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Enamel microstructure in Lemuridae (Mammalia, Primates): assessment of variability.

This study describes the molar enamel microstructure of seven lemurid primates: Hapalemur griseus, Varecia variegata, Lemur catta, Lemur macaco, Lemur fulvus rufus, Lemur fulvus fulvus, and Lemur fulvus albifrons. Contrary to earlier accounts, which reported little or no prism decussation in lemurid enamel, both Lemur and Varecia molars contain a prominent inner layer of decussating prisms (Hunter-Schreger bands), in addition to an outer radial prism layer, and a thin, nonprismatic enamel surface layer. In contrast, Hapalemur enamel consists entirely of radial and, near the surface, nonprismatic enamel. In addition, for all species, prism packing patterns differ according to depth from the tooth surface, and for all species but Varecia (which also has the thinnest enamel of any lemurid), average prism area increases from the enamel-dentine junction to the surface; this may be a developmental solution to the problem of accommodating a larger outer surface area with enamel deposited from a fixed number of cells. Finally, contradicting some previous reports, Pattern 1 prisms predominate only in the most superficial prismatic enamel. In the deeper enamel, prism cross-sections include both closed (Pattern 1) and arc-shaped (Pattern 2 or, most commonly, Pattern 3). This sequence of depth-related pattern change is repeated in all taxa. It should also be emphasized that all taxa can exhibit all three prism patterns in their mature enamel. The high degree of quantitative and qualitative variation in prism size, shape, and packing suggests that these features should be used cautiously in phylogenetic studies. Hapalemur is distinguished from the other lemurids by unique, medially constricted or rectangular prism cross-sections at an intermediate depth and the absence of prism decussation, but, without further assessment of character polarity, these differences do not clarify lemurid phylogenetic relations. Some characters of enamel microstructure may represent synapomorphies of Lemuridae, or of clades within Lemuridae, but homoplasty is likely to be common. Homoplasy of enamel characters may reflect functional constraints.

Ameloblasts↗

Shape of the lateral mandibular outline in Lemuridae: a quantitative analysis of variability using elliptical Fourier analysis.

While several morphometric analyses in lemurids have focused on the craniofacial complex, the characterization of their mandibular morphology has received less attention. The mandibular outline, in lateral perspective, was quantified using elliptical Fourier analysis, in an osteological sample encompassing 189 lemurid mandibles (66 Eulemur, 51 Hapalemur, 22 Lemur and 50 Varecia), and compared using multivariate statistical techniques. The taxonomic value of this outline in Lemuridae was demonstrated by the existence of significant separations between the four genera studied. In particular, the mandibular morphology of Hapalemur was markedly different from that in the group Eulemur-Lemur-Varecia. Excluding Hapalemur from analysis, the distinctions between Eulemur, Lemur and Varecia were enhanced suggesting the existence of more subtle intergeneric differences in mandibular morphology. Variation in mandibular form was greatest in Hapalemur and smallest in Eulemur and Varecia (as demonstrated by the mean values of interindividual distances); variation was higher in Lemur than in Eulemur and Varecia, but not higher than in Hapalemur. This morphological diversity may be related to functional adaptation in response to particular dietary habits. The patterns of intergeneric and intrageneric shape variations of the mandible in Lemuridae presented here provide a valuable resource for the analysis of variation among living and fossil lemurids.

Animals↗

Phylogeny of the lemuridae revisited: evidence from communication signals.

Phylogenetic relationships among the extant lemurid prosimians were assessed cladistically using stereotyped vocal, olfactory, and visual communication characters. Among our results are 3 findings of particular importance. First, our data are consistent with those from several recent studies of highly repeated DNA fragments in supporting a close phyletic affinity between Lemur catta and the genus Hapalemur. Moreover, our results indicate that L. catta is nested within the Hapalemur clade as the sister taxon to Hapalemur griseus/Hapalemur aureus. We interpret character states shared between Hapalemur simus and L. catta as primitive retentions by L. catta. Second, our findings agree with the DNA data in proposing a sister group relationship for Eulemur coronatus and Eulemur rubriventer. Third, our results question the validity of assigning Varecia variegata to the Lemuridae. For the characters we examined, Varecia more resembled indrids than lemurids, and the position of Varecia could be swapped with any of our outgroups (Indri, Propithecus, Daubentonia) without affecting tree topology. Previous workers sometimes have linked Varecia with various lemurids on grounds of ambiguously defined characters or on incorrect data gleaned from the literature. In those studies, the placement of Varecia in the Lemuridae usually has depended more on the minimization of character state conflicts (i.e. parsimony), than on demonstrable synapomorphies. In addition, data from DNA research have failed to demonstrate any pattern that links Varecia with Lemur, Hapalemur, or Eulemur. Results of the present study suggest that shared Varecia-indrid character states may be symplesiomorphic retentions in the Indridae, and that Varecia could be phyletically more primitive than either the indrids or lemurids.

