Two Major Extinction Events in the Evolutionary History of Turtles: One Caused by an Asteroid, the Other by Hominins.

AbstractWe live in a time of accelerated biological extinctions that has the potential to mirror past mass extinction events. However, the rarity of mass extinctions and the restructuring of diversity they cause complicate direct comparisons between the current extinction crisis and earlier events. Among animals, turtles (Testudinata) are one of few groups that have both a rich fossil record and sufficiently stable ecological and functional roles to enable meaningful comparisons between the end-Cretaceous mass extinction (∼66 Ma) and the ongoing wave of extinctions. Here we analyze the fossil record of the entire turtle clade and identify two peaks in extinction rates over their evolutionary history. The first coincides with the Cretaceous-Paleogene transition, reflecting patterns previously reported for other taxa. The second major extinction event started in the Pliocene and continues until now. This peak is detectable only for terrestrial turtles and started much earlier in Africa and Eurasia than elsewhere. On the basis of the timing, geography, and functional group of this extinction event, we postulate a link to co-occurring hominins rather than climate change as the cause. These results lend further support to the view that negative biodiversity impacts were already incurred by our ancestors and related lineages and demonstrate the severity of this continued impact through human activities.

The importance of migratory drop-off for island colonization in birds.

Seasonal migration is an underappreciated driver of animal diversification. Changes in migratory behaviour may favour the establishment of sedentary founder populations and promote speciation if there is sufficient reproductive isolation between sedentary and migratory populations. From a systematic literature review, we here quantify the role of migratory drop-off-the loss of migratory behaviour-in promoting speciation in birds on islands. We identify at least 157 independent colonization events likely initiated by migratory species that led to speciation, including 44 cases among recently extinct species. By comparing, for all islands, the proportion of island endemic species that derived from migratory drop-off with the proportion of migratory species among potential colonizers, we showed that seasonal migration has a larger effect on island endemic richness than direct dispersal. We also found that the role of migration in island colonization increases with the geographic isolation of islands. Furthermore, the success of speciation events depends in part on species biogeographic and ecological factors, here positively associated with greater range size and larger flock sizes. These results highlight the importance of shifts in migratory behaviour in the speciation process and calls for greater consideration of migratory drop-off in the biogeographic distribution of birds.

Disproportionate extinction of South American mammals drove the asymmetry of the Great American Biotic Interchange.

The interchange between the previously disconnected faunas of North and South America was a massive experiment in biological invasion. A major gap in our understanding of this invasion is why there was a drastic increase in the proportion of mammals of North American origin found in South America. Four nonmutually exclusive mechanisms may explain this asymmetry: 1) Higher dispersal rate of North American mammals toward the south, 2) higher origination of North American immigrants in South America, 3) higher extinction of mammals with South American origin, and 4) similar dispersal rate but a larger pool of native taxa in North versus South America. We test among these mechanisms by analyzing ∼20,000 fossil occurrences with Bayesian methods to infer dispersal and diversification rates and taxonomic selectivity of immigrants. We find no differences in the dispersal and origination rates of immigrants. In contrast, native South American mammals show higher extinction. We also find that two clades with North American origin (Carnivora and Artiodactyla) had significantly more immigrants in South America than other clades. Altogether, the asymmetry of the interchange was not due to higher origination of immigrants in South America as previously suggested, but resulted from higher extinction of native taxa in southern South America. These results from one of the greatest biological invasions highlight how biogeographic processes and biotic interactions can shape continental diversity.

Phylogenetic and functional clustering illustrate the roles of adaptive radiation and dispersal filtering in jointly shaping late-Quaternary mammal assemblages on oceanic islands.

Islands frequently harbour unique assemblages of species, yet their ecological roles and differences are largely ignored in island biogeography studies. Here, we examine eco-evolutionary processes structuring mammal assemblages on oceanic islands worldwide, including all extant and extinct late-Quaternary mammal species. We find island mammal assemblages tend to be phylogenetically clustered (share more recent evolutionary histories), with clustering increasing with island area and isolation. We also observe that mammal assemblages often tend to be functionally clustered (share similar traits), but the strength of clustering is weak and generally independent from island area or isolation. These findings indicate the important roles of in situ speciation and dispersal filtering in shaping island mammal assemblages under pre-anthropogenic conditions, notably through adaptive radiation of a few clades (e.g. bats, with generally high dispersal abilities). Our study demonstrates that considering the functional and phylogenetic axes of diversity can better reveal the eco-evolutionary processes of island community assembly.

