John P. Hunter

Model of Tooth Morphogenesis Predicts Carabelli Cusp Expression, Size, and Symmetry in Humans

Background The patterning cascade model of tooth morphogenesis accounts for shape development through the interaction of a small number of genes. In the model, gene expression both directs development and is controlled by the shape of developing teeth. Enamel knots (zones of nonproliferating epithelium) mark the future sites of cusps. In order to form, a new enamel knot must escape the inhibitory fields surrounding other enamel knots before crown components become spatially fixed as morphogenesis ceases. Because cusp location on a fully formed tooth reflects enamel knot placement and tooth size is limited by the cessation of morphogenesis, the model predicts that cusp expression varies with intercusp spacing relative to tooth size. Although previous studies in humans have supported the models implications, here we directly test the models predictions for the expression, size, and symmetry of Carabelli cusp, a variation present in many human populations. Methodology/Principal Findings In a dental cast sample of upper first molars (M1s) (187 rights, 189 lefts, and 185 antimeric pairs), we measured tooth area and intercusp distances with a Hirox digital microscope. We assessed Carabelli expression quantitatively as an area in a subsample and qualitatively using two typological schemes in the full sample. As predicted, low relative intercusp distance is associated with Carabelli expression in both right and left samples using either qualitative or quantitative measures. Furthermore, asymmetry in Carabelli area is associated with asymmetry in relative intercusp spacing. Conclusions/Significance These findings support the models predictions for Carabelli cusp expression both across and within individuals. By comparing right-left pairs of the same individual, our data show that small variations in developmental timing or spacing of enamel knots can influence cusp pattern independently of genotype. Our findings suggest that during evolution new cusps may first appear as a result of small changes in the spacing of enamel knots relative to crown size.

Spiny Norman in the Garden of Eden? Dispersal and early biogeography of Placentalia

The persistent finding of clades endemic to the southern continents (Afrotheria and Xenarthra) near the base of the placental mammal tree has led molecular phylogeneticists to suggest an origin of Placentalia, the crown group of Eutheria, somewhere in the southern continents. Basal splits within the Placentalia have then been associated with vicariance due to the breakup of Gondwana. Southern-origin scenarios suffer from several problems. First, the place of origin of Placentalia cannot be reconstructed using phylogenetic reasoning without reference to outgroups. When available outgroups are considered, a Laurasian origin is most parsimonious. Second, a model of pure vicariance would require that basal placental splits occurred not with the breakup of Gondwana, but of Pangea in the Late Triassic—Early Jurassic. This event long preceded even the oldest molecular divergence estimates for the Placentalia and was coeval only with the earliest mammals in the fossil record. Third, a problem with the number of dispersal events that would be required emerges under different southern-origin scenarios. In considering the geographic distribution of the major placental clades at their first appearance (mostly Early Cenozoic), it becomes clear that a Laurasian center of origin would require fewer dispersal events. Southern-origin models would require at least twice the number of dispersal events in comparison with a model of Laurasian origins. This number of required dispersal events increases if extinct groups of placental mammals are also considered. Results are similar assuming a morphology-based phylogeny. These facts, along with earlier findings speaking against a major placental radiation deep in the Cretaceous without leaving fossil evidence, suggest an origin of Placentalia somewhere in Laurasia with few supraordinal splits occurring before the last 5–10 million years of the Cretaceous.

Metamerism, morphogenesis, and the expression of Carabelli and other dental traits in humans.

The patterning cascade model of tooth morphogenesis has emerged as a useful tool in explaining how tooth shape develops and how tooth evolution may occur. Enamel knots, specialized areas of dental epithelium where cusps initiate, act as signaling centers that direct the growth of surrounding tissues. For a new cusp to form, an enamel knot must form beyond the inhibition fields of other enamel knots. The model predicts that the number and size of cusps depends on the spacing between enamel knots, reflected in the spacing between cusps. Recently, work by our group demonstrated that the model predicted Carabelli trait expression in human first molars. Here we test whether differences in Carabelli trait expression along the molar row can also be predicted by the model. Crown areas and intercusp distances were measured from dental casts of 316 individuals with a digital microscope. Although absolute cusp spacing is similar in first and second molars, the smaller size and more triangular shape of second molars results in larger cusp spacing relative to size and, likely, less opportunity for the Carabelli trait to form. The presence and size of the hypocone (HY) and a range of small accessory cusps in a larger sample of 340 individuals were also found to covary with the Carabelli trait in a complex way. The results of this study lend further support to the view that the dentition develops, varies, and evolves as a single functional complex.

