Testing macro-evolutionary models using incomplete molecular phylogenies.

Incomplete taxon sampling due to underestimation of present-day biodiversity biases diversification analysis by favouring slowdowns in speciation rates towards the recent time. For instance, in diversification dynamics studies in Crocodylia, long-term low net-diversification rates and slowdowns in speciation rates have been suggested to characterize crocodylian evolution. However, crocodylian cryptic diversity has never been considered. Here, we explore the effects of incorporating cryptic diversity into a diversification dynamics analysis of extant crocodylians. We inferred a time-calibrated cryptic-species-level phylogeny using cytochrome b sequences of 45 lineages compared with the formally recognized 26 crocodylian species. Diversification rate estimates using the cryptic-species-level phylogeny show increasing speciation and net-diversification rates towards the present time, which contrasts with previous findings. Cryptic diversity should be considered in future macroevolutionary analyses; however, the representation of cryptic extinct taxa represents a major challenge. Additionally, further investigation of crocodylian diversification dynamics under different underlying genomic data is encouraged upon advances in population genetics. Our case study adds to the diversification dynamics knowledge of extant taxa and demonstrates that cryptic species and robust taxonomic assessment are essential to study recent biodiversity dynamics with broad implications for evolutionary biology and ecology.

Species diversity patterns are governed by complex interactions among biotic and abiotic factors over time and space, but are essentially the result of the diversification dynamics (differential speciation and extinction rates) over the long‐term evolutionary history of a clade. Previous studies have suggested that temporal variation in global temperature drove long‐term diversity changes in Crocodylia, a monophyletic group of large ectothermic organisms. We use a large database of crocodylian fossil occurrences (192 spp.) and body mass estimations, under a taxic approach, to characterize the global diversification dynamics of crocodylians since the Cretaceous, and their correlation with multiple biotic and abiotic factors in a Bayesian framework. The diversification dynamic of crocodylians, which appears to have originated in the Turonian (c. 92.5 Ma), is characterized by several phases with high extinction and speciation rates within a predominantly low long‐term mean rate. Our results reveal long‐term diversification dynamics of Crocodylia to be a highly complex process driven by a combination of biotic and abiotic factors which influenced the speciation and extinction rates in dissimilar ways. Higher crocodylian extinction rates are related to low body mass disparity, indicating selective extinctions of taxa at both ends of the body mass spectrum. Speciation rate slowdowns are noted when the diversity of the clade is high and the warm temperate climatic belt is reduced. Our finding supports the idea that temporal variations of body mass disparity, self‐diversity, and the warm climate belt size provided more direct mechanistic explanations for crocodylian diversification than do proxies of global temperature.

The topic of this thesis is the latitudinal diversity gradient: the general increase in numbers of species from high latitudes towards the equator. Although it is a well-documented and very general pattern, there is little consensus among biologists as to the causes of high tropical species richness. In Chapter 1 I give an overview of the latitudinal diversity gradient and hypotheses proposed to explain it, and outline a framework for developing and testing hypotheses. The emphasis in this thesis is on non-equilibrium hypotheses, and in particular on the idea that rates of species diversification are higher at low latitudes. In Chapter 2 I directly test the hypothesis that rates of species diversification increase towards the equator, using the phylogenetic method of sister-group comparisons. For birds and butterflies, 1 show that there does indeed appear to be an increase in rates of diversification towards lower latitudes. One possible explanation for this pattern links climatic conditions at low latitudes to faster speciation, via a causal chain which includes a higher rate of molecular evolution. In Chapter 3 I test the prediction that rates of molecular evolution are faster at low latitudes, using phylogenies reconstructed from DNA sequence data for birds. Although the results provide no evidence for a latitudinal effect on rates of cytb and ND2 evolution in birds, this chapter demonstrates a way in which further tests on a wider range of genes and taxa can be carried out as more sequence data becomes available. If rates of diversification are higher in the tropics, this may result from latitudinal gradients in life history traits which could influence rates of speciation or extinction. However, previous attempts to test for such patterns have rarely controlled for phylogenetic relationships among species, and have never controlled for geographic range overlap. In Chapter 4 I present a method for analyzing latitudinal variation in life history traits which takes both of these problems into account. For birds, this method indicates strong latitudinal variation in geographic range size and clutch size, less strong variation in body size and niche width, and no variation in the strength of sexual selection. While this does not prove that life history plays a part in generating the latitudinal diversity gradient, a robust demonstration of latitudinal variation in life history traits is an important prerequisite for any hypotheses which link life history with high tropical species richness. Speciation and extinction rates are believed to vary with species' life history and ecology. If speciation or extinction rates also vary with latitude, we should expect species with certain traits to show stronger latitudinal diversity gradients than others. We should also expect to see latitudinal variation in the macroecological structure of species assemblages. Chapters 5 and 6 confirm these expectations. In Chapter 5 I show that smaller-bodied bird species have steeper latitudinal diversity gradients than larger species. This is reflected in systematic latitudinal variation in the shape of body size frequency distributions, usually thought to be relatively consistent across regions. In Chapter 6 I show that body size - abundance relationships in the Australian marsupial fauna differ considerably between temperate and tropical subsets of the fauna. Whereas the temperate species display the typical negative relationship, the tropical species show no significant relationship. This pattern is consistent with the explanation that extinction rates vary with respect to body size, abundance and the latitude in which a species occurs. Together, the results of the analyses presented in this thesis provide evidence in favour of the non-equilibrium view that there are more species in the tropics because rates of species diversification are higher. It seems likely that this is due to latitudinal variation in environmental conditions, leading to latitudinal variation in species' life histories and the structure of species assemblages, and to latitudinal variation in rates of speciation or extinction. However, it is still difficult to judge whether it is variation in speciation rate (cradle model) or extinction rate (museum model) which is of primary importance, or if both are equally important. Further work on this question, applying the large-scale comparative methodology used here, will be necessary to progress towards a full understanding of the high species richness of the tropics.

