Dental microwear texture analysis of two families of subfossil lemurs from Madagascar.

This study employs dental microwear texture analysis to reconstruct the diets of two families of subfossil lemurs from Madagascar, the archaeolemurids and megaladapids. This technique is based on three-dimensional surface measurements utilizing a white-light confocal profiler and scale-sensitive fractal analysis. Data were recorded for six texture variables previously used successfully to distinguish between living primates with known dietary differences. Statistical analyses revealed that the archaeolemurids and megaladapids have overlapping microwear texture signatures, suggesting that the two families occasionally depended on resources with similar mechanical properties. Even so, moderate variation in most attributes is evident, and results suggest potential differences in the foods consumed by the two families. The microwear pattern for the megaladapids indicates a preference for tougher foods, such as many leaves, while that of the archaeolemurids is consistent with the consumption of harder foods. The results also indicate some intraspecific differences among taxa within each family. This evidence suggests that the archaeolemurids and megaladapids, like many living primates, likely consumed a variety of food types.

A reconstruction of the Vienna skull of Hadropithecus stenognathus.

Franz Sikora found the first specimen and type of the recently extinct Hadropithecus stenognathus in Madagascar in 1899 and sent it to Ludwig Lorenz von Liburnau of the Austrian Imperial Academy of Sciences. Later, he sent several more specimens including a subadult skull that was described by Lorenz von Liburnau in 1902. In 2003, some of us excavated at the locality and found more specimens belonging to this species, including much of a subadult skeleton. Two frontal fragments were found, and these, together with most of the postcranial bones, belong to the skull. CT scans of the skull and other jaw fragments were made in Vienna and those of the frontal fragments at Penn State University. The two fragments have been reunited with the skull in silico, and broken parts from one side of the skull have been replaced virtually by mirror-imaged complete parts from the other side. The parts of the jaw of another individual of a slightly younger dental age have also been reconstructed virtually from CT scans with mirror imaging and by using the maxillary teeth and temporomandibular joints as a guide to finish the reconstruction. Apart from forming a virtual skull for biomechanical and systematic analysis, we were also able to make a virtual endocast. Missing anterior pieces were reconstructed by using part of an endocast of the related Archaeolemur majori. The volume is 115 ml. Hadropithecus and Archaeolemur seem to have had relatively large brains compared with the other large-bodied subfossil lemurs.

New discoveries of skeletal elements of Hadropithecus stenognathus from Andrahomana Cave, southeastern Madagascar.

Remains of what appears to be a single, subadult Hadropithecus stenognathus were recovered from a previously unexcavated site at Andrahomana Cave (southeastern Madagascar). Specimens found comprise isolated teeth and cranial fragments (including the frontal processes of the orbits), as well as a partial postcranial skeleton. They include the first associated fore- and hind-limb bones, confirming the hind-limb attributions made by Godfrey and co-workers in 1997, and refuting earlier attributions by Lamberton in 1937/1938. Of particular interest here are the previously unknown elements, including a sacrum, other vertebrae and ribs, some hand bones, and the distal epiphysis of a femur. We briefly discuss the functional implications of previously unknown elements. Hadropithecus displayed a combination of characters reminiscent of lemurids, others more like those of the larger-bodied Old World monkeys, and still others more like those of African apes. Yet other characteristics appear unique. Lemurid-like postcranial characteristics may be primitive for the Archaeolemuridae. Hadropithecus diverges from the Lemuridae in the direction of Archaeolemur, but more extremely so. Thus, for example, it exhibits a stronger reduction in the size of the hamulus of the hamate, greater anteroposterior compression of the femoral shaft, and greater asymmetry of the femoral condyles. Nothing in its postcranial anatomy signals a close relationship to either the Indriidae or the Palaeopropithecidae.

The hands and feet of Archaeolemur: metrical affinities and their functional significance.

