Alu elements and the phylogeny of capuchin (Cebus and Sapajus) monkeys.

Three families of New World monkeys, the Pitheciidae, Atelidae, and Cebidae, are currently recognized. The monophyly of the Cebidae is supported unequivocally by the presence of ten unique Alu elements, which are absent from the other two families. In this paper, the five genomic regions containing these Alu elements were sequenced in specimens representing nine capuchin (Cebus, Sapajus) species in order to identify mutations that may help elucidate the taxonomy and phylogenetic relationships of the cebids. The results confirmed the presence of previously described Alu elements in the capuchins. An Alu insertion present in the Cebidae2 genomic region belonging to the AluSc subfamily was amplified and sequenced only in Sapajus. No amplified or unspecific product was obtained for all other species studied here. An AluSc insertion present in the CeSa1 region was found only in Cebus, Sapajus, and Saimiri. Cebidae4 was characterized by two insertions, an AluSz6 shared by all cebids, and a complete SINE (AluSx3) found only in the capuchins (Cebus and Sapajus). The genomic region Cebidae5 revealed two insertion events, one of the AluSx subfamily, which was shared by all cebids, and another (AluSc8), that was unique to Cebus, offering a straightforward criterion for the differentiation of the two genera, Cebus and Sapajus. The Cebidae6 region showed four distinct insertion events: a 52-bp simple repeat ((TATG) n), two very ancient repeats (MIRc) and a TcMar-Tigger shared by all New World monkeys studied so far, and an Alu insertion of the AluSx subfamily present exclusively in the cebids. The phylogenetic tree confirmed the division of the capuchins into two genera, Cebus and Sapajus, and suggested the southern species Sapajus nigritus robustus and S. cay as the earliest and second earliest offshoots in this genus, respectively. This supports a southern origin for the Sapajus radiation.

Chromosome evolution in new world monkeys (Platyrrhini).

During the last decades, New World monkey (NWM, Platyrrhini, Anthropoideae) comparative cytogenetics has shed light on many fundamental aspects of genome organisation and evolution in this fascinating, but also highly endangered group of neotropical primates. In this review, we first provide an overview about the evolutionary origin of the inferred ancestral NWM karyotype of 2n = 54 chromosomes and about the lineage-specific chromosome rearrangements resulting in the highly divergent karyotypes of extant NWM species, ranging from 2n = 16 in a titi monkey to 2n = 62 in a woolly monkey. Next, we discuss the available data on the chromosome phylogeny of NWM in the context of recent molecular phylogenetic analyses. In the last part, we highlight some recent research on the molecular mechanisms responsible for the large-scale evolutionary genomic changes in platyrrhine monkeys.

Evolution of the SEC1 gene in New World monkey lineages (Primates, Platyrrhini).

The structure and evolution of the SEC1 gene were examined for the first time in New World primates of the genera Alouatta, Aotus, Ateles, Brachyteles, Callicebus, Callithrix, Cebus, Chiropotes, Lagothrix, Leontopithecus, Pithecia, Saguinus, and Saimiri. This gene has a high CG content (63.8%) and an estimated heterogeneous size ranging from 795 (Callithrix) to 1041 bp (Pithecia), due to numerous indel events. Similar to other fucosyltransferases, three conserved regions are shared by these primates, except for the callitrichines, Aotus and Pithecia, in which indel events resulted in premature stop codons that are related to the production of a supposedly non-functional protein. Phylogenetic analysis of the SEC1 gene, transition/transversion rates, and nucleotide sequence alignment support the hypothesis that primate SEC1 evolved by divergent evolution, and that the lack of activity in some lineages occurred independently at least twice in New World primates, once in the Aotus-Cebus-Callitrichinae group and again in Pithecia. Likelihood-based inference of ancestral states for the activity of SEC1 leads us to suppose that inactivation of SEC1 in the Callitrichinae was a result of a more complex series of events than in Pithecia.

Atelinae phylogenetic relationships: the trichotomy revived?

