Edward Byrd Davis

Climate refugia: joint inference from fossil records, species distribution models and phylogeography

Climate refugia, locations where taxa survive periods of regionally adverse climate, are thought to be critical for maintaining biodiversity through the glacial-interglacial climate changes of the Quaternary. A critical research need is to better integrate and reconcile the three major lines of evidence used to infer the existence of past refugia - fossil records, species distribution models and phylogeographic surveys - in order to characterize the complex spatiotemporal trajectories of species and populations in and out of refugia. Here we review the complementary strengths, limitations and new advances for these three approaches. We provide case studies to illustrate their combined application, and point the way towards new opportunities for synthesizing these disparate lines of evidence. Case studies with European beech, Qinghai spruce and Douglas-fir illustrate how the combination of these three approaches successfully resolves complex species histories not attainable from any one approach. Promising new statistical techniques can capitalize on the strengths of each method and provide a robust quantitative reconstruction of species history. Studying past refugia can help identify contemporary refugia and clarify their conservation significance, in particular by elucidating the fine-scale processes and the particular geographic locations that buffer species against rapidly changing climate.

The Impact of the Species–Area Relationship on Estimates of Paleodiversity

Estimates of paleodiversity patterns through time have relied on datasets that lump taxonomic occurrences from geographic areas of varying size per interval of time. In essence, such estimates assume that the species–area effect, whereby more species are recorded from larger geographic areas, is negligible for fossil data. We tested this assumption by using the newly developed Miocene Mammal Mapping Project database of western North American fossil mammals and its associated analysis tools to empirically determine the geographic area that contributed to species diversity counts in successive temporal bins. The results indicate that a species–area effect markedly influences counts of fossil species, just as variable spatial sampling influences diversity counts on the modern landscape. Removing this bias suggests some traditionally recognized peaks in paleodiversity are just artifacts of the species–area effect while others stand out as meriting further attention. This discovery means that there is great potential for refining existing time-series estimates of paleodiversity, and for using species–area relationships to more reliably understand the magnitude and timing of such biotically important events as extinction, lineage diversification, and long-term trends in ecological structure.

The California Hotspots Project: identifying regions of rapid diversification of mammals.

The high rate of anthropogenic impact on natural systems mandates protection of the evolutionary processes that generate and sustain biological diversity. Environmental drivers of diversification include spatial heterogeneity of abiotic and biotic agents of divergent selection, features that suppress gene flow, and climatic or geological processes that open new niche space. To explore how well such proxies perform as surrogates for conservation planning, we need first to map areas with rapid diversification —‘evolutionary hotspots’. Here we combine estimates of range size and divergence time to map spatial patterns of neo‐endemism for mammals of California, a global biodiversity hotspot. Neo‐endemism is explored at two scales: (i) endemic species, weighted by the inverse of range size and mtDNA sequence divergence from sisters; and (ii) as a surrogate for spatial patterns of phenotypic divergence, endemic subspecies, again using inverse‐weighting of range size. The species‐level analysis revealed foci of narrowly endemic, young taxa in the central Sierra Nevada, northern and central coast, and Tehachapi and Peninsular Ranges. The subspecies endemism‐richness analysis supported the last four areas as hotspots for diversification, but also highlighted additional coastal areas (Monterey to north of San Francisco Bay) and the Inyo Valley to the east. We suggest these hotspots reflect the major processes shaping mammal neo‐endemism: steep environmental gradients, biotic admixture areas, and areas with recent geological/climate change. Anthropogenic changes to both environment and land use will have direct impacts on regions of rapid divergence. However, despite widespread changes to land cover in California, the majority of the hotspots identified here occur in areas with relatively intact ecological landscapes. The geographical scope of conserving evolutionary process is beyond the scale of any single agency or nongovernmental organization. Choosing which land to closely protect and/or purchase will always require close coordination between agencies.

Merging paleobiology with conservation biology to guide the future of terrestrial ecosystems