Recent expeditions to Madagascar have recovered abundant skeletal remains of Archaeolemur, one of the so-called "monkey lemurs" known from Holocene deposits scattered across the island. These new skeletons are sufficiently complete to permit reassembly of entire hands and feet--postcranial elements crucial to drawing inferences about substrate preferences and positional behavior. Univariate and multivariate analysis of intrinsic hand and foot proportions, phalangeal indices, relative pollex and hallux lengths, phalangeal curvature, and distal phalangeal shape reveal a highly derived and unique morphology for an extinct strepsirrhine that diverges dramatically from that of living lemurs and converges in some respects on that of Old World monkeys (e.g., mandrills, but not baboons or geladas). The hands and feet of Archaeolemur are relatively short (extremely so relative to body size); the carpus and tarsus are both "long" relative to total hand and foot lengths, respectively; phalangeal indices of both the hands and feet are low; both pollex and hallux are reduced; the apical tufts of the distal phalanges are very broad; and the proximal phalanges are slightly curved (but more so than in baboons). Overall grasping capabilities may have been compromised to some extent, and dexterous handling of small objects seems improbable. Deliberate and noncursorial quadrupedalism was most likely practiced on both the ground and in the trees. A flexible locomotor repertoire in conjunction with a eurytopic trophic adaptation allowed Archaeolemur to inhabit much of Madagascar and may explain why it was one of the latest surviving subfossil lemurs.

Ontogenetic correlates of diet in Malagasy lemurs.

There is a well-documented relationship between development and other life-history parameters among anthropoid primates. Smaller-bodied anthropoids tend to mature more rapidly than do larger-bodied species. Among anthropoids of similar body sizes, folivorous species tend to grow and mature more quickly than do frugivorous species, thus attaining adult body size at an earlier age. This pattern conforms to the expectations of Janson and van Schaik's "ecological risk aversion hypothesis," which predicts that rates of growth and maturation should vary in inverse relation to the intensity of intraspecific feeding competition. According to the ecological risk aversion hypothesis (RAH), species experiencing high intraspecific feeding competition will grow and mature slowly to reduce the risk of mortality due to food shortages. Species experiencing low levels of intraspecific feeding competition will shorten the juvenile period to reduce the overall duration of this high-risk portion of the life cycle. This paper focuses on development and maturation in lemurs. We show that folivorous lemurs (such as indriids) grow and mature more slowly than like-sized frugivorous lemurs (e.g., most lemurids), but tend to exhibit faster dental development. Their dental developmental schedules are accelerated on an absolute scale, relative to craniofacial growth, and relative to particular life-history landmarks, such as weaning. Dental development has a strong phylogenetic component: even those lemurids that consume substantial amounts of foliage have slower dental development than those indriids that consume substantial amounts of fruit. Implications of these results for the RAH are discussed, and an explanation for this hypothesis' failure to predict lemur growth schedules is offered. We propose that the differing developmental schedules of folivorous and frugivorous lemurs may reflect different solutions to the ecological problem of environmental instability: some rely on a strategy of low maternal input and slow returns, while others rely on a strategy of high maternal input and fast returns.

Teeth, brains, and primate life histories.

This paper explores the correlates of variation in dental development across the order Primates. We are particularly interested in how 1) dental precocity (percentage of total postcanine primary and secondary teeth that have erupted at selected absolute ages and life cycle stages) and 2) dental endowment at weaning (percentage of adult postcanine occlusal area that is present at weaning) are related to variation in body or brain size and diet in primates. We ask whether folivores have more accelerated dental schedules than do like-sized frugivores, and if so, to what extent this is part and parcel of a general pattern of acceleration of life histories in more folivorous taxa. What is the adaptive significance of variation in dental eruption schedules across the order Primates? We show that folivorous primate species tend to exhibit more rapid dental development (on an absolute scale) than comparably sized frugivores, and their dental development tends to be more advanced at weaning. Our data affirm an important role for brain (rather than body) size as a predictor of both absolute and relative dental development. Tests of alternative dietary hypotheses offer the strongest support for the foraging independence and food processing hypotheses.

