Ecological structure of diversity-dependent diversification in Phanerozoic marine bivalves.

Rigorous analysis of diversity-dependence-the hypothesis that the rate of proliferation of new species is inversely related to standing diversity-requires consideration of the ecology of the organisms in question. Differences between infaunal marine bivalves (living entirely within the sediment) and epifaunal forms (living partially or completely above the sediment-water interface) predict that these major ecological groups should have different diversity dynamics: epifaunal species may compete more intensely for space and be more susceptible to predation and physical disturbance. By comparing detrended standing diversity with rates of diversification, origination, and extinction in this exceptional fossil record, we find that epifaunal bivalves experienced significant, negative diversity-dependence in origination and net diversification, whereas infaunal forms show little appreciable relationship between diversity and evolutionary rates. This macroevolutionary contrast is robust to the time span over which dynamics are analysed, whether mass-extinction rebounds are included in the analysis, the treatment of stratigraphic ranges that are not maximally resolved, and the details of detrending. We also find that diversity-dependence persists over hundreds of millions of years, even though diversity itself rises nearly exponentially, belying the notion that diversity-dependence must imply equilibrial diversity dynamics.

Diversity-Dependent Diversification in the History of Marine Animals.

AbstractBy comparing detrended estimates of diversity (taxonomic richness) and rates of origination, extinction, and net diversification, I show that at the global scale over the course of the Phanerozoic eon, rates of diversification and origination are negatively correlated with diversity. By contrast, extinction rates are only weakly correlated with diversity for the most part. These results hold for both genus- and species-level data and for many alternative analytical protocols. The asymmetry between extinction on the one hand and origination and net diversification on the other hand supports a model whereby extinction is largely driven by abiotic perturbations, with subsequent origination filling the void left by depleted diversity. Diversity dependence is somewhat weaker, but still evident, if the initial Ordovician radiation or rebounds from major mass extinctions are omitted from analysis; thus, diversity dependence is influenced, but not dominated, by these special intervals of Earth history. In the transition from Paleozoic to post-Paleozoic time, diversity dependence of origination weakens while that of extinction strengthens; however, diversity dependence of net diversification barely changes in strength. Despite nuances, individual clades largely yield results consistent with those for the aggregate data on all animals. On the whole, diversity-dependent diversification appears to be a pervasive factor in the macroevolution of marine animal life.

Drivers of diversification in freshwater gastropods vary over deep time.

Unravelling the drivers of species diversification through geological time is of crucial importance for our understanding of long-term evolutionary processes. Numerous studies have proposed different sets of biotic and abiotic controls of speciation and extinction rates, but typically they were inferred for a single, long geological time frame. However, whether the impact of biotic and abiotic controls on diversification changes over time is poorly understood. Here, we use a large fossil dataset, a multivariate birth-death model and a comprehensive set of biotic and abiotic predictors, including a new index to quantify tectonic complexity, to estimate the drivers of diversification for European freshwater gastropods over the past 100 Myr. The effects of these factors on origination and extinction are estimated across the entire time frame as well as within sequential time windows of 20 Myr each. Our results find support for temporal heterogeneity in the factors associated with changes in diversification rates. While the factors impacting speciation and extinction rates vary considerably over time, diversity-dependence and topography are consistently important. Our study highlights that a high level of heterogeneity in diversification rates is best captured by incorporating time-varying effects of biotic and abiotic factors.

Understanding the effect of competition during evolutionary radiations: an integrated model of phenotypic and species diversification.

Competition can drive macroevolutionary change, for example during adaptive radiations. However, we still lack a clear understanding of how it shapes diversification processes and patterns. To better understand the macroevolutionary consequences of competition, as well as the signal left on phylogenetic data, we developed a model linking trait evolution and species diversification in an ecological context. We find four main results: first, competition spurs trait diversity but not necessarily species richness; second, competition produces slowdowns in species diversification even in the absence of explicit ecological limits, but not in phenotypic diversification even in the presence of such limits; third, early burst patterns do not provide a reliable way of testing for adaptive radiations; and fourth, looking for phylogenetic signal in trait data and support for phenotypic models incorporating competition is a better alternative. Our results clarify the macroevolutionary consequences of competition and could help design more powerful tests of adaptive radiations in nature.

Environmental limits to mammal diversity vary with latitude and global temperature.