This research examines phylogenetic relationships between members of the Atelinae subfamily (Alouatta, Ateles, Brachyteles, and Lagothrix), based on analysis of three genetic regions. Two loci, cytochrome c oxidase subunit II (COII) and the hypervariable I portion of the control region, are part of the mitochondrial genome. The other is a single-copy nuclear gene, Aldolase A Intron V. Analysis of these genetic regions provides support for tribe Alouattini containing the Alouatta species, while tribe Atelini contains the other three genera. However, these three genetic regions produce conflicting results for relationships among tribe Atelini members. Previous genetic studies supported grouping Brachyteles with Lagothrix, leaving Ateles in a separate subclade. The present data sets vary based on the genetic region analyzed and method of analysis suggesting all possible cladistic relationships. These results are more consistent with investigations of morphology and behavior among these primates. The primary cause of discrepancy between this study and previous genetic studies is postulated to reside in increased sampling in the present study of genetic variation among members of the Atelinae, specifically Ateles. The present study utilized samples of Ateles from all postulated species for this genetically variable primate, while previous studies used only one or two species of Ateles. This paper demonstrates that shifting relationships are produced when different species of Ateles are used to reconstruct phylogenies. This research concludes that a trichotomy should still be supported between members of tribe Atelini until further analyses, which include additional Atelinae haplotypes are conducted.

The lowest diploid number (2n = 16) yet found in any primate: Callicebus lugens (Humboldt, 1811).

Morphologic, molecular and karyologic analyses of Callicebus lugens (Humboldt, 1811) of known geographic origin supported the proposition that this is a valid species. Morphologic and morphometric analyses showed evident differences between C. lugens and two other related taxa of the same group (Callicebus purinus and Callicebus torquatus). Cytochrome b DNA analyses (maximum parsimony, neighbour joining and maximum likelihood) were congruent in showing a strong association between C. lugens and Callicebus sp. of the torquatus group in one branch and a sister branch further divided into two clades: one with species of the personatus group and another, with species of the moloch group. Karyotypic analysis showed that C. lugens has the lowest diploid chromosome number of the primate order (2n = 16). Comparisons with other congeneric species clearly supported the proposition that C. lugens is karyotypically similar to others of the torquatus group.

RFLP analysis of mtDNA from six platyrrhine genera: phylogenetic inferences.

This study investigates the phylogenetic relationships of 10 species of platyrrhine primates using RFLP analysis of mtDNA. Three restriction enzymes were used to determine the restriction site haplotypes for a total of 276 individuals. Phylogenetic analysis using maximum parsimony was employed to construct phylogenetic trees. We found close phylogenetic relationships between Alouatta, Lagothrix and Ateles. We also found a close relationship between Cebus and Aotus, with Saimiri clustering with the atelines. Haplotype diversity was found in four of the species studied, in Cebus albifrons, Saimiri sciureus, Lagothrix lagotricha and Ateles fusciceps. These data provide additional information concerning the phylogenetic relationships between these platyrrhine genera and species.

A comparison of phenotypic variation and covariation patterns and the role of phylogeny, ecology, and ontogeny during cranial evolution of new world monkeys.

Similarity of genetic and phenotypic variation patterns among populations is important for making quantitative inferences about past evolutionary forces acting to differentiate populations and for evaluating the evolution of relationships among traits in response to new functional and developmental relationships. Here, phenotypic co variance and correlation structure is compared among Platyrrhine Neotropical primates. Comparisons range from among species within a genus to the superfamily level. Matrix correlation followed by Mantel's test and vector correlation among responses to random natural selection vectors (random skewers) were used to compare correlation and variance/covariance matrices of 39 skull traits. Sampling errors involved in matrix estimates were taken into account in comparisons using matrix repeatability to set upper limits for each pairwise comparison. Results indicate that covariance structure is not strictly constant but that the amount of variance pattern divergence observed among taxa is generally low and not associated with taxonomic distance. Specific instances of divergence are identified. There is no correlation between the amount of divergence in covariance patterns among the 16 genera and their phylogenetic distance derived from a conjoint analysis of four already published nuclear gene datasets. In contrast, there is a significant correlation between phylogenetic distance and morphological distance (Mahalanobis distance among genus centroids). This result indicates that while the phenotypic means were evolving during the last 30 millions years of New World monkey evolution, phenotypic covariance structures of Neotropical primate skulls have remained relatively consistent. Neotropical primates can be divided into four major groups based on their feeding habits (fruit-leaves, seed-fruits, insect-fruits, and gum-insect-fruits). Differences in phenotypic covariance structure are correlated with differences in feeding habits, indicating that to some extent changes in interrelationships among skull traits are associated with changes in feeding habits. Finally, common patterns and levels of morphological integration are found among Platyrrhine primates, suggesting that functional/developmental integration could be one major factor keeping covariance structure relatively stable during evolutionary diversification of South American monkeys.