Adaptive and phylogenetic significance of ontogenetic sequences in Archaeolemur, subfossil lemur from Madagascar.

Among the best known of recently extinct Malagasy lemurs is Archaeolemur, which is represented by many hundreds of specimens. The phylogenetic affinities of this taxon are unclear, especially in light of recent preliminary analysis of ancient DNA which does not support its previously accepted close relationship with the living Indridae. We examined the nearly complete skeletons of two adults and one juvenile and other less complete specimens to reconstruct aspects of the ontogeny of Archaeolemur. To compare the development of Archaeolemur to that of living strepsirrhines we collected data on Propithecus verreauxi, Eulemur fulvus, and Lemur catta. Additionally, because Archaeolemur exhibits some morphological convergences with distantly related papionins, we tested for convergence in the developmental patterns of Archaeolemur and Macaca fascicularis. Data include the status of tooth eruption, craniofacial sutural closure, and postcranial epiphyseal fusion, as well as linear measurements. We used discriminant function analysis and other tools to explore ontogenetic similarities and differences. The adaptive and phylogenetic significance of ontogenetic information is discussed. Our analysis shows that Archaeolemur displays a clear strepsirrhine pattern of development with only minor macaque convergences. Among the Strepsirrhini, Archaeolemur is slightly more similar developmentally to E. fulvus and L. catta than to P. verreauxi. Some of the distinctive features of the ontogeny of Archaeolemur may be related to diet, while others bear apparent testimony to a relatively rapid absolute pace of growth and development.

Is follicular atresia biphasic?

OBJECTIVE: To examine the rate of human follicular depletion and the interpretation of curved scatters on log-linear plots. DESIGN: Four mathematical models were tested with use of data drawn from published autopsy studies and histologic analyses of ovaries. SETTING: None. PATIENT(S): None. INTERVENTION(S): None. MAIN OUTCOME MEASURE(S): None. RESULT(S): Human oocyte depletion data do not support the inference of a biphasic follicular atresia. On original measurement scales there is no perturbation in the data between ages 37 and 40, and the instantaneous rate of follicle loss is lower after age 40 than ever before. CONCLUSION(S): There is no abrupt increase in the "rate" of follicular atresia that corresponds with a drop in fecundability or an increase in risk of chromosomal abnormalities at approximately age 38. The apparent abrupt increase in rate of follicular depletion is an artifact of log-linear transformation.

Reappraisal of the postcranium of Hadropithecus (Primates, Indroidea).

Hadropithecus stenognathus (Lorenz von Liburnau [1899] Anz. Akad. Wiss. Wien 36:255-257), a giant extinct lemur from Madagascar, has been reconstructed as primarily terrestrial and probably cursorial on the basis of its postcranial anatomy, especially long bone gracility and interlimb proportions. We show here that aspects of this reconstruction are almost certainly incorrect. Hindlimb bones of Archaeolemur have been misattributed to Hadropithecus, and new hindlimb allocations (including newly recognized elements such as the calcaneus) indicate that Hadropithecus had a robust body build and lacked osteological specializations for cursoriality. We review the evidence for the existence of "Bradylemur" and offer a view of archaeolemurid positional behavior that includes terrestrial and arboreal components. Body size and limb proportions of Hadropithecus are reassessed in light of our new allocations.

Phalangeal curvature and positional behavior in extinct sloth lemurs (Primates, Palaeopropithecidae).

