52,000 years of woolly rhinoceros population dynamics reveal extinction mechanisms.

The extinction of the woolly rhinoceros (Coelodonta antiquitatis) at the onset of the Holocene remains an enigma, with conflicting evidence regarding its cause and spatiotemporal dynamics. This partly reflects challenges in determining demographic responses of late Quaternary megafauna to climatic and anthropogenic causal drivers with available genetic and paleontological techniques. Here, we show that elucidating mechanisms of ancient extinctions can benefit from a detailed understanding of fine-scale metapopulation dynamics, operating over many millennia. Using an abundant fossil record, ancient DNA, and high-resolution simulation models, we untangle the ecological mechanisms and causal drivers that are likely to have been integral in the decline and later extinction of the woolly rhinoceros. Our 52,000-y reconstruction of distribution-wide metapopulation dynamics supports a pathway to extinction that began long before the Holocene, when the combination of cooling temperatures and low but sustained hunting by humans trapped woolly rhinoceroses in suboptimal habitats along the southern edge of their range. Modeling indicates that this ecological trap intensified after the end of the last ice age, preventing colonization of newly formed suitable habitats, weakening stabilizing metapopulation processes, triggering the extinction of the woolly rhinoceros in the early Holocene. Our findings suggest that fragmentation and resultant metapopulation dynamics should be explicitly considered in explanations of late Quaternary megafauna extinctions, sending a clarion call to the fragility of the remaining large-bodied grazers restricted to disjunct fragments of poor-quality habitat due to anthropogenic environmental change.

Changes in the functional diversity of modern bird species over the last million years.

Despite evidence of declining biosphere integrity, we currently lack understanding of how the functional diversity associated with changes in abundance among ecological communities has varied over time and before widespread human disturbances. We combine morphological, ecological, and life-history trait data for >260 extant bird species with genomic-based estimates of changing effective population size (Ne) to quantify demographic-based shifts in avian functional diversity over the past million years and under pre-anthropogenic climate warming. We show that functional diversity was relatively stable over this period, but underwent significant changes in some key areas of trait space due to changing species abundances. Our results suggest that patterns of population decline over the Pleistocene have been concentrated in particular regions of trait space associated with extreme reproductive strategies and low dispersal ability, consistent with an overall erosion of functional diversity. Further, species most sensitive to climate warming occupied a relatively narrow region of functional space, indicating that the largest potential population increases and decreases under climate change will occur among species with relatively similar trait sets. Overall, our results identify fluctuations in functional space of extant species over evolutionary timescales and represent the demographic-based vulnerability of different regions of functional space among these taxa. The integration of paleodemographic dynamics with functional trait data enhances our ability to quantify losses of biosphere integrity before anthropogenic disturbances and attribute contemporary biodiversity loss to different drivers over time.

The population history of northeastern Siberia since the Pleistocene.

Northeastern Siberia has been inhabited by humans for more than 40,000 years but its deep population history remains poorly understood. Here we investigate the late Pleistocene population history of northeastern Siberia through analyses of 34 newly recovered ancient genomes that date to between 31,000 and 600 years ago. We document complex population dynamics during this period, including at least three major migration events: an initial peopling by a previously unknown Palaeolithic population of 'Ancient North Siberians' who are distantly related to early West Eurasian hunter-gatherers; the arrival of East Asian-related peoples, which gave rise to 'Ancient Palaeo-Siberians' who are closely related to contemporary communities from far-northeastern Siberia (such as the Koryaks), as well as Native Americans; and a Holocene migration of other East Asian-related peoples, who we name 'Neo-Siberians', and from whom many contemporary Siberians are descended. Each of these population expansions largely replaced the earlier inhabitants, and ultimately generated the mosaic genetic make-up of contemporary peoples who inhabit a vast area across northern Eurasia and the Americas.

Response of an Afro-Palearctic bird migrant to glaciation cycles.