Animal Communication↗

Phylogenetic relationships among Lemuridae (Primates): evidence from mtDNA.

The family Lemuridae includes four genera: Eulemur, Hapalemur, Lemur,Varecia. Taxonomy and phylogenetic relationships between L. catta, Eulemur and Hapalemur, and of Varecia to these other lemurids, continue to be hotly debated. Nodal relationships among the five Eulemur species also remain contentious. A mitochondrial DNA sequence dataset from the ND 3, ND 4 L, ND 4 genes and five tRNAs (Gly, Arg, His, Ser, Leu) was generated to try to clarify phylogenetic relationships w ithin the Lemuridae. Samples (n=39) from all ten lemurid species were collected and analysed. Three Daubentonia madagascariensis were included as outgroup taxa. The approximately 2400 bp sequences were analysed using maximum parsimony, neighbor-joining and maximum likelihood methods. The results support monophyly of Eulemur, a basal divergence of Varecia, and a sister-group relationship for Lemur/Hapalemur. Based on tree topology, bootstrap values, and pairwise distance comparisons, we conclude thatVarecia and Eulemur both represent distinct genera separate from L. catta. H. griseus andH. aureus form a clade with strong support, but the sequence data do not permit robust resolution of the trichotomy involving H. simus, H. aureus/H. griseus and L. catta. Within Eulemur there is strong support for a clade containing E. fulvus, E. mongoz and E. rubriventer. However, analyses failed to clearly resolve relationships among those three species or with the more distantly related E. coronatus and E. macaco. Our sequencing data support the current subspecific status of E.m. macaco and E.m. flavifrons, and that of V.v. variegata and V.v. rubra. However, tree topology and relatively large genetic distances among individual V.v. variegata indicate that there may be more phylogenetic structure within this taxon than is indicated by current taxonomy.

Animals↗

Phylogeny and character behavior in the family Lemuridae.

A phylogenetic analysis of the family Lemuridae was accomplished using multiple gene partitions and morphological characters. The results of the study suggest that several nodes in the lemurid phylogeny can be robustly resolved; however, the relationships of the species within the genus Eulemur are problematically nonrobust. The genus Varecia is strongly supported as the basal genus in the family. Hapalemur and Lemur catta are strongly supported as sister taxa and together are the sister group to the genus Eulemur. E. mongoz is the most basal species in the genus Eulemur. E. fulvus subspecies form a monophyletic group with three distinct lineages. E. coronatus is strongly supported as the sister taxon to E. macaco. The relationships of E. rubriventer, E. fulvus, and the E. macaco-E. coronatus pair are unresolved. Our combined molecular and morphological analysis demonstrates the lack of influence that morphology has on the simultaneous analysis tree when these two kinds of data are given equal weight. The effects of several extreme weighting schemes (removal of transitions and of third positions in protein-coding regions) and maximum-likelihood analysis were also explored. We suggest that these other forms of inference add little to resolving the problematic relationships of the species in the genus Eulemur.

Animals↗

Taxonomic relationships and sampling effects among Lepilemuridae and Lemuridae using a partial cytochrome b gene.

Partial cytochrome b sequences were used to study relationships between three Lepilemuridae species (Lepilemur dorsalis, L. septentrionalis and L. leucopus) and other Lemuridae species. L. dorsalis were subdivided into two sub-groups, according to their capture area (Nosy-Be island and Sahamalaza peninsula). Relationships deduced from phylogenetic trees as well as genetic distances lead to the classification of the Lepilemurs analysed here into separate species. These Lepilemurs form a monophyletic clade which is the sister clade of all other Lemurs used in this study. Reconstructions using randomly chosen sequences and step by step addition of sequences indicate that phylogenetic results for closely related species need to be analysed with caution, if only a small number of sequences are used to obtain them.

