A digital collection of rare and endangered lemurs and other primates from the Duke Lemur Center.

Scientific study of lemurs, a group of primates found only on Madagascar, is crucial for understanding primate evolution. Unfortunately, lemurs are among the most endangered animals in the world, so there is a strong impetus to maximize as much scientific data as possible from available physical specimens. MicroCT scanning efforts at Duke University have resulted in scans of more than 100 strepsirrhine cadavers representing 18 species from the Duke Lemur Center. An error study of the microCT scanner recovered less than 0.3% error at multiple resolution levels. Scans include specimen overviews and focused, high-resolution selections of complex anatomical regions (e.g., cranium, hands, feet). Scans have been uploaded to MorphoSource, an online digital repository for 3D data. As captive (but free ranging) individuals, these specimens have a wealth of associated information that is largely unavailable for wild populations, including detailed life history data. This digital collection maximizes the information obtained from rare and endangered animals with minimal degradation of the original specimens.

Potential Rediscovery of a Distinct Slow Loris Nycticebus (Mammalia: Strepsirrhini: Lorisidae) from Pulau Tioman.

Several slow loris (Nycticebus) sightings have occurred on the island of Pulau Tioman, Peninsular Malaysia, from 2011 to 2018. Records discussed here represent the first confirmed sightings and photographic evidence of Nycticebus on Tioman since its discovery in 1915, refuting presumptions that the Tioman slow loris is extinct. Although originally considered a subspecies of the Sunda slow loris (Nycticebus coucang), several morphological characteristics apparent in all observed individuals, including the white interocular stripe, rufous colouration and pale dorsal stripe, are similar to the Philippine slow loris (Nycticebus menagensis). Further, the broad snout and ears may be unique to this population and suggest that the population may be distinct. I, therefore, recommend that future studies consider the taxonomic status of remote and isolated Nycticebus populations given the possibility that they may represent distinct and unrecognised taxa.

Using a multi-gene approach to infer the complicated phylogeny and evolutionary history of lorises (Order Primates: Family Lorisidae).

Extensive phylogenetic studies have found robust phylogenies are modeled by using a multi-gene approach and sampling from the majority of the taxa of interest. Yet, molecular studies focused on the lorises, a cryptic primate family, have often relied on one gene, or just mitochondrial DNA, and many were unable to include all four genera in the analyses, resulting in inconclusive phylogenies. Past phylogenetic loris studies resulted in lorises being monophyletic, paraphyletic, or an unresolvable trichotomy with the closely related galagos. The purpose of our study is to improve our understanding of loris phylogeny and evolutionary history by using a multi-gene approach. We used the mitochondrial genes cytochrome b, and cytochrome c oxidase subunit 1, along with a nuclear intron (recombination activating gene 2) and nuclear exon (the melanocortin 1 receptor). Maximum Likelihood and Bayesian phylogenetic analyses were conducted based on data from each locus, as well as on the concatenated sequences. The robust, concatenated results found lorises to be a monophyletic family (Lorisidae) (PP ≥ 0.99) with two distinct subfamilies: the African Perodictinae (PP ≥ 0.99) and the Asian Lorisinae (PP ≥ 0.99). Additionally, from these analyses all four genera were all recovered as monophyletic (PP ≥ 0.99). Some of our single-gene analyses recovered monophyly, but many had discordances, with some showing paraphyly or a deep-trichotomy. Bayesian partitioned analyses inferred the most recent common ancestors of lorises emerged ∼42 ±â€¯6 million years ago (mya), the Asian Lorisinae separated ∼30 ±â€¯9 mya, and Perodictinae arose ∼26 ±â€¯10 mya. These times fit well with known historical tectonic shifts of the area, as well as with the sparse loris fossil record. Additionally, our results agree with previous multi-gene studies on Lorisidae which found lorises to be monophyletic and arising ∼40 mya (Perelman et al., 2011; Pozzi et al., 2014). By taking a multi-gene approach, we were able to recover a well-supported, monophyletic loris phylogeny and inferred the evolutionary history of this cryptic family.