A well-documented pattern in the fossil record is a long-term decline in the origination rate of new taxa after diversity rebounds from a mass extinction. The mechanisms for this pattern remain elusive. In this article, we investigate the macroevolutionary predictions of an individual-based birth-death model (BDI model) where speciation and extinction rates emerge from population dynamics. We start with the simplest neutral model in which every individual has the same per capita rates of birth, death, and speciation. Although the prediction of the simplest neutral model agrees qualitatively with the fossil pattern, the predicted decline in per-species speciation rates is too fast to explain the long-term trend in fossil data. We thus consider models with variation among species in per capita rates of speciation and a suite of alternative assumptions about the heritability of speciation rate. The results show that interspecific variation in per capita speciation rate can induce differences among species in their ability to resist extinction because a low speciation rate confers a small but important demographic advantage. As a consequence, the model predicts an appropriately slow temporal decline in speciation rates, which provides a mechanistic explanation for the fossil pattern.

The movement of lineages into novel areas can promote ecological opportunity and adaptive radiation, leading to significant species diversity. Not all studies, however, have identified support for ecological opportunity associated with novel intercontinental colonizations. To gain key insights into the drivers of ecological opportunity, we tested whether intercontinental dispersals resulted in ecological opportunity using the Hydrangeaceae-Loasaceae clade, which has numerous centers of diversity across the globe. A time-calibrated phylogeny was reconstructed from four molecular markers. We tested for bursts of speciation rates followed by a decrease as expected phylogenetic patterns under an ecological opportunity model. Ancestral ranges were estimated using historical biogeographic analyses to examine the relationships of ancestral distributions and habitats with speciation and extinction rates. Hydrangeaceae and Loasaceae originated in arid Mesoamerica, then dispersed into South America, Eurasia, and eastern North America. Six clades experienced increased diversification rates, but those increases were not associated with transitions into new continental areas. Mentzelia section Bartonia was the only clade that exhibited a burst of speciation followed by a decrease. Both families originated in arid environments and experienced multiple transitions into mesic and tropical environments, but Loasaceae experienced a higher speciation-to-extinction ratio than Hydrangeaceae in the western Nearctic. Dispersal between continents did not trigger speciation rate shifts in Loasaceae and Hydrangeaceae. Instead, shifts occurred in regions inhabited by intrafamilial relatives and were likely driven by climate change in the Miocene, where species in drier microhabitats diversified into newly created habitats.

ObjectivesThis study examines how speciation and extinction rates vary across primates, with a focus on the recent macroevolutionary dynamics that have shaped extant primate biodiversity.Materials and methodsLineage‐specific macroevolutionary rates were estimated for each tip in a tree containing 307 species using a hidden‐state likelihood model. Differences in tip rates among major clades were evaluated using phylogenetic ANOVA. Differences among diurnal, nocturnal, and cathemeral lineages were also evaluated, based on previous work indicating that activity pattern influences primate diversification.ResultsRate variation in extant primates is low within clades and high between clades. As in previous studies, cercopithecoids stand out in having high net diversification rates, driven by high speciation rates and very low extinction rates. Platyrrhines combine high speciation and high extinction rates, giving them high rates of lineage turnover. Strepsirrhines and tarsiids have low rates of speciation, extinction, turnover, and net diversification. Hominoids are intermediate between platyrrhines and the strepsirrhine‐tarsiid group, and there is evidence for differentiation between hominids and hylobatids. Diurnal lineages have significantly higher speciation rates than nocturnal lineages.ConclusionsRecent anthropoid macroevolution has been characterized by marked variation in diversification dynamics among clades. Strepsirrhines and tarsiids are more uniform, despite divergent evolutionary and biogeographic histories. Higher speciation rates in diurnal lineages may be driven by greater ecological opportunity or reliance on visual signals for mate recognition. However, the differences among anthropoids indicate that factors other than activity pattern (e.g., clade competition, historical contingency) have had a more influential role in shaping recent primate diversification.

