Aaron R. Wood

Modularity of the rodent mandible: Integrating bones, muscles, and teeth

Summary Several models explain how a complex integrated system like the rodent mandible can arise from multiple developmental modules. The models propose various integrating mechanisms, including epigenetic effects of muscles on bones. We test five for their ability to predict correlations found in the individual (symmetric) and fluctuating asymmetric (FA) components of shape variation. We also use exploratory methods to discern patterns unanticipated by any model. Two models fit observed correlation matrices from both components: (1) parts originating in same mesenchymal condensation are integrated, (2) parts developmentally dependent on the same muscle form an integrated complex as do those dependent on teeth. Another fits the correlations observed in FA: each muscle insertion site is an integrated unit. However, no model fits well, and none predicts the complex structure found in the exploratory analyses, best described as a reticulated network. Furthermore, no model predicts the correlation between proximal parts of the condyloid and coronoid, which can exceed the correlations between proximal and distal parts of the same process. Additionally, no model predicts the correlation between molar alveolus and ramus and/or angular process, one of the highest correlations found in the FA component. That correlation contradicts the basic premise of all five developmental models, yet it should be anticipated from the epigenetic effects of mastication, possibly the primary morphogenetic process integrating the jaw coupling forces generated by muscle contraction with those experienced at teeth.

Evolution of the Earliest Horses Driven by Climate Change in the Paleocene-Eocene Thermal Maximum

Warming and Shrinking In most mammals, individual body sizes tend to be smaller in warmer regions and larger in cooler regions. Secord et al. (p. 959; see the Perspective by Smith) examined a high-resolution 175,000-year record of equid fossils deposited over a past climate shift—the Paleocene-Eocene Thermal Maximum—for changes in body size. Using oxygen isotopes collected from the teeth of co-occurring mammal species to track prevailing environmental temperature, a clear decrease in equid body size was seen during 130,000 years of warming, followed by a distinct increase as the climate cooled at the end of the period. These results indicate that temperature directly influenced body size in the past and may continue to have an influence as our current climate changes. Oxygen isotope measurements of fossil teeth show that the body size of the horse Sifrhippus decreased as temperature increased. Body size plays a critical role in mammalian ecology and physiology. Previous research has shown that many mammals became smaller during the Paleocene-Eocene Thermal Maximum (PETM), but the timing and magnitude of that change relative to climate change have been unclear. A high-resolution record of continental climate and equid body size change shows a directional size decrease of ~30% over the first ~130,000 years of the PETM, followed by a ~76% increase in the recovery phase of the PETM. These size changes are negatively correlated with temperature inferred from oxygen isotopes in mammal teeth and were probably driven by shifts in temperature and possibly high atmospheric CO2 concentrations. These findings could be important for understanding mammalian evolutionary responses to future global warming.

Building Developmental Integration into Functional Systems: Function-Induced Integration of Mandibular Shape

The mammalian mandible is a developmentally modular but functionally integrated system. Whether morphological integration can evolve to match the optimal pattern of functional integration may depend on the developmental origin of integration, specifically, on the role that direct epigenetic interactions play in shaping integration. These interactions are hypothesized to integrate modules and also to be highly conservative, potentially constraining the evolution of integration. Using the fox squirrel (Sciurus niger) mandible as a model system, we test five a priori developmental hypotheses that predict mandibular integration and we also explore for correlations between shapes of mandibular regions not anticipated by any of the developmental models. To determine whether direct epigenetic interactions are highly conserved in rodents, we examine the correlation structure of fluctuating asymmetry, and compare integration patterns between fox squirrels and prairie deer mice (Peromyscus maniculatus bairdii). In fox squirrels, we find a correlation structure unanticipated by all a priori developmental models: adjacent parts along the proximodistal jaw axis are correlated whereas more distant ones are not. The most notable exception is that the shape of the anterior incisor alveolus is correlated with the shape of the ramus (FA component) or coronoid (symmetric component). Those exceptions differ between species; in prairie deer mice, the molar alveolus is connected to more parts, and the incisor alveolus to fewer, than in fox squirrels. The structure of integration suggests that the mandible cannot be decomposed into parts but rather is a single connected unit, a result consistent with its functional integration. That match between functional and developmental integration may arise, at least in part, from function-induced growth, building developmental integration into the functional system and enabling direct epigenetic interactions to evolve when function does.

Cranial asymmetry in Eocene archaeocete whales and the evolution of directional hearing in water

Eocene archaeocete whales gave rise to all modern toothed and baleen whales (Odontoceti and Mysticeti) during or near the Eocene-Oligocene transition. Odontocetes have asymmetrical skulls, with asymmetry linked to high-frequency sound production and echolocation. Mysticetes are generally assumed to have symmetrical skulls and lack high-frequency hearing. Here we show that protocetid and basilosaurid archaeocete skulls are distinctly and directionally asymmetrical. Archaeocete asymmetry involves curvature and axial torsion of the cranium, but no telescoping. Cranial asymmetry evolved in Eocene archaeocetes as part of a complex of traits linked to directional hearing (such as pan-bone thinning of the lower jaws, mandibular fat pads, and isolation of the ear region), probably enabling them to hear the higher sonic frequencies of sound-producing fish on which they preyed. Ultrasonic echolocation evolved in Oligocene odontocetes, enabling them to find silent prey. Asymmetry and much of the sonic-frequency range of directional hearing were lost in Oligocene mysticetes during the shift to low-frequency hearing and bulk-straining predation.