Migration allows animals to exploit spatially separated and seasonally available resources at a continental to global scale. However, responding to global climatic changes might prove challenging, especially for long-distance intercontinental migrants. During glacial periods, when conditions became too harsh for breeding in the north, avian migrants have been hypothesized to retract their distribution to reside within small refugial areas. Here, we present data showing that an Afro-Palearctic migrant continued seasonal migration, largely within Africa, during previous glacial-interglacial cycles with no obvious impact on population size. Using individual migratory track data to hindcast monthly bioclimatic habitat availability maps through the last 120,000 y, we show altered seasonal use of suitable areas through time. Independently derived effective population sizes indicate a growing population through the last 40,000 y. We conclude that the migratory lifestyle enabled adaptation to shifting climate conditions. This indicates that populations of resource-tracking, long-distance migratory species could expand successfully during warming periods in the past, which could also be the case under future climate scenarios.

Process-explicit models reveal pathway to extinction for woolly mammoth using pattern-oriented validation.

Pathways to extinction start long before the death of the last individual. However, causes of early stage population declines and the susceptibility of small residual populations to extirpation are typically studied in isolation. Using validated process-explicit models, we disentangle the ecological mechanisms and threats that were integral in the initial decline and later extinction of the woolly mammoth. We show that reconciling ancient DNA data on woolly mammoth population decline with fossil evidence of location and timing of extinction requires process-explicit models with specific demographic and niche constraints, and a constrained synergy of climatic change and human impacts. Validated models needed humans to hasten climate-driven population declines by many millennia, and to allow woolly mammoths to persist in mainland Arctic refugia until the mid-Holocene. Our results show that the role of humans in the extinction dynamics of woolly mammoth began well before the Holocene, exerting lasting effects on the spatial pattern and timing of its range-wide extinction.

Spatiotemporal influences of climate and humans on muskox range dynamics over multiple millennia.

Processes leading to range contractions and population declines of Arctic megafauna during the late Pleistocene and early Holocene are uncertain, with intense debate on the roles of human hunting, climatic change, and their synergy. Obstacles to a resolution have included an overreliance on correlative rather than process-explicit approaches for inferring drivers of distributional and demographic change. Here, we disentangle the ecological mechanisms and threats that were integral in the decline and extinction of the muskox (Ovibos moschatus) in Eurasia and in its expansion in North America using process-explicit macroecological models. The approach integrates modern and fossil occurrence records, ancient DNA, spatiotemporal reconstructions of past climatic change, species-specific population ecology, and the growth and spread of anatomically modern humans. We show that accurately reconstructing inferences of past demographic changes for muskox over the last 21,000 years require high dispersal abilities, large maximum densities, and a small Allee effect. Analyses of validated process-explicit projections indicate that climatic change was the primary driver of muskox distribution shifts and demographic changes across its previously extensive (circumpolar) range, with populations responding negatively to rapid warming events. Regional analyses show that the range collapse and extinction of the muskox in Europe (~13,000 years ago) was likely caused by humans operating in synergy with climatic warming. In Canada and Greenland, climatic change and human activities probably combined to drive recent population sizes. The impact of past climatic change on the range and extinction dynamics of muskox during the Pleistocene-Holocene transition signals a vulnerability of this species to future increased warming. By better establishing the ecological processes that shaped the distribution of the muskox through space and time, we show that process-explicit macroecological models have important applications for the future conservation and management of this iconic species in a warming Arctic.

Species-specific responses of Late Quaternary megafauna to climate and humans.