The taxonomic evolution of Jurassic and Cretaceous calcareous nannofossil species is described using the following indices: species diversity, rate of speciation, rate of extinction, rate of diversification, rate of turnover, survivorship, and species accretion. The Jurassic prior to the late Oxfordian is characterized by positive diversification rates, that is, rates of speciation exceeded rates of extinction. Highest rates of diversification occurred in the late Lias and early Oxfordian. During the generally regressive latest Jurassic, diversification rates remained low and rates of extinctions exceed rates of speciation. In the early Cretaceous, rates of diversification are positive and peak in the early Valanginian, early Aptian, and middle Albian, after which time rates of extinction generally exceed rates of speciation. Such peaks in rate of evolution coincide with times of increased accumulation of organic carbon in the ocean (“anoxic events”). Peaks in rates of extinction result in very high rates of turnover during times of major regressions, in particular, in the Tithonian and Maastrichtian. Survivorship analyses for three datum planes (74.5, 144, and 160 Ma) show relatively constant extinction rates with some stepping in the older part; they are best explained by a temporally fluctuating abiotic environment causing changes in the probability of extinction. Species accretion curves are also relatively linear with some indication of changing rates of speciation. The coincidences of major changes in evolutionary rates with major paleoceanographic events are indicative of a predominantly abiotic control of nannoplankton evolution. Relationships of evolutionary rates of calcareous nannoplankton with deep ocean ventilation, sea level, and ocean fertility indicates that global tectonic processes are the ultimate causes of evolutionary change.

Speciation and extinction rates can be estimated from molecular phylogenies. Recently, a number of methods have been published showing that these rates can be estimated even if the phylogeny is incomplete, that is, if not all extant species are included. We show that the accuracy of such methods strongly depends on making the correct assumptions about how the sampling process was performed. We focus on phylogenies that are incomplete because some subclades (e.g., genera and families) are each represented as a single lineage. We show that previous methods implicitly assumed that such subclades are defined by randomly (or in an extreme deterministic way) choosing the edges that define the subclades from the complete species phylogeny. We show that these methods produce biased results if higher taxa are defined in a different manner. We introduce strict higher level phylogenies where subclades are defined so that the phylogeny is fully resolved from its origin to time x(cut), and fully unresolved thereafter, so that for all subclades, stem age > x(cut) > crown age. We present estimates of speciation and extinction rates from a phylogeny of birds in which this subclade definition was applied. However, for most higher level phylogenies in the literature, it is unclear how higher taxa were defined, but often such phylogenies can be easily transformed into strict higher level phylogenies, as we illustrate by estimating speciation and extinction rates from a near-complete but only partly resolved species-level phylogeny of mammals. The accuracy of our methods is verified using simulations.

The evolution of key innovations, novel traits that promote diversification, is often seen as major driver for the unequal distribution of species richness within the tree of life. In this study, we aim to determine the factors underlying the extraordinary radiation of the subfamily Bromelioideae, one of the most diverse clades among the neotropical plant family Bromeliaceae. Based on an extended molecular phylogenetic data set, we examine the effect of two putative key innovations, that is, the Crassulacean acid metabolism (CAM) and the water-impounding tank, on speciation and extinction rates. To this aim, we develop a novel Bayesian implementation of the phylogenetic comparative method, binary state speciation and extinction, which enables hypotheses testing by Bayes factors and accommodates the uncertainty on model selection by Bayesian model averaging. Both CAM and tank habit were found to correlate with increased net diversification, thus fulfilling the criteria for key innovations. Our analyses further revealed that CAM photosynthesis is correlated with a twofold increase in speciation rate, whereas the evolution of the tank had primarily an effect on extinction rates that were found five times lower in tank-forming lineages compared to tank-less clades. These differences are discussed in the light of biogeography, ecology, and past climate change.

