and paleontology is whether ecological interactions such as competition impose diversity dependence on speciation and extinction rates. Here, we analyze the fossil record of terrestrial mammalian carnivores in North America and Eurasia using a Bayesian framework to assess whether their diversity dynamics were affected by diversity dependence within and between families (12 in Eurasia, 10 in North America). We found eight instances of within-clade diversity dependence suppressing speciation rates and detected between-clade effects increasing extinction rates in six instances. Diversity dependence often involved lineages that migrated between continents and we found that speciation was more responsive to diversity changes within the clade, whereas extinction responded to diversity of taxa in other clades. The analysis of the fossil record of Carnivora suggests that interactions within and between clades are associated with different speciation and extinction regimes, opening room for a broader theory of diversity dependence.

Diversification in vipers: Phylogenetic relationships, time of divergence and shifts in speciation rates.

Snakes of the cosmopolitan family Viperidae comprise around 329 venomous species showing a striking heterogeneity in species richness among lineages. While the subfamily Azemiopinae comprises only two species, 70% of all viper species are arranged in the subfamily Crotalinae or the "pit vipers". The radiation of the pit vipers was marked by the evolution of the heat-sensing pits, which has been suggested to be a key innovation for the successful diversification of the group. Additionally, only crotalines were able to successfully colonize the New World. Here, we present the most complete molecular phylogeny for the family to date that comprises sequences from nuclear and mitochondrial genes representing 79% of all living vipers. We also investigated the time of divergence between lineages, using six fossils to calibrate the tree, and explored the hypothesis that crotalines have undergone an explosive radiation. Our phylogenetic analyses retrieved high support values for the monophyly of the family Viperidae, subfamilies Viperinae and Crotalinae, and 22 out of 27 genera, as well as well-supported intergeneric relationships throughout the family. We were able to recover a strongly supported sister clade to the New World pit vipers that comprises Gloydius, Ovophis, Protobothrops and Trimeresurus gracilis. Our results agree in many aspects with other studies focusing on the phylogenetics of vipers, but we recover new relationships as well. Despite the addition of new sequences we were not able to resolve some of the poor supported relationships previously suggested. Time of divergence estimates suggested that vipers started to radiate around the late Paleocene to middle Eocene with subfamilies most likely dating back to the Eocene. The invasion of the New World might have taken place sometime close to the Oligocene/Miocene boundary. Diversification analyses suggested a shift in speciation rates during the radiation of a sub-clade of pit vipers where speciation rates rapidly increased but slowed down toward the present. Thus, the evolution of the loreal pits alone does not seem to explain their explosive speciation rates. We suggest that climatic and geological changes in Asia and the invasion of the New World may have also contributed to the speciation shift found in vipers.

Omnivory in birds is a macroevolutionary sink.

Diet is commonly assumed to affect the evolution of species, but few studies have directly tested its effect at macroevolutionary scales. Here we use Bayesian models of trait-dependent diversification and a comprehensive dietary database of all birds worldwide to assess speciation and extinction dynamics of avian dietary guilds (carnivores, frugivores, granivores, herbivores, insectivores, nectarivores, omnivores and piscivores). Our results suggest that omnivory is associated with higher extinction rates and lower speciation rates than other guilds, and that overall net diversification is negative. Trait-dependent models, dietary similarity and network analyses show that transitions into omnivory occur at higher rates than into any other guild. We suggest that omnivory acts as macroevolutionary sink, where its ephemeral nature is retrieved through transitions from other guilds rather than from omnivore speciation. We propose that these dynamics result from competition within and among dietary guilds, influenced by the deep-time availability and predictability of food resources.

The challenges to inferring the regulators of biodiversity in deep time.

Attempts to infer the ecological drivers of macroevolution in deep time have long drawn inspiration from work on extant systems, but long-term evolutionary and geological changes complicate the simple extrapolation of such theory. Recent efforts to incorporate a more informed ecology into macroevolution have moved beyond the descriptive, seeking to isolate generating mechanisms and produce testable hypotheses of how groups of organisms usurp each other or coexist over vast timespans. This theme issue aims to exemplify this progress, providing a series of case studies of how novel modelling approaches are helping infer the regulators of biodiversity in deep time. In this Introduction, we explore the challenges of these new approaches. First, we discuss how our choices of taxonomic units have implications for the conclusions drawn. Second, we emphasize the need to embrace the interdependence of biotic and abiotic changes, because no living organism ignores its environment. Third, in the light of parts 1 and 2, we discuss the set of dynamic signatures that we might expect to observe in the fossil record. Finally, we ask whether these dynamics represent the most ecologically informative foci for research efforts aimed at inferring the regulators of biodiversity in deep time. The papers in this theme issue contribute in each of these areas.

The uncertain role of diversity dependence in species diversification and the need to incorporate time-varying carrying capacities.

There is no agreement among palaeobiologists or biologists as to whether, or to what extent, there are limits on diversification and species numbers. Here, we posit that part of the disagreement stems from: (i) the lack of explicit criteria for defining the relevant species pools, which may be defined phylogenetically, ecologically or geographically; (ii) assumptions that must be made when extrapolating from population-level logistic growth to macro-evolutionary diversification; and (iii) too much emphasis being placed on fixed carrying capacities, rather than taking into account the opportunities for increased species richness on evolutionary timescales, for example, owing to increased biologically available energy, increased habitat complexity and the ability of many clades to better extract resources from the environment, or to broaden their resource base. Thus, we argue that a more effective way of assessing the evidence for and against the ideas of bound versus unbound diversification is through appropriate definition of the relevant species pools, and through explicit modelling of diversity-dependent diversification with time-varying carrying capacities. Here, we show that time-varying carrying capacities, either increases or decreases, can be accommodated through changing intrinsic diversification rates (diversity-independent effects), or changing the effects of crowding (diversity-dependent effects).