Amino Acid Sequence↗

Prosencephalic asymmetries in Lemuridae.

This study was undertaken to determine if regional volumetric asymmetries are a function of sulcal complexity and/or brain size. A complete series of coronal sections of cerebra from six species of Lemuridae, a family of strepsirhines, was digitized. Regional volumes were integrated and indices of asymmetry were calculated. The most significant asymmetries were found in retrocalcarine cortex, suggesting that striate and extrastriate asymmetries emerged early in primate evolution. Results further indicated that the degree of regional volumetric asymmetries, as measured by our indices, does not vary with sulcal complexity and/or brain size.

Animals↗

Gene mapping of Microcebus murinus (Lemuridae): a comparison with man and Cebus capucinus (Cebidae).

The karyotype of microcebus murinus (MIM) (lemuridae) is considered by Dutrillaux (1979) as the closest to the karyotype ancestral to all primates. A large number of homoeologies exists between the banding patterns of MIM chromosomes and those of man (HSA). We report a comparison of the gene maps of these two species which confirms most of these homoeologies. Fifteen cell hybrids were obtained by fusing MIM fibroblasts and an HPRT- Chinese hamster cell line. Twenty-seven enzyme markers were investigated. The following assignments were demonstrated: NP to chromosome MIM 2, homoeologous to HSA 14; the syntenic group PGD-ENO1-PGM1 to MIM 3, homoeologous to HSA 1p; LDHA to MIM 5, homoeologous to HSA 11; Me1 to MIM 6, homoeologous to HSA 6; the syntenic group LDHB-CS-PEPB-ENO2-TPI to MIM 7, homoeologous to HSA 12; the syntenic group AK1-AK3 to MIM 10, which we considered to be homoeologous to HSA 9 (we do not consider MIM 9 to be homoeologous to HSA 9, as does Dutrillaux, 1979); GOT1 to MIM 15, homoeologous to HSA 10; the syntenic group HPRT-G6PD-PGK-GLA to MIM X. Synteny dissociation in three hybrids suggests closer linkage between G6PD and HPRT than between PGK-GLA and HPRT. Three syntenic groups, known in man, were confirmed in MIM but could not be assigned with full confidence: ACP1-MDH1, MP1-PKM2, and PEPD-GPI. GUK1 and PEPC, known to be syntenic in man, were found to be asyntenic in MIM and could not be assigned. PGM2 and SOD1 could not be assigned. A comparison of these gene assignments with those known in Cebus capucinus showed a remarkable homoeology for six chromosomes of the two species.

Animals↗

Chromosomal evolution in Malagasy lemurs. VII. Phylogenic relationships between Propithecus, Avahi (Indridae), Microcebus (Cheirogaleidae), and Lemur (Lemuridae).

A chromosomal banding study was carried out on Propithecus verreauxi verreauxi, P. verreauxi deckeni, and Avahi laniger laniger. Comparison of their karyotypes with those of Microcebus murinus and Lemur fulvus led to reconstruction of the ancestral Lemuriform karyotype and a determination that the branch leading to the Indridae was isolated very early, before the separation of the Lemuridae from the Cheirogaleidae. The karyotype of Avahi remained highly ancestral, whereas that of P. verreauxi was considerably modified, chiefly by Robersonian translocations.

Animals↗

Molar morphology and variation in two malagasy lemur families (Lemuridae and Indriidae).

The lemurs of Madagascar represent a radiation of primates exhibiting considerable ecological and morphological diversity. Dentally, all lemurs possess the characteristic strepsirhine anterior tooth comb, but exhibit variation in their postcanine teeth that may be related to dietary differences. In this study, I examine two factors that could complicate a strictly functional interpretation of tooth form variation in two families of Malagasy primates, the Lemuridae and Indriidae. (1) Allometry may be responsible for observed variation. Body size, not specific tooth features, may be the object of selection; tooth features may vary among taxa as a consequence of differences in body size. (2) Taxonomic affiliation may "explain" variation without recourse to functional explanations. Tooth morphology among closely-related taxa may be constrained developmentally or as a result of stabilizing selection. Morphological variation between families, therefore, may not be the result of current functional differences related to physical dietary properties, but may result from past events that are lineage-specific. Morphological features from the upper and lower second molars of seven lemurid and four indriid taxa are compared. The results of this study indicate that the majority of second molar features scale isometrically. Initial separation by families is warranted by the homogeneous slopes but different elevations in analyses of covariance between families. Intrafamilial variation is considerable for lemurids, but more discrete among indriids. Functional explanations for tooth form variability should take into consideration the degree of variation within taxa. For this particular dataset, the two families should be analyzed separately, and, because of the considerable overlap of subspecies with full species among lemurids, the lowest taxonomic unit recognized should be used.

