Lee Hsiang Liow

Are specialists at risk under environmental change? Neoecological, paleoecological and phylogenetic approaches

The question ‘what renders a species extinction prone’ is crucial to biologists. Ecological specialization has been suggested as a major constraint impeding the response of species to environmental changes. Most neoecological studies indicate that specialists suffer declines under recent environmental changes. This was confirmed by many paleoecological studies investigating longer-term survival. However, phylogeneticists, studying the entire histories of lineages, showed that specialists are not trapped in evolutionary dead ends and could even give rise to generalists. Conclusions from these approaches diverge possibly because (i) of approach-specific biases, such as lack of standardization for sampling efforts (neoecology), lack of direct observations of specialization (paleoecology), or binary coding and prevalence of specialists (phylogenetics); (ii) neoecologists focus on habitat specialization; (iii) neoecologists focus on extinction of populations, phylogeneticists on persistence of entire clades through periods of varying extinction and speciation rates; (iv) many phylogeneticists study species in which specialization may result from a lack of constraints. We recommend integrating the three approaches by studying common datasets, and accounting for range-size variation among species, and we suggest novel hypotheses on why certain specialists may not be particularly at risk and consequently why certain generalists deserve no less attention from conservationists than specialists.

Extinctions in ancient and modern seas

In the coming century, life in the ocean will be confronted with a suite of environmental conditions that have no analog in human history. Thus, there is an urgent need to determine which marine species will adapt and which will go extinct. Here, we review the growing literature on marine extinctions and extinction risk in the fossil, historical, and modern records to compare the patterns, drivers, and biological correlates of marine extinctions at different times in the past. Characterized by markedly different environmental states, some past periods share common features with predicted future scenarios. We highlight how the different records can be integrated to better understand and predict the impact of current and projected future environmental changes on extinction risk in the ocean.

Looking forward through the past : identification of 50 priority research questions in palaeoecology

Summary 1. Priority question exercises are becoming an increasingly common tool to frame future agendas in conservation and ecological science. They are an effective way to identify research foci that advance the field and that also have high policy and conservation relevance. 2. To date there has been no coherent synthesis of key questions and priority research areas for palaeoecology, which combines biological, geochemical and molecular techniques in order to reconstruct past ecological and environmental systems on timescales from decades to millions of years. 3. We adapted a well-established methodology to identify 50 priority research questions in palaeoecology. Using a set of criteria designed to identify realistic and achievable research goals, we selected questions from a pool submitted by the international palaeoecology research community and relevant policy practitioners. This article is protected by copyright. All rights reserved. Accepted Article 4. The integration of online participation, both before and during the workshop, increased international engagement in question selection. 5. The questions selected are structured around six themes: human–environment interactions in the Anthropocene; biodiversity, conservation, and novel ecosystems; biodiversity over long timescales; ecosystem processes and biogeochemical cycling; comparing, combining and synthesizing information from multiple records; and new developments in palaeoecology. 6. Future opportunities in palaeoecology are related to improved incorporation of uncertainty into reconstructions, an enhanced understanding of ecological and evolutionary dynamics and processes, and the continued application of long-term data for better-informed landscape management. 7. Synthesis Palaeoecology is a vibrant and thriving discipline and these 50 priority questions highlight its potential for addressing both pure (e.g. ecological and evolutionary, methodological) and applied (e.g. environmental and conservation) issues related to ecological science and global change.

Higher origination and extinction rates in larger mammals.

Do large mammals evolve faster than small mammals or vice versa? Because the answer to this question contributes to our understanding of how life-history affects long-term and large-scale evolutionary patterns, and how microevolutionary rates scale-up to macroevolutionary rates, it has received much attention. A satisfactory or consistent answer to this question is lacking, however. Here, we take a fresh look at this problem using a large fossil dataset of mammals from the Neogene of the Old World (NOW). Controlling for sampling biases, calculating per capita origination and extinction rates of boundary-crossers and estimating survival probabilities using capture-mark-recapture (CMR) methods, we found the recurring pattern that large mammal genera and species have higher origination and extinction rates, and therefore shorter durations. This pattern is surprising in the light of molecular studies, which show that smaller animals, with their shorter generation times and higher metabolic rates, have greater absolute rates of evolution. However, higher molecular rates do not necessarily translate to higher taxon rates because both the biotic and physical environments interact with phenotypic variation, in part fueled by mutations, to affect origination and extinction rates. To explain the observed pattern, we propose that the ability to evolve and maintain behavior such as hibernation, torpor and burrowing, collectively termed “sleep-or-hide” (SLOH) behavior, serves as a means of environmental buffering during expected and unexpected environmental change. SLOH behavior is more common in some small mammals, and, as a result, SLOH small mammals contribute to higher average survivorship and lower origination probabilities among small mammals.

