Colonial-driven extinction of the blue antelope despite genomic adaptation to low population size.

Low genomic diversity is generally indicative of small population size and is considered detrimental by decreasing long-term adaptability.1,2,3,4,5,6 Moreover, small population size may promote gene flow with congeners and outbreeding depression.7,8,9,10,11,12,13 Here, we examine the connection between habitat availability, effective population size (Ne), and extinction by generating a 40× nuclear genome from the extinct blue antelope (Hippotragus leucophaeus). Historically endemic to the relatively small Cape Floristic Region in southernmost Africa,14,15 populations were thought to have expanded and contracted across glacial-interglacial cycles, tracking suitable habitat.16,17,18 However, we found long-term low Ne, unaffected by glacial cycles, suggesting persistence with low genomic diversity for many millennia prior to extinction in ∼AD 1800. A lack of inbreeding, alongside high levels of genetic purging, suggests adaptation to this long-term low Ne and that human impacts during the colonial era (e.g., hunting and landscape transformation), rather than longer-term ecological processes, were central to its extinction. Phylogenomic analyses uncovered gene flow between roan (H. equinus) and blue antelope, as well as between roan and sable antelope (H. niger), approximately at the time of divergence of blue and sable antelope (∼1.9 Ma). Finally, we identified the LYST and ASIP genes as candidates for the eponymous bluish pelt color of the blue antelope. Our results revise numerous aspects of our understanding of the interplay between genomic diversity and evolutionary history and provide the resources for uncovering the genetic basis of this extinct species' unique traits.

Environmental context shapes the relationship between grass consumption and body size in African herbivore communities.

Though herbivore grass dependence has been shown to increase with body size across herbivore species, it is unclear whether this relationship holds at the community level. Here we evaluate whether grass consumption scales positively with body size within African large mammalian herbivore communities and how this relationship varies with environmental context. We used stable carbon isotope and community occurrence data to investigate how grass dependence scales with body size within 23 savanna herbivore communities throughout eastern and central Africa. We found that dietary grass fraction increased with body size for the majority of herbivore communities considered, especially when complete community data were available. However, the slope of this relationship varied, and rainfall seasonality and elephant presence were key drivers of the variation-grass dependence increased less strongly with body size where rainfall was more seasonal and where elephants were present. We found also that the dependence of the herbivore community as a whole on grass peaked at intermediate woody cover. Intraspecific diet variation contributed to these community-level patterns: common hippopotamus (Hippopotamus amphibius) and giraffe (Giraffa camelopardalis) ate less grass where rainfall was more seasonal, whereas Cape buffalo (Syncerus caffer) and savanna elephant (Loxodonta africana) grass consumption were parabolically related to woody cover. Our results indicate that general rules appear to govern herbivore community assembly, though some aspects of herbivore foraging behavior depend upon local environmental context.

Paleoecological evidence for environmental specialization in Paranthropus boisei compared to early Homo.

Since the discovery of Paranthropus boisei alongside early Homo at Olduvai Gorge and East Turkana, paleoanthropologists have attempted to understand the different evolutionary paths of these two hominin lineages. Conventional wisdom is that their prolonged phase of sympatry in eastern Africa reflects different adaptive strategies, with early Homo characterized as the ecologically flexible generalist and Paranthropus as the less versatile specialist. If correct, this should imply differences in their use of ancient environments, with early Homo occurring in a broader range of environmental contexts than Paranthropus. This prediction has yet to be subject to rigorous quantitative evaluation. In this study, we use the 2.0-1.4 Ma fossil bovid assemblages associated with early Homo and P. boisei at East Turkana (Kenya) to quantify the breadth of their environmental associations. We find that early Homo occurs in faunal assemblages indicative of a broader range of environments than P. boisei. A null model taking sampling into account shows that the broad environmental associations of early Homo are indistinguishable from random, whereas P. boisei is one of just a handful of large mammal taxa from East Turkana that has a narrower range of environmental associations than expected by chance. These results support the characterization of P. boisei as an ecological specialist relative to the more generalist Homo. Moreover, the narrow environmental associations observed of P. boisei, unlike those of almost all other C4 grass-consumers in the Turkana Basin, suggest that it likely did not feed on a spatially widespread C4 resource like the leaves, seeds, or rhizomes of grass.

Blue Turns to Gray: Paleogenomic Insights into the Evolutionary History and Extinction of the Blue Antelope (Hippotragus leucophaeus).