Analysis of Variance↗

Cineradiographic study of forelimb movements during quadrupedal walking in the brown lemur (Eulemur fulvus, Primates: Lemuridae).

Movements of forelimb joints and segments during walking in the brown lemur (Eulemur fulvus) were analyzed using cineradiography (150 frames/sec). Metric gait parameters, forelimb kinematics, and intralimb coordination are described. Calculation of contribution of segment displacements to stance propulsion shows that scapular retroversion in a fulcrum near the vertebral border causes more than 60% of propulsion. The contribution by the shoulder joint is 30%, elbow joint 5%, and wrist joint 1%. Correlation analysis was applied to reveal the interdependency between metric and kinematic parameters. Only the effective angular movement of the elbow joint during stance is speed-dependent. Movements of all other forelimb joints and segments are independent of speed and influence, mainly, linear gait parameters (stride length, stance length). Perhaps the most important result is the hitherto unknown and unexpected degree of scapular mobility. Scapular movements consist of ante-/retroversion, adduction/abduction, and scapular rotation about the longitudinal axis. Inside rotation of the scapula (60 degrees -70 degrees ), together with flexion in the shoulder joint, mediates abduction of the humerus, which is not achieved in the shoulder joint, and is therefore strikingly different from humeral abduction in man. Movements of the shoulder joint are restricted to flexion and extension. At touch down, the shoulder joint of the brown lemur is more extended compared to that of other small mammals. The relatively long humerus and forearm, characteristic for primates, are thus effectively converted into stride length. Observed asymmetries in metric and kinematic behavior of the left and right forelimb are caused by an unequal lateral bending of the spinal column.

Animals↗

Comparison of highly repeated DNA sequences in some Lemuridae and taxonomic implications.

Highly repeated DNA sequences of Eulemur fulvus mayottensis, E. coronatus, Lemur catta, and Hapalemur griseus griseus have been identified and compared. Sequence analysis of highly repeated DNA fragments isolated from L. catta and Hapalemur showed a high percentage of similarity (nearly 95%), as did fragments isolated from the two very close Eulemur species, whereas comparison of the DNA fragments isolated from the two Eulemur species and the L. catta/Hapalemur group showed a very low percentage (approximately 40%) of identity, as might be expected for distant species. These results confirm our previous data, obtained by Southern blot hybridization techniques on the same species, and strongly support the existence of a common trunk between L. catta and Hapalemur, but different from the leading to the Eulemur species.

Animals↗

The behavioral repertoire of the black-and-white ruffed lemur, Varecia variegata variegata (Primates: Lemuridae).

A stable social group of 7 semifree-ranging black-and-white ruffed lemurs (Varecia variegata variegata) was studied for 4 months to catalog the behavioral repertoire of this species. Observations focussed on particular aspects of behavior were conducted before and after this 4-month period to supplement information gathered. Behavior in 11 major categories is detailed: postures, terrestrial locomotion, arboreal locomotion, feeding behavior, vocalizations, scent-marking, affinitive social behavior, agonistic social behavior, play behavior, sexual behavior, and parental behavior. Ruffed lemurs frequently used body positions and locomotor patterns unusual among lemurids, including bipedal hanging and long-descent leaps. These behaviors reinforce dental evidence that Varecia are among the most frugivorous of the Malagasy lemurs. Low intragroup cohesion, infrequent social interaction, and antiphonal use of several long-distance vocalizations suggest that ruffed lemurs naturally exhibit fission-fusion sociality. Social structure based on interindividual familiarity probably extends across foraging parties for several of the diurnally active lemurs; however, thus far only Varecia seems likely to exhibit fission-fusion sociality analogous to that seen in spider monkeys and chimpanzees.

Animals↗