Understanding the mechanisms driving declines in biodiversity with latitude requires assessing if there are ecological limits to the number of species that can coexist, and if these limits vary with latitude, both of which are long-standing and currently debated questions. Here I show that diversification of North American mammals across the Cenozoic Era slowed as diversity increased. This damping of diversification rates indicates ecological limitation, which occurred even though diversity fluctuated through time and was almost never at an equilibrium 'saturation' point. The estimated environmental carrying capacity was correlated with global temperature positively at high latitudes and negatively at low latitudes. Geographical variation in how standing diversity affects diversification rates could help explain the latitudinal biodiversity gradient as well as changes in the strength of the gradient over time.

Sex and the shifting biodiversity dynamics of marine animals in deep time.

The fossil record of marine animals suggests that diversity-dependent processes exerted strong control on biodiversification: after the Ordovician Radiation, genus richness did not trend for hundreds of millions of years. However, diversity subsequently rose dramatically in the Cretaceous and Cenozoic (145 million years ago-present), indicating that limits on diversification can be overcome by ecological or evolutionary change. Here, we show that the Cretaceous-Cenozoic radiation was driven by increased diversification in animals that transfer sperm between adults during fertilization, whereas animals that broadcast sperm into the water column have not changed significantly in richness since the Late Ordovician (∼450 million years ago). We argue that the former group radiated in part because directed sperm transfer permits smaller population sizes and additional modes of prezygotic isolation, as has been argued previously for the coincident radiation of angiosperms. Directed sperm transfer tends to co-occur with many ecological traits, such as a predatory lifestyle. Ecological specialization likely operated synergistically with mode of fertilization in driving the diversification that began during the Mesozoic marine revolution. Plausibly, the ultimate driver of diversification was an increase in food availability, but its effects on the fauna were regulated by fundamental reproductive and ecological traits.

Diversity-dependent evolutionary rates in early Palaeozoic zooplankton.

The extent to which biological diversity affects rates of diversification is central to understanding macroevolutionary dynamics, yet no consensus has emerged on the importance of diversity-dependence of evolutionary rates. Here, we analyse the species-level fossil record of early Palaeozoic graptoloids, documented with high temporal resolution, to test directly whether rates of diversification were influenced by levels of standing diversity within this major clade of marine zooplankton. To circumvent the statistical regression-to-the-mean artefact, whereby higher- and lower-than-average values of diversity tend to be followed by negative and positive diversification rates, we construct a non-parametric, empirically scaled, diversity-independent null model by randomizing the observed diversification rates with respect to time. Comparing observed correlations between diversity and diversification rate to those expected from this diversity-independent model, we find evidence for negative diversity-dependence, accounting for up to 12% of the variance in diversification rate, with maximal correlation at a temporal lag of approximately 1 Myr. Diversity-dependence persists throughout the Ordovician and Silurian, despite a major increase in the strength and frequency of extinction and speciation pulses in the Silurian. By contrast to some previous work, we find that diversity-dependence affects rates of speciation and extinction nearly equally on average, although subtle differences emerge when we compare the Ordovician and Silurian.

Age-area scaling of extinction debt within isolated terrestrial vertebrate assemblages.

A new model of delayed species loss (extinction debt) within isolated communities is applied to a large data set of terrestrial vertebrate assemblages (n = 188) occupying habitat fragments or islands varying greatly in size and age. The model encapsulates previous approaches based on diversity-dependent (DD) extinction rates while allowing for a more flexible treatment of temporal dynamics. Three important results emerge. First, species loss rate slows down with the age of the isolate, a strong and general pattern largely unnoticed so far. Secondly, while being good candidates in the light of previous works, DD models fail to account for this pattern, a result that necessitates a search for other mechanisms. Thirdly, a simple diversity-independent model based on area (converted into population size) and age explains 97% of the variability in species loss rate and appears to be a promising predictive tool to handle extinction debt following habitat loss.

Environmental changes define ecological limits to species richness and reveal the mode of macroevolutionary competition.

Co-dependent geological and climatic changes obscure how species interact in deep time. The interplay between these environmental factors makes it hard to discern whether ecological competition exerts an upper limit on species richness. Here, using the exceptional fossil record of Cenozoic Era macroperforate planktonic foraminifera, we assess the evidence for alternative modes of macroevolutionary competition. Our models support an environmentally dependent macroevolutionary form of contest competition that yields finite upper bounds on species richness. Models of biotic competition assuming unchanging environmental conditions were overwhelmingly rejected. In the best-supported model, temperature affects the per-lineage diversification rate, while both temperature and an environmental driver of sediment accumulation defines the upper limit. The support for contest competition implies that incumbency constrains species richness by restricting niche availability, and that the number of macroevolutionary niches varies as a function of environmental changes.

