Mesozoic calcareous nannofossil evolution: Relation to paleoceanographic events

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.

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.

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.

Although theory predicts that dispersal has a pivotal influence on speciation and extinction rates, it can have contradictory effects on each, such that empirical quantification of its role is required. In many studies, dispersal reduction appears to promote diversification, although some comparisons of migratory and nonmigratory species suggest otherwise. We tested for a relationship between migratory status and diversification rate within the dominant radiation of temperate Southern Hemisphere freshwater fishes, the Galaxiidae. We reconstructed a molecular phylogeny comprising >95% of extant taxa, and applied State-dependent Speciation Extinction models to estimate speciation, extinction, and diversification rates. In contrast to some previous studies, we revealed higher diversification rates in nonmigratory lineages. The reduced gene flow experienced by nonmigratory galaxiids appears to have increased diversification under conditions of allopatry or local adaptation. Migratory galaxiid lineages, by contrast, are genetically homogeneous within landmasses, but may also be rarely able to diversify by colonizing other landmasses in the temperate Southern Hemisphere. Apparent contradictions among studies of dispersal-diversification relationships may be explained by the spatial context of study systems relative to species dispersal abilities, by means of the "intermediate dispersal" model; the accurate quantification of dispersal abilities will aid in the understanding of these proposed interactions.

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.

Biodiversity results from origination and extinction, justifying interest in identifying traits that influence this balance. Traits implicated in the success or failure of lineages include dispersal, colonization ability, and geographic range size. We investigated the impact of dispersal and range size on contemporary diversity in the Rosales. We used the multiple-state speciation and extinction (MuSSE) method to explore the effects on genus-level diversification of two genus-level traits (geographic range size and within-genus proclivity to speciate) and two species traits (seed dispersal and growth habit) and the multiple hidden-state speciation and extinction (MuHiSSE) method for species-level associations. Finally, we conducted a PGLS (phylogenetic least-squares) analysis to distinguish between speciation within genera versus origination of new genera. At the species level, animal dispersal enhances diversification rate in both woody and herbaceous lineages, while woody lineages without animal dispersal have higher extinction rates than speciation rates. At the genus level, herbaceous taxa have positive diversification rates regardless of other character states. Diversification rate variation is also explained by two interactions: (1) a three-way interaction between large geographic range, animal-mediated dispersal, and high within-genus species richness, whereby genera possessing all three traits have high diversification rates, and (2) a four-way interaction by which the three-way interaction is stronger in woody genera than in herbaceous genera. Colonization ability may underlie the relationship between dispersal type and range size and may influence past diversification rates by decreasing extinction rates during late Cenozoic climate volatility. Thus, colonization ability could be used to predict future extinction risk to aid conservation.

Whatever criteria are used to measure evolutionary success – species numbers, geographic range, ecological abundance, ecological and life history diversity, background diversification rates, or the presence of rapidly evolving clades – the legume family is one of the most successful lineages of flowering plants. Despite this, we still know rather little about the dynamics of lineage and species diversification across the family through the Cenozoic, or about the underlying drivers of diversification. There have been few attempts to estimate net species diversification rates or underlying speciation and extinction rates for legume clades, to test whether among-lineage variation in diversification rates deviates from null expectations, or to locate species diversification rate shifts on specific branches of the legume phylogenetic tree. In this study, time-calibrated phylogenetic trees for a set of species-rich legume clades – Calliandra, Indigofereae, Lupinus, Mimosa and Robinieae – and for the legume family as a whole, are used to explore how we might approach these questions. These clades are analysed using recently developed maximum likelihood and Bayesian methods to detect species diversification rate shifts and test for among-lineage variation in speciation, extinction and net diversification rates. Possible explanations for rate shifts in terms of extrinsic factors and/or intrinsic trait evolution are discussed. In addition, several methodological issues and limitations associated with these analyses are highlighted emphasizing the potential to improve our understanding of the evolutionary dynamics of legume diversification by using much more densely sampled phylogenetic trees that integrate information across broad taxonomic, geographical and temporal levels.