The blue antelope (Hippotragus leucophaeus) is the only large African mammal species to have become extinct in historical times, yet no nuclear genomic information is available for this species. A recent study showed that many alleged blue antelope museum specimens are either roan (Hippotragus equinus) or sable (Hippotragus niger) antelopes, further reducing the possibilities for obtaining genomic information for this extinct species. While the blue antelope has a rich fossil record from South Africa, climatic conditions in the region are generally unfavorable to the preservation of ancient DNA. Nevertheless, we recovered two blue antelope draft genomes, one at 3.4× mean coverage from a historical specimen (∼200 years old) and one at 2.1× mean coverage from a fossil specimen dating to 9,800-9,300 cal years BP, making it currently the oldest paleogenome from Africa. Phylogenomic analyses show that blue and sable antelope are sister species, confirming previous mitogenomic results, and demonstrate ancient gene flow from roan into blue antelope. We show that blue antelope genomic diversity was much lower than in roan and sable antelope, indicative of a low population size since at least the early Holocene. This supports observations from the fossil record documenting major decreases in the abundance of blue antelope after the Pleistocene-Holocene transition. Finally, the persistence of this species throughout the Holocene despite low population size suggests that colonial-era human impact was likely the decisive factor in the blue antelope's extinction.

El Niño frequency threshold controls coastal biotic communities.

El Niño has profound influences on ecosystem dynamics. However, we know little about how it shapes vertebrate faunal community composition over centennial time scales, and this limits our ability to forecast change under projections of future El Niño events. On the basis of correlations between geological records of past El Niño frequency and the species composition of bird and fish remains from a Baja California bone deposit that spans the past 12,000 years, we documented marked faunal restructuring when major El Niño events occurred more than five times per century. This tipping point has implications for the past and future ecology of eastern Pacific coastal environments.

No sustained increase in zooarchaeological evidence for carnivory after the appearance of Homo erectus.

The appearance of Homo erectus shortly after 2.0 Ma is widely considered a turning point in human dietary evolution, with increased consumption of animal tissues driving the evolution of larger brain and body size and a reorganization of the gut. An increase in the size and number of zooarchaeological assemblages after the appearance of H. erectus is often offered as a central piece of archaeological evidence for increased carnivory in this species, but this characterization has yet to be subject to detailed scrutiny. Any widespread dietary shift leading to the acquisition of key traits in H. erectus should be persistent in the zooarchaeological record through time and can only be convincingly demonstrated by a broad-scale analysis that transcends individual sites or localities. Here, we present a quantitative synthesis of the zooarchaeological record of eastern Africa from 2.6 to 1.2 Ma. We show that several proxies for the prevalence of hominin carnivory are all strongly related to how well the fossil record has been sampled, which constrains the zooarchaeological visibility of hominin carnivory. When correcting for sampling effort, there is no sustained increase in the amount of evidence for hominin carnivory between 2.6 and 1.2 Ma. Our observations undercut evolutionary narratives linking anatomical and behavioral traits to increased meat consumption in H. erectus, suggesting that other factors are likely responsible for the appearance of its human-like traits.

Seasonal strategies differ between tropical and extratropical herbivores.

Seasonal diet shifts and migration are key components of large herbivore population dynamics, but we lack a systematic understanding of how these behaviours are distributed on a macroecological scale. The prevalence of seasonal strategies is likely related to herbivore body size and feeding guild, and may also be influenced by properties of the environment, such as soil nutrient availability and climate seasonality. We evaluated the distribution of seasonal dietary shifts and migration across large-bodied mammalian herbivores and determined how these behaviours related to diet, body size and environment. We found that herbivore strategies were consistently correlated with their traits: seasonal diet shifts were most prevalent among mixed feeding herbivores and migration among grazers and larger herbivores. Seasonality also played a role, particularly for migration, which was more common at higher latitudes. Both dietary shifts and migration were more widespread among extratropical herbivores, which also exhibited more intermediate diets and body sizes. Our findings suggest that strong seasonality in extratropical systems imposes pressure on herbivores, necessitating widespread behavioural responses to navigate seasonal resource bottlenecks. It follows that tropical and extratropical herbivores may have divergent responses to global change, with intensifying herbivore pressure in extratropical systems contrasting with diminishing herbivore pressure in tropical systems.

Global response of fire activity to late Quaternary grazer extinctions.

Fire activity varies substantially at global scales because of the influence of climate, but at broad spatiotemporal scales, the possible effects of herbivory on fire activity are unknown. Here, we used late Quaternary large-bodied herbivore extinctions as a global exclusion experiment to examine the responses of grassy ecosystem paleofire activity (through charcoal proxies) to continental differences in extinction severity. Grassy ecosystem fire activity increased in response to herbivore extinction, with larger increases on continents that suffered the largest losses of grazers; browser declines had no such effect. These shifts suggest that herbivory can have Earth system­scale effects on fire and that herbivore impacts should be explicitly considered when predicting changes in past and future global fire activity.

