James B. Rossie

Congruence of molecules and morphology using a narrow allometric approach

There are many cases of incongruence between phylogenetic hypotheses produced from morphological data and those produced from molecular data. In such instances, many researchers prefer to accept the results of molecular phylogenies. For example, in a recent analysis of primate phylogenies based on craniodental characters, Collard and Wood [Collard M, Wood BA (2000) Proc Natl Acad Sci USA 97:5003–5006] argued that, because craniodental data do not yield relationships concordant with molecular studies, the results of studies that employ such characters must be considered suspect. As most of our knowledge of mammalian evolution and phylogenetic history comes from craniodental fossils, these results have dramatic implications. However, the aforementioned analysis did not take into account the potentially confounding effects of allometry on quantitative craniodental characters. In this article, we employ a previously undescribed narrow allometric coding method that accounts for such confounding influences in phylogenetic analyses of craniodental morphology. By using essentially the same raw data set as Collard and Wood [Collard M, Wood BA (2000) Proc Natl Acad Sci USA 97:5003–5006], 65 quantitative craniodental characters were adjusted in a parsimony analysis for the primate tribe Papionini, a group of monkeys argued to display extensive homoplasy. The resulting phylogenetic tree was congruent with the phylogenetic tree based on molecular data for these species, thereby meeting the “criterion of congruence.” These results suggest that morphological data, when treated properly, can be considered as reliable as molecular data in phylogenetic reconstruction. Rather than accepting phylogenetic hypotheses from one data source over another, cases of incongruence should be examined with greater scrutiny.

First cranial remains of a gondwanatherian mammal reveal remarkable mosaicism

Previously known only from isolated teeth and lower jaw fragments recovered from the Cretaceous and Palaeogene of the Southern Hemisphere, the Gondwanatheria constitute the most poorly known of all major mammaliaform radiations. Here we report the discovery of the first skull material of a gondwanatherian, a complete and well-preserved cranium from Upper Cretaceous strata in Madagascar that we assign to a new genus and species. Phylogenetic analysis strongly supports its placement within Gondwanatheria, which are recognized as monophyletic and closely related to multituberculates, an evolutionarily successful clade of Mesozoic mammals known almost exclusively from the Northern Hemisphere. The new taxon is the largest known mammaliaform from the Mesozoic of Gondwana. Its craniofacial anatomy reveals that it was herbivorous, large-eyed and agile, with well-developed high-frequency hearing and a keen sense of smell. The cranium exhibits a mosaic of primitive and derived features, the disparity of which is extreme and probably reflective of a long evolutionary history in geographic isolation.

Nasal Fossa of Mouse and Dwarf Lemurs (Primates, Cheirogaleidae)

Dimensions of the external midface in mammals are sometimes related to olfactory abilities (e.g., “olfactory snouts” of strepsirrhine primates). This association hinges on the largely unexplored relationship between the protruding midface and internal topography of the nasal fossae. Herein, serially sectioned heads of embryonic to adult cheirogaleid primates (mouse and dwarf lemurs) and a comparative sample were studied. To assess the anteroposterior distribution of olfactory epithelium (OE) within the nasal fossa, the surface area of OE and non‐OE was measured in two mouse lemurs (one adult, one infant). Prenatally, ethmoturbinal projections appear in an anteroposterior sequence. Fetal mouse lemurs, tenrecs, voles, and flying lemurs have four ethmoturbinals that project toward the nasal septum. Major distinctions among these mammals include the number of turbinals in recesses and the extent of the olfactory recess. Surface area measurements in the adult mouse lemur reveal that 31% of the entire nasal fossa is lined with OE. The majority is sequestered in a posterior recess (70% OE). Anterior to this space, only 28% of the nasal fossa is lined with OE. Ethmoturbinal I is lined with relatively less OE (35%) compared with more posterior ethmoturbinals (46–57%). Age comparisons support the idea that OE increases less than non‐OE between ages. Regionally, results suggest that most growth in surface area occurs in turbinals. But in all ethmoturbinals, surface area of non‐OE differs between ages more than that of OE. This study shows that the anterior part of the nasal fossa is mostly nonolfactory in Microcebus murinus. Anat Rec, 291:895–915, 2008.