Despite decades of research, the roles of climate and humans in driving the dramatic extinctions of large-bodied mammals during the Late Quaternary period remain contentious. Here we use ancient DNA, species distribution models and the human fossil record to elucidate how climate and humans shaped the demographic history of woolly rhinoceros, woolly mammoth, wild horse, reindeer, bison and musk ox. We show that climate has been a major driver of population change over the past 50,000 years. However, each species responds differently to the effects of climatic shifts, habitat redistribution and human encroachment. Although climate change alone can explain the extinction of some species, such as Eurasian musk ox and woolly rhinoceros, a combination of climatic and anthropogenic effects appears to be responsible for the extinction of others, including Eurasian steppe bison and wild horse. We find no genetic signature or any distinctive range dynamics distinguishing extinct from surviving species, emphasizing the challenges associated with predicting future responses of extant mammals to climate and human-mediated habitat change.

High proportion of smaller ranged hummingbird species coincides with ecological specialization across the Americas.

Ecological communities that experience stable climate conditions have been speculated to preserve more specialized interspecific associations and have higher proportions of smaller ranged species (SRS). Thus, areas with disproportionally large numbers of SRS are expected to coincide geographically with a high degree of community-level ecological specialization, but this suggestion remains poorly supported with empirical evidence. Here, we analysed data for hummingbird resource specialization, range size, contemporary climate, and Late Quaternary climate stability for 46 hummingbird-plant mutualistic networks distributed across the Americas, representing 130 hummingbird species (ca 40% of all hummingbird species). We demonstrate a positive relationship between the proportion of SRS of hummingbirds and community-level specialization, i.e. the division of the floral niche among coexisting hummingbird species. This relationship remained strong even when accounting for climate, furthermore, the effect of SRS on specialization was far stronger than the effect of specialization on SRS, suggesting that climate largely influences specialization through species' range-size dynamics. Irrespective of the exact mechanism involved, our results indicate that communities consisting of higher proportions of SRS may be vulnerable to disturbance not only because of their small geographical ranges, but also because of their high degree of specialization.

Linking environmental filtering and disequilibrium to biogeography with a community climate framework.

We present a framework to measure the strength of environmental filtering and disequilibrium of the species composition of a local community across time, relative to past, current, and future climates. We demonstrate the framework by measuring the impact of climate change on New World forests, integrating data for climate niches of more than 14000 species, community composition of 471 New World forest plots, and observed climate across the most recent glacial-interglacial interval. We show that a majority of communities have species compositions that are strongly filtered and are more in equilibrium with current climate than random samples from the regional pool. Variation in the level of current community disequilibrium can be predicted from Last Glacial Maximum climate and will increase with near-future climate change.

Integrating multiple lines of evidence into historical biogeography hypothesis testing: a Bison bison case study.

One of the grand goals of historical biogeography is to understand how and why species' population sizes and distributions change over time. Multiple types of data drawn from disparate fields, combined into a single modelling framework, are necessary to document changes in a species's demography and distribution, and to determine the drivers responsible for change. Yet truly integrated approaches are challenging and rarely performed. Here, we discuss a modelling framework that integrates spatio-temporal fossil data, ancient DNA, palaeoclimatological reconstructions, bioclimatic envelope modelling and coalescence models in order to statistically test alternative hypotheses of demographic and potential distributional changes for the iconic American bison (Bison bison). Using different assumptions about the evolution of the bioclimatic niche, we generate hypothetical distributional and demographic histories of the species. We then test these demographic models by comparing the genetic signature predicted by serial coalescence against sequence data derived from subfossils and modern populations. Our results supported demographic models that include both climate and human-associated drivers of population declines. This synthetic approach, integrating palaeoclimatology, bioclimatic envelopes, serial coalescence, spatio-temporal fossil data and heterochronous DNA sequences, improves understanding of species' historical biogeography by allowing consideration of both abiotic and biotic interactions at the population level.

Evaluating natural medicinal resources and their exposure to global change.

