Evolution and biogeographic history of the Saguinus mystax group (Primates, Callithrichidae).

The Saguinus mystax group traditionally includes three species, S. mystax, S. labiatus, and S. imperator. The additional inclusion of S. inustus is argued on molecular grounds, which have an important impact on our comprehension of the phenotypical evolution and biogeography of the group. Here, we investigate the evolutionary events leading to the diversification of the S. mystax group, integrating phylogenetic, temporal, and geographic information with the current knowledge of the Amazonian paleogeographical history. The examination of 208 specimens of Saguinus resulted in 25 morphological characters, of which 13 were used for the first time in a phylogenetic analysis of the genus. Morphological characters were also combined with molecular data and analyzed using Bayesian and Maximum Likelihood methods. Trees resulting from morphological and combined data recovered a monophyletic S. mystax group, including S. inustus, whose inclusion was supported by two morphological synapomorphies. Molecular based age estimates place the origin of Saguinus in the middle Miocene (17.4-13 million years ago [mya]), whereas the S. mystax group originated in an interval between 12 and 6 mya. Our results also suggest that the ancestral area of Saguinus was western Amazon, from where they dispersed to their current distribution after the end of the Pebas lakes system. The diversification events in the S. mystax group are related to the Pliocene development of the modern Amazon river network associated to the uplift of Fitzcarrald Arch.

Genetic contributions to dental dimensions in brown-mantled tamarins (Saguinus fuscicollis) and rhesus macaques (Macaca mulatta).

OBJECTIVES: The use of dental metrics in phylogenetic reconstructions of fossil primates assumes variation in tooth size is highly heritable. Quantitative genetic studies in humans and baboons have estimated high heritabilities for dental traits, providing a preliminary view of the variability of dental trait heritability in nonhuman primate species. To expand upon this view, the heritabilities and evolvabilities of linear dental dimensions are estimated in brown-mantled tamarins (Saguinus fuscicollis) and rhesus macaques (Macaca mulatta). MATERIALS AND METHODS: Quantitative genetic analyses were performed on linear dental dimensions collected from 302 brown-mantled tamarins and 364 rhesus macaques. Heritabilities were estimated in SOLAR using pedigrees from each population, and evolvabilities were calculated manually. RESULTS: Tamarin heritability estimates range from 0.19 to 0.99, and 25 of 26 tamarin estimates are significantly different from zero. Macaque heritability estimates range from 0.08 to 1.00, and 25 out of 28 estimates are significantly different from zero. DISCUSSION: Dental dimensions are highly heritable in captive brown-mantled tamarins and free-ranging rhesus macaques. The range of heritability estimates in these populations is broadly similar to those of baboons and humans. Evolvability tends to increase with heritability, although evolvability is high relative to heritability in some dimensions. Estimating evolvability helps to contextualize differences in heritability, and the observed relationship between evolvability and heritability in dental dimensions requires further investigation.

Re-description and assessment of the taxonomic status of Saguinus fuscicollis cruzlimai Hershkovitz, 1966 (Primates, Callitrichinae).

Cruz Lima's saddle-back tamarin Saguinus fuscicollis cruzlimai Hershkovitz, 1966, was described from a painting by Eládio da Cruz Lima in his book Mammals of Amazonia, Vol. 1, Primates (1945). The painting was of four saddle-back tamarins from the upper Rio Purus, one of them distinct and the inspiration for Hershkovitz to describe it as a new subspecies. Its exact provenance was unknown, however, and the specimen was lost. Surveys in the Purus National Forest in 2011 resulted in sightings of this tamarin along the north bank of the Rio Inauini, a left-bank tributary of the middle Purus, and also on the left bank of the Purus, north and south of the Rio Inauini. It is possible that it extends north as far as the Rio Pauini, and that S. f. primitivus Hershkovitz, 1977, occurs north of the Pauini as far the Rio Tapauá, both also left-bank tributaries of the Purus. Morphometric and molecular genetic analyses and the coloration of the pelage indicate that this tamarin differs from its neighbors sufficiently to be considered a full species. In his doctoral dissertation [2010, Taxonomy, Phylogeny and Distribution of Tamarins (Genus Saguinus Hoffmannsegg, 1807) Georg-August Universität, Göttingen], C. Matauschek found that saddle-back and black-mantle tamarins diverged from the tamarin lineage around 9.2 million years ago; time enough to warrant their classification in a distinct genus. Leontocebus Wagner, 1840, is the first name available. In this article we re-describe Cruz Lima's saddle-back tamarin. We propose a neotype with a precise locality, and make it a full species in the genus Leontocebus.