Recent paleontological discoveries in Madagascar document the existence of a diverse clade of palaeopropithecids or "sloth lemurs": Mesopropithecus (three species), Babakotia (one species), Palaeopropithecus (three species), and Archaeoindris (one species). This mini-radiation of now extinct ("subfossil") lemurs is most closely related to the living indrids (Indri, Propithecus, and Avahi). Whereas the extant indrids are known for their leaping acrobatics, the palaeopropithecids (except perhaps for the poorly known giant Archaeoindris) exhibit numerous skeletal design features for antipronograde or suspensory positional behaviors (e.g., high intermembral indices and mobile joints). Here we analyze the curvature of the proximal phalanges of the hands and feet. Computed as the included angle (theta), phalangeal curvature develops in response to mechanical use and is known to be correlated in primates with hand and foot function in different habitats; terrestrial species have straighter phalanges than their arboreal counterparts, and highly suspensory forms such as the orangutan possess the most curved phalanges. Sloth lemurs as a group are characterized by very curved proximal phalanges, exceeding those seen in spider monkeys and siamangs, and approaching that of orangutans. Indrids have curvatures roughly half that of sloth lemurs, and the more terrestrial, subfossil Archaeolemur possesses the least curved phalanges of all the indroids. Taken together with many other derived aspects of their postcranial anatomy, phalangeal curvature indicates that the sloth lemurs are one of the most suspensory clades of mammals ever to evolve.

Paradox of peramorphic paedomorphosis: heterochrony and human evolution.

This paper reviews Gould's clock model for heterochronic processes and uses that model to develop simple matrix representations of growth and shape change. Matrix representations of growth and development provide a common formulation for all heterochronic processes. In particular, we show how neoteny can be diagnosed using such a matrix approach. The literature is rife with contradictory representations of how neoteny affects growth allometries and the timing of developmental events, and therefore of the role of neoteny in human evolution. Through the use of multivariate models, we explore these relationships and the internal consistency of opposing views. Gould's neoteny hypothesis for human evolution has been criticized for a number of reasons. Humans do not grow slowly. The slopes of our growth allometries show no common pattern of change vis-à-vis those of our closest relatives. Humans prolong rather than reduce rates of growth and development of body parts; the brain, for example, ceases growing later in humans than in apes, but during this prolonged period of early ontogeny, it grows at a rapid pace. This paper evaluates Gould's hypothesis and its critiques by focusing on particular questions. Does neoteny imply slow growth? Does it imply a unidirectional change in the rates of growth of traits? Under neoteny, should the brain cease growing in ancestor and descendant at the same age? Does prolongation of phases of growth and development confute neoteny? On the other hand, is paedomorphosis an inevitable consequence of prolonged growth and development? We show that, for all of these questions, the answer is no.

Subfossil Indri indri from the Ankarana Massif of northern Madagascar.

Subfossil specimens of Indri indri have been recovered recently from the Ankarana Massif cave system in the far north of Madagascar. Taken together with material from the central highland site of Ampasambazimba, the range of this species appears to have once included much of the northern half of the island and to have extended north and west beyond the eastern rainforest (not unlike Hapalemur simus). It is probable that forest corridors connected the subfossil localities to the current range at some time in the past. Climatic desiccation (fluctuating or long-term) and/or human degradation of the environment may have created the disjunct distributions of living and subfossil I. indri. It is also possible that I. indri once included populations or subspecies that were better adapted to dry forest, woodland, or mosaic environments, habitats very different from those occupied by their living conspecifics. Such adaptive diversity would have been similar to that of Propithecus diadema which today has subspecies in the montane forests and one (P.d. perrieri) in the dry forests of the northeast. These discoveries add new information on range extensions to the distributional database for the primates of Madagascar, and illustrate the piecemeal process of their extinctions.

Limb joint surface areas and their ratios in Malagasy lemurs and other mammals.

Surface areas of humeral and femoral heads scale largely as a function of body size. However, differences in the relative sizes of these articular surfaces are correlated with differential joint mobility and force transmission through fore- and hindlimbs. They can therefore assist interpretation of the positional behavior of extinct species. In this paper, we document variation in ratios of humeral head surface area to femoral head surface area among extant primates and other mammals. We then examine a group of extinct primates: the subfossil lemurs of Madagascar. Many Malagasy lemurs, including some giant extinct species with very long forelimbs and short hindlimbs, have relatively small humeral heads and large femoral heads. We explore the adaptive implications of this pattern.

Sexual dimorphism in large-bodied primates: the case of the subfossil lemurs.