Mapping Africa's Biodiversity: More of the Same Is Just Not Good Enough.

Species distribution data are fundamental to the understanding of biodiversity patterns and processes. Yet, such data are strongly affected by sampling biases, mostly related to site accessibility. The understanding of these biases is therefore crucial in systematics, biogeography, and conservation. Here we present a novel approach for quantifying sampling effort and its impact on biodiversity knowledge, focusing on Africa. In contrast to previous studies assessing sampling completeness (percentage of species recorded in relation to predicted), we investigate whether the lack of knowledge of a site attracts scientists to visit these areas and collect samples of species. We then estimate the time required to sample 90% of the continent under a Weibull distributed biodiversity sampling rate and the number of sampling events required to record $ \ge $50% of the species. Using linear and spatial regression models, we show that previous sampling has been strongly influencing the resampling of areas, attracting repeated visits. This bias has existed for over two centuries, has increased in recent decades, and is most pronounced among mammals. It may take between 172 and 274 years, depending on the group, to achieve at least one sampling event per grid cell in the entire continent. Just one visit will, however, not be enough: in order to record $ \ge $50% of the current diversity, it will require at least 12 sampling events for amphibians, 13 for mammals, and 27 for birds. Our results demonstrate the importance of sampling areas that lack primary biodiversity data and the urgency with which this needs to be done. Current practice is insufficient to adequately classify and map African biodiversity; it can lead to incorrect conclusions being drawn from biogeographic analyses and can result in misleading and self-reinforcing conservation priorities. [Amphibians; birds; mammals; sampling bias; sampling gaps; Wallacean shortfall.].

Mammal diversity will take millions of years to recover from the current biodiversity crisis.

The incipient sixth mass extinction that started in the Late Pleistocene has already erased over 300 mammal species and, with them, more than 2.5 billion y of unique evolutionary history. At the global scale, this lost phylogenetic diversity (PD) can only be restored with time as lineages evolve and create new evolutionary history. Given the increasing rate of extinctions however, can mammals evolve fast enough to recover their lost PD on a human time scale? We use a birth-death tree framework to show that even if extinction rates slow to preanthropogenic background levels, recovery of lost PD will likely take millions of years. These findings emphasize the severity of the potential sixth mass extinction and the need to avoid the loss of unique evolutionary history now.

Brain expansion in early hominins predicts carnivore extinctions in East Africa.

While the anthropogenic impact on ecosystems today is evident, it remains unclear if the detrimental effect of hominins on co-occurring biodiversity is a recent phenomenon or has also been the pattern for earlier hominin species. We test this using the East African carnivore fossil record. We analyse the diversity of carnivores over the last four million years and investigate whether any decline is related to an increase in hominin cognitive capacity, vegetation changes or climatic changes. We find that extinction rates in large carnivores correlate with increased hominin brain size and with vegetation changes, but not with precipitation or temperature changes. While temporal analyses cannot distinguish between the effects of vegetation changes and hominins, we show through spatial analyses of contemporary carnivores in Africa that only hominin causation is plausible. Our results suggest that substantial anthropogenic influence on biodiversity started millions of years earlier than currently assumed.

Rethinking megafauna.