The current status of the New World monkey phylogeny.

Four DNA datasets were combined in tandem (6700 bp) and Maximum parsimony and Neighbor-Joining analyses were performed. The results suggest three groups emerging almost at the same time: Atelidae, Pitheciidae and Cebidae. The total analysis strongly supports the monophyly of the Cebidae family, grouping Aotus, Cebus and Saimiri with the small callitrichines. In the callitrichines, the data link Cebuela to Callithrix, place Callimico as a sister group of Callithrix/Cebuella, and show Saguinus to be the earliest offshoot of the callitrichines. In the family Pithecidae, Callicebus is the basal genus. Finally, combined molecular data showed congruent branching in the atelid clade, setting up Alouatta as the basal lineage and Brachyteles-Lagothrix as a sister group and the most derived branch. Two major points remain to be clarified in the platyrrhine phylogeny: (i) what is the exact branching pattern of Aotus, Cebus, Saimiri and the small callitrichines, and (ii), which two of these three lineages, pitheciines, atelines or cebids, are more closely related?

The current status of the New World monkey phylogeny

Four DNA datasets were combined in tandem (6700 bp) and Maximum parsimony and Neighbor-Joining analyses were performed. The results suggest three groups emerging almost at the same time: Atelidae, Pitheciidae and Cebidae. The total analysis strongly supports the monophyly of the Cebidae family, grouping Aotus, Cebus and Saimiri with the small callitrichines. In the callitrichines, the data link Cebuela to Callithrix, place Callimico as a sister group of Callithrix/Cebuella, and show Saguinus to be the earliest offshoot of the callitrichines. In the family Pithecidae, Callicebus is the basal genus. Finally, combined molecular data showed congruent branching in the atelid clade, setting up Alouatta as the basal lineage and Brachyteles-Lagothrix as a sister group and the most derived branch. Two major points remain to be clarified in the platyrrhine phylogeny: (i) what is the exact branching pattern of Aotus, Cebus, Saimiri and the small callitrichines, and (ii), which two of these three lineages, pitheciines, atelines or cebids, are more closely related?

The time of divergence between the two species of uacari monkeys: Cacajao calvus and Cacajao melanocephalus.

It has been suggested in the literature that primates of the genus Cacajao have been restricted to flooded-forest habitats of western Amazonia since their split from the Chiropotes line in the Tertiary. It has been proposed further that the differentiation of the two species of this genus, Cacajao melanocephalus and Cacajao calvus, occurred during the Pleistocene period as a result of the fragmentation of the Amazon forest and the isolation of populations in these forest fragments or refuges. However, recent evidence has shown that at least C. melanocephalus is not dependent on flooded-forest habitats, and molecular analysis of mitochondrial DNA shows that the two species had already differentiated during the Pliocene, thus Pleistocene glaciations do not explain the speciation in Cacajao. Considering that C. melanocephalus and its closest relative, Chiropotes, inhabit terra firme forests, it is suggested that preference for flooded-forest habitats may be an apomorphy in C. calvus.

The quaternary cuban platyrrhine Paralouatta varonai and the origin of Antillean monkeys.

We describe recently recovered dental and mandibular remains of the Cuban platyrrhine Paralouatta varonai, previously known from the holotype only (a nearly complete skull with very worn teeth). We also expand on the original description of the type specimen. Paralouatta is one of three extinct taxa of Greater Antillean Quaternary monkeys known from craniodental remains. The other two, Xenothrix mcgregori and Antillothrix bernensis, occurred in Jamaica and Hispaniola, respectively. It has been common practice to assume that Antillean monkeys were more closely related to individual mainland taxa than to each other. Thus, P. varonai was thought to be related to Alouatta; Antillothrix bernensis to Saimiri or Cebus; and X. mcgregori to Callicebus, or to callitrichines, or even to be of unknown affinity. With the discovery of well-preserved dental remains of Paralouatta, it can now be ascertained that this species was in fact very different from Alouatta. Cladistic analysis reveals a sister-group relationship between Antillothrix and Paralouatta, followed on the cladogram by Xenothrix and Callicebus (last taxon being the closest mainlaind relative of the Antillean clade). This conclusion has an important biogeographic implication: recognition of an Antillean clade, as advocated here, assumes only one primate colonization from the South American mainland, not several as previously believed.