Revalidation of Saguinus ursula Hoffmannsegg (Primates: Cebidae: Callitrichinae).

In this study, we review the taxonomy of Saguinus niger (É. Geoffroy) and revalidate Saguinus ursula Hoffmannsegg as a distinct species. The revalidation is based on pelage coloration, and the pattern of morphological divergence is corroborated by molecular data. Samples from the east bank of the Tocantins River (S. ursulus) were distinct from specimens of S. niger from the west bank in having mid-dorsal hair with an wide (5.0-55 mm) intermediary band of bright and golden buffy color; long (ca. 23-26 mm) dorsal hair at the inter-scapular region; and naked (not noticeably haired) face, hands and fingers. Saguinus ursulus and S. niger are allopatric, and Tocantins River is putatively acting as an effective barrier for gene flow. A lectotype to S. ursulus from syntypes was designated.

Mitochondrial phylogeny of tamarins (Saguinus, Hoffmannsegg 1807) with taxonomic and biogeographic implications for the S. nigricollis species group.

Tamarins of the genus Saguinus, subfamily Callitrichinae, represent one of the most diverse primate radiations. So far, about 35 taxa have been described, but detailed information about their taxonomy and phylogeny is still lacking. To further elucidate the phylogenetic relationships and the biogeographic history within the genus, and to contribute to a more reliable classification of its taxa, we sequenced the complete mitochondrial cytochrome b gene and the hypervariable region I of the D-loop. Therefore, we mainly used fecal samples from wild tamarins collected during two expeditions to the Peruvian Amazon, an area of high tamarin diversity. Our data suggest that the numerous taxa of the S. nigricollis species group are derived from a common ancestor that separated from the other representatives of the genus ~10 mya. Most taxa of the S. nigricollis group form monophyletic clusters, which mainly originated in a single rapid radiation ~2.9 mya. S. fuscicollis and S. nigricollis appear as polyphyletic taxa, but we could identify various clusters, which are mainly consistent with differences in coat coloration. We could confirm most of the existing taxa as distinct entities and suggest species status for fuscicollis, illigeri, lagonotus, leucogenys, nigricollis, nigrifrons, tripartitus, and weddelli. Our genetic data do not support a separate status for melanoleucus and graellsi, but due to differences in fur coloration, we give them subspecies status. The species group most likely originated in western Amazonia and diversified during the decline of the Acre wetland and the formation of the Amazonian river system.

The range of the golden-mantle tamarin, Saguinus tripartitus (Milne-Edwards, 1878): distributions and sympatry of four tamarins in Colombia, Ecuador, and northern Peru [corrected].

A detailed understanding of the range of the golden-mantle tamarin, Saguinus tripartitus (Milne Edwards, 1878), in Amazonian Peru and Ecuador is of particular relevance, not only because it is poorly known but also because it was on the basis of its supposed sympatry with the saddleback tamarin (S. fuscicollis lagonotus) that Thorington (Am J Primatol 15:367-371, 1988) argued that it is a distinct species rather than a saddleback tamarin subspecies, as was believed by Hershkovitz (Living new world monkeys, vol I. The University of Chicago Press, Chicago, 1977). A number of surveys have been carried out since 1988 in the supposed range of S. tripartitus, in both Ecuador and Peru. Here we summarize and discuss these issues and provide a new suggestion for the geographic range of this species; that is, between the ríos Napo and Curaray in Peru and extending east into Ecuador. We also review current evidence for the distributions of Spix's black-mantle tamarin (S. nigricollis nigricollis), Graells' black-mantle tamarin (S. n. graellsi), and the saddleback tamarin (S. fuscicollis lagonotus), which are also poorly known, and examine the evidence regarding sympatry between them. We conclude that despite the existence of a number of specimens with collecting localities that indicate overlap in their geographic ranges, the fact that the four tamarins are [corrected] of similar size and undoubtedly very similar in their feeding habits militates strongly against the occurrence of sympatry among them.

