Selected aspects of Lemur variegatus reproductive biology

Results from data collected during the 1978–1979 breeding season on the reproduction of Lemur variegatus at the San Diego Zoo provide information which generally supports previously published reports on this species. Comparison of selected results from these data to a larger data base of which they are a part makes it possible to resolve some of the discrepancies between reports. Certain aspects of the reproductive biology of this species may then be generally characterized with confidence: The onset of seasonal breeding as evidenced by estrous behavior begins as early as mid-December in the northern hemisphere and may continue through March; genital changes associated with estrus in females last 9.85 ± 1.67 days (± SD); female receptivity occurs 7.0 ± 1.53 days after the onset of these genital changes and lasts 12-24 hours, during which breeding occurs; gestation averages 99.47 ± 4.19 days; the peak birth season is April–May; litters normally contain two to three offspring, with full-term neonates weighing an average of 104.63 ± 19.10 grams. In addition, L variegatus appears to be highly resistant to the impact of captivity on both its reproductive physiology and behavior, as indicated by the 100% breeding success of the diversely reared and managed groups of study animals.     

The Behavior of Lemur variegatus Kerr 1792

This paper reports the social behavior of two groups of captive Lemur variegates. An intensive three-month study provided baseline data. This was supplemented by two years of follow-up observations. Various components of the captive behavioral repertoire are described. Data on feeding behavior, vocalizations, grooming, agonistic interactions, sexual behavior and infant development were collected.     

The significance of primate paleontology for anthropological studies

The correct use of taxonomic names must become widespread if a clear understanding of primate paleontology is to exist among anthropologists. Physical anthropologists are urged to acquire genuine competence in the paleontology, systematics, and taxonomy of mammals. Examples are given of improper taxonomic procedure and of the perpetuation of invalid names. The need for a stable and correct nomenclature of the primates is emphasized. The importance of examining actual fossil specimens is stressed. The taxonomy of the Hominoidea is discussed and a summary of invalid names in current use is given. Recently discovered fossils from Oligocene strata in the Egyptian Fayum are figured and the pertinence of these to the origins of higher primates is suggested.     

Toward a molecular paleontology of primate genomes

KpnI restriction of anthropoid primate DNAs, from a New World monkey to man, releases a series of segments that are remarkable among all of the alphoid DNAs in the constancy of their relative amounts in the various primate genomes, in their long-range organization, and in their internal sequence structure. These segments are labeled the KpnI A, B, C and D segments. Cross-hybridization analysis by Southern filter-transfer hybridization indicates that the KpnI segments represent separate and distinct families of alphoid DNAs. These families are termed the KpnI A, B, C and D families of alphoid sequences, of which only the KpnI A and B families were studied in detail here. - Evidence is presented suggesting that the KpnI segments do not exist as long, tandemly repeated sequences in the primate genome: rather, they may occur interspersed among other, perhaps nonalphoid sequences. From the stained gel patterns and from Southern filter-transfer hybridization experiments, the KpnI families appear to be absent from the genomes of the two prosimians studied - the galago and the black lemur. The KpnI A and B families are found among all of the anthropoid primates, including the New World capuchin monkey. The KpnI C family was detected in the genomes of the Old World anthropoid primates whereas the KpnI D family was detected only among the great apes and man. - The results are in accord with the observation (Musich et al., 1980) that with the continued evolutionary development of the primate Order, there has been a parallel trend toward an increased number and variety of alphoid DNA sequences. The properties of the KpnI families suggest that these sequences, unique among the alphoid DNAs, have been conservatively maintained throughout primate phylogeny and that they are among the most ancient of all primate DNAs.     

