Cranial morphology and adaptations in Eocene Adapidae. I. Sexual dimorphism in Adapis magnus and Adapis parisiensis

Adapis is one of the best known lemuriform fossil primates. Quantitative analysis of all well-preserved crania of Adapis magnus (n = 8) and Adapis parisiensis (n = 12) together with maxillary and mandibular dentitions preserving canines corroborates Stehlin's hypothesis that Adapis was sexually dimorphic. Males are from 13% to 16% larger than females in cranial length, corresponding to a weight dimorphism estimated at 44% to 56%, and have relatively broader skulls with more prominent sagittal and nuchal crests. Canine dimorphism ranges from 13% to 19%, which is equal to or only slightly greater than that expected as a result of body size dimorphism (i.e., relative canine dimorphism is slight or nonexistent). By comparison with living primates, the observed body size dimorphism in Adapis implies a polygynous breeding system. Cebus apella is a diurnal arboreal living primate with moderate body size dimorphism and slight relative canine dimorphism and one can speculate that Adapis lived in polygynous multimale troops of moderate size like those of C. appella. Adapis extends the geological history of sexual dimorphism and polygyny in primates back to the Eocene. Extant lemuriform primates are generally not dimorphic or polygynous and they clearly do not adequately represent the range of social adaptations present in Eocene primates. The evolutionary lineage from Adapis magnus to Adapis parisiensis exhibits reduction in body size and in relative canine size, and phyletic dwarfing in Adapis is possibly an adaptive response to increasing climatic seasonality and environmental instability in the late Eocene and early Oligocene.     

Biometrical characteristics of primate hands

The lenght proportions of the primate hands and their elements are analyzed in 43 extant genera and 6 fossil genera. The length of the hand in relation to the forelimb length does not characterize taxonomic groups, but rather locomotor modes, such as vertical-clinging-and-leaping, claw-climbing, and terrestrial quadrupedalism, as opposed to arboreal quadrupedalism. The relative lengths of the carpus, metacarpus, and digits appear mainly related to the phylogenetic history of the primates. Paraxony, instead of mesaxony, is the most frequent pattern of the simiiform hand, whereas hypermesaxony characterizes humans, hylobatids, and tarsiers. The proportions of the primitive euprimate hand are discussed in the light of the hand proportions of extant primates. Proportions drawn from hand remains ofMegaladapis edwardsi, Proconsul africanus, Mesopithecus pentelici, Notharctus, Adapis parisiensis, andPlesiadapis insignis are compared to those of extant primates, and discussed from both phylogenetical and functional points of view. To the memory of our colleague Jacques Lessertisseur.     

Bite force and body mass of the fossil rodent Telicomys giganteus (Caviomorpha,Dinomyidae)

An exceptionally well-preserved skull of the Pliocene rodent Telicomys giganteus allowed the first estimation of body mass and analysis of the bite mechanics of this species of South American giant rodent. In this study, we reconstructed the main anatomical features of the skull of this Pliocene rodent and related them to the bite force at the incisors. The average of an estimation body mass gives 100 kg. We also estimated the bite force using three different techniques. Two methods suggest that bite forces at the incisors have a range of 500–1000 N. However, the incisors seem to be stronger than expected for this bite force, implying that the bite forces may have been greater than 2000 N. We consider the hypothesis of defense against predators or other agonistic behavior to explain our results.     

Heterochrony: The evolution of ontogeny. By Michael L. McKinney and Kenneth J. McNamara. New York: Plenum Press. 1991. XIX + 437 pp. ISBN 0-306-43638-8. $ 49.50 (cloth)

Macaca fascicularis is broadly distributed in Southeast Asia across 30° of latitude and 35° of longitude (Indochinese Peninsula, Isthmus of Kra, Malay Peninsula, Greater and Lesser Sunda Islands, Philippine Islands, and numerous small, neighboring islands). The range is divisible into 1) a core area comprised of mainland Southeast Asia, Borneo, Sumatra, and Java (large land masses interconnected during the last glacial maximum, 18,000 B. P.); 2) shallow-water fringing islands, which are smaller islands connected to the core area during the last glacial maximum; and 3) deep-water fringing islands, which are peripheral islands not connected to the core area during the last glacial maximum. Skull length was used to study effects of latitude and insularity on patterns of size variation. The data are from 802 adult M. fascicularis specimens from 140 core-area localities, 63 shallow-water islands, and 29 deep-water islands. Sex-specific polynomial regressions of skull length on latitude were used to describe skull length variation in the core area. These regressions served as standards for evaluating variation among samples from shallow-water and deep-water islands. The core area exhibits Bergmannian latitudinal size clines through most of the species range. Thus, skull length decreases from about 8°S (Java) to the equator (Sumatra and Borneo), then increases as far north as about 13°N (Isthmus of Kra). Farther north, to the northernmost Indochinese localities at about 17°N, skull length in M. fascicularis decreases with increasing latitude, contrary to Bergmann's rule. Latitudinal size variation in shallow-water fringing islands generally parallels that in the core area. However, skull length tends to be smaller than in the core area at similar latitudes. Deep-water fringing islands are markedly more variable, with relatively small specimens in the Lesser Sunda Islands and relatively large specimens in the Nicobar Islands. These analyses illustrate how a primate species may vary in response to latitudinal temperature variation and to isolation. © 1993 Wiley-Liss, Inc.     