Minimal effects of latitude on present-day speciation rates in New World birds.

The tropics contain far greater numbers of species than temperate regions, suggesting that rates of species formation might differ systematically between tropical and non-tropical areas. We tested this hypothesis by reconstructing the history of speciation in New World (NW) land birds using BAMM, a Bayesian framework for modelling complex evolutionary dynamics on phylogenetic trees. We estimated marginal distributions of present-day speciation rates for each of 2571 species of birds. The present-day rate of speciation varies approximately 30-fold across NW birds, but there is no difference in the rate distributions for tropical and temperate taxa. Using macroevolutionary cohort analysis, we demonstrate that clades with high tropical membership do not produce species more rapidly than temperate clades. For nearly any value of present-day speciation rate, there are far more species in the tropics than the temperate zone. Any effects of latitude on speciation rate are marginal in comparison to the dramatic variation in rates among clades.

Ecology limits the diversity of the Cape flora: phylogenetics and diversification of the genus Tetraria.

Understanding the ecology and evolution of the hyper-diverse Cape flora is dependent on developing an understanding of its component parts, best epitomized by the Cape floral clades that have diversified and are largely endemic to the region. Here we employ a new dated phylogenetic hypothesis for the sedge genus Tetraria, one of the smaller Cape floral clades, to develop an understanding of timing and rates of diversification in the group. Specifically, we test whether diversification in Tetraria slowed as the number of extant lineages increased, suggesting that available ecological niche space has become increasingly saturated through time. The radiation of Tetraria began approximately 18million years ago, concordant with that of many other Cape clades. Diversification rates in the genus showed no drastic shifts in response to major environmental changes, but declined as lineage diversity accumulated, indicative of ecological limitation on speciation rates. This allows the development of heuristic predictions about the composition of Tetraria assemblages at various spatial scales, and suggests that closely related species should either be ecologically differentiated or have non-overlapping geographic distributions. The question of whether ecological limitation of diversity is a common phenomenon in other Cape lineages has important implications for our understanding of the evolution and ecology of the contemporary Cape flora as a whole.

Limited ecological opportunity influences the tempo of morphological evolution in birds.

According to classic models of lineage diversification and adaptive radiation, phenotypic evolution should accelerate in the context of ecological opportunity and slow down when niches become saturated.1,2 However, only weak support for these ideas has been found in nature, perhaps because most analyses make the biologically unrealistic assumption that clade members contribute equally to reducing ecological opportunity, even when they occur in different continents or specialize on different habitats and diets. To view this problem through a different lens, we adapted a new phylogenetic modeling approach that accounts for the fact that competition for ecological opportunity only occurs between species that coexist and share similar habitats and diets. Applying this method to trait data for nearly all extant species of landbirds,3 we find a widespread signature of decelerating trait evolution in lineages adapted to similar habitats or diets. The strength of this pattern was consistent across latitudes when comparing tropical and temperate assemblages. Our results provide little support for the idea that increased diversity and tighter packing of niches accentuates evolutionary slowdowns in the tropics and instead suggest that limited ecological opportunity can be an important factor determining the rate of morphological diversification at a global scale.

Branching patterns in phylogenies cannot distinguish diversity-dependent diversification from time-dependent diversification.

One of the primary goals of macroevolutionary biology has been to explain general trends in long-term diversity patterns, including whether such patterns correspond to an upscaling of processes occurring at lower scales. Reconstructed phylogenies often show decelerated lineage accumulation over time. This pattern has often been interpreted as the result of diversity-dependent (DD) diversification, where the accumulation of species causes diversification to decrease through niche filling. However, other processes can also produce such a slowdown, including time dependence without diversity dependence. To test whether phylogenetic branching patterns can be used to distinguish these two mechanisms, we formulated a time-dependent, but diversity-independent model that matches the expected diversity through time of a DD model. We simulated phylogenies under each model and studied how well likelihood methods could recover the true diversification mode. Standard model selection criteria always recovered diversity dependence, even when it was not present. We correct for this bias by using a bootstrap method and find that neither model is decisively supported. This implies that the branching pattern of reconstructed trees contains insufficient information to detect the presence or absence of diversity dependence. We advocate that tests encompassing additional data, for example, traits or range distributions, are needed to evaluate how diversity drives macroevolutionary trends.