Response to Comment on "A global environmental crisis 42,000 years ago".

Our study on the exact timing and the potential climatic, environmental, and evolutionary consequences of the Laschamps Geomagnetic Excursion has generated the hypothesis that geomagnetism represents an unrecognized driver in environmental and evolutionary change. It is important for this hypothesis to be tested with new data, and encouragingly, none of the studies presented by Picin et al. undermine our model.

Response to Comment on "A global environmental crisis 42,000 years ago".

Our paper about the impacts of the Laschamps Geomagnetic Excursion 42,000 years ago has provoked considerable scientific and public interest, particularly in the so-called Adams Event associated with the initial transition of the magnetic poles. Although we welcome the opportunity to discuss our new ideas, Hawks' assertions of misrepresentation are especially disappointing given his limited examination of the material.

Rethinking the ecological drivers of hominin evolution.

A central goal of paleoanthropology is understanding the role of ecological change in hominin evolution. Over the past several decades researchers have expanded the hominin fossil record and assembled detailed late Cenozoic paleoclimatic, paleoenvironmental, and paleoecological archives. However, effective use of these data is precluded by the limitations of pattern-matching strategies for inferring causal relationships between ecological and evolutionary change. We examine several obstacles that have hindered progress, and highlight recent research that is addressing them by (i) confronting an incomplete fossil record, (ii) contending with datasets spanning varied spatiotemporal scales, and (iii) using theoretical frameworks to build stronger inferences. Expanding on this work promises to transform challenges into opportunities and set the stage for a new phase of paleoanthropological research.

A global environmental crisis 42,000 years ago.

Geological archives record multiple reversals of Earth's magnetic poles, but the global impacts of these events, if any, remain unclear. Uncertain radiocarbon calibration has limited investigation of the potential effects of the last major magnetic inversion, known as the Laschamps Excursion [41 to 42 thousand years ago (ka)]. We use ancient New Zealand kauri trees (Agathis australis) to develop a detailed record of atmospheric radiocarbon levels across the Laschamps Excursion. We precisely characterize the geomagnetic reversal and perform global chemistry-climate modeling and detailed radiocarbon dating of paleoenvironmental records to investigate impacts. We find that geomagnetic field minima ~42 ka, in combination with Grand Solar Minima, caused substantial changes in atmospheric ozone concentration and circulation, driving synchronous global climate shifts that caused major environmental changes, extinction events, and transformations in the archaeological record.

Identifying the true number of specimens of the extinct blue antelope (Hippotragus leucophaeus).

Native to southern Africa, the blue antelope (Hippotragus leucophaeus) is the only large African mammal species known to have become extinct in historical times. However, it was poorly documented prior to its extinction ~ 1800 AD, and many of the small number of museum specimens attributed to it are taxonomically contentious. This places limitations on our understanding of its morphology, ecology, and the mechanisms responsible for its demise. We retrieved genetic information from ten of the sixteen putative blue antelope museum specimens using both shotgun sequencing and mitochondrial genome target capture in an attempt to resolve the uncertainty surrounding the identification of these specimens. We found that only four of the ten investigated specimens, and not a single skull, represent the blue antelope. This indicates that the true number of historical museum specimens of the blue antelope is even smaller than previously thought, and therefore hardly any reference material is available for morphometric, comparative and genetic studies. Our study highlights how genetics can be used to identify rare species in natural history collections where other methods may fail or when records are scarce. Additionally, we present an improved mitochondrial reference genome for the blue antelope as well as one complete and two partial mitochondrial genomes. A first analysis of these mitochondrial genomes indicates low levels of maternal genetic diversity in the 'museum population', possibly confirming previous results that blue antelope population size was already low at the time of the European colonization of South Africa.

Investigating Biotic Interactions in Deep Time.

Recent renewed interest in using fossil data to understand how biotic interactions have shaped the evolution of life is challenging the widely held assumption that long-term climate changes are the primary drivers of biodiversity change. New approaches go beyond traditional richness and co-occurrence studies to explicitly model biotic interactions using data on fossil and modern biodiversity. Important developments in three primary areas of research include analysis of (i) macroevolutionary rates, (ii) the impacts of and recovery from extinction events, and (iii) how humans (Homo sapiens) affected interactions among non-human species. We present multiple lines of evidence for an important and measurable role of biotic interactions in shaping the evolution of communities and lineages on long timescales.

Increased ecological resource variability during a critical transition in hominin evolution.

