Christopher J. Bell

Best Practices for Justifying Fossil Calibrations

Our ability to correlate biological evolution with climate change, geological evolution, and other historical patterns is essential to understanding the processes that shape biodiversity. Combining data from the fossil record with molecular phylogenetics represents an exciting synthetic approach to this challenge. The first molecular divergence dating analysis (Zuckerkandl and Pauling 1962) was based on a measure of the amino acid differences in the hemoglobin molecule, with replacement rates established (calibrated) using paleontological age estimates from textbooks (e.g., Dodson 1960). Since that time, the amount of molecular sequence data has increased dramatically, affording ever-greater opportunities to apply molecular divergence approaches to fundamental problems in evolutionary biology. To capitalize on these opportunities, increasingly sophisticated divergence dating methods have been, and continue to be, developed. In contrast, comparatively, little attention has been devoted to critically assessing the paleontological and associated geological data used in divergence dating analyses. The lack of rigorous protocols for assigning calibrations based on fossils raises serious questions about the credibility of divergence dating results (e.g., Shaul and Graur 2002; Brochu et al. 2004; Graur and Martin 2004; Hedges and Kumar 2004; Reisz and Muller 2004a, 2004b; Theodor 2004; van Tuinen and Hadly 2004a, 2004b; van Tuinen et al. 2004; Benton and Donoghue 2007; Donoghue and Benton 2007; Parham and Irmis 2008; Ksepka 2009; Benton et al. 2009; Heads 2011). The assertion that incorrect calibrations will negatively influence divergence dating studies is not controversial. Attempts to identify incorrect calibrations through the use of a posteriori methods are available (e.g., Near and Sanderson 2004; Near et al. 2005; Rutschmann et al. 2007; Marshall 2008; Pyron 2010; Dornburg et al. 2011). We do not deny that a posteriori methods are a useful means of evaluating calibrations, but there can be no substitute for a priori assessment of the veracity of paleontological data. Incorrect calibrations, those based upon fossils that are phylogenetically misplaced or assigned incorrect ages, clearly introduce error into an analysis. Consequently, thorough and explicit justification of both phylogenetic and chronologic age assessments is necessary for all fossils used for calibration. Such explicit justifications will help to ensure that divergence dating studies are based on the best available data. Unfortunately, the majority of previously published calibrations lack explicit explanations and justifications of the age and phylogenetic position of the key fossils. In the absence of explicit justifications, it is difficult to distinguish between correct and incorrect calibrations, and it becomes difficult to reevaluate previous claims in light of new data. Paleontology is a dynamic science, with new data and perspectives constantly emerging as a result of new discoveries (see Kimura 2010 for a recent case where the age of the earliest known record of a clade was more than doubled). Calibrations based upon the best available evidence at a given time can become inappropriate as the discovery of new specimens, new phylogenetic analyses, and ongoing stratigraphic and geochronologic revisions refine our understanding of the fossil record. Our primary goals in this paper are to establish the best practices for justifying fossils used for the temporal calibration of molecular phylogenies. Our examples derive mainly, but not exclusively, from the vertebrate fossil record. We hope that our recommendations will lead to more credible calibrations and, as a result, more reliable divergence dates throughout the tree of life. A secondary goal is to help the community (researchers, editors, and reviewers) who might be unfamiliar with fossils to understand and overcome the challenges associated with using paleontological data. In order to accomplish these goals, we present a specimen-based protocol for selecting and documenting relevant fossils and discuss future directions for evaluating and utilizing phylogenetic and temporal data from the fossil record. We likewise encourage biologists relying on nonfossil calibrations for molecular divergence estimates (e.g., ages of island or mountain range formations, continental drift, and biomarkers) to develop their own set of rigorous guidelines so that their calibrations may also be evaluated in a systematic way.

MAMMALIAN RESPONSE TO GLOBAL WARMING ON VARIED TEMPORAL SCALES

Abstract Paleontological information was used to evaluate and compare how Rocky Mountain mammalian communities changed during past global warming events characterized by different durations (350, ∼10,000–20,000, and 4 million years) and different per–100-year warming rates (1.0°C, 0.1°C, 0.06–0.08°C, 0.0002–0.0003°C per 100 years). Our goals were to determine whether biotic changes observed today are characteristic of or accelerated relative to what took place during past global warming events and to clarify the possible trajectory of mammalian faunal change that climate change may initiate. This determination is complicated because actual warming rates scale inversely with the time during which temperature is measured, and species with different life-history strategies respond (or do not) in different ways. Nevertheless, examination of past global warming episodes suggested that approximately concurrent with warming, a predictable sequence of biotic events occurs at the regional scale of the central and northern United States Rocky Mountains. First, phenotypic and density changes in populations are detectable within 100 years. Extinction of some species, noticeable changes in taxonomic composition of communities, and possibly reduction in species richness follow as warming extends to a few thousand years. Faunal turnover nears 100% and species diversity may increase when warm temperatures last hundreds of thousands to millions of years, because speciation takes place and faunal changes initiated by a variety of shorter-term processes accumulate. Climate-induced faunal changes reported for the current global warming episode probably do not yet exceed the normal background rate, but continued warming during the next few decades, especially combined with the many other pressures of humans on natural ecosystems, has a high probability of producing effects that have not been experienced often, if ever, in mammalian history.