The rise and fall of species: implications for macroevolutionary and macroecological studies

Knowing the geographic extents of species is crucial for understanding the causes of diversity distributions and modes of speciation and extinction. Species geographic ranges are often viewed as approximately constant in size in geological time, even though climate change studies have shown that historical and modern species geographic distributions are not static. Here, we use an extensive global microfossil database to explore the temporal trajectories of geographic extents over the entire lifespan of marine nannoplankton, diatom, planktic foraminifer and radiolarian species. We show that geographic extents are not static over geological time-scales. Temporal trajectories of species geographic ranges are asymmetric: the rise is quicker than the fall. We propose that once a species has overcome its initial difficulties in geographic establishment, it rises to its peak geographic extent. However, once this peak value is reached, it will also have a maximal number of species to interact with. The negative of these biotic interactions could then cause a gradual geographic decline. We discuss the multiple implications of our findings with reference to macroecological and macroevolutionary studies.

Red Queen: from populations to taxa and communities

Biotic interactions via the struggle for control of energy and the interactive effects of biota with their physical environment characterize Van Valens Red Queen (VRQ). Here, we review new evidence for and against a VRQ view of the world from studies of increasing temporal and spatial scales. Interactions among biota and with the physical environment are important for generating and maintaining diversity on diverse timescales, but detailed mechanisms remain poorly understood. We recommend directly estimating the effect of biota and the physical environment on ecological and evolutionary processes. Promising approaches for elucidating VRQ include using mathematical modelling, controlled experimental systems, sampling and processes-oriented approaches for analysing data from natural systems, while paying extra attention to biotic interactions discernable from the fossil record.

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.

Bayesian Estimation of Speciation and Extinction from Incomplete Fossil Occurrence Data

The temporal dynamics of species diversity are shaped by variations in the rates of speciation and extinction, and there is a long history of inferring these rates using first and last appearances of taxa in the fossil record. Understanding diversity dynamics critically depends on unbiased estimates of the unobserved times of speciation and extinction for all lineages, but the inference of these parameters is challenging due to the complex nature of the available data. Here, we present a new probabilistic framework to jointly estimate species-specific times of speciation and extinction and the rates of the underlying birth-death process based on the fossil record. The rates are allowed to vary through time independently of each other, and the probability of preservation and sampling is explicitly incorporated in the model to estimate the true lifespan of each lineage. We implement a Bayesian algorithm to assess the presence of rate shifts by exploring alternative diversification models. Tests on a range of simulated data sets reveal the accuracy and robustness of our approach against violations of the underlying assumptions and various degrees of data incompleteness. Finally, we demonstrate the application of our method with the diversification of the mammal family Rhinocerotidae and reveal a complex history of repeated and independent temporal shifts of both speciation and extinction rates, leading to the expansion and subsequent decline of the group. The estimated parameters of the birth-death process implemented here are directly comparable with those obtained from dated molecular phylogenies. Thus, our model represents a step towards integrating phylogenetic and fossil information to infer macroevolutionary processes.

Lower Extinction Risk in Sleep-or-Hide Mammals

An ever larger proportion of Earth’s biota is affected by the current accelerating environmental change. The mismatches between organisms and their environments are now increasing in both magnitude and frequency, resulting in lowered fitness and hence the decline of populations. Under this scenario, species with behavioral and/or physiological traits that provide them shelter from the environment are predicted to be less vulnerable to population declines than species that are always exposed to the elements. Here, we coded 4,536 living mammal species for sleep‐or‐hide (SLOH) behavior, including hibernation, torpor, and the use of burrows, among other related traits. We demonstrate that species that exhibit SLOH behavior are underrepresented in high‐risk International Union for Conservation of Nature Red List categories. We found that SLOH behavior contributes to lowering extinction risk even after we accounted for other factors that directly or indirectly buffer species against extinction, such as larger geographic ranges and smaller body sizes. This result is robust to analyses using phylogenetically independent contrasts. Sleep‐or‐hide behavior, made possible by a related suite of physiological adaptations, allows mammals to function at lower metabolic rates and/or buffer them from changing physical elements. Mammals with SLOH behavior have a greater propensity to survive in the current extinction crisis and probably also in past crises because of reduced exposure to environmental stress.

The role of biotic forces in driving macroevolution: beyond the Red Queen.

A multitude of hypotheses claim that abiotic factors are the main drivers of macroevolutionary change. By contrast, Van Valens Red Queen hypothesis is often put forward as the sole representative of the view that biotic forcing is the main evolutionary driver. This imbalance of hypotheses does not reflect our current knowledge: theoretical work demonstrates the plausibility of biotically driven long-term evolution, whereas empirical work suggests a central role for biotic forcing in macroevolution. We call for a more pluralistic view of how biotic forces may drive long-term evolution that is compatible with both phenotypic stasis in the fossil record and with non-constant extinction rates. Promising avenues of research include contrasting predictions from relevant theories within ecology and macroevolution, as well as embracing both abiotic and biotic proxies while modelling long-term evolutionary data. By fitting models describing hypotheses of biotically driven macroevolution to data, we could dissect their predictions and transcend beyond pattern description, possibly narrowing the divide between our current understanding of micro- and macroevolution.