Detecting local diversity-dependence in diversification.

Whether there are ecological limits to species diversification is a hotly debated topic. Molecular phylogenies show slowdowns in lineage accumulation, suggesting that speciation rates decline with increasing diversity. A maximum-likelihood (ML) method to detect diversity-dependent (DD) diversification from phylogenetic branching times exists, but it assumes that diversity-dependence is a global phenomenon and therefore ignores that the underlying species interactions are mostly local, and not all species in the phylogeny co-occur locally. Here, we explore whether this ML method based on the nonspatial diversity-dependence model can detect local diversity-dependence, by applying it to phylogenies, simulated with a spatial stochastic model of local DD speciation, extinction, and dispersal between two local communities. We find that type I errors (falsely detecting diversity-dependence) are low, and the power to detect diversity-dependence is high when dispersal rates are not too low. Interestingly, when dispersal is high the power to detect diversity-dependence is even higher than in the nonspatial model. Moreover, estimates of intrinsic speciation rate, extinction rate, and ecological limit strongly depend on dispersal rate. We conclude that the nonspatial DD approach can be used to detect diversity-dependence in clades of species that live in not too disconnected areas, but parameter estimates must be interpreted cautiously.

The influence of ecological and geographic limits on the evolution of species distributions and diversity.

The role of ecological limits in regulating the distribution and diversification of species remains controversial. Although such limits must ultimately arise from constraints on local species coexistence, this spatial context is missing from most macroevolutionary models. Here, we develop a stochastic, spatially explicit model of species diversification to explore the phylogenetic and biogeographic patterns expected when local diversity is bounded. We show how local ecological limits, by regulating opportunities for range expansion and thus rates of speciation and extinction, lead to temporal slowdowns in diversification and predictable differences in equilibrium diversity between regions. However, our models also show that even when regions have identical diversity limits, the dynamics of diversification and total number of species supported at equilibrium can vary dramatically depending on the relative size of geographic and local ecological niche space. Our model predicts that small regions with higher local ecological limits support a higher standing diversity and more balanced phylogenetic trees than large geographic areas with more stringent constraints on local coexistence. Our findings highlight how considering the spatial context of diversification can provide new insights into the role of ecological limits in driving variation in biodiversity across space, time, and clades.

Phylogenetic tests for evolutionary innovation: the problematic link between key innovations and exceptional diversification.

Evolutionary innovation contributes to the spectacular diversity of species and phenotypes across the tree of life. 'Key innovations' are widely operationalized within evolutionary biology as traits that facilitate increased diversification rates, such that lineages bearing the traits ultimately contain more species than closely related lineages lacking the focal trait. In this article, I briefly review the inference, analysis and interpretation of evolutionary innovation on phylogenetic trees. I argue that differential rates of lineage diversification should not be used as the basis for key innovation tests, despite the statistical tractability of such approaches. Under traditional interpretations of the macroevolutionary 'adaptive zone', we should not necessarily expect key innovations to confer faster diversification rates upon lineages that possess them relative to their extant sister clades. I suggest that a key innovation is a trait that allows a lineage to interact with the environment in a fundamentally different way and which, as a result, increases the total diversification-but not necessarily the diversification rate-of the parent clade. Considered alone, branching patterns in phylogenetic trees are poorly suited to the inference of evolutionary innovation due to their inherently low information content with respect to the processes that produce them. However, phylogenies may be important for identifying transformational shifts in ecological and morphological space that are characteristic of innovation at the macroevolutionary scale.This article is part of the themed issue 'Process and pattern in innovations from cells to societies'.

Phylogenetic estimates of speciation and extinction rates for testing ecological and evolutionary hypotheses.

Phylogenies are used to estimate rates of speciation and extinction, reconstruct historical diversification scenarios, and link these to ecological and evolutionary factors, such as climate or organismal traits. Recent models can now estimate the effects of binary, multistate, continuous, and biogeographic characters on diversification rates. Others test for diversity dependence (DD) in speciation and extinction, which has become recognized as an important process in numerous clades. A third class incorporates flexible time-dependent functions, enabling reconstruction of major periods of both expanding and contracting diversity. Although there are some potential problems (particularly for estimating extinction), these methods hold promise for answering many classic questions in ecology and evolution, such as the origin of adaptive radiations, and the latitudinal gradient in species richness.