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.     

Cranial morphology and adaptations in Eocene Adapidae. II. The Cambridge skull of Adapis parisiensis

One of the most complete skulls of the early primate Adapis parisiensis is in the collection of the Department of Zoology, Cambridge University. This exceptionally well-preserved male skull, from Quercy in southern France, is important in showing relatively small orbits that are highly convergent, a distinct ethmoid component in the medial orbital wall, very small infraorbital foramina, a well-preserved auditory region with the stapedial canal about twice the diameter of the canal for the promontory artery, and a well-preserved braincase 8.8 cm³ in endocranial volume. The frontal lobe of the brain in the Cambridge skull described here is less expanded than that reported previously in a British Museum skull. The average body weight of Adapis parisiensis is estimated to have been about 2.0 kg, and that of Adapis magnus is estimated to have been about 8.4 to 9.0 kg. The encephalization quotient (EQ) of Adapis parisiensis is estimated to have been 0.45, which is well below the range found in modern prosimians. There is some indication that the size of the foramen magnum has increased with increasing brain size during primate evolution. Adapis parisiensis appears to have been a medium-sized, visually oriented, diurnal, sexually dimorphic arboreal folivore.     

Canine size and shape in male anthropoid primates

While studies of canine dimorphism in primates are common, only a few have examined canine tooth size independently within each sex. Recently, Greenfield and Washburn (Am. J. Phys. Anthropol. 84:17–34, 1991) proposed that there are two types of male canines which reflect different allometric scaling patterns of canine crown height against canine occlusal dimensions. They also suggest that proportional canine shape, measured as canine crown height (or projection) relative to the occlusal dimensions, provides an estimate of the canine's function as a weapon, though they provide no test of this hypothesis. This analysis critically examines the claim that there are two types of male canines among anthropoids. It then tests the hypothesis that relative male canine size (measured against body weight) and proportional canine shape are related to estimates of intermale competition, diet, and substrate (used as a surrogate measure of predation pressure). While there is strong taxonomic variation in canine size and shape among male anthropoids, no evidence is found for two discrete canine types. Rather, within families and subfamilies, canine dimensions scale isometrically against body weight and against each other, with a continuum of canine shapes among different taxa. While variation in male canine size is associated with intermale competition and substrate, even when taxonomic variation is controlled, variation in proportional canine shape is not. Neither canine size nor shape are generally associated with variation in diet. © 1993 Wiley-Liss, Inc.     

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.     

Intrasexual competition and canine dimorphism in anthropoid primates.

A number of factors, including sexual selection, body weight, body-weight dimorphism, predation, diet, and phylogenetic inertia have been proposed as influences on the evolution of canine dimorphism in anthropoid primates. Although these factors are not mutually exclusive, opinions vary as to which is the most important. The role of sexual selection has been questioned because mating system, which should reflect its strength, poorly predicts variation in canine dimorphism, particularly among polygynous species. Kay et al. (1988) demonstrate that a more refined estimate of intermale competition explains a large proportion of the variation in canine dimorphism in platyrrhine primates. We expand their analysis, developing a more generalized measure of intermale competition based on the frequency and intensity of male-male agonism. We examine the relative influences of predation (inferred by substrate use), female body weight, body-weight dimorphism, diet, and sexual selection on the evolution of anthropoid canine dimorphism. Intermale competition is very strongly associated with canine dimorphism. Predation also has a marked effect on canine dimorphism, in that savanna-dwelling species consistently show greater canine dimorphism than other species, all other factors being held equal. Body-weight dimorphism is also strongly associated with canine dimorphism, though apparently through a common selective basis, rather than through allometric effects. Body weight seems to play only a minor, indirect role in the evolution of canine dimorphism. Diet plays no role. Likewise, we find little evidence that phylogenetic inertia is a constraint on the evolution of canine dimorphism.     

The skeleton of early Eocene Cantius, oldest lemuriform primate

A recently discovered partial skeleton of the adapid Cantius trigonodus from the early Eocene Willwood Formation of the Bighorn Basin, Wyoming, documents substantial new information about the anatomy of the oldest lemuriform primates. It is very similar in all features to its descendant, middle Eocene Notharctus, and both exhibit numerous resemblances to certain extant Malagasy lemurs, particularly Lepilemur, Propithecus, Lemur, and Hapalemur griseus. Like these forms, Cantius had relatively long hind limbs and short forelimbs. Forelimb traits (prominent brachialis flange of the humerus, well-developed olecranon process of the ulna, and strong shafts of the ulna and radius) suggest active use of the forelimbs in progression. Specializations in the hind limb (e.g., expanded articular surface of the femoral head, narrow and elevated patellar trochlea and prominent lateral trochlear ridge, posteriorly oriented femoral and tibial condyles, narrow and elongate talus, and hallucal metatarsal with prominent peroneal tubercle) indicate capabilities for leaping and for powerful grasping with an opposable hallux. Cantius was presumably primitive in having a relatively long ischium and much more distal inferior tibial tuberosity than most extant lemurs--traits suggesting that powerful extension of the thigh and flexion at the knee were important in its locomotion and posture. We interpret Cantius as an active arboreal quadruped with a propensity for leaping. The existence of this skeletal structure in one of the oldest primates of modern aspect suggests that it represents the primitive lemuriform morphology.     