The uniqueness of Daubentonia

The aberrant features of the genus Daubentonia, such as the superficially rodent-like dentition, the globose and foreshortened brain case, and the filiform third manual digit have long been known. But the current assessment of the genus as lemuriform, and within that group as closest to the indriids, depends upon greater weight being placed upon other characteristics such as the cranial arterial pattern, the molariform teeth, and the developmental characteristics of the dentition. Prior multivariate morphometric studies have shown that though the shoulder structure of Daubentonia is uniquely different from that of all other primates, the structure of its pelvis may not be especially different from that of many relatively non-specialized primates. A large series of studies have been summated here in which many different anatomical regions (shoulder, arm, forearm, forelimb as a whole, pelvis, femur, hindlimb as a whole, forelimb and hindlimb combined, and total bodily proportions including limbs, trunk, and head) have been characterized osteometrically in a wide range of primate genera. The resulting data sets have been studied by discriminant function analyses. The differences that have been found are large enough that it can be confidently asserted that in its postcranial skeleton, Daubentonia is more different from the primates as a whole than is any other primate genus. These differences are big enough that their statistical and biological significance is not at all in doubt, notwithstanding the very small numbers of available specimens of this rare genus. They are so great that functional implications exist though they cannot, in our present state of knowledge of the habits of the genus, be ascribed with any certainty. They are so great indeed, paralleling the enormous differences of Daubentonia from other primates in its dentition, skull and cheiridia, that we may prefer to keep open minds about its taxonomic placement.     

Tooth and cranial disparity in the fossil relatives of Sphenodon (Rhynchocephalia) dispute the persistent ‘living fossil’ label

The tuatara (Sphenodon punctatus) is the only living representative of Rhynchocephalia, a group of small vertebrates that originated about 250 million years ago. The tuatara has been referred to as a living fossil; however, the group to which it belongs included a much greater diversity of forms in the Mesozoic. We explore the morphological diversity of Rhynchocephalia and stem lepidosaur relatives (Sphenodon plus 13 fossil relatives) by employing a combination of geometric morphometrics and comparative methods. Geometric morphometrics is used to explore cranium size and shape at interspecific scale, while comparative methods are employed to test association between skull shape and size and tooth number after taking phylogeny into account. Two phylogenetic topologies have been considered to generate a phylomorphospace and quantify the phylogenetic signal in skull shape data, the ancestral state reconstruction as well as morphological disparity using disparity through time plots (DTT). Rhynchocephalia exhibit a significant phylogenetic signal in skull shape that compares well with that computed for other extinct vertebrate groups. A consistent form of allometry has little impact on skull shape evolution while the number of teeth significantly correlates with skull shape also after taking phylogeny into account. The ancestral state reconstruction demonstrates a dramatic shape difference between the skull of Sphenodon and its much larger Cretaceous relative Priosphenodon. Additionally, DTT demonstrates that skull shape disparity is higher between rather than within clades while the opposite applies to skull size and number of teeth. These results were not altered by the use of competing phylogenic hypotheses. Rhynchocephalia evolved as a morphologically diverse group with a dramatic radiation in the Late Triassic and Early Jurassic about 200 million years ago. Differences in size are not marked between species whereas changes in number of teeth are associated with co‐ordinated shape changes in the skull to accommodate larger masticatory muscles. These results show that the tuatara is not the product of evolutionary stasis but that it represents the only survivor of a diverse Mesozoic radiation whose subsequent decline remains to be explained.     