Toward a molecular paleontology of primate genomes

Families of related, but nonidentical repetitive DNA sequences, termed the alphoid DNAs, have been identified and characterized in representative species from seven major primate Families. The sequences appear as old as the primate Order itself: they are found in a prosimian (lemur), in a New World monkey, and in all Old World primates examined, including man. The alphoid DNAs are uniquely primate sequences and they may represent the most abundant repetitive DNAs in the primate genome. — A classification scheme for two major families of alphoid DNAs is proposed that is based upon restriction enzyme analysis and Southern blotting with radioactive probes prepared from component DNA (Maio, 1971) and from the human EcoRI dimer sequences (Manuelidis, 1976). The family of alphoid DNAs that hybridizes readily with component is termed the HindIII family of alphoid DNAs. This family shows an almost universal distribution among present-day primates. The family of DNA sequences that hybridizes readily with the human EcoRI dimer probe is termed the EcoRI dimer family of alphoid DNAs. This family may be restricted to the great apes and man. The two probes permitted the discrimination of different, but related alphoid families in present-day primates. Multiple alphoid sequence families are found within the genomes of individual primates and the major primate taxa can be characterized by the representations of the various alphoid DNAs within their genomes. — An Appendix is presented (Brown et al., 1981) indicating that competition hybridization effects may influence the autoradiographic banding patterns, and hence, the interpretations of Southern filter-transfer hybridizations when dealing with related repetitive sequences such as the alphoid DNAs that are present in abundance in eukaryotic genomes.     

Aspects of reproduction in ruffed lemurs (Lemur variegatus).

Results of breeding of ruffed lemurs (Lemur variegatus) at the Duke Primate Facility provide information concerning estrous cycle, sexual behavior, age of first conception, gestation period, parturition, litter size. L. variegatus differs from other Lemur species in these respects.     

Middle Eocene primate tarsals from China: implications for haplorhine evolution

We describe tarsal remains of primates recovered from the Middle Eocene (approximately 45 mya) Shanghuang fissures in southern Jiangsu Province, China. These tarsals document the existence of four higher-level taxa of haplorhine primates and at least two adapid species. The meager and poorly preserved adapid material exhibits some similarities to European adapines like Adapis. The haplorhine primates are divided into two major groups: a "prosimian group" consisting of Tarsiidae and an unnamed group that is anatomically similar to Omomyidae; and an "anthropoid group" consisting of Eosimiidae and an unnamed group of protoanthropoids. The anthropoid tarsals are morphologically transitional between omomyids (or primitive haplorhines) and extant telanthropoids, providing the first postcranial evidence for primates which bridge the prosimian-anthropoid gap. All of the haplorhines are extremely small (most are between 50-100 g), and the deposits contain the smallest euprimates ever documented. The uniqueness of this fauna is further highlighted by the fact that no modern primate community contains as many tiny primates as does the fauna from Shanghuang.     

Prosimian hemoglobins. III. The primary structures of the duplicated alpha-globin chains of Lemur variegatus

The amino acid sequences of the alpha chains of hemoglobins purified from Lemur variegatus erythrocytes have been determined. The sequences were determined primarily from peptides generated from treatment of the isolated alpha chains with cyanogen bromide or warm formic acid. The ordering of the peptides from both alpha globins was based on the homology between lemur hemoglobins and those of other primates. The genetic difference at position 15 (Asn vs. Lys) explains the phenotypic characteristic of two hemoglobin species during alkaline electrophoresis. The function of certain residues is discussed in the context of other known sequences. The dispersion of the amino acid changes noted in lemur species falls mostly within the first 75 residues of the alpha chain (exons 1 and 2). The extent of divergence of the L. variegatus alpha-globin chains from the Lemur fulvus alpha globin is similar to that seen for the beta-globin chains of these species. This degree of separation (11-16 residues) is consistent with an extended period of independent evolution by these congeneric species after their divergence.     