The Maxillary Sinus in Three Genera of New World Monkeys: Factors That Constrain Secondary Pneumatization

The air filled cavities of paranasal sinuses are thought by some to appear opportunistically in spatial “gaps” within the craniofacial complex. Anthropoid primates provide excellent natural experiments for testing this model, since not all species possess a full complement of paranasal sinuses. In this study, two genera of monkeys (Saguinus and Cebuella) which form maxillary sinuses (MS) as adults were compared to squirrel monkeys (Saimiri spp.), in which a MS does not form. Using microCT and histomorphometric methods, the spatial position of paranasal spaces was assessed and size of the adjacent dental sacs was measured. In Saguinus, secondary pneumatization is underway perinatally, and the sinus extends alongside deciduous premolars (dp). The MS overlaps all permanent molars in the adult. In Saimiri, the homologous space (maxillary recess) extends no farther posterior than the first deciduous premolar at birth and extends no farther than the last premolar in the adult. Differences in dental size and position may account for this finding. For example, Saimiri has significantly larger relative dp volumes, and enlarged orbits, which encroach on the internasal space to a greater degree when compared to Saguinus. These factors limit space for posterior expansion of the maxillary recess. These findings support the hypothesis that secondary pneumatization is a novel, opportunistic growth mechanism that removes “unneeded” bone. Moreover, paranasal spaces occur in association with semiautonomous skeletal elements that border more than one functional matrix, and the spatial dynamics of these units can act as a constraint on pneumatic expansion of paranasal spaces. Anat Rec, 2010.

The Phylogenetic Significance of Anthropoid Paranasal Sinuses

In this study, the phylogenetic significance of anthropoid paranasal sinus anatomy is explored. New information reported in recent years has precipitated new hypotheses of sinus homology and more than doubled the number of anthropoid genera for which confident assessments of sinus identity can be made. As a result, it is likely that the phylogenetic meaning of commonly cited characters such as the ethmoid and frontal sinuses will change. The traditional method of “character mapping” is employed to test hypotheses of sinus homology and to reconstruct the ancestral states for sinus characters in major anthropoid clades. Results show that most sinuses appear to be primitive retentions in anthropoids, with their absences in various genera representing losses. Accordingly, many of these sinuses are potential anthropoid synapomorphies. Anat Rec, 291:1485–1498, 2008.

Ontogeny of the nasolacrimal duct in primates: functional and phylogenetic implications

The ontogeny of the nasolacrimal ducts (NLD) and canals (NLC) are investigated in strepsirrhine and haplorhine primates. Developmental series of serially sectioned fetal, perinatal and adult specimens, in combination with juvenile and adult skulls subjected to high‐resolution computed tomography, reveal that the vertical NLC and NLD of adult tarsiers and anthropoids are produced by the degeneration of a more horizontal anterior arm of the NLD that is present only transiently in haplorhines, but is maintained throughout life in strepsirrhines. This degeneration manifests as an ‘unzipping’ of the anterior arm by means of progressive enlargement (in a rostral direction) of a caudally placed opening of the NLD (at the base of the vertical NLC), followed by breakdown of the resulting epithelial groove. The similar mode by which the anterior arm of the membranous NLD degenerates in tarsiers and anthropoids strongly suggests that the conditions in these two taxa are homologous, and provides additional evidence for a monophyletic Haplorhini. The functional relationship between the nasolacrimal duct and the vomeronasal organ is reviewed in light of this evidence, and it is suggested that these changes in the haplorhine NLD were functionally linked to the development of anatomical haplorhinism of the oronasal complex.

Terrestrial adaptations in the hands of Equatorius africanus revisited.

Interpretations of the postcranial anatomy of East African early and middle Miocene large-bodied hominoids (e.g., Proconsul, Afropithecus, Turkanapithecus, Nacholapithecus) have suggested that these diverse primates utilized positional behaviors dominated by arboreal quadrupedalism. Preliminary descriptions of the Equatorius africanus partial skeleton (KNM-TH 28860) and other forelimb specimens, however, have argued that this animal relied more on terrestrial locomotion compared to its contemporaries, possibly similar to extant large papionin monkeys. In this paper, we reevaluate this interpretation by examining intrinsic hand proportions based on the lengths of the third proximal phalanx and fifth metacarpal in Equatorius in reference to a large sample of extant catarrhine primate taxa. We focused on the lengths of these hand bones because the ratio between phalanx and metacarpal lengths has been previously documented to discriminate terrestrial from arboreal mammalian taxa, including primates. The Equatorius hand displays semi-terrestrial hand proportions with a relatively shorter proximal phalanx compared to most arboreal monkeys. Its proximal phalanx, however, is relatively longer than those of habitually terrestrial monkeys (e.g., Theropithecus, Papio). Accordingly, although Equatorius retains some arboreal quadrupedal characteristics, these results corroborate the previous inference that it engaged in more terrestrial locomotion than earlier Miocene apes such as Proconsul. We suggest that the postcranial skeleton of Equatorius evinces the earliest signs of semi-terrestriality in the hominoid fossil record. It is likely that the terrestrial specialization utilized by living hominoids, e.g., knuckle-walking, evolved separately.