Medicinal plants and their bioactive molecules are integral components of nature and have supported the health of human societies for millennia. However, the prevailing view of medicinal biodiversity solely as an ecosystem-decoupled natural resource of commercial value prevents people from fully benefiting from the capacity of nature to provide medicines and from assessing the vulnerability of this capacity to the global environmental crisis. Emerging scientific and technological developments and traditional knowledge allow for appreciating medicinal plant resources from a planetary health perspective. In this Personal View, we highlight and integrate current knowledge that includes medicinal, biodiversity, and environmental change research in a transdisciplinary framework to evaluate natural medicinal resources and their vulnerability in the anthropocene. With Europe as an application case, we propose proxy spatial indicators for establishing the capacity, potential societal benefits, and economic values of native medicinal plant resources and the exposure of these resources to global environmental change. The proposed framework and indicators aim to be a basis for transdisciplinary research on medicinal biodiversity and could guide decisions in addressing crucial multiple Sustainable Development Goals, from accessible global health care to natural habitat protection and restoration.

Was the Late Ordovician mass extinction truly exceptional?

The Late Ordovician mass extinction event is the oldest of the five great extinction events in the fossil record. It has long been regarded as an outlier among mass extinctions, primarily due to its association with a cooling climate. However, recent temporally better resolved fossil biodiversity estimates complicate this view, providing growing evidence for a prolonged but punctuated biodiversity decline modulated by changes in atmospheric composition, ocean chemistry, and viable habitat area. This evolving view invokes extinction drivers similar to those that occurred during other major extinctions; some are even factors in the current human-induced biodiversity crisis. Even this very ancient and, at first glance, exceptional event conveys important lessons about the intensifying 'sixth mass extinction'.

Species-specific traits mediate avian demographic responses under past climate change.

Anticipating species' responses to environmental change is a pressing mission in biodiversity conservation. Despite decades of research investigating how climate change may affect population sizes, historical context is lacking, and the traits that mediate demographic sensitivity to changing climate remain elusive. We use whole-genome sequence data to reconstruct the demographic histories of 263 bird species over the past million years and identify networks of interacting morphological and life history traits associated with changes in effective population size (Ne) in response to climate warming and cooling. Our results identify direct and indirect effects of key traits representing dispersal, reproduction and survival on long-term demographic responses to climate change, thereby highlighting traits most likely to influence population responses to ongoing climate warming.

Diversification of flowering plants in space and time.

The rapid diversification and high species richness of flowering plants is regarded as 'Darwin's second abominable mystery'. Today the global spatiotemporal pattern of plant diversification remains elusive. Using a newly generated genus-level phylogeny and global distribution data for 14,244 flowering plant genera, we describe the diversification dynamics of angiosperms through space and time. Our analyses show that diversification rates increased throughout the early Cretaceous and then slightly decreased or remained mostly stable until the end of the Cretaceous-Paleogene mass extinction event 66 million years ago. After that, diversification rates increased again towards the present. Younger genera with high diversification rates dominate temperate and dryland regions, whereas old genera with low diversification dominate the tropics. This leads to a negative correlation between spatial patterns of diversification and genus diversity. Our findings suggest that global changes since the Cenozoic shaped the patterns of flowering plant diversity and support an emerging consensus that diversification rates are higher outside the tropics.

Earth beyond six of nine planetary boundaries.

This planetary boundaries framework update finds that six of the nine boundaries are transgressed, suggesting that Earth is now well outside of the safe operating space for humanity. Ocean acidification is close to being breached, while aerosol loading regionally exceeds the boundary. Stratospheric ozone levels have slightly recovered. The transgression level has increased for all boundaries earlier identified as overstepped. As primary production drives Earth system biosphere functions, human appropriation of net primary production is proposed as a control variable for functional biosphere integrity. This boundary is also transgressed. Earth system modeling of different levels of the transgression of the climate and land system change boundaries illustrates that these anthropogenic impacts on Earth system must be considered in a systemic context.

Genetic diversity loss in the Anthropocene.