Concern for megafauna is increasing among scientists and non-scientists. Many studies have emphasized that megafauna play prominent ecological roles and provide important ecosystem services to humanity. But, what precisely are 'megafauna'? Here, we critically assess the concept of megafauna and propose a goal-oriented framework for megafaunal research. First, we review definitions of megafauna and analyse associated terminology in the scientific literature. Second, we conduct a survey among ecologists and palaeontologists to assess the species traits used to identify and define megafauna. Our review indicates that definitions are highly dependent on the study ecosystem and research question, and primarily rely on ad hoc size-related criteria. Our survey suggests that body size is crucial, but not necessarily sufficient, for addressing the different applications of the term megafauna. Thus, after discussing the pros and cons of existing definitions, we propose an additional approach by defining two function-oriented megafaunal concepts: 'keystone megafauna' and 'functional megafauna', with its variant 'apex megafauna'. Assessing megafauna from a functional perspective could challenge the perception that there may not be a unifying definition of megafauna that can be applied to all eco-evolutionary narratives. In addition, using functional definitions of megafauna could be especially conducive to cross-disciplinary understanding and cooperation, improvement of conservation policy and practice, and strengthening of public perception. As megafaunal research advances, we encourage scientists to unambiguously define how they use the term 'megafauna' and to present the logic underpinning their definition.

Soil fertility and flood regime are correlated with phylogenetic structure of Amazonian palm communities.

BACKGROUND AND AIMS: Identifying the processes that generate and maintain biodiversity requires understanding of how evolutionary processes interact with abiotic conditions to structure communities. Edaphic gradients are strongly associated with floristic patterns but, compared with climatic gradients, have received relatively little attention. We asked (1) How does the phylogenetic composition of palm communities vary along edaphic gradients within major habitat types? and (2) To what extent are phylogenetic patterns determined by (a) habitat specialists, (b) small versus large palms, and (c) hyperdiverse genera? METHODS: We paired data on palm community composition from 501 transects of 0.25 ha located in two main habitat types (non-inundated uplands and seasonally inundated floodplains) in western Amazonian rain forests with information on soil chemistry, climate, phylogeny and metrics of plant size. We focused on exchangeable base concentration (cmol+ kg-1) as a metric of soil fertility and a floristic index of inundation intensity. We used a null model approach to quantify the standard effect size of mean phylogenetic distance for each transect (a metric of phylogenetic community composition) and related this value to edaphic variables using generalized linear mixed models, including a term for spatial autocorrelation. KEY RESULTS: Overall, we recorded 112 008 individuals belonging to 110 species. Palm communities in non-inundated upland transects (but not floodplain transects) were more phylogenetically clustered in areas of low soil fertility, measured as exchangeable base concentration. In contrast, floodplain transects with more severe flood regimes (as inferred from floristic structure) tended to be phylogenetically clustered. Nearly half of the species recorded (44 %) were upland specialists while 18 % were floodplain specialists. In both habitat types, phylogenetic clustering was largely due to the co-occurrence of small-sized habitat specialists belonging to two hyperdiverse genera (Bactris and Geonoma). CONCLUSIONS: Edaphic conditions are associated with the phylogenetic community structure of palms across western Amazonia, and different factors (specifically, soil fertility and inundation intensity) appear to underlie diversity patterns in non-inundated upland versus floodplain habitats. By linking edaphic gradients with palm community phylogenetic structure, our study reinforces the need to integrate edaphic conditions in eco-evolutionary studies in order to better understand the processes that generate and maintain tropical forest diversity. Our results suggest a role for edaphic niche conservatism in the evolution and distribution of Amazonian palms, a finding with potential relevance for other clades.

Global nutrient transport in a world of giants.

The past was a world of giants, with abundant whales in the sea and large animals roaming the land. However, that world came to an end following massive late-Quaternary megafauna extinctions on land and widespread population reductions in great whale populations over the past few centuries. These losses are likely to have had important consequences for broad-scale nutrient cycling, because recent literature suggests that large animals disproportionately drive nutrient movement. We estimate that the capacity of animals to move nutrients away from concentration patches has decreased to about 8% of the preextinction value on land and about 5% of historic values in oceans. For phosphorus (P), a key nutrient, upward movement in the ocean by marine mammals is about 23% of its former capacity (previously about 340 million kg of P per year). Movements by seabirds and anadromous fish provide important transfer of nutrients from the sea to land, totalling ∼150 million kg of P per year globally in the past, a transfer that has declined to less than 4% of this value as a result of the decimation of seabird colonies and anadromous fish populations. We propose that in the past, marine mammals, seabirds, anadromous fish, and terrestrial animals likely formed an interlinked system recycling nutrients from the ocean depths to the continental interiors, with marine mammals moving nutrients from the deep sea to surface waters, seabirds and anadromous fish moving nutrients from the ocean to land, and large animals moving nutrients away from hotspots into the continental interior.