A clade of New World primates with distinctive alphoid satellite DNAs.

Centromerically located alphoid satellite DNAs are present in all primates. They typically consist of arrays of a 340-bp monomeric unit that is composed of related, but diverged, 170-bp subunits. A unique monomeric unit has recently been described: the alphoid satellite monomers of the neotropical primate Chiropotes satanas (bearded saki) are typically 539 bp in length. In addition, a number of smaller satellite sequences are present in this species. Analysis of two primates closely related to Chiropotes, Pithecia irrorata (saki) and Cacajao melanocephalus (uakari), show that they also contain unique alphoid satellites that are different from those of Chiropotes and different from one another. Southern blot and sequence analyses suggest that an alphoid satellite rearrangement(s) occurred early in the history of the tribe Pitheciini (Chiropotes, Pithecia, Cacajao) and that rearrangements are continuing to occur in this group of primates.

Nuciruptor rubricae, a new pitheciin seed predator from the Miocene of Colombia.

A new genus and species of platyrrhine primate, Nuciruptor rubricae, are added to the increasingly diverse primate fauna from the middle Miocene of La Venta, Columbia. This species displays a number of dental and gnathic features indicating that it is related to living and extinct Pitheciinae (extant Callicebus, Pithecia, Chiropotes, Cacajao, and the Colombian middle Miocene Cebupithecia sarmientoi). Nuciruptor is markedly more derived than Callicebus but possesses a less derived mandibular form and incisor-canine complex than extant and extinct pitheciins (Cebupithecia, Pithecia, Chiropotes, and Cacajao), suggesting that it is a primitive member of the tribe Pitheciini within the larger monophyletic Pitheciinae. Nuciruptor has procumbent and moderately elongate lower incisors and low-crowned molars, suggesting that is was a seed predator, as are living pitheciins. Its estimated body size of approximately 2.0 kg places it within the size range of extant pitheciines. The dental and gnathic morphology of Nuciruptor clarifies several aspects of dental character evolution in Pitheciinae and makes it less likely that the enigmatic Mohanamico hershkovitzi (m. Miocene, Columbia) is a pitheciin.

Radiation and speciation of spider monkeys, genus Ateles, from the cytogenetic viewpoint.

The chromosomes of 22 animals of four subspecies of the genes Ateles (A. paniscus paniscus, A. p. chamek, A. belzebuth hybridus, and A. b. marginatus) were compared using G/C banding and NOR (nucleolar organizer region) staining methods. The cytogenetic data of Ateles in the literature were also used to clarify the phylogenetic relationships of the species and subspecies and to infer the routes of radiation and speciation of these taxa. Chromosomes 6 and 7 that showed more informative geographic variation and the apomorphic form 4/12, exclusively in A. p. paniscus, are the keys for understanding the evolution, radiation, and specification of the Ateles taxa. The ancestral populations of the genus originated in the southwestern Amazon Basin (the occurrence area of A. paniscus chamek) and spread in the Amazon Basin and westward, crossing the Andes and colonizing Central America and northwesternmost regions of South America. The evolutionary history of the northern South American taxa is interpreted using the model of biogeographical evolution postulated by Haffer [Science 185:131-137, 1969]. Ateles paniscus paniscus is the genetically most differentiated form and probably derives from A. belzebuth hybridus. Based on the karyotype differences, the populations of Ateles can be divided into four different groups. These findings indicate the necessity of a more coherent taxonomic arrangement for the taxa of Ateles.

[Parasitological evidence on the phylogeny of hominids and cebids]. / Evidencia parasitológica sobre la filogenia de los homínidos y los cébidos.

A systematic revision of the ectoparasites (lice) of the hominids and ceboids supports the Trogloditian hypothesis, according to which the genus Homo is the sister of Pan, and the genus Gorilla the sister group of both. The phylogenetic analysis of this matrix derived from the study of primate lice shows an C.I. of 0.71 for the Trogloditian hypothesis including the ceboids in the analysis.