Corpus callosum in sexually dimorphic and nondimorphic primates.

The midsagittal area and other morphological measures were taken on the corpus callosum of four different species of primate: Macaca mulatta, M. fascicularis, Callithrix jacchus, and Saguinus oedipus. The first two species are strongly dimorphic, whereas the New World forms show little dimorphism with regard to overall body size, canines, and brain weight. Neither total corpus callosal area (TOTALCC), or other parts of the corpus callosum (CC) showed any significant sexual dimorphism in any of the primate species sampled. Only in M. mulatta did a sexual dimorphism appear to be significant. In males of this species, the dorsoventral width of the splenium was larger than in females. In addition, the anterior commissure (ANTCOMM) evinced no sexual dimorphism in the different species. Brain weight was significantly dimorphic in only M. mulatta, and when ratio data were used to correct for brain weight, no significant differences were found in the corpus callosum. This is in contrast to Homo sapiens, where the relative size of the CC has been reported to be larger in females, and particularly so in the posterior, or splenial portion of the CC. Correlation coefficients were calculated for the various variables within each species. In general, most of the callosal measures are significantly inter-correlated, although the exact pattern varies for each species. Thus, unlike Homo sapiens, or pongids such as Gorilla and Pan, neither New nor Old World monkeys show any striking evidence for sexual dimorphism in the corpus callosum.     

Sex-based divergence in head shape and diet in the Eastern lubber grasshopper (Romalea microptera)

Biologists are becoming increasingly aware of sex-based differences in ecologically important traits (locomotor performance, feeding morphology, thermoregulatory behavior). Yet, the overwhelming majority of these studies have been performed on vertebrates, despite often striking examples of sexual size dimorphism among the insects. Here, I tested whether adult male and female Eastern lubber grasshoppers differ in size/shape and feeding ecology. The morphological data clearly showed sex-based differences in several aspects of head and body size, with females being significantly larger in all aspects. Moreover, the sexes also differed in two aspects of size-adjusted morphology: head width and pronotum width, with females having relatively wider heads and thoraxes than males. Multiple regression analysis indicated that width of consumed foliage was positively related to pronotum width and foliage thickness was positively related to pronotum width, head width, and size-adjusted head width. Females consumed wider and thicker foliage (primarily smooth cord grass, Spartina alterniflora) than males, which most frequently consumed the narrow-leafed forb hemp sesbania (Sesbania macrocarpa). Therefore, the sex-based differences in size and shape in this grasshopper are correlated with differences in consumed foliage shape.     

Immunoglobulin allotypes (Gm,Am, and Km) in non-human primates

The immunoglobulin (Ig) allotypes (Gm, Am, and Km systems) are the genetic markers of the human IgG1, IgG2, IgG3(Gm), IgA2(Am), and kappa light chain(Km). The Gm system, with 18 allotypes shows the greatest degree of polymorphism and we define two Am and three Km allotypes. In this review, we report all the results observed in non-human primates belonging to Hominoidea, Cercopithecoidea, Ceboidea, Lorisoidea, Lemuroidea, and Tupaoidea superfamilies (72 species and subspecies). They concern published data and new unpublished ones. The distribution of the human allotypes and their localization are reported, as well as discordant results observed in some cases with anti-allotype reagents of the same specificity (human and animal origin). Some allotypes are restricted to man. Hominoidea have the greatest number of Gm allotypes and the richest polymorphism. Relatively few allotypes have been found in Cercopithecoidea and Prosimians; most Platyrrhinian species have no allotype. The epitopic polymorphism has been interpreted in terms of evolution of Ig allotypes from primate to man and of the phylogenetic relationships of non-human primate species.     