Science for a wilder Anthropocene: Synthesis and future directions for trophic rewilding research.

Trophic rewilding is an ecological restoration strategy that uses species introductions to restore top-down trophic interactions and associated trophic cascades to promote self-regulating biodiverse ecosystems. Given the importance of large animals in trophic cascades and their widespread losses and resulting trophic downgrading, it often focuses on restoring functional megafaunas. Trophic rewilding is increasingly being implemented for conservation, but remains controversial. Here, we provide a synthesis of its current scientific basis, highlighting trophic cascades as the key conceptual framework, discussing the main lessons learned from ongoing rewilding projects, systematically reviewing the current literature, and highlighting unintentional rewilding and spontaneous wildlife comebacks as underused sources of information. Together, these lines of evidence show that trophic cascades may be restored via species reintroductions and ecological replacements. It is clear, however, that megafauna effects may be affected by poorly understood trophic complexity effects and interactions with landscape settings, human activities, and other factors. Unfortunately, empirical research on trophic rewilding is still rare, fragmented, and geographically biased, with the literature dominated by essays and opinion pieces. We highlight the need for applied programs to include hypothesis testing and science-based monitoring, and outline priorities for future research, notably assessing the role of trophic complexity, interplay with landscape settings, land use, and climate change, as well as developing the global scope for rewilding and tools to optimize benefits and reduce human-wildlife conflicts. Finally, we recommend developing a decision framework for species selection, building on functional and phylogenetic information and with attention to the potential contribution from synthetic biology.

To adapt or go extinct? The fate of megafaunal palm fruits under past global change.

Past global change may have forced animal-dispersed plants with megafaunal fruits to adapt or go extinct, but these processes have remained unexplored at broad spatio-temporal scales. Here, we combine phylogenetic, distributional and fruit size data for more than 2500 palm (Arecaceae) species in a time-slice diversification analysis to quantify how extinction and adaptation have changed over deep time. Our results indicate that extinction rates of palms with megafaunal fruits have increased in the New World since the onset of the Quaternary (2.6 million years ago). In contrast, Old World palms show a Quaternary increase in transition rates towards evolving small fruits from megafaunal fruits. We suggest that Quaternary climate oscillations and concurrent habitat fragmentation and defaunation of megafaunal frugivores in the New World have reduced seed dispersal distances and geographical ranges of palms with megafaunal fruits, resulting in their extinction. The increasing adaptation to smaller fruits in the Old World could reflect selection for seed dispersal by ocean-crossing frugivores (e.g. medium-sized birds and bats) to colonize Indo-Pacific islands against a background of Quaternary sea-level fluctuations. Our macro-evolutionary results suggest that megafaunal fruits are increasingly being lost from tropical ecosystems, either due to extinctions or by adapting to smaller fruit sizes.

PHYLACINE 1.2: The Phylogenetic Atlas of Mammal Macroecology.

Data needed for macroecological analyses are difficult to compile and often hidden away in supplementary material under non-standardized formats. Phylogenies, range data, and trait data often use conflicting taxonomies and require ad hoc decisions to synonymize species or fill in large amounts of missing data. Furthermore, most available data sets ignore the large impact that humans have had on species ranges and diversity. Ignoring these impacts can lead to drastic differences in diversity patterns and estimates of the strength of biological rules. To help overcome these issues, we assembled PHYLACINE, The Phylogenetic Atlas of Mammal Macroecology. This taxonomically integrated platform contains phylogenies, range maps, trait data, and threat status for all 5,831 known mammal species that lived since the last interglacial (~130,000 years ago until present). PHYLACINE is ready to use directly, as all taxonomy and metadata are consistent across the different types of data, and files are provided in easy-to-use formats. The atlas includes both maps of current species ranges and present natural ranges, which represent estimates of where species would live without anthropogenic pressures. Trait data include body mass and coarse measures of life habit and diet. Data gaps have been minimized through extensive literature searches and clearly labelled imputation of missing values. The PHYLACINE database will be archived here as well as hosted online so that users may easily contribute updates and corrections to continually improve the data. This database will be useful to any researcher who wishes to investigate large-scale ecological patterns. Previous versions of the database have already provided valuable information and have, for instance, shown that megafauna extinctions caused substantial changes in vegetation structure and nutrient transfer patterns across the globe.