Djebelemur, a tiny pre-tooth-combed primate from the Eocene of Tunisia: a glimpse into the origin of crown strepsirhines.

BACKGROUND: Molecular clock estimates of crown strepsirhine origins generally advocate an ancient antiquity for Malagasy lemuriforms and Afro-Asian lorisiforms, near the onset of the Tertiary but most often extending back to the Late Cretaceous. Despite their inferred early origin, the subsequent evolutionary histories of both groups (except for the Malagasy aye-aye lineage) exhibit a vacuum of lineage diversification during most part of the Eocene, followed by a relative acceleration in diversification from the late Middle Eocene. This early evolutionary stasis was tentatively explained by the possibility of unrecorded lineage extinctions during the early Tertiary. However, this prevailing molecular view regarding the ancient origin and early diversification of crown strepsirhines must be viewed with skepticism due to the new but still scarce paleontological evidence gathered in recent years. METHODOLOGICAL/PRINCIPAL FINDINGS: Here, we describe new fossils attributable to Djebelemur martinezi, a≈50 Ma primate from Tunisia (Djebel Chambi). This taxon was originally interpreted as a cercamoniine adapiform based on limited information from its lower dentition. The new fossils provide anatomical evidence demonstrating that Djebelemur was not an adapiform but clearly a distant relative of lemurs, lorises and galagos. Cranial, dental and postcranial remains indicate that this diminutive primate was likely nocturnal, predatory (primarily insectivorous), and engaged in a form of generalized arboreal quadrupedalism with frequent horizontal leaping. Djebelemur did not have an anterior lower dentition as specialized as that characterizing most crown strepsirhines (i.e., tooth-comb), but it clearly exhibited a transformed antemolar pattern representing an early stage of a crown strepsirhine-like adaptation ("pre-tooth-comb"). CONCLUSIONS/SIGNIFICANCE: These new fossil data suggest that the differentiation of the tooth-comb must postdate the djebelemurid divergence, a view which hence constrains the timing of crown strepsirhine origins to the Middle Eocene, and then precludes the existence of unrecorded lineage extinctions of tooth-combed primates during the earliest Tertiary.

Taxonomy of the Bornean slow loris, with new species Nycticebus kayan (Primates, Lorisidae).

More species of nocturnal primates are now recognized than in the past, because many are cryptic species. Subtle morphological disparities, such as pelage pattern and color variation, vocal cues, and genetics have aided in elucidating the number of diagnosable species in a genus. The slow lorises (genus Nycticebus) once included only two species, but recent taxonomic studies resulted in the description of three additional species; further incompletely explored variability characterizes each of the currently described species. The Bornean loris in particular is characterized by pelage and body size variation. In this study, we explored facemask variation in the Bornean loris (N. menagensis). Differing facemask patterns, particularly influenced by the amount of white on the face, significantly clustered together by geographic regions, separated by notable geographic boundaries. Our results support the recognition of four species of Bornean lorises: N. menagensis, N. bancanus, N. borneanus, and N. kayan. Genetic studies are required to support these findings and to refine further our understanding of the marked variability within the Bornean loris populations.

Molecular cytogenetic studies in strepsirrhine primates, Dermoptera and Scandentia.

Since the first chromosome painting study between human and strepsirrhine primates was performed in 1996, nearly 30 species in Strepsirrhini, Dermoptera and Scandentia have been analyzed by cross-species chromosome painting. Here, the contribution of chromosome painting data to our understanding of primate genome organization, chromosome evolution and the karyotype phylogenetic relationships within strepsirrhine primates, Dermoptera and Scandentia is reviewed. Twenty-six to 43 homologous chromosome segments have been revealed in different species with human chromosome-specific paint probes. Various landmark rearrangements characteristic for each different lineage have been identified, as cytogenetic signatures that potentially unite certain lineages within strepsirrhine primates, Dermoptera and Scandentia.