Anthropogenic habitat loss and climate change are reducing species' geographic ranges, increasing extinction risk and losses of species' genetic diversity. Although preserving genetic diversity is key to maintaining species' adaptability, we lack predictive tools and global estimates of genetic diversity loss across ecosystems. We introduce a mathematical framework that bridges biodiversity theory and population genetics to understand the loss of naturally occurring DNA mutations with decreasing habitat. By analyzing genomic variation of 10,095 georeferenced individuals from 20 plant and animal species, we show that genome-wide diversity follows a mutations-area relationship power law with geographic area, which can predict genetic diversity loss from local population extinctions. We estimate that more than 10% of genetic diversity may already be lost for many threatened and nonthreatened species, surpassing the United Nations' post-2020 targets for genetic preservation.

Climate change threatens European conservation areas.

Europe has the world's most extensive network of conservation areas. Conservation areas are selected without taking into account the effects of climate change. How effectively would such areas conserve biodiversity under climate change? We assess the effectiveness of protected areas and the Natura 2000 network in conserving a large proportion of European plant and terrestrial vertebrate species under climate change. We found that by 2080, 58 ± 2.6% of the species would lose suitable climate in protected areas, whereas losses affected 63 ± 2.1% of the species of European concern occurring in Natura 2000 areas. Protected areas are expected to retain climatic suitability for species better than unprotected areas (P < 0.001), but Natura 2000 areas retain climate suitability for species no better and sometimes less effectively than unprotected areas. The risk is high that ongoing efforts to conserve Europe's biodiversity are jeopardized by climate change. New policies are required to avert this risk.

Ice age climate, evolutionary constraints and diversity patterns of European dung beetles.

Current climate and Pleistocene climatic changes are both known to be associated with geographical patterns of diversity. We assess their associations with the European Scarabaeinae dung beetles, a group with high dispersal ability and well-known adaptations to warm environments. By assessing spatial stationarity in climate variability since the last glacial maximum (LGM), we find that current scarab richness is related to the location of their limits of thermal tolerance during the LGM. These limits mark a strong change in their current species richness-environment relationships. Furthermore, northern scarab assemblages are nested and composed of a phylogenetically clustered subset of large-range sized generalist species, whereas southern ones are diverse and variable in composition. Our results show that species responses to current climate are limited by the evolution of assemblages that occupied relatively climatically stable areas during the Pleistocene, and by post-glacial dispersal in those that were strongly affected by glaciations.

Climate change, humans, and the extinction of the woolly mammoth.

Woolly mammoths inhabited Eurasia and North America from late Middle Pleistocene (300 ky BP [300,000 years before present]), surviving through different climatic cycles until they vanished in the Holocene (3.6 ky BP). The debate about why the Late Quaternary extinctions occurred has centred upon environmental and human-induced effects, or a combination of both. However, testing these two hypotheses-climatic and anthropogenic-has been hampered by the difficulty of generating quantitative estimates of the relationship between the contraction of the mammoth's geographical range and each of the two hypotheses. We combined climate envelope models and a population model with explicit treatment of woolly mammoth-human interactions to measure the extent to which a combination of climate changes and increased human pressures might have led to the extinction of the species in Eurasia. Climate conditions for woolly mammoths were measured across different time periods: 126 ky BP, 42 ky BP, 30 ky BP, 21 ky BP, and 6 ky BP. We show that suitable climate conditions for the mammoth reduced drastically between the Late Pleistocene and the Holocene, and 90% of its geographical range disappeared between 42 ky BP and 6 ky BP, with the remaining suitable areas in the mid-Holocene being mainly restricted to Arctic Siberia, which is where the latest records of woolly mammoths in continental Asia have been found. Results of the population models also show that the collapse of the climatic niche of the mammoth caused a significant drop in their population size, making woolly mammoths more vulnerable to the increasing hunting pressure from human populations. The coincidence of the disappearance of climatically suitable areas for woolly mammoths and the increase in anthropogenic impacts in the Holocene, the coup de grâce, likely set the place and time for the extinction of the woolly mammoth.