Louis L. Jacobs

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.

Neogene mammalian faunal change in southern Asia: Correlations with climatic, tectonic, and eustatic events

The fluvial Neogene Siwalik formations of northern Pakistan span long time intervals with only minor hiatuses and, being highly fossiliferous, are uniquely suited for studies of change in mammalian faunas. Magnetostratigraphic correlations of a critical stratigraphic section give dates for 45 middle and late Miocene biostratigraphic events. These mark either first appearances or extinctions in the mammal fauna and show that in the Siwaliks there were major fauna turnovers at between 20 and 16 Ma and at 9.5 and 7.4 Ma. Two minor faunal events are dated at 13.2 and about 12 Ma. Many species making their first appearance were immigrants from Europe or Africa and indicate when connections to those regions existed. Immigration and extinction were the dominant modes of faunal change; in situ evolution was much less important. The Siwalik biostratigraphic record correlates closely to climatic, oceanographic, and tectonic events, which probably controlled immigration into southern Asia. Abiotic events were therefore important factors affecting evolution of the mammal communities.

Geology and palaeontology of Neogene strata of Pakistan

A joint study of the Potwar Plateau of Pakistan is yielding abundant material for stratigraphic and palaeontological reassessment.

Neogene palaeontology and geochronology of the Baringo Basin, Kenya

The period from 14 to four million years is poorly known in Africa, but during this time the Ethiopian fauna became established and hominids originated. The sedimentary sequence of the Tugen Hills in the Baringo area of Kenya provides important geological, environmental and plaeontological data concerning this interval. Concordant radiometric and palaeomagnetic determinations within the type section of the Ngorora Formation show that it spans more than 2 m.y., from 13 m.y.a. to less than 10 m.y.a., and from chrons 14 to 9. Other dates refine the calibration of the Younger Mpcsida, Lukeino and Chemeron units. Palaeontological results include the collection from the Ngorora Formation of one of the best Neogene macrofloras in Africa, and more fauna, including hominoids. No equids have been recorded older than 10 m.y.a. We also report new fauna from the more recent units.

Early Cretaceous (Comanchean) vertebrates of central Texas

ABSTRACT Vertebrates from the Comanche Series (Lower Cretaceous) in central Texas occur in the superposed Twin Mountains, Glen Rose, and Paluxy formations. Stratigraphie position and relationship to marine units are more clearly defined for the central Texas localities than for the classic mammal-producing sites in the Antlers Formation of north-central Texas. The diverse terrestrial to marine faunas include new records for the ray Rhinobatos, a ptychodont (cf. Hylaeobatis ornata), and the salmoniform Enchodus. Anurans, salamanders, lacertilians, and mammals representing early forms relevant to the emergence of extant higher taxa are present but fragmentary. Crocodilians are represented by at least three taxa and theropods by more than three. Eight species of mammals have been named from the Comanche Series, with perhaps as many as four other unnamed species represented. Paleoenvironments appear to control the distribution of taxa: dinosaurs are found in coastal settings and are abundant in some terrestri...

Neogene Siwalik mammalian lineages: Species longevities, rates of change, and modes of speciation

Abstract A long depositional sequence from northern Pakistan provides a good fossil record of terrestrial vertebrates for the interval of 18-7 Ma. Making allowances for possible range extensions, we use this record as a direct measure of species longevities. There is a correlation between body size and longevity, smaller mammals frequently being short-lived and larger taxa showing durations up to ca. 10 m.y. The distribution of small mammal longevities indicates an exponential decrease in frequency from a high modal value in the smallest increment measured (0–200,000 yrs). The most frequent value for large mammals is also the smallest increment measured (1 m.y.), but that distribution may not be unimodal. Small mammal taxa of short duration are concentrated late in the sequence, after 9 Ma especially. The middle Miocene fauna is more stable, with species showing longer durations. The contrast in longevities corresponds with hypothesized greater environmental stability in the middle Miocene. For comparison, the Paleogene sequence of Wyoming indicates short median species durations, with few surveyed taxa lasting over 2 m.y. Siwalik mammals show diverse modes of evolution, but stasis in at least some features is usual, with species boundaries corresponding to morphological breaks. Up to half of the Siwalik rodent and artiodactyl species surveyed likely immigrated from outside the biogeographic province, and for a few, historical data are sufficient to stipulate when and by what route they came to the Indian subcontinent.

