Tiago B. Quental

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.

Diversity dynamics: molecular phylogenies need the fossil record

Over the last two decades, new tools in the analysis of molecular phylogenies have enabled study of the diversification dynamics of living clades in the absence of information about extinct lineages. However, computer simulations and the fossil record show that the inability to access extinct lineages severely limits the inferences that can be drawn from molecular phylogenies. It appears that molecular phylogenies can tell us only when there have been changes in diversification rates, but are blind to the true diversity trajectories and rates of origination and extinction that have led to the species that are alive today. We need to embrace the fossil record if we want to fully understand the diversity dynamics of the living biota.

Recent Synchronous Radiation of a Living Fossil

Despite their ancient origin, the majority of extant cycad species radiated within the past 10 million years. Modern survivors of previously more diverse lineages are regarded as living fossils, particularly when characterized by morphological stasis. Cycads are often cited as a classic example, reaching their greatest diversity during the Jurassic–Cretaceous (199.6 to 65.5 million years ago) then dwindling to their present diversity of ~300 species as flowering plants rose to dominance. Using fossil-calibrated molecular phylogenies, we show that cycads underwent a near synchronous global rediversification beginning in the late Miocene, followed by a slowdown toward the Recent. Although the cycad lineage is ancient, our timetrees indicate that living cycad species are not much older than ~12 million years. These data reject the hypothesized role of dinosaurs in generating extant diversity and the designation of today’s cycad species as living fossils.

When Can Decreasing Diversification Rates Be Detected with Molecular Phylogenies and the Fossil Record

Traditionally, patterns and processes of diversification could only be inferred from the fossil record. However, there are an increasing number of tools that enable diversification dynamics to be inferred from molecular phylogenies. The application of these tools to new data sets has renewed interest in the question of the prevalence of diversity-dependent diversification. However, there is growing recognition that the absence of extinct species in molecular phylogenies may prevent accurate inferences about the underlying diversification dynamics. On the other hand, even though the fossil record provides direct data on extinct species, its incompleteness can also mask true diversification processes. Here, using computer-generated diversity-dependent phylogenies, we mimicked molecular phylogenies by eliminating extinct lineages. We also simulated the fossil record by converting the temporal axis into discrete intervals and imposing a variety of preservation processes on the lineages. Given the lack of reliable phylogenies for many fossil marine taxa, we also stripped away phylogenetic information from the computer-generated phylogenies. For the simulated molecular phylogenies, we examined the efficacy of the standard metric (the γ statistic) for identifying decreasing rates of diversification. We find that the underlying decreasing rate of diversification is detected only when the rate of change in the diversification rate is high, and if the molecular phylogeny happens to capture the diversification process as the equilibrium diversity is first reached or shortly thereafter. In contrast, estimating rates of diversification from the simulated fossil record captures the expected zero rate of diversification after equilibrium is reached under a wide range of preservation scenarios. The ability to detect the initial decreasing rate of diversification is lost as the temporal resolution of the fossil record drops and with a decreased quality of preservation. When the rate of change of the diversification rate is low, the γ statistic will typically fail to detect the decreasing rate of diversification, as will the fossil record, although the fossil record still retains the signature of the diversity dependence in yielding approximately zero diversification rates. Thus, although a significantly negative γ value for a molecular phylogeny indicates a decreasing rate of diversification, a nonsignificantly negative or positive γ value might mean exponential diversification, or a slowly decreasing rate of diversification, or simply species turnover at a constant diversity. The fossil record can be of assistance in helping choose among these possibilities.

How the Red Queen Drives Terrestrial Mammals to Extinction

Background Extinction Diversity results through both the processes of species origination and extinction. However, studies of extinction have tended to focus on mass extinctions, despite the fact that the background extinction represents a greater loss in terms of the absolute number of extinct taxa. In order to identify what factors affect this rate of background extinction, Quental and Marshall (p. 290, published online 20 June) explored the dynamics of 19 mammalian clades and compared the rates of expansions and declines among taxa to expected models assuming random processes. Most clades decline to extinction in a “driven” manner—that is, faster than expected by chance alone. Loss of diversity among Cenozoic land mammals suggests a failure to keep pace with a deteriorating environment. 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.

Extinction During Evolutionary Radiations: Reconciling the Fossil Record with Molecular Phylogenies

Recent application of time-varying birth—death models to molecular phylogenies suggests that a decreasing diversification rate can only be observed if there was a decreasing speciation rate coupled with extremely low or no extinction. However, from a paleontological perspective, zero extinction rates during evolutionary radiations seem unlikely. Here, with a more comprehensive set of computer simulations, we show that substantial extinction can occur without erasing the signal of decreasing diversification rate in a molecular phylogeny. We also find, in agreement with the previous work, that a decrease in diversification rate cannot be observed in a molecular phylogeny with an increasing extinction rate alone. Further, we find that the ability to observe decreasing diversification rates in molecular phylogenies is controlled (in part) by the ratio of the initial speciation rate (Lambda) to the extinction rate (Mu) at equilibrium (the LiMe ratio), and not by their absolute values. Here we show in principle, how estimates of initial speciation rates may be calculated using both the fossil record and the shape of lineage through time plots derived from molecular phylogenies. This is important because the fossil record provides more reliable estimates of equilibrium extinction rates than initial speciation rates.

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

Significance Extinction is a ubiquitous feature of biodiversity history, and although many lineages increase in diversity through time, most of them eventually decline and get replaced. Dinosaurs and mammals represent an extreme and iconic example of such replacement. Here we investigate the causes of the sequential wax and wane of three subfamilies in the dog family Canidae. Contrary to current expectation, we find that competition from phylogenetically distant, but ecologically similar, clades played a more substantial role in canid diversification than climate change and body size evolution. Our results provide novel quantitative evidence indicating that competition from multiple clades can actively drive the displacement and extinction of entire lineages. 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.

A molecular phylogeny of the stingless bee genus Melipona (Hymenoptera: Apidae)

Stingless bees (Meliponini) constitute a diverse group of highly eusocial insects that occur throughout tropical regions around the world. The meliponine genus Melipona is restricted to the New World tropics and has over 50 described species. Melipona, like Apis, possesses the remarkable ability to use representational communication to indicate the location of foraging patches. Although Melipona has been the subject of numerous behavioral, ecological, and genetic studies, the evolutionary history of this genus remains largely unexplored. Here, we implement a multigene phylogenetic approach based on nuclear, mitochondrial, and ribosomal loci, coupled with molecular clock methods, to elucidate the phylogenetic relationships and antiquity of subgenera and species of Melipona. Our phylogenetic analysis resolves the relationship among subgenera and tends to agree with morphology-based classification hypotheses. Our molecular clock analysis indicates that the genus Melipona shared a most recent common ancestor at least approximately 14-17 million years (My) ago. These results provide the groundwork for future comparative analyses aimed at understanding the evolution of complex communication mechanisms in eusocial Apidae.

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.

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).