Urinary estrogens during pregnancy of the ruffed lemur (Lemur variegatus)

Although estradiol-17 beta (E2) induces premature regression of the corpus luteum (CL), its role in spontaneous luteolysis which occurs at the end of the nonfertile cycle has not been demonstrated. We compared the effects of an estrogen antagonist on E2-induced and spontaneous luteolysis by administering clomiphene (10 mg/day) to cynomolgus macaques during the luteal phase in the presence and absence of exogenous E2 (supplied by subcutaneous Silastic implants). Other animals received either vehicle or E2 implants. Luteal function was assessed by progesterone concentrations and luteal phase length. Clomiphene maintained normal luteal function in the presence of luteolytic levels of E2 in five of six monkeys. However, clomiphene alone did not prolong luteal function beyond that observed in monkeys receiving vehicle. To assess the direct effect of clomiphene on the CL, we incubated monkey luteal cells with human chorionic gonadotropin and clomiphene, E2, or clomiphene plus E2. Clomiphene (1500 ng/ml) alone and E2 (1000 ng/ml) alone significantly (P less than 0.05) inhibited progestin production. Clomiphene and E2 together depressed progestin production to an even greater extent. The data suggest that the mechanisms involved in E2-induced and spontaneous luteolysis differ.     

Ramapithecus and Sivapithecus from China: Some implications for higher primate evolution

The pattern of overall dental dimensions in over 900 teeth of ramapithecines from Lufeng in China is examined using frequency distribution histograms and fitted normal curves, and compared with data for extant hominoids. A prior study has demonstrated unequivocally that at least two groups of animals must have existed at Lufeng [Wu and Oxnard, 1983; Oxnard, 1983a]. The present investigation confirms this finding in more detail. In addition it shows that one fossil group possesses smaller teeth with a lesser degree of sexual dimorphism and approximately equal numbers of adult males and females, and the other possesses larger teeth with a rather larger degree of sexual dimorphism and a female-male ratio that may have approximated from as low as 2:1 to as high as 4:1. Comparisons of patterns of difference along the tooth row demonstrate that both these forms differ from modern apes in their sexual dimorphism, the smaller form being more like humans than the larger, which is more like apes, especially orangutans. Comparisons of the areas of the canine teeth with each of the other functional segments of the tooth row again show that the smaller form is basically similar to modern humans and that the larger resembles extant great apes. Comparisons of other functional dental areas seem to relate to dietary and masticatory functions. Thus the cutting areas are large relative to the chewing areas in omnivorous humans, whereas in the essentially vegetarian great apes this ratio is smaller. The smaller fossil resembles the human condition and may have been somewhat omnivorous; the larger one more resembles the apes and may have been somewhat more vegetarian. However, these comparisons also show that the way in which the larger form resembles the apes is associated with special development of the canines, which is different from that in any modern ape. Comparisons show that the canines in the larger form project far beyond the normal line of tooth crowns. Finally, comparisons show that canine sexual dimorphism in height is marked in the larger form. Neither of these last two features is true of the smaller fossil. These findings have implications for our understanding of the evolution of early pongids and hominids, and for the evolution of primate sexual dimorphisms and dental mechanisms.     

Karyotype abnormalities in two primate species, Pygathrix nemaeus and Lemur coronatus.

The karyotypes of 7 douc langurs (Pygathrix nemaeus) and 3 crowned lemurs (Lemur coronatus) were examined. Abnormalities in 23.5% of the karyotypes of 1 male douc langur were associated with a history of fathering stillborns and abortuses (38%). Karyotype analysis of an apparently normal female lemur revealed three differing karyotypes, one normal and two abnormal.     

Functional implications of primate enamel thickness.

Recent evolutionary interpretations of Hominoidea have postulated functional relationships between tooth form, diet and masticatory biomechanics. A major consideration is the durability of the tooth under certain dietary conditions. Teeth with low cusps and thicker enamel are able to withstand heavy mastication of abrasive food bolus for a longer period. When comparisons are made between species of higher primates the variables of tooth size, cusp morphology, and enamel thickness appear to be related but until now no systematic analysis has been made to determine the functional relevance of several dental dimensions. This study provides data gained from comparisons of dentition of nine species of primates. Histological sections were made of the post canine teeth and 21 dimensions were compared. The relevant dimensions identified serve to withstand dental wear. The distribution of thicker enamel corresponded to the observed wear planes. Humans had thicker enamel than pongids while the macaque had the thinnest. These preliminary results tend to support theories which explain low, thick, enameled cusps in hominids.     