Tocantins river as an effective barrier to gene flow in Saguinus niger populations

The Saguinus represent the basal genus of the Callitrichinae subfamily. Traditionally this genus is divided into three groups: Hairy, Mottled and Bare-face, however, molecular data failed to validate these groups as monophyletic units, as well as raised some subspecies to the species status. This is the case of the former subspecies Saguinus midas midas and S. midas niger, which are now considered as different species. In the present study, we sequenced a portion of the D-loop mtDNA region in populations from the East bank of the Xingu and from both banks of the Tocantins river, in order to test the effectiveness of large rivers as barriers to the gene flow in Saguinus. According to our results, the populations from the East and West banks of the Tocantins river are more divergent than true species like S. mystax and S. imperator. The Tocantins river may be acting as a barrier to gene flow, and consequently these very divergent populations may represent distinct taxonomic entities (species?).

Tamarin alpha-interferon is active in mouse liver upon intramuscular gene delivery.

BACKGROUND: The hepatitis C virus (HCV) is responsible for a severe and widespread form of hepatitis for which a durable and effective therapy has not yet been established. The only approved therapy against hepatitis C, alpha-interferon protein intramuscular administration, presents numerous drawbacks that might be overcome by adopting a gene therapy approach. HCV exclusively infects humans and chimpanzees, hence an acceptable animal model for hepatitis C pharmacological studies is not available. Recently, tamarins infected by GB virus B (GBV-B) have been proposed as a surrogate animal model for HCV infection. The aim of the present study was the production of tamarin interferon (tIFN) through delivery of tIFN-coding DNA to evaluate the feasibility of a gene therapy approach based on IFN electro-gene transfer (EGT) in future studies with primates. METHODS: Production and biological activity of cloned tamarin interferon was monitored in cultured cells upon transfection and in mice upon muscle EGT of the corresponding plasmid DNA, respectively. RESULTS: A tamarin gene encoding a protein homologous to human interferon-alpha2 (hIFN-alpha2) has been cloned. The tamarin IFN-alpha (tIFN-alpha) protein shows antiviral activity in a cell-based assay. Upon EGT of the corresponding gene in mouse muscles, tIFN-alpha is detectable at high levels in serum for at least 4 months. Most important, activity of tIFN, measured as enhancement of mRNA levels of genes induced by type I IFNs, is also detectable in the liver of EGT-treated mice. CONCLUSION: The present study demonstrates that the delivery of tIFN-alpha DNA via intramuscular injection yields a functional protein able to produce biological effects inside a remote target organ, the liver. This finding, besides the specific purpose of the present study, is of general relevance with a view to establishing therapeutic protocols based on EGT.

Phylogenetic relationships of the Callitrichinae (Platyrrhini, primates) based on beta2-microglobulin DNA sequences.

The phylogenetic relationships of callitrichine primates have been determined by DNA sequence analyses of exons 1, 2, and 3 of the beta2-microglobulin gene. Parsimony, distance, and maximum likelihood analyses of ca. 900 base pairs of 21 taxa, representing all callitrichine genera, indicated that Saguinus was the most basal offshoot. Within Saguinus, S. fuscicollis appeared as the first divergent lineage followed by an unresolved trichotomy formed by S. mystax/S. imperator, S. midas/S. bicolor, and S. oedipus. A second callitrichine lineage was formed by Leontopithecus; each of the three species studied showed identical nucleotide sequences. Callimico appeared as the sister taxon of Callithrix/Cebuella. Genetic distances within this latter group were very small, although a stronger association between Cebuella and species of the Callithrix argentata group was observed. The inclusion of Cebuella in the genus Callithrix is suggested. These studies indicated that tamarins are more plesiomorphic than marmosets in agreement with the phyletic dwarfism hypothesis.

Historical biogeography of tamarins, genus Saguinus: the molecular phylogenetic evidence.

Hypotheses of the historical biogeography of tamarins (genus Saguinus) based on variation in coat colors and body size are tested using phylogenetic relationships inferred from mitochondrial DNA (mtDNA) sequence data. Samples from all 12 species of Saguinus and several subspecies are included in the analysis. Approximately 1,200 bases of mtDNA sequence from the cytochrome b and D-loop regions are reported for the tamarins and several outgroup taxa. Parsimony analysis of the mtDNA sequence data reveals Saguinus to be a monophyletic taxon composed of two major clades: one, the Small-bodied clade, contains S. nigricollis, S. tripartitus, and S. fuscicollis, and the other, the Large-bodied clade, contains the other nine species. The phylogenetic relationships among tamarins inferred from the mtDNA sequence data reject previous hypotheses for the historical biogeography of tamarins and suggest different dispersal routes for this group of New World monkeys. The molecular data suggest that tamarins dispersed across South America in two major waves from an origin somewhere south of the Amazon. One wave moved in a westerly direction, whereas the other moved in a northeastern direction toward the Amazon delta and then west along the northern portion of the continent into northern Colombia and Panama.