Tropical rain forest conversion and perspectives in the conservation of wild primates (Alouatta and Ateles) in Mexico

The original distribution of the tropical rain forest and of the populations of Alouatta palliata, Al. pigra, and the two subspecies of Ateles geoffroyi in southern Mexico have been reduced by at least 90% in the last 40 years as a result of conversion of natural habitat to pasture and agricultural fields. This dramatic conversion has been caused mainly by the rapid growth of the human population in the southern states of the country. In the region of Los Tuxtlas in southern Veracruz, where the only longitudinal popululational and ecological studies of A. palliata and At. g. vellerosus have taken place, only 15% of the original extension of the tropical rain forest remains today. The intensive destruction of suitable primate habitat in this region has resulted in an accelerated process of extinction of the primate species. It is estimated that only about 200 At. g. vellerosus and about 1200 Al. palliata exist in the remaining small portion of their original habitat. Today, the distribution of the three primate species in Mexico is intensively and extensively fragmented, and only five potential foci for conservation exist in the country. Urgent action is required to protect the primate populations in the region of Los Tuxtlas and at the other four foci, as some of these populations may disappear by 1995.     

Goeldi's monkeys: A primate paradox?

“A primate with the skull of a Callicebus, the mandible and feet of a marmoset and the tail and teeth of Pseudocebus [=Cebus] ….” (Riberio, 1941 as cited in Hershkovitz 1 p. 866). Goeldi's monkeys are the least understood species of platyrrhine. The monkeys' small body size, black coloration, tendency to forage in the low forest understory, and cryptic nature, make them difficult to observe in the wild. Until recently, they had never been the focus of a long‐term field study and as a result, little was known of the monkeys' behavior and ecology. Goeldi's monkeys comprise only one recognized species, Callimico goeldii, and have an unusual suite of anatomical and reproductive traits. These traits have created considerable confusion for taxonomists and physical anthropologists.     

Molar scaling in strepsirrhine primates

We examined how maxillary molar dimensions change with body and skull size estimates among 54 species of living and subfossil strepsirrhine primates. Strepsirrhine maxillary molar areas tend to scale with negative allometry, or possibly isometry, relative to body mass. This observation supports several previous scaling analyses showing that primate molar areas scale at or slightly below geometric similarity relative to body mass. Strepsirrhine molar areas do not change relative to body mass(0.75), as predicted by the metabolic scaling hypothesis. Relative to basicranial length, maxillary molar areas tend to scale with positive allometry. Previous claims that primate molar areas scale with positive allometry relative to body mass appear to rest on the incorrect assumption that skull dimensions scale isometrically with body mass. We identified specific factors that help us to better understand these observed scaling patterns. Lorisiform and lemuriform maxillary molar scaling patterns did not differ significantly, suggesting that the two infraorders had little independent influence on strepsirrhine scaling patterns. Contrary to many previous studies of primate dental allometry, we found little evidence for significant differences in molar area scaling patterns among frugivorous, folivorous, and insectivorous groups. We were able to distinguish folivorous species from frugivorous and insectivorous taxa by comparing M1 lengths and widths. Folivores tend to have a mesiodistally elongated M1 for a given buccolingual M1 width when compared to the other two dietary groups. It has recently been shown that brain mass has a strong influence on primate dental eruption rates. We extended this comparison to relative maxillary molar sizes, but found that brain mass appears to have little influence on the size of strepsirrhine molars. Alternatively, we observed a strong correlation between the relative size of the facial skull and relative molar areas among strepsirrhines. We hypothesize that this association may be underlain by a partial sharing of the patterning of development between molar and facial skull elements.     

Paleobiology of the oligopithecines,the earliest known anthropoid primates

Anthropoid primates of the subfamily Oligopithecinae are late Eocene in age, and have a known distribution of Northeast Africa and the Arabian Peninsula. Body sizes of the three known oligopithecine species are estimated from allometric molar size regressions to be 700–1000 g forOligopithecus savagei, 600–900 g forCatopithecus browni, and 500 g for the least well-known and smallest species,Proteopithecus sylviae. Occlusal features of the molar teeth, considered in conjunction with body size, suggest that all three species were frugivorous and insectivorous. The orbital size ofCatopithecus indicates a diurnal activity cycle. A relatively broad interobital region in this species may indicate prosimian-like or callitrichid-like olfactory adaptations. Structural features of the crushed skull suggest thatCatopithecus had a smaller cranial capacity than those of extant anthropoids with a similar body size. Fossil plants and birds from localities yielding oligopithecines suggest a wet, warm, tropical, forested, swampy environment. These paleobiological inferences about the extinct oligopithecines are discussed in relation to questions about primate adaptations near the prosimian-anthropoid transition.     