Looking back to move forward The current impacts of humanity on nature are rapid and destructive, but species turnover and change have occurred throughout the history of life. Although there is much debate about the best approaches to take in conservation, ultimately, we need to permit or enhance the resilience of natural systems so that they can continue to adapt and function into the future. In a Review, Barnosky et al. argue that the best way to do this is to look back at paleontological history as a way to understand how ecological resilience is maintained, even in the face of change. Science, this issue p. eaah4787 BACKGROUND The pace and magnitude of human-caused global change has accelerated dramatically over the past 50 years, overwhelming the capacity of many ecosystems and species to maintain themselves as they have under the more stable conditions that prevailed for at least 11,000 years. The next few decades threaten even more rapid transformations because by 2050, the human population is projected to grow by 3 billion while simultaneously increasing per capita consumption. Thus, to avoid losing many species and the crucial aspects of ecosystems that we need—for both our physical and emotional well-being—new conservation paradigms and integration of information from conservation biology, paleobiology, and the Earth sciences are required. ADVANCES Rather than attempting to hold ecosystems to an idealized conception of the past, as has been the prevailing conservation paradigm until recently, maintaining vibrant ecosystems for the future now requires new approaches that use both historical and novel conservation landscapes, enhance adaptive capacity for ecosystems and organisms, facilitate connectedness, and manage ecosystems for functional integrity rather than focusing entirely on particular species. Scientific breakthroughs needed to underpin such a paradigm shift are emerging at the intersection of ecology and paleobiology, revealing (i) which species and ecosystems will need human intervention to persist; (ii) how to foster population connectivity that anticipates rapidly changing climate and land use; (iii) functional attributes that characterize ecosystems through thousands to millions of years, irrespective of the species that are involved; and (iv) the range of compositional and functional variation that ecosystems have exhibited over their long histories. Such information is necessary for recognizing which current changes foretell transitions to less robust ecological states and which changes may signal benign ecosystem shifts that will cause no substantial loss of ecosystem function or services. Conservation success will also increasingly hinge on choosing among different, sometimes mutually exclusive approaches to best achieve three conceptually distinct goals: maximizing biodiversity, maximizing ecosystem services, and preserving wilderness. These goals vary in applicability depending on whether historical or novel ecosystems are the conservation target. Tradeoffs already occur—for example, managing to maximize certain ecosystem services upon which people depend (such as food production on farm or rangelands) versus maintaining healthy populations of vulnerable species (such as wolves, lions, or elephants). In the future, the choices will be starker, likely involving decisions such as which species are candidates for managed relocation and to which areas, and whether certain areas should be off limits for intensive management, even if it means losing some species that now live there. Developing the capacity to make those choices will require conservation in both historical and novel ecosystems and effective collaboration of scientists, governmental officials, nongovernmental organizations, the legal community, and other stakeholders. OUTLOOK Conservation efforts are currently in a state of transition, with active debate about the relative importance of preserving historical landscapes with minimal human impact on one end of the ideological spectrum versus manipulating novel ecosystems that result from human activities on the other. Although the two approaches are often presented as dichotomous, in fact they are connected by a continuum of practices, and both are needed. In most landscapes, maximizing conservation success will require more integration of paleobiology and conservation biology because in a rapidly changing world, a long-term perspective (encompassing at least millennia) is necessary to specify and select appropriate conservation targets and plans. Although adding this long-term perspective will be essential to sustain biodiversity and all of the facets of nature that humans need as we continue to rapidly change the world over the next few decades, maximizing the chances of success will also require dealing with the root causes of the conservation crisis: rapid growth of the human population, increasing per capita consumption especially in developed countries, and anthropogenic climate change that is rapidly pushing habitats outside the bounds experienced by today’s species. Fewer than 900 mountain gorillas are left in the world, and their continued existence depends upon the choices humans make, exemplifying the state of many species and ecosystems. Can conservation biology save biodiversity and all the aspects of nature that people need and value as 3 billion more of us are added to the planet by 2050, while climate continues to change to states outside the bounds that most of today’s ecosystems have ever experienced? Photo: E. A. Hadly, at Volcanoes National Park, Rwanda Conservation of species and ecosystems is increasingly difficult because anthropogenic impacts are pervasive and accelerating. Under this rapid global change, maximizing conservation success requires a paradigm shift from maintaining ecosystems in idealized past states toward facilitating their adaptive and functional capacities, even as species ebb and flow individually. Developing effective strategies under this new paradigm will require deeper understanding of the long-term dynamics that govern ecosystem persistence and reconciliation of conflicts among approaches to conserving historical versus novel ecosystems. Integrating emerging information from conservation biology, paleobiology, and the Earth sciences is an important step forward on the path to success. Maintaining nature in all its aspects will also entail immediately addressing the overarching threats of growing human population, overconsumption, pollution, and climate change.

Stable isotope constraints on the elevation history of the Sierra Nevada Mountains, California

Research on the uplift history of the Sierra Nevada mountain range has yielded seemingly conflicting results. Some studies argue for substantial uplift within the past 3–5 m.y.; others suggest that high elevations may have existed since the Cretaceous. The rain shadow across the Sierra Nevada is associated with a strong isotopic gradient, with lower δ18O values in precipitation on the leeward side of the range. Reconstruction of the δ18O value of meteoric water as a monitor of paleoelevation has focused mainly on the leeward side of the Sierras, but interpretation of the results of these studies may be complicated by shifts in global climate and regional moisture sources. We address these concerns by analyzing the δ18O value of tooth enamel bioapatite from contemporaneous mammalian fossils on either side of the present Sierra range. By sampling across the range, δ18O differences induced by a rain shadow can be isolated from other complicating factors. Our results indicate that the Sierra rain shadow has existed since at least 16 Ma, which is an important constraint on models for the tectonic evolution of the western United States. Unfortunately, temporal resolution for localities is too coarse to differentiate between glacial and interglacial localities during the past 2 m.y., so we cannot evaluate if there was a latest Cenozoic pulse of uplift or elevation loss.