Mammals from the St. Mary River Formation (Upper Cretaceous), Montana

ABSTRACT The St. Mary River Formation (Fm) crops out in restricted parts of southwestern Alberta and northwestern Montana. Mammals are poorly known from the formation, but material collected from Alberta has played a role in recognizing an ‘Edmontonian’ Land Mammal Age between the better sampled Judithian (∼79–74 Ma) and Lancian (∼67–65 Ma) land mammal ages. New and well-preserved multituberculate and metatherian material collected from a single locality in the lower third of the St. Mary River Fm of Montana adds complexity to the interpretation of a discrete ‘Edmontonian’ Land Mammal Age. We report here three taxa of multituberculates (Paracimexomys propriscus, sp. nov., Nidimys occultus, gen. et sp. nov., and a primitive ptilodontoid of comparable size to the smallest species of Mesodma Jepsen, 1940, and Cimexomys Sloan and Van Valen, 1965) and two metatherian taxa (Leptalestes toevsi, sp. nov., and Turgidodon russelli). Paracimexomys propriscus and Turgidodon russelli are probably conspecific with Judithian forms that did not survive to the Lancian. Leptalestes toevsi and Nidimys occultus are taxa unique to the ‘Edmontonian’ but may represent lineages that separated from their closest relatives prior to the Judithian. Lack of Lancian-aspect mammals contrasts sharply with other ‘Edmontonian’ faunas, including an older fauna recovered from the Williams Fork Fm of Colorado, suggesting that the replacement of Judithian mammals by Lancian forms was a complex transition. We tentatively suggest that the Lancian fauna may have expanded into the northern part of the Western Interior in response to the appearance of new terrestrial habitats as sea level fell.

Lower Jaw of the Early Paleocene Mammal Alveugena and its Interpretation as a Transitional Fossil

Abstract The Paleogene Order Taeniodonta Cope, 1876—peculiar heavy-bodied mammals, some with ever-growing cheek teeth—are grouped with the Late Cretaceous eutherian Cimolestes Marsh, 1889, along with a host of other taxa in a superordinal group, the Cimolesta. Taeniodonts were thought to have arisen from Cimolestes indirectly, through Paleocene Procerberus Sloan and Van Valen, 1965. The recently described Paleocene Alveugena Eberle, 1999, until now known only from the upper dentition, has been put forth as a transitional form between cimolestids and taeniodonts on phylogenetic and biostratigraphic grounds. An older taeniodont, the Late Cretaceous Schowalteria Fox and Naylor, 2003, has since been described, complicating taeniodont origins. We describe here a lower jaw that we refer to Alveugena from the lower part of the Ludlow Member of the Fort Union Formation in North Dakota. The lower jaw comes from strata of early Early Paleocene age (Puercan 1 North American Land Mammal Age) ~8.5 m above a Cretaceous-Paleogene boundary, identified using palynological criteria. A cladistic analysis is here presented using new data on Schowalteria and Alveugena, added to that of Cimolestes, Procerberus formicarum Sloan and Van Valen, 1965, P. grandis Middleton and Dewar, 2004, and Onychodectes. This analysis revealed Alveugena as the sister taxon of the taeniodonts but with a closer relationship to Cimolestes than Procerberus, suggesting that taeniodonts evolved from a Cimolestes-like ancestor. We discuss the age relations of early taeniodonts and related taxa and propose a scenario of ancestor-descendent relations that minimizes, but does not eliminate, implied stratigraphic gaps.