Description of a new kind of MHC DNA sequence in Saguinus oedipus (cotton-top tamarin).

The MHC class I genes of the New World primate the cotton-top tamarin (Saguinus oedipus) are an exception to the high polymorphism and variability usually displayed by this multigene family. In the present work, the cloning and sequencing of a new pseudogene, tentatively named Saoe-Mhc-N4, in this primate species are reported. This new sequence has two characteristic deletions at exon 2, making it very unlikely that any putative protein from this sequence was an antigen-presenting molecule. Comparison of intron 1, intron 2, partial exon 1, exon 2 and partial exon 3 showed little similarity with those of classical class I genes and pseudogenes in S. oedipus and in other primates. Phylogenetic analysis grouped this Saoe-Mhc-N4 sequence with other pseudogenes in S. oedipus. Thus, it seems that Saoe-Mhc-N4 is an inactivated gene or a pseudogene which has been originated by the common process of duplication and subsequent inactivation of MHC class I loci in this primate species.

Riverine barriers and gene flow in Amazonian saddle-back tamarins.

We describe patterns of genotypic and phenotypic variation in saddle-back tamarin (Saguinus fuscicollis) populations along the central and upper Rio Juruá, western Brazilian Amazonia. The genetic data are sequence haplotypes of the mitochondrial cytochrome b gene; phenotypic data are pelage colour variants that define sharply demarcated subspecies of this extremely variable tamarin species. We show that gene flow occurs between adjacent subspecies, but that this phenomenon is restricted to the headwater section of the river, which is consistent with expectations from the riverine barrier hypothesis. In this model, the major first-order tributaries of the Amazon form effective barriers to dispersal, with between-bank gene flow limited to the narrowed sections of headwater streams and parallel divergence increasing along both banks from the headwaters to the mouth of a given river. In meandering rivers such as the Rio Juruá, we suggest passive transfer through river channel dynamics as the main mechanism permitting genetic contact between populations on opposite banks of the river. Finally, we argue that in the case of plant and animal species that are largely restricted to unflooded (terra firme) forests, such as tamarins, seasonally flooded (várzea) forest can operate as a critical additional barrier to between-bank gene flow.

Fluctuating asymmetry in tamarin (Saguinus) cranial morphology: intra- and interspecific comparisons between taxa with varying levels of genetic heterozygosity.

Fluctuating asymmetry has been proposed as a measure of developmental homeostasis and an indicator of populations under stress. However, controversy surrounds not only the validity of an association between fluctuating asymmetry and levels of protein heterozygosity, but also whether fluctuating asymmetry can be used to identify populations under genetic and environmental stress. The relationship between levels of heterozygosity and developmental homeostasis is considered by comparing levels of cranial fluctuating asymmetry in three tamarin samples with contrasting levels of heterozygosity: (1) low heterozygosity cotton-top tamarins (N = 324), (2) presumably normally heterozygous Illiger's saddle-back tamarins (N = 208), and (3) relatively highly heterozygous hybrids between saddle-back tamarin subspecies (N = 31). All specimens originated at the Oak Ridge Associated Universities' Marmoset Research Center. A nested ANOVA design was used to separate out variation due to individual differences, side-to-side differences (fluctuating asymmetry), and measurement error. We found statistically significant levels of fluctuating asymmetry in nearly all of the traits surveyed and a negative correlation between levels of fluctuating asymmetry and genetic heterozygosity. Efforts to use fluctuating asymmetry to identify populations endangered by reduced genetic variability and/or under stress may be inhibited by small sample sizes, neglect of repeated measures, and lack of appropriate reference populations.

"Giant" tamarin from the Miocene of Colombia.