We still have much to learn about the evolution of taxonomic diversity gradients through geologic time. For example, have latitudinal gradients always been as steep as they are now, or is this a phenomenon linked to some form of Cenozoic global climatic differentiation? The fossil record offers potential to address this sort of problem, and this study reconstructs latitudinal diversity gradients for the last (Tithonian) stage of the Jurassic period using marine bivalves. At this time of relative global warmth, bivalves were cosmopolitan in their distribution and the commonest element within macrobenthic assemblages.Analysis of 31 regional bivalve faunas demonstrates that Tithonian latitudinal gradients were present in both hemispheres, though on a much smaller magnitude than today. The record of the Northern Hemisphere gradient is more complete and shows a steep fall in values at the tropical/temperate boundary; the Southern Hemisphere gradient exhibits a more regular decline in diversity with increasing latitude.Tithonian latitudinal gradients were underpinned by a tropical bivalve fauna that comprises almost equal numbers of epifaunal and infaunal taxa. The epifaunal component was dominated by three pteriomorph families, the Pectinidae, Limidae and Ostreidae, that may be regarded as a long-term component of tropical bivalve diversity. Of the mixture of older and newer “heteroconch” families that formed the bulk of the infaunal component, the latter radiated spectacularly through the Late Cretaceous and Cenozoic to dominate tropical bivalve faunas at the present day. This pulse of heteroconch diversification, which was a major cause of the steepening of the bivalve latitudinal gradient, provides important evidence that rates of speciation may be negatively correlated with latitude.Nevertheless, we cannot exclude the possibility that elevated extinction rates in the highest latitudes also contributed to the marked steepening of bivalve latitudinal gradients over the last 150 Myr. Rates of extinction within epifaunal bivalve taxa appear to have been higher in these regions through the Cretaceous period, but this was largely before any significant global climatic deterioration. Infaunal bivalve clades have had differential success over this time period in the polar regions. Whereas, in comparison with the Tropics, heteroconchs are very much reduced in numbers today, the anomalodesmatans are much better represented, and the protobranchs have positively thrived. We are beginning to appreciate that low temperature per se may not be a primary cause of elevated rates of extinction. Food supply may be an equally important control on both rates of speciation and extinction; those bivalves that have been able to adapt to the extreme seasonality of food supply have flourished in the polar regions.

Determining whether speciation and extinction rates depend on the state of a particular character has been of long-standing interest to evolutionary biologists. To assess the effect of a character on diversification rates using likelihood methods requires that we be able to calculate the probability that a group of extant species would have evolved as observed, given a particular model of the character's effect. Here we describe how to calculate this probability for a phylogenetic tree and a two-state (binary) character under a simple model of evolution (the "BiSSE" model, binary-state speciation and extinction). The model involves six parameters, specifying two speciation rates (rate when the lineage is in state 0; rate when in state 1), two extinction rates (when in state 0; when in state 1), and two rates of character state change (from 0 to 1, and from 1 to 0). Using these probability calculations, we can do maximum likelihood inference to estimate the model's parameters and perform hypothesis tests (e.g., is the rate of speciation elevated for one character state over the other?). We demonstrate the application of the method using simulated data with known parameter values.

Recently, it has been shown with large data sets of extinct mammals that large-bodied lineages experienced higher speciation and extinction rates; with extant mammals, it has been shown that body size evolution is accelerated during speciation. Therefore, it is interesting to investigate whether mammalian body size evolution is faster in large-bodied lineages. Phylogenetic analysis assuming size-independent speciation rates suggested that the rate of body size evolution increases with body size, whereas size differences in recent sister species (that are little affected by species turnover) appear to be independent of size. This supports the hypothesis that high rates of species turnover increase the rate at which interspecific differences accumulate in large-bodied clades, whereas rates of evolution in single lineages are approximately size invariant. Similarly, these findings support the notion that mammalian body size evolution is indeed concentrated in speciation events.

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Phylogenetic trees of only extant species contain information about the underlying speciation and extinction pattern. In this review, I provide an overview over the different methodologies that recover the speciation and extinction dynamics from phylogenetic trees. Broadly, the methods can be divided into two classes: (i) methods using the phylogenetic tree shapes (i.e. trees without branch length information) allowing us to test for speciation rate variation and (ii) methods using the phylogenetic trees with branch length information allowing us to quantify speciation and extinction rates. I end the article with an overview on limitations, open questions and challenges of the reviewed methodology.

Squamates may be an attractive group in which to study the influence of sex chromosomes on speciation rates because of the repeated evolution of heterogamety (both XY and ZW), as well as an apparently large number of taxa with environmental sex-determination.