Functional morphology of cercopithecoid primate metacarpals

The primate fossil record suggests that terrestriality was more common in the past than it is today, particularly among cercopithecoid primates. Whether or not a fossil primate habitually preferred terrestrial substrates has typically been inferred from its forelimb anatomy. Because extant large-bodied terrestrial cercopithecine monkeys utilize digitigrade hand postures during locomotion, being able to identify if a fossil primate habitually adopted digitigrade postures would be particularly revealing of terrestriality in this group. This paper examines the functional morphology of metacarpals in order to identify osteological correlates of digitigrade versus palmigrade hand postures. Linear measurements were obtained from 324 individuals belonging to digitigrade and palmigrade cercopithecoid species and comparisons were made between hand posture groups. Digitigrade taxa have shorter metacarpals, relative to both body mass and humerus length, than palmigrade taxa. Also, digitigrade taxa tend to have metacarpals with smaller dorsoventral diameters, relative to the product of body mass and metacarpal length, compared to palmigrade taxa. The size and shape of the metacarpal heads do not significantly differ between hand posture groups. Multivariate analyses suggest that metacarpal shape can only weakly discriminate between hand posture groups. In general, while there are some morphological differences in the metacarpals between hand posture groups, similarities also exist that are likely related to the fact that even digitigrade cercopithecoids can adopt palmigrade hand postures in different situations (e.g., terrestrial running, arboreal locomotion), and/or that the functional demands of different hand postures are not reflected in all aspects of metacarpal morphology. Therefore, the lack of identifiable adaptations for specific hand postures in extant cercopithecoids makes it difficult to determine a preference for specific habitats from fossil primate hand bones.     

A complex sensory organ in the nose skin of the prosimian primate Lemur catta

Most mammals have nose tips covered by glabrous skin, a labronasal area, or rhinarium. The surface of the rhinarium of Lemur catta has a dermatoglyphic pattern consisting of epidermal domes. Below the domes, epidermal pegs dip down into the dermis. In and below the tip of the epidermal peg, a complex sensory organ is found. It consists of an association of innervated Merkel cells, lamellate (Pacini‐like) bodies with a central nerve, and a ring of unmyelinated nerve endings in the epidermis. The Merkel cells are situated basally in the epidermis and the lamellated bodies just below the epidermis. The unmyelinated nerve endings related to the organ ascend in a circle straight through the epidermis ending below the corneal layer. From these nerve terminals, horizontal spikes enter the keratinocytes. The three components occur together forming an organ and are innervated from a common nerve plexus. The morphology of the complex sensory organ of the lemur shares most crucial components with Eimer's organs in moles, echidna, and platypus, while some structures are lacking, for example, the specific central pillar of keratinocytes, the cuticular cap, and a central unmyelinated fiber. The presence of the essentials of an Eimer's organ in many mammals suggests that a wider definition is motivated. J. Morphol. 276:649–656, 2015. © 2015 Wiley Periodicals, Inc.     

The ear ossicles and the evolution of the primate ear: A biomechanical approach

From a morphometric viewpoint the variability of human and other primate ear ossicles appears to be suitable for the study of taxonomic and phylogenetic distinction among Primates. It may also be of interest to determine whether they are useful to show differences in the perception of sound from the environment and from conspecifics. The energy transmitted through the ossicles is mantained by the action of different leverages. These modify the action of the ossicles from relatively wide, low energy, movements of the hammer to the smaller, high energy, movements of the stirrup. It seems that the pongid type of ossicle leverage combination saves more energy, possibly with a certain loss of subtle information, but this may be more useful in the wild than decoding voice modulation. The human type leverage, being less demultiplied, may produce a major loss of energy but, perhaps, a more precise conservation of sound information useful for speech communication.