Distribution of Olfactory and Nonolfactory Surface Area in the Nasal Fossa of Microcebus murinus: Implications for Microcomputed Tomography and Airflow Studies

The nasal fossa of most mammals exemplifies extreme skeletal complexity. Thin scrolls of bone (turbinals) that both elaborate surface area (SA) and subdivide nasal space are used as morphological proxies for olfactory and respiratory physiology. The present study offers additional details on the nasal fossa of the adult mouse lemur (Microcebus murinus), previously described by Smith and Rossie (Smith and Rossie [ 2008 ]; Anatomical Record 291:895–915). Additional, intervening histological sections of the specimen were used to map and quantify the distribution of olfactory and nonolfactory mucosa on the smaller turbinal of the frontal recess (FR; frontoturbinal) and those that occur between ethmoturbinals (ETs; interturbinals). A second adult Microcebus specimen, available as a dried skull, was scanned using microcomputed tomography (microCT) and reconstructed to infer the position of these turbinals within the nasal airway. Overall, turbinal bones comprise more than half of internal nasal SA. All ETs combined comprise about 30% of total nasal fossa SA, and contribute nearly half of all olfactory SA. Of these, the nasoturbinal (NT) is most completely covered with olfactory mucosa, whereas ET I is least covered with olfactory mucosa. The FR contributes significantly to total olfactory SA (ca. 20%). This recess and the single frontoturbinal within it lie in a more lateral pathway of airflow compared with interturbinals, which lie in more central zone just anterior to the olfactory recess of Microcebus. Variations in the turbinals and recesses that complicate central and paranasal in primates should be investigated further in light of zone‐specific distributions of olfactory receptors (ORs) that differ between these regions in rodents. Anat Rec, 2011

Fate of the nasal capsular cartilages in prenatal and perinatal tamarins (Saguinus geoffroyi) and extent of secondary pneumatization of maxillary and frontal sinuses.

Development of the nasal capsule cartilages was studied in seven Geoffroys tamarins (Saguinus geoffroyi), including one fetus, five neonates and one infant. Four additional postnatal specimens of the genus were studied (one 5‐month‐old and three adults) to determine the magnitude of postnatal expansion of the paranasal sinuses. Alcian blue histochemistry and osteopontin immunohistochemistry were employed in selected subadult specimens to characterize cartilage matrix. The fetal S. geoffroyi possesses a continuous nasal capsule, including a zona anularis; the primordial maxillary sinuses are surrounded by cartilage. Secondary pneumatization is in progress in all older specimens, which have sinuses that are more than twofold larger compared to that of the fetus. Results indicate that extensive ossification of the middle part of the nasal capsule (pars intermedia) is occurring in the perinatal timeframe, forming portions of the ethmoid bone. Anteriorly, the nasal capsule comprises isolated fragments in perinatal specimens, which are fewer and smaller in the infant and in a 5‐month‐old S. midas, and nearby multinucleate cells suggest that osteoclasts break apart these initially continuous elements. Fragments of the pars intermedia and the tectum nasi are found transiently between mucosa and the sites of secondary pneumatization. The maxillary sinus mucosa is highly vascular in most perinatal specimens. Histochemical and immunohistochemical findings show that cartilage of endochondral bones and non‐ossifying parts are distinct in the perinatal time period. These results indicate that breakdown of the capsular cartilage precedes secondary pneumatization as previously suggested. There are portions of the cartilage of the recessus maxillaris and tectum nasi that transiently block mucosa from interfacing directly with bone. Vascularization may play a role in the breakdown of cartilages as well as the onset of secondary pneumatization. Since cartilage has the capacity to produce substances that trigger angiogenesis and bone resorption, further detailed characterization of the cartilage bordering sites of secondary pneumatization is merited. Anat Rec, 291:1397–1413, 2008. ©2008 Wiley‐Liss, Inc.

Are We Looking for Loads in All the Right Places? New Research Directions for Studying the Masticatory Apparatus of New World Monkeys

New World monkeys display a wide range of masticatory apparatus morphologies related to their diverse diets and feeding strategies. While primatologists have completed many studies of the platyrrhine masticatory apparatus, particularly morphometric analyses, we collectively acknowledge key shortcomings in our understanding of the function and evolution of the platyrrhine feeding apparatus. Our goal in this contribution is to review several recent, and in most cases ongoing, efforts to address some of the deficits in our knowledge of how the platyrrhine skull is loaded during feeding. We specifically consider three broad research areas: (1) in vivo physiological studies documenting mandibular bone strains during feeding, (2) metric analyses assessing musculoskeletal functional morphology and performance, as well as (3) the initiation of a physiological ecology of feeding that measures in vivo masticatory mechanics in a natural environment. We draw several conclusions from these brief reviews. First, we need better documentation of in vivo strain patterns in the platyrrhine skull during feeding given their empirical role in developing adaptive hypotheses explaining masticatory apparatus form. Second, the greater accuracy of new technologies, such as CT scanning, will allow us to better describe the functional consequences of jaw form. Third, performance studies are generally lacking for platyrrhine jaws, muscles, and teeth and offer exciting avenues for linking form to feeding behavior and diet. Finally, attempts to bridge distinct research agendas, such as collecting in vivo physiological data during feeding in natural environments, present some of the greatest opportunities for novel insights into platyrrhine feeding biology. Anat Rec, , 2011.