A nearly complete but badly crushed skull and mandible of Lagonimico conclucatus, gen. et sp. nov. is described from the La Victoria Formation, Colombia. The specimen is of middle Miocene age and dates from about 13.5 Ma. Features of the dentition suggest Lagonimico is a sister group to living Callitrichinae (Saguinus, Leontopithecus, Callithrix, and Cebuella). These features include having elongate compressed lower incisors, a reduced P2 lingual moiety, and the absence of upper molar hypocones. The new taxon also has autapomorphies, such as a relatively deep jaw, that rule it out of the direct ancestry of any living callitrichine. This animal is assigned to a new tribe of the callitrichine clade. The orbits of L. conclucatus are small, suggesting diurnal habits. Inflated, low-crowned (bunodont) cheek teeth with short, rounded shearing crests, as well as premolar simplification and M3 size reduction, suggest fruit- or gum-eating adaptations, as among many living callitrichines. Procumbent and slightly elongate lower incisors suggest this species could use its front teeth as a gouge, perhaps for harvesting tree gum. Estimates from jaw size suggest Lagonimico weighed about 1,200 g, about the size of Callicebus, the living titi monkey of South America. Judged from tooth size and jaw length, Lagonimico would have been slightly smaller than Callicebus, but still larger than Callimico or any living callitrichine. Therefore, many of the distinctive anatomical features of the callitrichine clade, sometimes explained by phyletic dwarfing, may have evolved at larger body size. Evolutionary size reduction may have occurred in parallel in callitrichines and Callimico.

Systematics of the Saguinus oedipus group of the bare-face tamarins: evidence from facial morphology.

The systematics of the Saguinus oedipus group within the bare-face tamarins remains open to question. Hershkovitz (Living New World Monkeys (Platyrrhini), Vol.1. Chicago: University of Chicago Press, 1977) places the cotton-top and rufus-naped tamarins as subspecies of Saguinus oedipus (S. o. oedipus and S. o. geoffroyi, respectively). In contrast, several other authors have argued that these two taxa should be considered separate species (S. oedipus and S. geoffroyi). Phylogenetic relationships within the group are also disputed. Resolving these different interpretations has been difficult in part because no study of this group has included an objective measure of expected levels of specific vs. subspecific variation. We used facial measurements from 179 adult crania to address the systematics of this group and included a related species that is known to include multiple subspecies. Our sample included three taxa from the S. oedipus group of the bare-face tamarins (S. oedipus, S. geoffroyi, and S. leucopus) and six subspecies from the related hairy-face tamarin species S. fuscicollis. Comparisons to S. leucopus provided a relative measure of species-level differences. Analyses that included S. fuscicollis provided a measure of subspecific variation. There was no evidence of facial sexual dimorphism in any of these taxa. A variety of multivariate statistical analyses including discriminant function and cluster analysis suggest that S. oedipus and S. geoffroyi differ morphologically at a level consistent with species-level distinctions. The extent of differences between these taxa is large. The differences in their facial morphology was on the order of differences between S. oedipus or S. geoffroyi and S. leucopus rather than the extent of variation among S. fuscicollis subspecies. Furthermore, a comparison of collecting localities revealed that the variation we observed among S. oedipus and S. geoffroyi was not clinical but presented a large morphological discontinuity at the boundary between taxa. Our analyses also suggested that S. leucopus is more similar to S. oedipus than is either to S. geoffroyi. Finally, it may be that there are some distinct species within the S. fuscicollis group. However, this hypothesis, along with other phylogenetic relationships suggested by this study, will require more data and further study.

Variations in dental measurements between Saguinus species and their systematic relationships.

Multivariate analysis is applied to dental measurements of Saguinus species to analyse their systematic relationships. The shape distance between Saguinus midas midas and S. midas niger is larger than that between S. nigricollis and S. fuscicollis, both of which are generally recognized as valid species. In dental form, S. bicolor is the closest relative of S. midas. S. inustus is not linked to S. leucopus. S. geoffroyi and S. leucopus, as S. inustus shows closer affinity with S. labiatus and S. mystax than with the former 3 species.

Genetic variations in albumin and transferrin as species markers in plasma of Callithricidae.

Albumin (Alb) and transferrin (Tf) polymorphism in plasma of Callithricidae was investigated by means of starch gel electrophoresis. In 52 blood samples of three species (Saguinus mystax, S. oedipus and S. labiatus), four Alb phenotypes (Alb 1, Alb 2, Alb 3 and Alb 2-3) and two Tf phenotypes (Tf 1 and Tf 2) were observed. No Alb variant was found in S. oedipus and S. mystax.