New Extinct Mekosuchine Crocodile from Vanuatu, South Pacific

Abstract We describe a new species of crocodile (Reptilia: Crocodyloidea: Mekosuchinae) from a maxilla recovered at the Arapus archaeological site, on the island of Efate, Vanuatu, South Pacific. As with mekosuchine species in New Caledonia and Fiji, Mekosuchus kalpokasi sp. nov. was a small, possibly terrestrial carnivore that is now extinct. The differences between the Efate specimen and previously described species of Mekosuchus warrant recognition of a new species. Based on its association with Efates earliest known human inhabitants, dating approximately 3000 cal yr B.P., the extinction of M. kalpokasi and other insular mekosuchines may have been anthropogenic. The lack of adequately dated pre-Quaternary and Quaternary vertebrate fossil records from Vanuatu, New Caledonia, and Fiji (as well as other smaller islands) precludes determining the timing and route of dispersal of mekosuchine crocodyloids.

Food Habits of the Glossy Snake, Arizona elegans, with Comparisons to the Diet of Sympatric Long-nosed Snakes, Rhinocheilus lecontei

We studied the diet of the North American glossy snake, Arizona elegans, by examining stomach contents of more than 700 museum specimens, and supplemented our findings with published dietary records. Fifty percent of 107 prey were lizards and 44% were mammals; birds and snakes composed the remaining prey. Most lizard prey were diurnal, and presumably were captured when they were inactive by nocturnally wide-foraging glossy snakes. Conversely, most rodent prey were nocturnal heteromyids that we suspect were ambushed by A. elegans, thus raising the possibility that these snakes use alternative hunting tactics on different prey types. Ninety-five percent of the specimens with food contained a single item, and all 49 prey for which we determined direction of ingestion were swallowed head-first Although smaller A. elegans consumed mammals occasionally, specimens that ate mammals were significantly larger than those that fed on lizards, and glossy snakes that took birds were larger thap those that ate mammals. Larger glossy snakes ate larger prey and added birds to their diet, but they continued to eat lizards and mammals, which suggests that there is no absolute ontogenetic change in the diet of A. elegans. For any given body size, A. elegans has a longer head, and thus a larger gape than the sympatric long-nosed snake, Rhinocheilus lecontei. This difference in relative head length may explain why smaller A. elegans are capable of predation on mammals, whereas smaller R. lecontei feed almost exclusively on lizards, and may also account in part for the higher frequency of stout-bodied phrynosomatid lizards and of mammals in the diet of glossy snakes.

Evolution, climatic change and species boundaries: perspectives from tracing Lemmiscus curtatus populations through time and space

To provide empirical evidence of species boundaries and the role of climatic change in affecting evolution, we documented evolution of the sagebrush vole, Lemmiscus curtatus, through hundreds of thousands of years by following populations from the middle Pleistocene to the present. We found that: (i) extant representatives of the species culminate a morphological transition that was initiated within an unusually arid and warm interglacial period, perhaps related to the shift from glacial–interglacial cycles dominated by a 41 000 year periodicity to those dominated by a 100 000 year rhythm; and (ii) sympatry of extant and extinct morphotypes persisted for more than 800 000 years. This exceptionally detailed tracing of extinct populations into extant ones suggests that species such as the one we studied are real entities in space, that their boundaries become fuzzy (although potentially diagnosable) through time and that unusual climatic warming may initiate significant evolutionary change manifested at the morphological level.

Not Enough Skeletons in the Closet: Collections‐Based Anatomical Research in an Age of Conservation Conscience

The emergence of new technologies and improved computing power helped to introduce a renewed vitality in morphological research in recent decades. This is especially apparent in the new advances made in understanding the evolutionary morphology of the skeletal system in extinct and extant squamate reptiles. The new data generated as a result of the recent increase in attention are relevant not only for systematic analyses but also are valuable in their own right for contributing to holistic perspectives on organismal evolution, mosaic evolution in the rates of change in different anatomical systems, and broader patterns of macroevolution. A global community of morphological researchers now can share data through online digital collections, but opportunities for continued advance are hindered because we lack even basic data on patterns of variation of the skeletal system for virtually all squamate lineages. Most work on skeletal morphology of squamates is based on a sample size of n = 1; this is an especially noticeable phenomenon for studies relying on X‐ray computed tomography technology. We need new collections of skeletal specimens, both material and digital, and new approaches to the study of skeletal morphology. Promising areas for continued research include the recent focus on skeletal elements not traditionally included in morphological studies (especially systematic analyses based upon morphological data) and efforts to elucidate patterns of variation and phylogenetically informative features of disarticulated skeletal elements. Anat Rec, 297:344–348, 2014.