Large body size has evolved repeatedly in the order Primates, not merely among anthropoids but also among prosimians. Whereas high degrees of sexual size dimorphism characterize many of the large-bodied anthropoids, this is not the case for extinct large-bodied lemurs. This paper uses finite mixture analysis and other techniques to ascertain just how much skull length dimorphism might be embedded in the generally unimodal distributions of skull lengths of giant extinct lemurs from single localities, and then compares these results with known skull length dimorphisms in extant lemurs and large-bodied catarrhines. We show that low levels of skull length sexual dimorphism (or none at all) characterize subfossil lemurs, and we explore several possible explanations for this phenomenon. Traditional explanations of sexual size dimorphism generally focus on body size or mating systems. These are not sufficient to explain the variation in sexual dimorphism that can be observed in the order Primates.

Phylogenetic and functional affinities of Babakotia (primates), a fossil lemur from northern Madagascar.

Recent paleontological expeditions to the Ankarana range of northern Madagascar have recovered the partial remains of four individuals of a newly recognized extinct lemur, Babakotia radofilai. Craniodental and postcranial material serve to identify Babakotia as a member of the palaeopropithecids (also including the extinct genera Palaeopropithecus, Archaeoindris, and Mesopropithecus). Living indrids form the sister group to this fossil clade. The postcranial anatomy indicates that Babakotia was a medium-sized (approximately 15 kg) indroid whose inferred positional behaviors were primarily slow climbing and hanging. Although it is probable that a leaping component typified the ancestral positional repertoire of all Malagasy lemurs, the mosaic nature of the locomotor skeleton of Babakotia further suggests that vertical climbing and hang-feeding rather than ricochetal leaping were primitive for indrids and palaeopropithecids and that the dramatic saltatory adaptations of the living indrids postdate the divergence of these two lineages.

Size, space, and adaptation in some subfossil lemurs from Madagascar.

We examine several explanations for the geographic pattern of body size variation exhibited by the subfossil lemur Archaeolemur. Part and partial correlation analysis and multiple regression analysis are applied in a stepwise, hierarchical fashion to help to determine variable interdependencies. Variance in site means for body size is best explained by the richness of the plant community and by several correlated climatic variables (bioclimatic zone and mean annual rainfall). Body size differentiation in Archaeolemur roughly mirrors patterns observed among many other Malagasy lemur species and subspecies groups. This consistency alone suggests that common ecological factors have strongly affected size differentiation in lemurs, most probably (as suggested by our correlation analyses) by uniformly influencing the productivity of their niches. Smaller individuals tend to inhabit arid regions, and larger individuals tend to inhabit wetter regions. The interplay between selective differentiation and allopatric speciation appears to have yielded the concordant pattern of size variation observed in Malagasy lemurs.

Revision of Hapalemur (Prohapalemur) gallieni (Standing 1905).

Cranial and mandibular remains of the subfossil lemur Hapalemur (Prohapalemur) gallieni (Standing 1905) from Ampasambazimba in central Madagascar are reexamined and are shown here to belong to the rare but perhaps still extant species Hapalemur simus. Past descriptive errors and too limited comparisons have hampered previous taxonomic assessments of the three mandibular rami, two partial maxillae, and one partial cranium ascribed to H. (Prohapalemur) gallieni. These and other subfossil H. simus recently discovered at the Grotte d'Andrafiabe, Ankarana Massif (in the very northernmost part of Madagascar), and at the Grottes d'Anjohibe, near Mahajanga (northwest coast), show that H. simus was once extensively distributed on Madagascar. Records associated with 9 additional individuals in museum collections show that, at least until about 100 years ago, H. simus occupied much of the humid eastern forests of Madagascar, from the forests east of Fianarantsoa (where it lives today if it has not very recently become extinct) to as far north as "Passumbée' (Ampasimbe) which was located in the region of the Bay of Antongil. This paper reviews what is known of that distribution and the reasons for the taxonomic confusion surrounding the large species of Hapalemur.