Although climate change is considered to have been a large-scale driver of African human evolution, landscape-scale shifts in ecological resources that may have shaped novel hominin adaptations are rarely investigated. We use well-dated, high-resolution, drill-core datasets to understand ecological dynamics associated with a major adaptive transition in the archeological record ~24 km from the coring site. Outcrops preserve evidence of the replacement of Acheulean by Middle Stone Age (MSA) technological, cognitive, and social innovations between 500 and 300 thousand years (ka) ago, contemporaneous with large-scale taxonomic and adaptive turnover in mammal herbivores. Beginning ~400 ka ago, tectonic, hydrological, and ecological changes combined to disrupt a relatively stable resource base, prompting fluctuations of increasing magnitude in freshwater availability, grassland communities, and woody plant cover. Interaction of these factors offers a resource-oriented hypothesis for the evolutionary success of MSA adaptations, which likely contributed to the ecological flexibility typical of Homo sapiens foragers.

A Late Pleistocene human humerus from Rusinga Island, Lake Victoria, Kenya.

In 2010, a hominin right humerus fragment (KNM-RU 58330) was surface collected in a small gully at Nyamita North in the Late Pleistocene Wasiriya Beds of Rusinga Island, Kenya. A combination of stratigraphic and geochronological evidence suggests the specimen is likely between ∼49 and 36 ka in age. The associated fauna is diverse and dominated by semiarid grassland taxa. The small sample of associated Middle Stone Age artifacts includes Levallois flakes, cores, and retouched points. The 139 mm humeral fragment preserves the shaft from distal to the lesser tubercle to 14 mm below the distal end of the weakly projecting deltoid tuberosity. Key morphological features include a narrow and weakly marked pectoralis major insertion and a distinctive medial bend in the diaphysis at the deltoid insertion. This bend is unusual among recent human humeri but occurs in a few Late Pleistocene humeri. The dimensions of the distal end of the fragment predict a length of 317.9 ± 16.4 mm based on recent samples of African ancestry. A novel method of predicting humeral length from the distance between the middle of the pectoralis major and the bottom of the deltoid insertion predicts a length of 317.3 mm ± 17.6 mm. Cross-sectional geometry at the midshaft shows a relatively high percentage of cortical bone and a moderate degree of flattening of the shaft. The Nyamita humerus is anatomically modern in its morphology and adds to the small sample of hominins from the Late Pleistocene associated with Middle Stone Age artifacts known from East Africa. It may sample a population closely related to the people of the out-of-Africa migration.

Micro Methods for Megafauna: Novel Approaches to Late Quaternary Extinctions and Their Contributions to Faunal Conservation in the Anthropocene.

Drivers of Late Quaternary megafaunal extinctions are relevant to modern conservation policy in a world of growing human population density, climate change, and faunal decline. Traditional debates tend toward global solutions, blaming either dramatic climate change or dispersals of Homo sapiens to new regions. Inherent limitations to archaeological and paleontological data sets often require reliance on scant, poorly resolved lines of evidence. However, recent developments in scientific technologies allow for more local, context-specific approaches. In the present article, we highlight how developments in five such methodologies (radiocarbon approaches, stable isotope analysis, ancient DNA, ancient proteomics, microscopy) have helped drive detailed analysis of specific megafaunal species, their particular ecological settings, and responses to new competitors or predators, climate change, and other external phenomena. The detailed case studies of faunal community composition, extinction chronologies, and demographic trends enabled by these methods examine megafaunal extinctions at scales appropriate for practical understanding of threats against particular species in their habitats today.

Early hominins evolved within non-analog ecosystems.

Present-day African ecosystems serve as referential models for conceptualizing the environmental context of early hominin evolution, but the degree to which modern ecosystems are representative of those in the past is unclear. A growing body of evidence from eastern Africa's rich and well-dated late Cenozoic fossil record documents communities of large-bodied mammalian herbivores with ecological structures differing dramatically from those of the present day, implying that modern communities may not be suitable analogs for the ancient ecosystems of hominin evolution. To determine when and why the ecological structure of eastern Africa's herbivore faunas came to resemble those of the present, here we analyze functional trait changes in a comprehensive dataset of 305 modern and fossil herbivore communities spanning the last ∼7 Myr. We show that nearly all communities prior to ∼700 ka were functionally non-analog, largely due to a greater richness of non-ruminants and megaherbivores (species >1,000 kg). The emergence of functionally modern communities precedes that of taxonomically modern communities by 100,000s of years, and can be attributed to the combined influence of Plio-Pleistocene C4 grassland expansion and pulses of aridity after ∼1 Ma. Given the disproportionate ecological impacts of large-bodied herbivores on factors such as vegetation structure, hydrology, and fire regimes, it follows that the vast majority of early hominin evolution transpired in the context of ecosystems that functioned unlike any today. Identifying how past ecosystems differed compositionally and functionally from those today is key to conceptualizing ancient African environments and testing ecological hypotheses of hominin evolution.