Effects of seasonality on brain size evolution: evidence from strepsirrhine primates.

Seasonal changes in energy supply impose energetic constraints that affect many physiological and behavioral characteristics of organisms. As brains are costly, we predict brain size to be relatively small in species that experience a higher degree of seasonality (expensive brain framework). Alternatively, it has been argued that larger brains give animals the behavioral flexibility to buffer the effects of habitat seasonality (cognitive buffer hypothesis). Here, we test these two hypotheses in a comparative study on strepsirrhine primates (African lorises and Malagasy lemurs) that experience widely varying degrees of seasonality. We found that experienced seasonality is negatively correlated with relative brain size in both groups, controlling for the effect of phylogenetic relationships and possible confounding variables such as the extent of folivory. However, relatively larger-brained lemur species tend to experience less variation in their dietary intake than indicated by the seasonality of their habitat. In conclusion, we found clear support for the hypothesis that seasonality restricts brain size in strepsirrhines as predicted by the expensive brain framework and weak support for the cognitive buffer hypothesis in lemurs.

Phylogenetic relationships among the Lorisoidea as indicated by craniodental morphology and mitochondrial sequence data.

The phylogeny of the Afro-Asian Lorisoidea is controversial. While postcranial data attest strongly to the monophyly of the Lorisidae, most molecular analyses portray them as paraphyletic and group the Galagidae alternately with the Asian or African lorisids. One of the problems that has bedevilled phylogenetic analysis of the group in the past is the limited number of taxa sampled for both ingroup families. We present the results of a series of phylogenetic analyses based on 635 base pairs (bp) from two mitochondrial genes (12S and 16S rRNA) with and without 36 craniodental characters, for 11 galagid and five lorisid taxa. The outgroup was the gray mouse lemur (Microcebus murinus). Analyses of the molecular data included maximum parsimony (MP), neighbor joining (NJ), maximum likelihood (ML), and Bayesian methods. The model-based analyses and the combined "molecules+morphology" analyses supported monophyly of the Lorisidae and Galagidae. The lorisids form two geographically defined clades. We find no support for the taxonomy of Galagidae as proposed recently by Groves [Primate Taxonomy, Washington, DC: Smithsonian Institution Press. 350 p, 2001]. The taxonomy of Nash et al. [International Journal of Primatology 10:57-80, 1989] is supported by the combined "molecules+morphology" analysis; however, the model-based analyses suggest that Galagoides may be an assemblage of species united by plesiomorphic craniodental characters.

Comparative penile morphology of East African galagos of the genus Galagoides (family Galagidae): implications for taxonomy.

Recent studies on the comparative penile morphology of galagos have revealed complex patterns that vary among both genera and species, and help with species identification. So far the penile morphologies of 14 galago species have been described and an identification key has been proposed. The present study extends and revises previous work. Wild Galagoides cocos, G. granti, G. zanzibaricus and G. rondoensis from the Eastern Arc Mountains and coastal forests of Tanzania and Kenya were live-trapped, and one species (G. orinus) was examined using a museum specimen. Penile morphology was photographed, traced, and described qualitatively. All of the mature males had penile spines. Spines were absent or indistinct in immature males of all of the species. The penile morphologies of G. cocos, G. granti, and G. zanzibaricus are similar in their overall distribution and type of spines, but differ in the shape of the glans penis. Both G. orinus and G. rondoensis have divergent penile morphologies compared to all other galagos, and are probably phylogenetically distinct. The results support other recent morphological and behavioral studies that consider these five galagos to be distinct species. The evolution of the baculum and spines is thought to be linked to sexual selection in multimale mating systems, but the mechanisms involved are not entirely understood. Adult male G. rondoensis appear to display the penile spines by exposing the distal section of the penis.

Kinematics of vertical climbing in lorises and Cheirogaleus medius.