Garden of Eden or "Fool's Paradise"? Phylogeny, dispersal, and the southern continent hypothesis of placental mammal origins

Where did the modern lineages of placental mammals originate? Recent molecular data seemingly have overturned not only schemata of placental relationships based on morphological data, but also hypotheses about the time and place of origin of the modern lineages. The original hypothesis of Northern Hemisphere origin, based on the fossil record, has been replaced by a “Garden of Eden” hypothesis of origins on a southern continent, based on molecular phylogenies. But, do the molecular data really support this new view of placental mammal origins? Recent molecular phylogenies have converged on the finding of two basal placental clades (Springer et al. 1997; Stanhope et al. 1998; Madsen et al. 2001; Murphy et al. 2001), Afrotheria and Xenarthra, each endemic to separate southern continents, and a third clade, Boreoeutheria, of apparent northern continent affinity (Murphy et al. 2001). This finding, in association with molecular divergence estimates starting in the mid Cretaceous (see Springer et al. 2003 for a recent synthesis), has been used to support a mid Cretaceous origin of placentals in Gondwana (Eizirik et al. 2001; Murphy et al. 2001). These divergence time estimates imply a radiation of the ordinal lineages starting ∼105 million years ago (Springer et al. 2003), millions of years prior to the appearance of undoubted crown placentals in the early Cenozoic (Foote et al. 1999; Novacek 1999; Meng et al. 2003; Wible et al. 2004; Asher et al. 2005). A biogeographic scenario proposed to account for Gondwanan origins calls for vicariance, associated with mid-Cretaceous separation of Africa from South America, followed by later dispersal into the northern continents in the Late Cretaceous. This biogeographic scenario has been criticized on varied paleontological grounds (Ji et al. 2002; Archibald 2003; Luo et al. 2003; Hunter and Janis …

Phylogeny of the Taeniodonta: evidence from dental characters and stratigraphy

ABSTRACT The Taeniodonta is a group of eutherian mammals from the Paleogene of North America, which evolved rapidly in the Paleocene to achieve, in some forms, large body size, hypselodont (i.e., evergrowing) canine and postcanine teeth, and peculiar patterns of tooth wear. Eleven genera of taeniodonts occur in two subgroups, recognized at the level of families or subfamilies depending on author, the Conoryctidae and the Stylinodontidae. There has not been a comprehensive computer-assisted phylogenetic analysis of the taeniodonts, and questions have arisen over the monophyly of the taeniodonts and the conoryctids. Cladistic analyses based on thirty-seven dental characters using NONA and Winclada showed that two subclades of Taeniodonta are well supported, a clade consisting of the conoryctids exclusive of Onychodectes (i.e., Conoryctella, Conoryctes, and Huerfanodon) and a clade consisting of all the known stylinodontids (Wortmania, Schochia, Psittacotherium, Ectoganus, and Stylinodon). Stratocladistic analysis, which takes into account the temporal sequence of taxa in the fossil record, supports the results of the morphological analysis. The Late Cretaceous taeniodont Schowalteria occupies the most basal position in taeniodont phylogeny, pre-dating an inferred conoryctid-stylinodontid split in the early Paleocene, and establishing the taeniodonts as monophyletic.

Evolution and function of the upper molar talon and its dietary implications in microbats

The evolution of mammalian molars has been marked by transitions representing significant changes in shape and function. One such transition is the addition and elaboration of the talon, the distolingual region of the ancestral tribosphenic upper molar of therian mammals and some extinct relatives. This study uses suborder Microchiroptera as a case study to explore the adaptive implications of the expansion of the talon on the tribosphenic molar, specifically focusing on the talons role in the compression and shear of food during breakdown. Three‐dimensional computer renderings of casts of the upper left first molars were created for microbat species of a variety of dietary categories (frugivore, etc.) and physical properties of food (hard and soft). Relief Index (RFI) was measured to estimate the topography and function of the whole tooth and of the talon and trigon (the remaining primitive tribosphenic region) individually, in order to examine 1) how the shape of the whole tooth, trigon, and talon reflects the compromise between their crushing and shearing functions, 2) how whole tooth, trigon, and talon function differs according to diet, and 3) how the presence of the talon affects overall molar function. Results suggest that RFI of both the whole tooth and the trigon varies according to dietary groups, with frugivores having greater crushing function when compared with the other groups. The talon, however, consistently has low RFI (a flatter topography), and its presence lowers the RFI of the whole tooth across all dietary categories, suggesting that the talon is primarily functioning in crushing during food breakdown. The potential benefits of a crushing talon for microbats of various dietary groups are discussed. J. Morphol. 276:1368–1376, 2015.