The Osteoderms and Palpebral in Lanthanotus borneensis (Squamata: Anguimorpha)

is rarely collected, probably because itis nocturnal, fossorial, and semiaquatic (Harrisson,1962; Manthey and Grossman, 1997). Few specimensexist in collections worldwide, and skeletons are ex-tremely rare. As a result of limited access to speci-mens, many phylogenetic analyses that include thisspecies relied upon the same specimen (REE 1445, col-lection of Richard Etheridge, San Diego State Univer-sity) to score osteological characters (e.g., Pregill et al.,1986; Estes et al., 1988; Norell and Gao, 1997; Gao andNorell, 1998).This problem is not unique to

Fossils, Diet, and Conservation of Black-Footed Ferrets (Mustela Nigripes)

Abstract A new middle Pleistocene record of Mustela nigripes is reported from Cathedral Cave, White Pine County, Nevada. The specimen dates to 750,000–850,000 years ago and represents one of the oldest remains recovered of the black-footed ferret. Forty-two percent of fossil faunas known to contain M. nigripes do not contain Cynomys, the common prey of black-footed ferrets in historic times. Consideration of dietary information and habitat requirements of M. nigripes and its sister taxon, M. eversmanni (steppe ferret), reveals ancestral behavioral repertoires for ferrets. We suggest that the historically documented “obligate” predator–prey relationship between M. nigripes and Cynomys was a secondary effect of colonization by black-footed ferrets of Cynomys-dominated habitats sometime in the past 800,000 years. A phylogenetic perspective on the behavior of ferrets combined with paleontological data indicates a broader range of possibilities for conservation of the black-footed ferret.

Observations on dental variation in Microtus from the Cudahy Ash Pit Fauna, Meade County, Kansas and implications for Irvingtonian microtine rodent biochronology

ABSTRACT A thorough re-examination of the Microtus remains from the Cudahy Ash Pit fauna in Meade County, Kansas revealed a greater degree of morphological variation than previously reported for this fauna. Morphological variants of the ml sample include typical M. paroperarius morphotypes with only four closed triangles, morphotypes with five closed triangles, and specimens with intermediate morphologies in which well-developed fifth triangles show variable degrees of partial closure. Morphological variants of the M2 include specimens with a well-developed posterolingual dentine field often considered to be indicative of the presence of M. pennsylvanicus. A survey of six additional species of North American Microtus revealed that the posterolingual dentine field is present as a regular feature in several species and cannot be used to confidently identify M. pennsylvanicus. Current North American microtine rodent biochronologies utilize the first appearance of M. pennsylvanicus to define the youngest micr...

Comparative Skull Morphology of Uropeltid Snakes (Alethinophidia: Uropeltidae) with Special Reference to Disarticulated Elements and Variation

Uropeltids form a diverse clade of highly derived, fossorial snakes that, because of their phylogenetic position among other alethinophidian lineages, may play a key role in understanding the early evolution of cranial morphology in snakes. We include detailed osteological descriptions of crania and mandibles for eight uropeltid species from three nominal genera (Uropeltis, Rhinophis, and Brachyophidium) and emphasize disarticulated elements and the impact of intraspecific variation on previously proposed morphological characters used for phylogenetic analysis. Preliminary analysis of phylogenetic relationships strongly supports a clade composed exclusively of species of Plectrurus, Uropeltis, and Rhinophis. However, monophyly of each of those genera and Melanophidium is not upheld. There is moderate support that Sri Lankan species (e.g., Rhinophis and Uropeltis melanogaster) are monophyletic with respect to Indian uropeltids. Previously proposed characters that are phylogenetically informative include the shape of the nasals, length of the occipital condyle, level of development of the posteroventral process of the dentary, and participation of the parietal in the optic foramen. Additionally, thirty new features that may be systematically informative are identified and described, but were not verified for their utility. Such verification must await availability of additional disarticulated cranial material from a larger sample of taxa. All characters require further testing through increased focus on sources and patterns of intraspecific variation, inclusion of broader taxonomic samples in comparative studies, and exploration of skeletal development, sexual dimorphism, and biogeographic patterns. Additionally, trends in the relative enlargement of the sensory capsules, reduction in cranial ossification and dentition, fusion of elements, and the appearance of novel morphological conditions, such as the structure and location of the suspensorium, may be related to fossoriality and miniaturization in some uropeltid taxa, and may complicate analysis of relationships within Uropeltidae and among alethinophidian snakes.