Continental faunal exchange and the asymmetrical radiation of carnivores.

Lineages arriving on islands may undergo explosive evolutionary radiations owing to the wealth of ecological opportunities. Although studies on insular taxa have improved our understanding of macroevolutionary phenomena, we know little about the macroevolutionary dynamics of continental exchanges. Here we study the evolution of eight Carnivora families that have migrated across the Northern Hemisphere to investigate if continental invasions also result in explosive diversification dynamics. We used a Bayesian approach to estimate speciation and extinction rates from a substantial dataset of fossil occurrences while accounting for the incompleteness of the fossil record. Our analyses revealed a strongly asymmetrical pattern in which North American lineages invading Eurasia underwent explosive radiations, whereas lineages invading North America maintained uniform diversification dynamics. These invasions into Eurasia were characterized by high rates of speciation and extinction. The radiation of the arriving lineages in Eurasia coincide with the decline of established lineages or phases of climate change, suggesting differences in the ecological settings between the continents may be responsible for the disparity in diversification dynamics. These results reveal long-term outcomes of biological invasions and show that the importance of explosive radiations in shaping diversity extends beyond insular systems and have significant impact at continental scales.

The role of clade competition in the diversification of North American canids.

The history of biodiversity is characterized by a continual replacement of branches in the tree of life. The rise and demise of these branches (clades) are ultimately determined by changes in speciation and extinction rates, often interpreted as a response to varying abiotic and biotic factors. However, understanding the relative importance of these factors remains a major challenge in evolutionary biology. Here we analyze the rich North American fossil record of the dog family Canidae and of other carnivores to tease apart the roles of competition, body size evolution, and climate change on the sequential replacement of three canid subfamilies (two of which have gone extinct). We develop a novel Bayesian analytic framework to show that competition from multiple carnivore clades successively drove the demise and replacement of the two extinct canid subfamilies by increasing their extinction rates and suppressing their speciation. Competitive effects have likely come from ecologically similar species from both canid and felid clades. These results imply that competition among entire clades, generally considered a rare process, can play a more substantial role than climate change and body size evolution in determining the sequential rise and decline of clades.

How the Red Queen drives terrestrial mammals to extinction.

Most species disappear by the processes of background extinction, yet those processes are poorly understood. We analyzed the evolutionary dynamics of 19 Cenozoic terrestrial mammalian clades with rich fossil records that are now fully extinct or in diversity decline. We find their diversity loss was not just a consequence of "gamblers ruin" but resulted from the evolutionary loss to the Red Queen, a failure to keep pace with a deteriorating environment. Diversity loss is driven equally by both depressed origination rates and elevated extinction rates. Although we find diversity-dependent origination and extinction rates, the diversity of each clade only transiently equaled the implied equilibrium diversity. Thus, the processes that drove diversity loss in terrestrial mammal clades were fundamentally nonequilibrial and overwhelmed diversity-dependent processes.

The molecular phylogenetic signature of clades in decline.

Molecular phylogenies have been used to study the diversification of many clades. However, current methods for inferring diversification dynamics from molecular phylogenies ignore the possibility that clades may be decreasing in diversity, despite the fact that the fossil record shows this to be the case for many groups. Here we investigate the molecular phylogenetic signature of decreasing diversity using the most widely used statistic for inferring diversity dynamics from molecular phylogenies, the γ statistic. We show that if a clade is in decline its molecular phylogeny may show evidence of the decrease in the diversification rate that occurred between its diversification and decline phases. The ability to detect the change in diversification rate depends largely on the ratio of the speciation rates of the diversification and decline phases, the higher the ratio the stronger the signal of the change in diversification rate. Consequently, molecular phylogenies of clades in relative rapid decline do not carry a signature of their decreasing diversification. Further, the signal of the change in diversification rate, if present, declines as the diversity drop. Unfortunately, the molecular signature of clades in decline is the same as the signature produced by diversity dependent diversification. Given this similarity, and the inability of current methods to detect declining diversity, it is likely that some of the extant clades that show a decrease in diversification rate, currently interpreted as evidence for diversity dependent diversification, are in fact in decline. Unless methods can be developed that can discriminate between the different modes of diversification, specifically diversity dependent diversification and declining diversity, we will need the fossil record, or data from some other source, to distinguish between these very different diversity trajectories.

Has the Earth's sixth mass extinction already arrived?

Palaeontologists characterize mass extinctions as times when the Earth loses more than three-quarters of its species in a geologically short interval, as has happened only five times in the past 540 million years or so. Biologists now suggest that a sixth mass extinction may be under way, given the known species losses over the past few centuries and millennia. Here we review how differences between fossil and modern data and the addition of recently available palaeontological information influence our understanding of the current extinction crisis. Our results confirm that current extinction rates are higher than would be expected from the fossil record, highlighting the need for effective conservation measures.