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.

Mitochondrial and nuclear genomes must be co-adapted to ensure proper cellular respiration and energy production. Mito-nuclear incompatibility reduces individual fitness and induces hybrid infertility, which can drive reproductive barriers and speciation. Here, we develop a birth-death model for evolution in spatially extended populations under selection for mito-nuclear co-adaptation. Mating is constrained by physical and genetic proximity, and offspring inherit nuclear genomes from both parents, with recombination. The model predicts macroscopic patterns including a community's species diversity, species abundance distribution, speciation and extinction rates, as well as intraspecific and interspecific genetic variation. We explore how these long-term outcomes depend upon the parameters of reproduction: individual fitness governed by mito-nuclear compatibility, constraints on mating compatibility and ecological carrying capacity. We find that strong selection for mito-nuclear compatibility reduces the equilibrium number of species after a radiation, increasing species' abundances and simultaneously increasing both speciation and extinction rates. The negative correlation between species diversity and diversification rates in our model agrees with the broad empirical pattern of lower diversity and higher speciation/extinction rates in temperate regions, compared to the tropics. We conclude that these empirical patterns may be caused in part by latitudinal variation in metabolic demands and corresponding variation in selection for mito-nuclear function.

High-level phylogenies are very common in evolutionary analyses, although they are often treated as incomplete data. Here, we provide statistical tools to analyze what we name "clade data," which are the ages of clades together with their numbers of species. We develop a general approach for the statistical modeling of variation in speciation and extinction rates, including temporal variation, unknown variation, and linear and nonlinear modeling. We show how this approach can be generalized to a wide range of situations, including testing the effects of life-history traits and environmental variables on diversification rates. We report the results of an extensive simulation study to assess the performance of some statistical tests presented here as well as of the estimators of speciation and extinction rates. These latter results suggest the possibility to estimate correctly extinction rate in the absence of fossils. An example with data on fish is presented.

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.

BackgroundAcross the tree of life there are numerous evolutionary transitions between different habitats (i.e., aquatic and terrestrial or marine and freshwater). Many of these dramatic evolutionary shifts parallel developmental shifts that require physiological, anatomical and behavioral changes for survival and reproduction. Diadromy (scheduled movement between marine and freshwater) has been characterized as a behavior that acts as an evolutionary intermediate state between marine and freshwater environments, implying that diadromous lineages are evolutionarily transient. This hypothesis comes with assumptions regarding the rates of evolutionary transitions in and out of diadromy as well as rates of speciation and extinction in diadromous fishes.ResultsBased on a published phylogeny of 7822 species of ray-finned fishes, state speciation and extinction models of evolutionary transition between marine, freshwater, and diadromous species suggest transition rates out of diadromy are 5–100 times higher that transition between marine and freshwater or into diadromy. Additionally, high speciation and low extinction rates separate diadromous fishes from marine and freshwater species. As a result, net diversification (net diversification = speciation – extinction) is about 7–40 times higher in diadromous fishes compared to freshwater and marine respectively. Together the transition, speciation, and extinction rates suggest diadromy is the least stable of the three states.ConclusionEvolutionary transitions to diadromy are rare in fishes. However, once established, diversification rates in diadromous lineages are high compared to both marine and freshwater species. Diadromous lineages tend to be more transient than marine or freshwater lineages and are found to give rise to marine and freshwater specialists in addition to diadromous descendants. Although diadromy is not a necessary evolutionary intermediate between marine and freshwater, these results support the interpretation of diadromy as an important, occasionally intermediate state, that contributes to biodiversity in fishes in all environments. This evolutionary instability of diadromous lineages is counteracted by their relatively high diversification rates. These findings highlight the importance of integrating the dynamics of diversification and major evolutionary transitions for understanding macroevolutionary patterns.

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.

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 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.