First North American fossil monkey and early Miocene tropical biotic interchange

New World monkeys (platyrrhines) are a diverse part of modern tropical ecosystems in North and South America, yet their early evolutionary history in the tropics is largely unknown. Molecular divergence estimates suggest that primates arrived in tropical Central America, the southern-most extent of the North American landmass, with several dispersals from South America starting with the emergence of the Isthmus of Panama 3–4 million years ago (Ma). The complete absence of primate fossils from Central America has, however, limited our understanding of their history in the New World. Here we present the first description of a fossil monkey recovered from the North American landmass, the oldest known crown platyrrhine, from a precisely dated 20.9-Ma layer in the Las Cascadas Formation in the Panama Canal Basin, Panama. This discovery suggests that family-level diversification of extant New World monkeys occurred in the tropics, with new divergence estimates for Cebidae between 22 and 25 Ma, and provides the oldest fossil evidence for mammalian interchange between South and North America. The timing is consistent with recent tectonic reconstructions of a relatively narrow Central American Seaway in the early Miocene epoch, coincident with over-water dispersals inferred for many other groups of animals and plants. Discovery of an early Miocene primate in Panama provides evidence for a circum-Caribbean tropical distribution of New World monkeys by this time, with ocean barriers not wholly restricting their northward movements, requiring a complex set of ecological factors to explain their absence in well-sampled similarly aged localities at higher latitudes of North America.

Multivariate stasis in the dental morphology of the Paleocene-Eocene condylarth Ectocion

Abstract Evolutionary stasis has often been explained by stabilizing selection, intrinsic constraints, or, more recently, by spatially patterned population dynamics. To distinguish which of these mechanisms explains a given case of stasis in the fossil record, stasis must first be rigorously documented in a high-resolution stratigraphic time series of fossil specimens. Furthermore, past studies of evolutionary mode in fossil mammalian lineages have often been limited to univariate traits (e.g., molar crown area). It is reasonable to assume that tooth shape, a multivariate trait, reflects important additional aspects of tooth form and function. Here we present the results of a geometric morphometric analysis of the lower dentition of the Paleocene-Eocene condylarth species Ectocion osbornianus collected from the Bighorn and Clarks Fork Basins of northwestern Wyoming. Tooth margin shape, cusp configuration, and shearing crest shape were digitized for the last lower premolar, p4, and for two lower molars, m1 and m3. Multivariate statistical tests of evolutionary mode were used to analyze the change in shape variance over time in addition to the magnitude and direction of shape change. Test results characterize the shape time series as consisting of counteracting changes with less change than expected under a random walk (i.e., stasis). The temporal structure of shape variance implies that the sampled E. osbornianus most likely represent a single population, which is not concordant with the population dynamic mechanism of stasis. Stabilizing selection and/or intrinsic constraints remain as the mechanisms that could explain stasis in the lower dental shape of E. osbornianus despite the variable environmental conditions of the Paleocene–Eocene.

Postcranial Functional Morphology of Hyracotherium (Equidae, Perissodactyla) and Locomotion in the Earliest Horses

A nearly complete skeleton of Hyracotherium grangeri is described from the early Wasatchian (early Eocene) of the Clarks Fork Basin in northwestern Wyoming. This specimen includes a virtually complete, well-preserved pre-caudal vertebral column allowing the first thorough investigation of the locomotory abilities of these early Eocene horses. The posterior thorax (T) and lumbus (L) are divided into a facultatively dorsostable region (T15-L3) and an obligately dorsostable region (L3-L7). The facultatively dorsostable region is characterized by robust, cranially-oriented neural spines and well-developed attachment sites for epaxial musculature, whereas the obligately dorsostable region is characterized by embracing zygapophyses and less developed spines and attachment sites. Limb morphology exhibits a mixture of primitive characters and derived features associated with cursoriality. As described by previous authors, limb mobility is restricted at the elbow and ankle due to interlocking humero-radial and tibio-astragalar articulations, respectively. In contrast, the presence of a rounded femoral head and well-developed pelvic and femoral attachment sites for hindlimb adductor muscles suggests a highly mobile hip joint. Limited inversion of the manus and pes may have been possible via differential movement between the proximal and distal carpal elements and at the transverse tarsal joint, respectively. The obligately dorsostable region of the vertebral column likely resisted variably-oriented torque applied by hip musculature, thereby preventing dislocation of the pelvis and lumbus. The facultatively dorsostable region would have facilitated dynamic positioning of the center of mass during rapid acceleration. Brief comparisons with Orohippus and Mesohippus postcrania are used to discuss the selective pressures imposed by changes in body mass and habitat on the postcranial evolution of Paleogene horses.

