Multilevel analysis of integration and disparity in the mammalian skull.

Biological variation is often considered in a scalable hierarchy, e.g., within the individual, within the populations, above the species level. Morphological integration, the concept of covariation among constituent parts of an organism, is also hierarchical; the degree to which these "modules" covary is a matter of the scale of the study as well as underlying processes driving the covariation. Multilevel analyses of trait covariation are a valuable tool to infer the origins and historical persistence of morphological diversity. Here, we investigate concordance in patterns of integration and modularity across three biological levels of variation: within a species, within two genera-level radiations, and among species at the family level. We demonstrate this approach using the skull of mammalian family Leporidae (rabbits and hares), which is morphologically diverse and has a rare-among-mammals functional signal of locomotion adaptation. We tested three alternative hypotheses of modularity; from the most supported we investigated disparity and integration of each module to infer which is most responsible for patterns of cranial variation across these levels, and whether variation is partitioned consistently across levels. We found a common pattern of modularity underlies leporid cranial diversity, though there is inconsistency across levels in each module's disparity and integration. The face module contributes the most to disparity at all levels, which we propose is facilitating evolutionary diversity in this clade. Therefore, the distinctive facial tilt of leporids is an adaptation to locomotory behavior facilitated by a modular system that allows lineages to respond differently to selection pressures.

Evolutionary morphology of the rabbit skull.

The skull of leporids (rabbits and hares) is highly transformed, typified by pronounced arching of the dorsal skull and ventral flexion of the facial region (i.e., facial tilt). Previous studies show that locomotor behavior influences aspects of cranial shape in leporids, and here we use an extensive 3D geometric morphometrics dataset to further explore what influences leporid cranial diversity. Facial tilt angle, a trait that strongly correlates with locomotor mode, significantly predicts the cranial shape variation captured by the primary axis of cranial shape space, and describes a small proportion (13.2%) of overall cranial shape variation in the clade. However, locomotor mode does not correlate with overall cranial shape variation in the clade, because there are two district morphologies of generalist species, and saltators and cursorial species have similar morphologies. Cranial shape changes due to phyletic size change (evolutionary allometry) also describes a small proportion (12.5%) of cranial shape variation in the clade, but this is largely driven by the smallest living leporid, the pygmy rabbit (Brachylagus idahoensis). By integrating phylogenetic history with our geometric morphometric data, we show that the leporid cranium exhibits weak phylogenetic signal and substantial homoplasy. Though these results make it difficult to reconstruct what the 'ancestral' leporid skull looked like, the fossil records suggest that dorsal arching and facial tilt could have occurred before the origin of the crown group. Lastly, our study highlights the diversity of cranial variation in crown leporids, and highlights a need for additional phylogenetic work that includes stem (fossil) leporids and includes morphological data that captures the transformed morphology of rabbits and hares.

Ecological correlates to cranial morphology in Leporids (Mammalia, Lagomorpha).

The mammalian order Lagomorpha has been the subject of many morphometric studies aimed at understanding the relationship between form and function as it relates to locomotion, primarily in postcranial morphology. The leporid cranial skeleton, however, may also reveal information about their ecology, particularly locomotion and vision. Here we investigate the relationship between cranial shape and the degree of facial tilt with locomotion (cursoriality, saltation, and burrowing) within crown leporids. Our results suggest that facial tilt is more pronounced in cursors and saltators compared to generalists, and that increasing facial tilt may be driven by a need for expanded visual fields. Our phylogenetically informed analyses indicate that burrowing behavior, facial tilt, and locomotor behavior do not predict cranial shape. However, we find that variables such as bullae size, size of the splenius capitus fossa, and overall rostral dimensions are important components for understanding the cranial variation in leporids.

Response to comment on "The placental mammal ancestor and the post-K-Pg radiation of placentals".

Tree-building with diverse data maximizes explanatory power. Application of molecular clock models to ancient speciation events risks a bias against detection of fast radiations subsequent to the Cretaceous-Paleogene (K-Pg) event. Contrary to Springer et al., post-K-Pg placental diversification does not require "virus-like" substitution rates. Even constraining clade ages to their model, the explosive model best explains placental evolution.

A new fossil thryonomyid from the Late Miocene of the United Arab Emirates and the origin of African cane rats.

Cane rats (Thryonomyidae) are represented today by two species inhabiting sub-Saharan Africa. Their fossil record is predominately African, but includes several Miocene species from Arabia and continental Asia that represent dispersal events from Africa. For example, Paraulacodus indicus, known from the Miocene of Pakistan, is closely related to living Thryonomys. Here we describe a new thryonomyid, Protohummus dango, gen. et sp. nov., from the late Miocene Baynunah Formation of the United Arab Emirates. The new thryonomyid is less derived than "Thryonomys" asakomae from the latest Miocene of Ethiopia and clarifies the origin of crown Thryonomys and the evolutionary transition from Paraulacodus. A phylogenetic analysis shows Protohummus dango to be morphologically intermediate between Paraulacodus spp. and extinct and living Thryonomys spp. The morphological grade and phylogenetic position of Protohummus dango further supports previous biochronological estimates of the age of the Baynunah Formation (ca. 6-8 Ma).