Patterns, biases and prospects in the distribution and diversity of Neotropical snakes.

Motivation: We generated a novel database of Neotropical snakes (one of the world's richest herpetofauna) combining the most comprehensive, manually compiled distribution dataset with publicly available data. We assess, for the first time, the diversity patterns for all Neotropical snakes as well as sampling density and sampling biases. Main types of variables contained: We compiled three databases of species occurrences: a dataset downloaded from the Global Biodiversity Information Facility (GBIF), a verified dataset built through taxonomic work and specialized literature, and a combined dataset comprising a cleaned version of the GBIF dataset merged with the verified dataset. Spatial location and grain: Neotropics, Behrmann projection equivalent to 1° × 1°. Time period: Specimens housed in museums during the last 150 years. Major taxa studied: Squamata: Serpentes. Software format: Geographical information system (GIS). Results: The combined dataset provides the most comprehensive distribution database for Neotropical snakes to date. It contains 147,515 records for 886 species across 12 families, representing 74% of all species of snakes, spanning 27 countries in the Americas. Species richness and phylogenetic diversity show overall similar patterns. Amazonia is the least sampled Neotropical region, whereas most well-sampled sites are located near large universities and scientific collections. We provide a list and updated maps of geographical distribution of all snake species surveyed. Main conclusions: The biodiversity metrics of Neotropical snakes reflect patterns previously documented for other vertebrates, suggesting that similar factors may determine the diversity of both ectothermic and endothermic animals. We suggest conservation strategies for high-diversity areas and sampling efforts be directed towards Amazonia and poorly known species.

Shallow size-density relations within mammal clades suggest greater intra-guild ecological impact of large-bodied species.

Population densities of species have a predictable relationship with their body mass on a global scale. This relationship is known as the size-density relationship (SDR). The relationship was originally found to be directly opposite of metabolic rate scaling, which led to the hypothesis of energetic equivalence. However, recent studies have suggested that the SDR varies between clades. Specifically, the SDR for certain mammal clades has been found to be less negative than the relationship across all mammals. The aim of the present study is to estimate phylogenetic variation in the scaling relationship, using a data-driven identification of natural phylogenetic substructure in the body size-density relation, and discuss its potential drivers. The classic model is often used to estimate natural population densities, and a further, practical aim is to improve it by incorporating variability among phylogenetic groups. We expand the model for the SDR relation of mammals to include clade-specific variation. We used a dataset with population and body mass estimates of 924 terrestrial mammal species, covering 97 families, and applied an algorithm identifying group-specific changes in the relationship across a family-level phylogeny. We show increased performance in species density estimation is achieved by incorporating clade-specific changes in the relationship compared to the classic model (increasing r2 from .56 to .74 and ΔAICc  = 466). While the global SDR across clades was confirmed to be similar to previous findings (r = -.74), the relationship within all sub-clades was less negative than the overall trend. Our results show that data-driven identification of phylogenetic substructure in the size-density relation substantially improves predictive accuracy of the model. The less negative relationship within clades compared to the overall trend and compared to within clade metabolic scaling suggest that the energetic equivalence rule does not hold. This relationship shows that large species within clades use proportionally more energy than smaller species. Therefore, our results are consistent with a greater intra-guild ecological impact of large-bodied species via partial monopolisation of resources by the largest species of a given guild, and hence size-asymmetric intra-guild competition.

Resurrection of the Island Rule: Human-Driven Extinctions Have Obscured a Basic Evolutionary Pattern.