Temporal Calibration and Biochronology of the Centenario Fauna, Early Miocene of Panama

New excavations along the Panama Canal have yielded a growing Early Miocene assemblage of mammals referred to as the Centenario Fauna. Despite the area’s proximity to South America, the mammals of the Centenario Fauna have entirely North American affinities. The Centenario Fauna is distributed throughout a ∼115-m stratigraphic interval encompassing the uppermost Culebra and Cucaracha Formations within the Panama Canal basin. Previously published ages constrain the age of the lower limit of the Centenario Fauna to no younger than ∼19 Ma, but the upper limit has remained problematical. A fresh exposure of the Cucaracha tuff, a prominent marker horizon within our measured sections, has yielded two new radioisotopic determinations: (1) an 40Ar/39Ar age of 18.96 ± 0.90 Ma and (2) a U-Pb zircon age of 18.81 ± 0.30 Ma. In addition, magnetostratigraphic data indicate that the Centenario Fauna occurs within chron C5Er, from 18.78 to 19.05 Ma on the geomagnetic polarity timescale of Gee and Kent. These correlations further confirm the calibration of the latest Arikareean (Ar4) to early Hemingfordian (He1) transition in Nebraska, at the base of chron C5Er, at about 19.05 Ma. The Centenario Fauna occurs at the beginning of the Hemingfordian North American Land Mammal Age, i.e., He1. A broad faunal province existed during the early Hemingfordian that can be recognized across a north-south range of 5000 km throughout North America, with the southernmost limits defined by the Centenario Fauna of Panama.

Evolutionary Patterns among Living and Fossil Kogiid Sperm Whales: Evidence from the Neogene of Central America.

Kogiids are known by two living species, the pygmy and dwarf sperm whale (Kogia breviceps and K. sima). Both are relatively rare, and as their names suggest, they are closely related to the sperm whale, all being characterized by the presence of a spermaceti organ. However, this organ is much reduced in kogiids and may have become functionally different. Here we describe a fossil kogiid from the late Miocene of Panama and we explore the evolutionary history of the group with special attention to this evolutionary reduction. The fossil consists of cranial material from the late Tortonian (~7.5 Ma) Piña facies of the Chagres Formation in Panama. Detailed comparison with other fossil and extant kogiids and the results of a phylogenetic analysis place the Panamanian kogiid, herein named Nanokogia isthmia gen. et sp. nov., as a taxon most closely related to Praekogia cedrosensis from the Messinian (~6 Ma) of Baja California and to Kogia spp. Furthermore our results show that reduction of the spermaceti organ has occurred iteratively in kogiids, once in Thalassocetus antwerpiensis in the early-middle Miocene, and more recently in Kogia spp. Additionally, we estimate the divergence between extant species of Kogia at around the late Pliocene, later than previously predicted by molecular estimates. Finally, comparison of Nanokogia with the coeval Scaphokogia cochlearis from Peru shows that these two species display a greater morphological disparity between them than that observed between the extant members of the group. We hypothesize that this reflects differences in feeding ecologies of the two species, with Nanokogia being more similar to extant Kogia. Nanokogia shows that kogiids have been part of the Neotropical marine mammal communities at least since the late Miocene, and gives us insight into the evolutionary history and origins of one of the rarest groups of living whales.

Downslope Fossil Contamination: Mammal-Bearing Fluvial Conglomerates and the Paleocene–Eocene Faunal Transition (Willwood Formation, Bighorn Basin, Wyoming)

Abstract Downslope fossil contamination is the result of erosion and subsequent redeposition of fossil material onto lower stratigraphic horizons. This produces time-averaged and potentially anomalous faunal records. Here, we describe vertebrate concentrations in Bighorn Basin (Wyoming) conglomerates that are early Wasatchian (earliest Eocene) in age (Wa-1) and rest erosionally upon Wa-0 strata deposited during the Paleocene–Eocene thermal maximum (PETM). The Wa-1 conglomerates were deposited during river channel migration and sheetflooding onto abandoned parts of an avulsion belt immediately after the PETM. Dark-colored Wa-1 fossil teeth eroding from the conglomerates are now mixed in places with the lighter-colored teeth of Wa-0 mammals. The spatial distribution of the conglomerate fossils and a vertical model of downslope contamination, based on species proportions from overlying stratigraphic intervals, are used to calculate an expected contribution of fossil contaminants to an assemblage. Results of this model are applied to address the principal weakness of the hypothesis that transient decreases in mammalian body size during the PETM were an evolutionary dwarfing response to climate change. Rare occurrences of large taxa with congeners of small size would refute the argument for evolutionary dwarfing, but our results indicate that such rare occurrences can be explained by downslope contamination alone. We conclude more generally that alluvial architecture is important for understanding the potential for downslope fossil contamination and that complications imposed by this type of contamination can be assessed quantitatively.