The type of climbing exhibited by apes and atelines is argued to have been important in the evolution of specialized locomotion, such as suspensory locomotion and bipedalism. However, little is known about the mechanics of climbing in primates. Previous work shows that Asian apes and atelines use larger joint excursions and longer strides than African apes and the Japanese macaque, respectively. This study expands knowledge of climbing mechanics by providing the first quantitative kinematic data for vertical climbing in four prosimian species: three lorisid species (Loris tardigradus, Nycticebus coucang, and Nycticebus pygmaeus) that share with apes and atelines morphological traits arguably related to climbing, and a more generalized quadruped, Cheirogaleus medius. Subjects were videotaped as they climbed up a wooden pole. Kinematic values, such as step length and limb excursions, were calculated and compared between species. The results of this study show that lorises, like Asian apes and spider monkeys, use relatively larger joint excursions and longer steps than does C. medius during climbing. These data lend further support to the idea that some primate species (e.g., lorises, atelines, and apes) are more specialized kinematically and morphologically for climbing than others. Pilot data suggest that such kinematic differences in climbing style across broad phylogenetic groups may relate to the energetics of climbing. Such data may be important for understanding the morphological and kinematic adaptations to climbing exhibited by some primates.

Fossil evidence for an ancient divergence of lorises and galagos.

Morphological, molecular, and biogeographic data bearing on early primate evolution suggest that the clade containing extant (or 'crown') strepsirrhine primates (lemurs, lorises and galagos) arose in Afro-Arabia during the early Palaeogene, but over a century of palaeontological exploration on that landmass has failed to uncover any conclusive support for that hypothesis. Here we describe the first demonstrable crown strepsirrhines from the Afro-Arabian Palaeogene--a galagid and a possible lorisid from the late middle Eocene of Egypt, the latter of which provides the earliest fossil evidence for the distinctive strepsirrhine toothcomb. These discoveries approximately double the previous temporal range of undoubted lorisiforms and lend the first strong palaeontological support to the hypothesis of an ancient Afro-Arabian origin for crown Strepsirrhini and an Eocene divergence of extant lorisiform families.

Failure of the ILD to determine data combinability for slow loris phylogeny.

Tests for incongruence as an indicator of among-data partition conflict have played an important role in conditional data combination. When such tests reveal significant incongruence, this has been interpreted as a rationale for not combining data into a single phylogenetic analysis. In this study of lorisiform phylogeny, we use the incongruence length difference (ILD) test to assess conflict among three independent data sets. A large morphological data set and two unlinked molecular data sets--the mitochondrial cytochrome b gene and the nuclear interphotoreceptor retinoid binding protein (exon 1)--are analyzed with various optimality criteria and weighting mechanisms to determine the phylogenetic relationships among slow lorises (Primates, Loridae). When analyzed separately, the morphological data show impressive statistical support for a monophyletic Loridae. Both molecular data sets resolve the Loridae as paraphyletic, though with different branching orders depending on the optimality criterion or character weighting used. When the three data partitions are analyzed in various combinations, an inverse relationship between congruence and phylogenetic accuracy is observed. Nearly all combined analyses that recover monophyly indicate strong data partition incongruence (P = 0.00005 in the most extreme case), whereas all analyses that recover paraphyly indicate lack of significant incongruence. Numerous lines of evidence verify that monophyly is the accurate phylogenetic result. Therefore, this study contributes to a growing body of information affirming that measures of incongruence should not be used as indicators of data set combinability.

Karyotype polymorphism in the slender loris (Loris tardigradus).

Three wild-caught Sri Lankan and two captive-bred slender lorises (Loris tardigradus) in Adelaide Zoo, South Australia, were karyotyped from leucocyte cultures. The founder male and one of the founder females were of the grey subspecies L. tardigradus grandis, of which L. tardigradus nordicus is probably a synonym. The other founder female was a small red-brown L. tardigradus tardigradus. All three wild-caught individuals were karyotypically distinct from each other and their offspring showed the expected heterozygosity. The L. tardigradus tardigradus karyotype was no more distinct from the grey subspecies karyotypes than they were from each other. On present evidence, Indian and Sri Lanka lorises appear to be chromosomally distinct.