Sexual differences in the anterior dentition in African primates

A study was made of ranges of variation of the anterior dentition of various African nonhuman primates. Comparisons of the dentitions were made between different species and sex differences within each species were determined. Among the nonhuman primate groups studied were: Gorilla gorilla gorilla, Pan troglodytes, Pan paniscus, Cercopithecus nictitans, Cercocebus albigena and Colobus badius. In monkeys the canine teeth of the males are considerably larger than those of the females. There are also considerable differences in size in the rest of the anterior dentition. In apes, and specifically only gorillas, distinct sex differences are only found in the maxillary canines. In the chimpanzees, sex differences in the dentition are much smaller and there is considerable overlap in the ranges of variation. There are no fundamental differences in the size of the rest of the anterior dentition in the apes. The present study shows that differences due to sex in the anterior dentition, excluding the canine, are not as great as has been considered. If we consider the fossil record of man, whose morphological complex includes a much reduced canine, the probability will be that sex differences in the rest of the dentition will be negligible. Given the fragmentary nature of the fossil record, it is, therefore, highly unlikely that the determination of the sex of any fossil hominid specimen can be accurately made based solely on the evidence of its dentition.     

Notharctine primates (Adapiformes) from the early to middle Eocene (Wasatchian-Bridgerian) of Wyoming: transitional species and the origins of Notharctus and Smilodectes

Notharctine adapiform primates are an abundant element of early (Wasatchian) and middle (Bridgerian) Eocene faunal assemblages from the western interior of North America. Early Eocene notharctine samples are dominated by Cantius with Pelycodus and Copelemur being much rarer and more restricted in their geographic distribution. Cantius is replaced in the middle Eocene by Notharctus and Smilodectes, both of which are common but less widespread, being best known from southwestern Wyoming. The origin of these two middle Eocene taxa has not been well understood, due to a lack of transitional Wasatchian-Bridgerian notharctine faunal samples or because known samples had not been adequately studied. Field work at South Pass in the Greater Green River Basin has produced a relatively large sample of earliest Bridgerian notharctines. Combining this sample with a large, but previously under-studied, sample of notharctines from the latest Wasatchian and earliest Bridgerian in the Wind River Basin has clarified the relationships among Notharctus,Smilodectes, and earlier occurring notharctines. Notharctus first appears in the latest Wasatchian (Wa7), represented by N. venticolus. Phylogenetic analysis supports a Notharctus clade that shares sister taxon status with Cantius nunienus and indicates that Notharctus arose through bifurcation of the lineage containing the last common ancestor of C. nunienus and Notharctus. The origins of Smilodectes are less clear. Phylogenetic analysis supports a clade consisting of Smilodectes and Copelemur, but the origins of both taxa are not established as yet. North American notharctines are typified by relatively low taxonomic diversity, but relatively high abundance and high dental morphological variation (disparity). These attributes are opposite to those of North American omomyids, reflecting differences in ecomorphospace between these two primate radiations.     

Multimale mating and absence of canine tooth dimorphism in woolly spider monkeys (Brachyteles arachnoides)

The relatively low degree of canine tooth dimorphism in Australopithecus afarensis has been used as “primary evidence” to support the concept of a mating system of monogamous pair-bonding and male provisioning. A recent field study of woolly spider monkeys shows that these large primates, which lack canine tooth (and body size) dimorphism, are characterized by apolygynous mating system. Male parental care of infants is absent in this species. These data support the view that a lack of canine tooth dimorphism in an anthropoid species does not necessarily imply either a monogamous, pair-bonded mating system or male parental care.     

Derived,still living cockroach genus Cariblattoides (Blattida: Blattellidae) from the Eocene sediments of Green River in Colorado,USA

Abstract Cariblattoides labandeirai sp.n. from the Eocene sediments of Green River in Colorado, USA bear only two plesiomorphies, but also several significant autapomorphies within the advanced and highly derived living cockroach genus. Thus, Cariblattoides with extant occurrence in the Caribbean and South America was historically common in the Nearctic, and represents important evidence for the occurrence of derived living genera of cockroaches ～50 Ma ago. Generally, the vast majority of living genera were absent during the Palaeocene, thus the diversification of most living cockroach lineages near the Palaeocene/Eocene boundary must have been extremely rapid. Females of living C. suave, the type species, have identical (sophisticated) coloration of pronotum, but the most related living taxa are C. piraiensis and C. fontesi from Brazil (supported by phylogenetical analysis).     

Comparison of four simple methods for estimating sexual dimorphism in fossils

Estimating sexual dimorphism in skeletal and dental features of fossil species is difficult when the sex of individuals cannot be reliably determined. Several different methods of estimating dimorphism in this situation have been suggested: extrapolation from coefficients of variation, division of a sample about the mean or median into two subsamples which are then treated as males and females, and finite mixture analysis (specifically for estimating the maximum dimorphism that could be present in a unimodal distribution). The accuracy of none of these methods has been thoroughly investigated and compared in a controlled manner. Such analysis is necessary because the accuracy of all methods is potentially affected by fluctuations in either sample size, sex ratio, or the magnitude of intrasexual variability. Computer modeling experiments show that the mean method is the least sensitive to fluctuations in these parameters and generally provides the best estimates of dimorphism. However, no method can accurately estimate low to moderate levels of dimorphism, particularly if intrasexual variability is high and sex ratios are skewed. © 1994 Wiley-Liss, Inc.     