Islands are or have been occupied by unusual species, such as dwarf proboscideans and giant rodents. The discussion of the classical but controversial island rule-which states that mammalian body sizes converge on intermediate sizes on islands-has been stimulated by these unusual species. In this study, we use an unprecedented global data set of the distributions and body sizes of late Quaternary mammal species and a novel analytical method to analyze body size evolution on islands. The analyses produced strong support for the island rule. Islands have suffered massive human-driven losses of species, and we found that the support for the island rule was substantially stronger when the many late Quaternary extinct species were also considered (particularly the tendency for dwarfing in large taxa). The decisive support for the island rule in this study confirms that evolution plays out in a markedly different way on islands and that human impact may obscure even fundamental evolutionary patterns.

An all-evidence species-level supertree for the palms (Arecaceae).

Several attempts have been made to generate complete species-level phylogenies for large clades, enabling comprehensive analyses of ecological or evolutionary hypotheses at the species level. No such phylogeny has, however, been generated for any major plant group yet, but here we generate such a phylogeny for the palm family (Arecaceae). We do this using a novel Bayesian approach, estimating the validity of intra-generic taxonomic groupings as topological constraints to assist in placing species without genetic or morphological data. From these we implement those that are supported by genetic or morphological data for a given genus or for related genera. The intergeneric relationships in our new phylogeny are surprisingly different from earlier phylogenies in the placement of genera within tribes, but largely identical to previous findings in the deeper branches in the phylogeny, pointing to the need for incorporating phylogenetic uncertainty in analyses based on this phylogeny. Initial analyses of the new phylogeny suggest non-constancy in diversification rates over time within genera, with an apparent increase in diversification rate over time, but no evidence for any geographic variation in the magnitude of this increase. We hope that our study will stimulate further evolutionary or ecological studies using palms as study organisms as well as discussions of the optimal way to place the many species without genetic or morphological data.

A species-level phylogeny of all extant and late Quaternary extinct mammals using a novel heuristic-hierarchical Bayesian approach.

Across large clades, two problems are generally encountered in the estimation of species-level phylogenies: (a) the number of taxa involved is generally so high that computation-intensive approaches cannot readily be utilized and (b) even for clades that have received intense study (e.g., mammals), attention has been centered on relatively few selected species, and most taxa must therefore be positioned on the basis of very limited genetic data. Here, we describe a new heuristic-hierarchical Bayesian approach and use it to construct a species-level phylogeny for all extant and late Quaternary extinct mammals. In this approach, species with large quantities of genetic data are placed nearly freely in the mammalian phylogeny according to these data, whereas the placement of species with lower quantities of data is performed with steadily stricter restrictions for decreasing data quantities. The advantages of the proposed method include (a) an improved ability to incorporate phylogenetic uncertainty in downstream analyses based on the resulting phylogeny, (b) a reduced potential for long-branch attraction or other types of errors that place low-data taxa far from their true position, while maintaining minimal restrictions for better-studied taxa, and (c) likely improved placement of low-data taxa due to the use of closer outgroups.

Global late Quaternary megafauna extinctions linked to humans, not climate change.

The late Quaternary megafauna extinction was a severe global-scale event. Two factors, climate change and modern humans, have received broad support as the primary drivers, but their absolute and relative importance remains controversial. To date, focus has been on the extinction chronology of individual or small groups of species, specific geographical regions or macroscale studies at very coarse geographical and taxonomic resolution, limiting the possibility of adequately testing the proposed hypotheses. We present, to our knowledge, the first global analysis of this extinction based on comprehensive country-level data on the geographical distribution of all large mammal species (more than or equal to 10 kg) that have gone globally or continentally extinct between the beginning of the Last Interglacial at 132,000 years BP and the late Holocene 1000 years BP, testing the relative roles played by glacial-interglacial climate change and humans. We show that the severity of extinction is strongly tied to hominin palaeobiogeography, with at most a weak, Eurasia-specific link to climate change. This first species-level macroscale analysis at relatively high geographical resolution provides strong support for modern humans as the primary driver of the worldwide megafauna losses during the late Quaternary.