Patterns of faunal turnover and diversity in the Neogene Siwaliks of Northern Pakistan

Abstract The fluvial Neogene Siwalik formations of northern Pakistan contain a long and richly fossiliferous sequence of terrestrial vertebrate faunas in which patterns of faunal turnover and changes in diversity can be documented and analyzed for intervals having durations of 0.5 m.y. The complete sequence extends from circa 18.5 to 1 Ma, but the part between 18.5 and 5.5 Ma is best sampled, and most intervals within it are well represented. Thirteen orders of Siwalik mammals have been identified, with well-sampled intervals having 50 or more species. Most Siwalik mammals, however, are either rodents or artiodactyls. Bovids are the most common and most speciose of the larger mammals, while murid and “cricetid” rodents dominate the small mammal assemblages. Between 18.5 and 5.5 Ma species diversity varied considerably. Among artiodactyls and rodents the number of species first increased between 15 and 13 Ma and then fell. Data on stratigraphic ranges of rodents and artiodactyls show that faunal change in the Siwaliks was episodic, occurring during short intervals with high turnover followed by longer periods with considerably less change. Maxima of first appearances occurred at approximately 13.5 and 8.5 Ma, while maxima of last occurrences were at 12.5 and 8.0 Ma. Some of the observed faunal events can be correlated to climatic and environmental changes. The Middle Miocene diversification occurred during a period of global cooling, while the latest Miocene decline in diversity and increased turnover accompanied oxygen and carbon isotopic changes that correlate to globally increasing seasonality and aridity. Other correlations are ambiguous. The marked decrease in diversity and the major turnover events between 13 and 8 Ma do not correspond to known local or global events. The Neogene Siwaliks and Paleogene Bighorn-Crazy Mountains sequence in Wyoming and Montana share many similarities. They have equivalent levels of temporal resolution and similar levels of completeness of their fossil records. Siwalik ordinal abundance and diversity patterns differ markedly from those of the Paleogene, but generic, and probably species, diversity was approximately the same, although the Siwalik faunas may have been slightly less diverse. Over time, changes in diversity were of comparable magnitude, with monotonic trends persisting for more than 5 million years. The magnitude of faunal turnover was also similar, ranging from less than half to 3.5 times that expected. In both sequences faunal change appears to have been episodic, with strong pulses between intervals of low turnover. The Siwaliks, in contrast to the Paleogene sequence, may have had more distinct pulses and longer intervals between pulses. Neither sequence has peaks of first occurrences coinciding with peaks of last occurrences.

Mammal-like dentition in a mesozoic crocodylian.

Crocodylian teeth are generally conical with little differentiation in shape along the tooth row. The mandible is incapable of any fore-aft movement, and feeding typically involves little or no intraoral processing. Complex, multi-cusped, mammal-like teeth differentiated along the tooth row have been found in a Cretaceous crocodylian from Malawi. The morphology of the teeth and mandible indicates that food items were processed by back-to-front (proal) movement of the mandible, unlike living crocodylians but as in some mammals and Sphenodon (the tuatara).

Problems in Muroid Phylogeny: Relationship to Other Rodents and Origin of Major Groups

The Muroidea include most of the diverse mouse-like rodents living today. The extant families of muroid rodents recognized by us are Muridae (true rats and mice), Cricetidae (hamsters, diverse hypsodont groups, and many American lineages), Gerbillidae (gerbils, sand rats and jirds) and several smaller groups, most of which have been given familial rank elsewhere. These are Nesomyidae (including Afrocricetodontinae), Rhizomyidae, Dendromuridae, Petromyscidae, Spalacidae, Cricetomyidae, Platacanthomyidae, and Lophiomyidae. Arvicoline (microtine) genera are not considered to constitute a family because they are late derivatives of advanced cricetids and because they form a polyphyletic group (C. A. Repenning, personal communication).

Faunal interchange and Miocene terrestrial vertebrates of southern Asia

Problems of stratigraphic completeness and poor temporal resolution make analysis of faunal change in terrestrial sequences difficult. The fluvial Neogene Siwalik formations of India and Pakistan are an exception. They contain a long vertebrate record and have good chronostrati- graphic control, making it possible to assess the influence of biotic interchange on Siwalik fossil communities. In Pakistan, the interval between 18 and 7 Ma has been most intensively studied and changes in diversity and relative abundance of ruminant artiodactyls and muroid rodents are documented with temporal resolution of 200,000 years. Within this interval, diversity varies con- siderably, including an abrupt rise in species number between 15 and 13 Ma, followed by a decline in ruminant diversity after 12 Ma and a decline in muroid diversity in two steps at 13 and 10 Ma. Significant changes in relative abundance of taxa include an increase in bovids between 16.5 and 15 Ma, a decrease in tragulids after 9 Ma, and a very abrupt increase in murids at 12 Ma. Megacri- cetodontine rodents also decrease significantly at 12 Ma, and smaller declines -re recorded among myocricetodontine and copemyine rodents after 16 Ma. An increase of dendromurine rodents at 15.5 Ma is also observed. There is also a trend of progressive size increase among giraffoids and bovids throughout the sequence. We have also investigated relationships between biotic interchange and diversity, body size, and relative abundance, concluding that (1) the rapid increase in ruminant and muroid diversity was largely due to immigration, whereas in situ speciation had only a secondary role; (2) during intervals of increasing diversity, resident lineages did not have higher than average rates of in situ speciation; (3) during intervals with rising diversity, greater extinction did not accompany increased immi- gration; (4) during intervals with falling diversity, there may have been greater extinction in recently invading lineages; and (5) change in diversity was independent of changes in relative abundance and body size.