New early Eocene anaptomorphine primate (Omomyidae) from the Washakie Basin,Wyoming, with comments on the phylogeny and paleobiology of anaptomorphines

Recent paleontological collecting in the Washakie Basin, southcentral Wyoming, has resulted in the recovery of over 100 specimens of omomyid primates from the lower Eocene Wasatch Formation. Much of what is known about anaptomorphine omomyids is based upon work in the Bighorn and Wind River Basins of Wyoming. This new sample documents greater taxonomic diversity of omomyids during the early Eocene and contributes to our understanding of the phylogeny and adaptations of some of these earliest North American primates. A new middle Wasatchian (Lysitean) anaptomorphine, Anemorhysis savagei, n. sp., is structurally intermediate between Teilhardina americana and other species of Anemorhysis and may be a sister group of other Anemorhysis and Trogolemur. Body size estimates for Anemorhysis, Tetonoides, Trogolemur, and Teilhardina americana indicate that these animals were extremely small, probably less than 50 grams. Analysis of relative shearing potential of lower molars of these taxa indicates that some were primarily insectivorous, some primarily frugivorous, and some may have been more mixed feeders. Anaptomorphines did not develop the extremes of molar specialization for frugivory or insectivory seen in extant prosimians. Incisor enlargement does not appear to be associated with specialization in either fruits or insects but may have been an adaptation for specialized grooming or food manipulation. © 1994 Wiley-Liss, Inc.     

The termites of Early Eocene Cambay amber, with the earliest record of the Termitidae (Isoptera)

The fauna of termites (Isoptera) preserved in Early Eocene amber from the Cambay Basin (Gujarat, India) are described and figured. Three new genera and four new species are recognized, all of them Neoisoptera – Parastylotermes krishnai Engel & Grimaldi, sp. n. (Stylotermitidae); Prostylotermes kamboja Engel & Grimaldi, gen. et sp. n. (Stylotermitidae?); Zophotermes Engel, gen. n., with Zophotermes ashoki Engel & Singh, sp. n. (Rhinotermitidae: Prorhinotermitinae); and Nanotermes isaacae Engel & Grimaldi, gen. et sp. n. (Termitidae: Termitinae?). Together these species represent the earliest Tertiary records of the Neoisoptera and the oldest definitive record of Termitidae, a family that comprises >75% of the living species of Isoptera. Interestingly, the affinities of the Cambay amber termites are with largely Laurasian lineages, in this regard paralleling relationships seen between the fauna of bees and some flies. Diversity of Neoisoptera in Indian amber may reflect origin of the amber deposit in Dipterocarpaceae forests formed at or near the paleoequator.     

Postsettlement growth of two estuarine crab species, Chasmagnathus granulata and Cyrtograpsus angulatus (Crustacea, Decapoda, Grapsidae): laboratory and field investigations

The estuarine grapsid crabs Chasmagnathus granulata and Cyrtograpsus angulatus belong to the most typical and dominant inhabitants of brackish coastal lagoons in southeastern South America. In a combined laboratory and field investigation of juvenile growth, we measured the increase in body size in these species under controlled conditions as well as in field experiments (in Mar Chiquita lagoon, Argentina), seasonal changes in size frequency distribution of a natural population, and growth related changes in selected morphometric traits of male and female juveniles (relations between carapace width, carapace length, propodus height and length of the cheliped, and pleon width). At 24°C, Cy. angulatus grew faster than Ch. granulata; it reached the crab-9 instar (C9; 13 mm carapace width) after 92 days, while Ch. granulata required 107 days to reach the C8 instar (7.4 mm). At 12°C, growth ceased in both species. The pleon begins to show sexual differences in the C5 (Cy. angulatus) and C8 instar (Ch. granulata), respectively, while the chelae differentiate earlier in Ch. granulata than in Cy. angulatus (in C4 vs C6). In the field, growth was maximal in summer, and was generally faster than in laboratory cultures. However, there is great individual variability in size (about 25% even in the first crab instar) and in size increments at ecdysis, increasing throughout juvenile growth. Our data indicate that, in the field, small-scale and short-term variations in feeding conditions, temperature, and salinity account for an extremely high degree of variability in the absolute and relative rates of growth as well as in the time to sexual differentiation. Received in revised form: 20 September 2001 Electronic Publication