The placental mammal ancestor and the post-K-Pg radiation of placentals.

To discover interordinal relationships of living and fossil placental mammals and the time of origin of placentals relative to the Cretaceous-Paleogene (K-Pg) boundary, we scored 4541 phenomic characters de novo for 86 fossil and living species. Combining these data with molecular sequences, we obtained a phylogenetic tree that, when calibrated with fossils, shows that crown clade Placentalia and placental orders originated after the K-Pg boundary. Many nodes discovered using molecular data are upheld, but phenomic signals overturn molecular signals to show Sundatheria (Dermoptera + Scandentia) as the sister taxon of Primates, a close link between Proboscidea (elephants) and Sirenia (sea cows), and the monophyly of echolocating Chiroptera (bats). Our tree suggests that Placentalia first split into Xenarthra and Epitheria; extinct New World species are the oldest members of Afrotheria.

Early evidence for complex social structure in Proboscidea from a late Miocene trackway site in the United Arab Emirates.

Many living vertebrates exhibit complex social structures, evidence for the antiquity of which is limited to rare and exceptional fossil finds. Living elephants possess a characteristic social structure that is sex-segregated and multi-tiered, centred around a matriarchal family and solitary or loosely associated groups of adult males. Although the fossil record of Proboscidea is extensive, the origin and evolution of social structure in this clade is virtually unknown. Here, we present imagery and analyses of an extensive late Miocene fossil trackway site from the United Arab Emirates. The site of Mleisa 1 preserves exceptionally long trackways of a herd of at least 13 individuals of varying size transected by that of a single large individual, indicating the presence of both herding and solitary social modes. Trackway stride lengths and resulting body mass estimates indicate that the solitary individual was also the largest and therefore most likely a male. Sexual determination for the herd is equivocal, but the body size profile and number of individuals are commensurate with those of a modern elephant family unit. The Mleisa 1 trackways provide direct evidence for the antiquity of characteristic and complex social structure in Proboscidea.

Diversity in the later Paleogene proboscidean radiation: a small barytheriid from the Oligocene of Dhofar Governorate, Sultanate of Oman.

Despite significant recent improvements to our understanding of the early evolution of the Order Proboscidea (elephants and their extinct relatives), geographic sampling of the group's Paleogene fossil record remains strongly biased, with the first ~30 million years of proboscidean evolution documented solely in near-coastal deposits of northern Africa. The considerable morphological disparity that is observable among the late Eocene and early Oligocene proboscideans of northern Africa suggests that other, as yet unsampled, parts of Afro-Arabia might have served as important centers for the early diversification of major proboscidean clades. Here we describe the oldest taxonomically diagnostic remains of a fossil proboscidean from the Arabian Peninsula, a partial mandible of Omanitherium dhofarensis (new genus and species), from near the base of the early Oligocene Shizar Member of the Ashawq Formation, in the Dhofar Governorate of the Sultanate of Oman. The molars and premolars of Omanitherium are morphologically intermediate between those of Arcanotherium and Barytherium from northern Africa, but its specialized lower incisors are unlike those of other known Paleogene proboscideans in being greatly enlarged, high-crowned, conical, and tusk-like. Omanitherium is consistently placed close to late Eocene Barytherium in our phylogenetic analyses, and we place the new genus in the Family Barytheriidae. Some features of Omanitherium, such as tusk-like lower second incisors, the possible loss of the lower central incisors, an enlarged anterior mental foramen, and inferred elongate mandibular symphysis and diminutive P(2), suggest a possible phylogenetic link with Deinotheriidae, an extinct family of proboscideans whose origins have long been mysterious.

Evolutionary patterns in the dentition of duplicidentata (mammalia) and a novel trend in the molarization of premolars.

BACKGROUND: The cusp homology of Lagomorpha has long been problematic largely because their teeth are highly derived relative to their more typically tribosphenic ancestors. Within this context, the lagomorph central cusp has been particularly difficult to homologize with other tribosphenic cusps; authors have previously considered it the paracone, protocone, metacone, amphicone, or an entirely new cusp. METHODOLOGY/PRINCIPAL FINDINGS: Here we present newly described fossil duplicidentates (Lagomorpha and Mimotonidae) in the context of a well-constrained phylogeny to establish a nomenclatural system for cusps based on the tribosphenic pattern. We show that the central cusp of lagomorphs is homologous with the metaconule of other mammals. We also show that the buccal acquisition of a second cusp on the premolars (molarization) within duplicidentates is atypical with respect to other mammalian lineages; within the earliest lagomorphs, a second buccal cusp is added mesially to an isolated buccal cusp. CONCLUSIONS/SIGNIFICANCE: The distal shift of the 'ancestral' paracone within early duplicidentates amounts to the changing of a paracone into a metacone in these lineages. For this reason, we support a strictly topological approach to cusp names, and suggest a discontinuity in nomenclature to capture the complexity of the interplay between evolutionary history and the developmental process that have produced cusp patterns in duplicidentates.