Evolution of ruminant headgear: a review

The horns, ossicones and antlers of ruminants are familiar and diverse examples of cranial appendages. We collectively term ruminant cranial appendages ‘headgear’; this includes four extant forms: antlers (in cervids), horns (in bovids), pronghorns (in pronghorn antelope) and ossicones (in giraffids). Headgear evolution remains an open and intriguing question because phylogenies (molecular and morphological), adult headgear structure and headgear development (where data are available) all suggest different pictures of ruminant evolution. We discuss what is known about the evolution of headgear, including the evidence motivating previous hypotheses of single versus multiple origins, and the implications of recent phylogenetic revisions for these hypotheses. Inclusion of developmental data is critical for progress on the question of headgear evolution, and we synthesize the scattered literature on this front. The areas most in need of attention are early development in general; pronghorn and ossicone development in particular; and histological study of fossil forms of headgear. An integrative study of headgear development and evolution may have ramifications beyond the fields of systematics and evolution. Researchers in organismal biology, as well as those in biomedical fields investigating skin, bone and regenerative medicine, may all benefit from insights produced by this line of research.

QUANTITATIVE MORPHOLOGICAL PROXIES FOR FOSSORIALITY IN SMALL MAMMALS

Abstract Burrowing behavior is widespread among mammals and has generated a diverse array of adaptive responses to the physical demands of this lifestyle. While extensive research has been devoted to the morphological, ecological, and evolutionary implications of burrowing, it remains difficult to compare burrowing adaptations between mammals of widely divergent ancestry. A reliable quantitative proxy for fossoriality (burrowing) is necessary for such comparisons as well as for detailed descriptions of ecology from specimens of rare, extinct, and fossil mammals. This study presents several quantitative indices of the morphology of burrowing mammals based on 20 measurements of skull and skeletal morphology taken from 123 different mammalian species, both burrowing and nonburrowing. Discriminant analyses revealed that these quantitative characters successfully distinguish nonburrowing taxa from those that are adapted to a burrowing lifestyle. Additionally, more subtle distinctions between subterranean taxa (which rarely emerge above ground) and other burrowers as well as between mammals using different methods of burrow excavation were identified from these characters. A test of these indices using 6 extinct species yielded results consistent with more-detailed descriptions of the functional morphology of these taxa, indicating that our quantitative proxies provide an important basis for comparisons of fossorial adaptations across divergent mammalian clades.

Biodiversity and Topographic Complexity: Modern and Geohistorical Perspectives

Topographically complex regions on land and in the oceans feature hotspots of biodiversity that reflect geological influences on ecological and evolutionary processes. Over geologic time, topographic diversity gradients wax and wane over millions of years, tracking tectonic or climatic history. Topographic diversity gradients from the present day and the past can result from the generation of species by vicariance or from the accumulation of species from dispersal into a region with strong environmental gradients. Biological and geological approaches must be integrated to test alternative models of diversification along topographic gradients. Reciprocal illumination among phylogenetic, phylogeographic, ecological, paleontological, tectonic, and climatic perspectives is an emerging frontier of biogeographic research.

Extending the utility of artiodactyl postcrania for species-level identifications using multivariate morphometric analyses

Studies of paleoecology are most powerful when relative abundance data are available at fine taxonomic scales and large sample sizes. Postcranial elements are abundant but seldom identified to species, reducing potential sample size. We investigate whether antilocaprid astragali, abundant in the Late Miocene deposits of the Great Basin, can be identified to species, improving sample sizes. Our analysis of African and Asian bovid data from the literature suggests species should be distinguishable using astragalar dimensions. For our case study we use three species of antilocaprids, Ilingoceros alexandrae, Ilingoceros schizoceras, and Sphenophalos nevadanus from the Hemphillian (~8 Ma) Thousand Creek Fauna of northwestern Nevada. These species are diagnosed by their horncores, but previous comparisons of their dentition have shown no clear separation between the species. Our analysis of >200 antilocaprid astragali from Thousand Creek indicates there is enough variation to tentatively reject the hypothesis of only one species, but the distribution does not allow assignment of individual astragali to species. Combined with horncore morphology, our results suggest differences in male-male competition and a slight difference in body size kept the two genera out of competition while ecological similarity and/or shared ancestry created a continuous distribution of astragalar dimensions. The data cannot resolve whether I. alexandrae and I. schizoceras are distinct species. Additionally, we explored the range of effectiveness of a published discriminant function developed to derive environmental preference from African bovid astragali. Applying this discriminant function to Antilocapra proved ineffective, likely a consequence of the distinct evolutionary histories of antilocaprids and bovids.

The Miocene MammaL Mapping Project (Miomap): An Online Database of Arikareean Through Hemphillian Fossil Mammals

Abstract The Miocene Mammal Mapping Project (MIOMAP), a relational database of all published mammalian vertebrate localities between 30 and 5 million years old from the western United States, is now online for use by the paleontological community. The database is housed at the University of California at Berkeley, served through the Berkeley Natural History Museums, and accessible via the University of California Museum of Paleontology website. Here we outline the salient features of the database to facilitate its use and provide the information needed for users to adapt the data to their own needs. Online queries of the database can be accessed via http://www.ucmp.berkeley.edu/miomap and made through HTML forms or an interactive map created using open source MapServer 4.0 software and Google Earth™. We also highlight past work done using the database and some of its potential applications.