A new genus and species of adapid primate from the middle Eocene of Alsace, and a new genus for 'Adapis' ruetimeyeri Stehlin, 1912

A new primate genus and species, represented by isolated teeth, is described from the middle Eocene Alsatian site of Bouxwiller. This new form is closely related to Egerkingen 'Adapis' ruetimeyeri, for which a new genus is proposed because of the important distinctions from type Adapis present in its dentition. Nonetheless, both new genera are closely related to Adapis and Leptadapis.     

Sexual dimorphism and allometry in primate ossa coxae

Five measurements were taken on the ossa coxae of 454 adult primates representing Ceboidea, Cercopithecoidea and Hominoidea. Sex differences in these variables and their relationships to overall body size and sexual dimorphism were tested by means of Student's t-test and regression analysis. The study attempts to clarify the nature of primate pelvic sexual dimorphism, including allometric effects, and more specifically, test the assertion made by Mobb and Wood (1977) that sexual dimorphism in body size in not an important determinant in pelvic sex differences. Variables that contribute to the size of the birth canal tend to be larger in females than males in all taxa studied except two. In these, Hylobates and Alouatta, there were no significant differences between the sexes for any of the five variables. In general, sexual dimorphism in variables contributing to the size of the birth canal was correlated (r ? 0.8) with sexual dimorphism in body size. Furthermore, the coefficients of allometry underlying pelvic sex differences were shown to be moderately correlated (r ? 0.5) with sexual dimorphism in size. The influence of other adaptive factors on primate pelvic sexual dimorphism are also briefly discussed.     

Selection in a cycling population: differential response among skeletal traits

Abstract Population density cycles influence phenotypic evolution through both density‐dependent selection during periods of high density and through enhanced genetic drift during periods of low density. We investigated the response of different phenotypic traits to the same density cycles in a population of the yellow‐necked mouse, Apodemus flavicollis, from Bia?owieza National Park in Poland. We examined nonmetric skull traits, skull and mandible size, skull and mandible shape, and transferrin allele frequencies. We found that all of the traits changed significantly over the seven‐year study period. The greatest changes in nonmetric traits and mandible size occurred during periods of increasing density, and the magnitude of changes in skull and mandible shape was correlated with the magnitude of density changes. Frequencies of transferrin alleles changed the most when population density was in decline. Changes among the five phenotypic traits were generally uncorrelated with one another, except for skull and mandible shape. Nonmetric traits were selectively neutral when assessed with Q_ST/F_ST analysis, whereas mandible size, mandible shape, and skull shape showed evidence of fairly strong selection. Selection on skull size was weak or nonexistent. We discuss how different assumptions about the genetic components of variance affect Q_ST estimates when phenotypic variances are substituted for genetic ones. We also found that change in mandible size, mandible shape, skull size, and skull shape were greater than expected under a neutral model given reasonable assumptions about heritability and effective population size.     

Basicranial flexion,relative brain size,and facial kyphosis in nonhuman primates

Numerous hypotheses explaining interspecific differences in the degree of basicranial flexion have been presented. Several authors have argued that an increase in relative brain size results in a spatial packing problem that is resolved by flexing the basicranium. Others attribute differences in the degree of basicranial flexion to different postural behaviors, suggesting that more orthograde animals require a ventrally flexed pre-sella basicranium in order to maintain the eyes in a correct forward-facing orientation. Less specific claims are made for a relationship between the degree of basicranial flexion and facial orientation. In order to evaluate these hypotheses, the degree of basicranial flexion (cranial base angle), palate orientation, and orbital axis orientation were measured from lateral radiographs of 68 primate species and combined with linear and volumetric measures as well as data on the size of the neocortex and telencephalon. Bivariate correlation and partial correlation analyses at several taxonomic levels revealed that, within haplorhines, the cranial base angle decreases with increasing neurocranial volume relative to basicranial length and is positively correlated with angles of facial kyphosis and orbital axis orientation. Strepsirhines show no significant correlations between the cranial base angle and any of the variables examined. It is argued that prior orbital approximation in the ancestral haplorhine integrated the medial orbital walls and pre-sella basicranium into a single structural network such that changes in the orientation of one necessarily affect the other. Gould's (“Ontogeny and Phylogeny.” Cambridge: Belknap Press, 1977) hypothesis, that the highly flexed basicranium of Homo may be due to a combination of a large brain and a relatively short basicranium, is corroborated. © 1993 Wiley-Liss, Inc.     