Evidencia parasitológica sobre la filogenia de los homínidos y los cébidos / Parasitological evidence about the phylogeny of the hominoids and the ceboids

A systematic revision of the ectoparasites (lice) of the hominids and ceboids supports the Trogloditian hypothesis, according to which the genus Homo is the sister of Pan, and the genus Gorilla the sister group of both. The phylogenetic analysis of this matrix derived from the study of primate lice shows an C.I. of 0.71 for the Trogloditian hypothesis including the ceboids in the analysis

A complete skeleton of the giant South American primate Protopithecus.

A complete skeleton of a large-bodied New World monkey has been found in Pleistocene cave deposits in the Brazilian state of Bahia. It demonstrates an unprecedented combination of body size, locomotor and cranial morphology. Skeletal features indicate an animal of approximately 25 kg, more than twice the mass of any living South American monkey. We refer the specimen to Protopithecus brasiliensis Lund, 1838, a large Pleistocene primate originally represented by only a proximal femur and distal humerus. The skeleton resembles species of two distinct New World monkey lineages. The cranium is modified for an enlarged vocal sac typical of living howler monkeys, and the postcranium includes suspensory and brachiating components of locomotion as seen in living spider and woolly spider monkeys. This skeleton confirms that adaptive diversity in neotropical primates was greater in the recent past, and that current interpretations of how their distinctive adaptations evolved should be revised.

DNA evidence on the phylogenetic systematics of New World monkeys: support for the sister-grouping of Cebus and Saimiri from two unlinked nuclear genes.

Previous inferences from epsilon-globin gene sequences on cladistic relationships among the 16 extant genera of Ceboidea (the New World monkeys) were tested by strength of grouping and bootstrap values for the clades in the most parsimonious trees found: for this epsilon data set enlarged with additional Cebus and Saimiri orthologues; for another nuclear DNA sequence data set consisting of IRBP (interstitial retinol-binding protein gene) intron 1 orthologues; and for tandemly combined epsilon and IRBP sequences. Different ceboid species of the same genus always grouped strongly together as demonstrated by results on Cebus (capuchin monkeys), Saimiri (squirrel monkeys), Callicebus (titi monkeys), Aotus (night monkeys), Ateles (spider monkeys), and Alouatta (howler monkeys). Other strong groupings that could be represented as monophyletic taxa in a cladistic classification were: Cebuella (pygmy marmoset) and Callithrix (marmoset) into subtribe Callitrichina; Callitrichina, Callimico (Goeldi's monkey), Leontopithecus (lion tamarin), and Saguinus (tamarin) into subfamily Callitrichinae; Callitrichinae, Aotus, Cebus, and Saimiri into family Cebidae; Cacajao (uakari monkey) and Chiropotes (saki) into subtribe Chiropotina; Chiropotina and Pithecia (bearded saki) into tribe Pitheciini; Pitheciini and Callicebus into subfamily Pitheciinae; Brachyteles (woolly spider monkey), Lagothrix (woolly monkey), and Ateles into tribe Atelini; and Atelini and Alouatta into subfamily Atelinae. In addition the epsilon and IRBP results congruently grouped (but at lesser strengths) Brachyteles and Lagothrix into subtribe Brachytelina within Atelini, and also Cebus and Saimiri into subfamily Cebinae within Cebidae. Because the IRBP results weakly grouped Pitheciinae with Cebidae, whereas the epsilon results weakly grouped Pitheciinae with Atelinae, the present evidence is best represented in an interim cladistic classification of ceboids by dividing the superfamily Ceboidea into three families: Atelidae, Pitheciidae, and Cebidae.

An Early Miocene anthropoid skull from the Chilean Andes.

Partly because of their poor fossil record, the relationships of neotropical platyrrhine monkeys to other groups of primates and to each other remain perhaps the most poorly known for any major primate clade. Here we report the discovery of a complete platyrrhine skull from the Andes of central Chile, by far the best preserved Tertiary primate cranium from South America. This find, coupled with recent phylogenetic analyses of higher groups of anthropoid primates, has the potential to revise substantially our understanding of platyrrhine interrelationships, indicating, among other points, significant modification to reconstruction of the ancestral platyrrhine morphotype and a likely African origin for New World monkeys. A 40Ar/39Ar radioisotopic date directly associated with the skull indicates an Early Miocene age, marking the first report of South American mammals of this age from outside Argentine Patagonia. Finally, this discovery demonstrates the enormous potential of vastly distributed, but virtually untapped, Andean volcaniclastic deposits to yield further insights into the origin and diversification of South American primates.