Brains of Vespertilionids II. Vespertilioninae with special reference to Tylonycteris

As shown in Part I, the Vespertilioninae have on the average the lowest encephalization index (EI) of all the Vespertilionid subfamilies available, and the average size indices (Sis) of most of their brain parts are also lowest. There are, however, clear differences between the genera. The highest indices for the total brain and for many brain parts (OBL, DIE, TEL, PAL, SEP, STR, SCH) were found in Myotis, the highest Sis for NEG and MES in Scotophilus, for CER in Lasiurus, for BOL in Rhogeessa, and for HIP in Cbalinolobus. The lowest values for all brain parts except BOL were found in Tylonycteris (for BOL in Glauconycteris). The average EI of the flat-headed bamboo bats Tylonycteris pachypus and T. robustula was 60, i. e., ²/₅ less than that of the non-Tylonycteris Vespertilionids, which, as the reference group, have an average EI of 100. The brain size reduction may well be related to the adaptation to extreme flat-headedness. The amount of reduction in the various brain parts differs: it is strongest (about ¹/₂) in higher but more dispensable brain parts (STR, HIP, NEO) and distinctly lower (about ¹/₄) in structures closely involved in the fundamental vegetative functions (OBL, MES). Genera with conservative skull characteristics may have derivative characteristics of the brains, and vice versa.     

Molar occlusion and jaw mechanics of the Eocene primate Adapis

Wear facets on molars of the Eocene primate Adapis magnus are described. Striations on these wear facets indicate three separate directions of mandibular movement during mastication. One direction corresponds to a first stage of mastication involving orthal retraction of the mandible. The remaining two directions correspond to buccal and lingual phases of a second stage of mastication involving a transverse movement of the mandible. The mechanics of jaw adduction are analysed for both the orthal retraction and transverse stages of mastication. During the orthal retraction stage the greatest component of bite force is provided by the temporalis muscles acting directly against the food with the mandible functioning as a link rather than as a lever. A geometrical argument suggests that during the transverse stage of mastication bite force is provided by the temporalis muscles of both sides, the ipsilateral medial and lateral pterygoid muscles, and the contralateral masseter muscle.     

Environment and space as drivers of variation in skull shape in two widely distributed South‐American Tayassuidae,Pecari tajacu and Tayassu pecari (Mammalia: Cetartiodactyla)

The influence of the environment on the geographical variation of morphological traits has been recognized in a number of taxa. Pecari tajacu and Tayassu pecari are ideal models to investigate intraspecific geographic variation in skull because of their wide and heterogeneous geographical distribution in South America. We used geometric morphometric procedures to examine the geographical variation in skull shape of 294 adult specimens of these species from 134 localities. We quantified to what extent skull shape variation was explained by environment, skull size and geographical space using variation partitioning analysis. We detected a strong pattern of geographic variation for P. tajacu skull shape, but not for T. pecari. The environment seems to be the major selective force that drives skull shape variation in both species. Nevertheless, other spatially structured processes (e.g. genetic drift, gene flow) might also have affected variation in the skull shape of the more widespread species P. tajacu. Allometric relationships might reflect the biomechanical constraints that are thought to be strong enough to limit size‐related changes in T. pecari skull shape.     

Skull structure of the flying fish Cheilopogon pinnatibarbatus (Beloniformes, Exocoetidae)

The skull of the flying fish Cheilopogon pinnatibarbatus is first described in comparison with literature data on other four-winged flying fishes (subfamily Cypselurinae). The skull of Ch. pinnatibarbatus is characterized by the following features: (1) a multitude (about 40) of minute pores in the canal of the lateral line of the nasale; (2) a big opening in the roof of the myodome; (3) the lateral line canal of dentale by far does not reach the symphysis; (4) the tip of praeoperculum does not reach the upper edge of the hyomandibulare; (5) the posterior part of the angulare is weakly covered by the articulare and almost reaches from the outside the joint for articulation with the quadratum. Ppublished in Voprosy Ikhtiologii, 2007, Vol. 47, No. 3, pp. 284–291. This article was submitted by the authors in English.     

Human Induced Rotation and Reorganization of the Brain of Domestic Dogs

Domestic dogs exhibit an extraordinary degree of morphological diversity. Such breed-to-breed variability applies equally to the canine skull, however little is known about whether this translates to systematic differences in cerebral organization. By looking at the paramedian sagittal magnetic resonance image slice of canine brains across a range of animals with different skull shapes (N = 13), we found that the relative reduction in skull length compared to width (measured by Cephalic Index) was significantly correlated to a progressive ventral pitching of the primary longitudinal brain axis (r = 0.83), as well as with a ventral shift in the position of the olfactory lobe (r = 0.81). Furthermore, these findings were independent of estimated brain size or body weight. Since brachycephaly has arisen from generations of highly selective breeding, this study suggests that the remarkable diversity in domesticated dogs'' body shape and size appears to also have led to human-induced adaptations in the organization of the canine brain.