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.     

Molecular phylogeny of ateline new world monkeys (Platyrrhini, atelinae) based on gamma-globin gene sequences: evidence that brachyteles is the sister group of lagothrix

Nucleotide sequences, each spanning approximately 7 kb of the contiguous gamma1 and gamma2 globin genomic loci, were determined for seven species representing all extant genera (Ateles, Lagothrix, Brachyteles, and Alouatta) of the New World monkey subfamily Atelinae. After aligning these seven ateline sequences with outgroup sequences from several other primate (non-ateline) genera, they were analyzed by maximum parsimony, maximum likelihood, and neighbor-joining algorithms. All three analyzes estimated the same phylogenetic relationships: [Alouatta [Ateles (Brachyteles, Lagothrix)]]. Brachyteles and Lagothrix are sister-groups supported by 100% of bootstrap replications in the parsimony analyses. Ateles joins this clade, followed by the basal genus Alouatta; these joinings were strongly supported, again with 100% bootstrap values. This cladistic pattern for the four ateline genera is congruent with that obtained in previous studies utilizing epsilon-globin, IRBP, and G6PD nuclear genomic sequences as well as mitochondrial COII sequences. Because the number of aligned nucleotide positions is much larger in the present datasetoff than in any of these other datasets, much stronger support was obtained for the cladistic classification that divides subfamily Atelinae into tribes Alouattini (Alouatta) and Atelini, while the latter divides into subtribes Atelina (Ateles) and Brachytelina (Brachyteles and Lagothrix).     

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

The chromosomes of 22 animals of four subspecies of the genus 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 group. These findings indicate the necessity of a more coherent taxonomic arrangement for the taxa of Ateles. Am. J. Primatol. 42:167–178, 1997. © 1997 Wiley-Liss, Inc.     

Atelinae adaptations: behavioral strategies and ecological constraints.

Comparisons between the four genera that make up the Atelinae reveal two distinct behavioral patterns, one in which energy expenditure is minimized (Alouatta) and one in which energy intake is maximized (Lagothrix, Ateles, and Brachyteles). Among the atelins, Lagothrix and Ateles devote over 75% of their annual feeding time to fruit, while Brachyteles devotes between 50% and 67% of their feeding time to leaves. Pronounced seasonality in the Atlantic coastal forest inhabited by Brachyteles may be responsible for its more folivorous diet. Alouatta falls in the body size range of Lagothrix and is much smaller than Ateles and Brachyteles. Nonetheless, Alouatta is more folivorous than sympatric atelins. The atelins also share a rapid, suspensory mode of locomotion that appears to enable them to minimize travel time between widely dispersed fruit sources. Alouatta, by contrast, employs a slower, but more energetically efficient, quadrupedal locomotion. Ranging patterns among the Atelinae are consistent with both diet and locomotor abilities: Atelins travel daily distances up to 5,000 m; Alouatta ranges are much shorter. Further distinctions are evident in Atelinae grouping patterns. Alouatta remains in small cohesive groups that occupy home ranges less than 60 ha in size. Both Lagothrix and Ateles have large groups that fission to reduce the costs of intragroup feeding competition when preferred fruits occur in small patches within much larger community ranges. While greater reliance on low-energy foods such as leaves may release Brachyteles from similar competitive constraints, their tendency toward fluid grouping associations is consistent with the pursuit of a frugivorous diet.     

Chromosomal phylogeny of Lagothrix, Brachyteles, and Cacajao

Based on a comparison of the karyotypes of two Plathyrrhini species, Cacajao melanocephalus (Pitheciinae) and Brachyteles arachnoides (Atelinae), with those of two previously studied species, Lagothrix lagothrica (Atelinae) and C calvus rubicundus (Pitheciinae), it appears that the two Cacajao species have undergone the same number of chromosome rearrangements since they diverged from their common ancestor and that the karyotype of Brachyteles is ancestral to that of Lagothrix. The chromosomal phylogeny of these four species is proposed. A Y-autosome translocation is present in the karyotypes of the two Cacajao species.     

Nuclear DNA variation in spider monkeys (Ateles)

Phylogenetic relationships based on DNA sequence variation for the aldolase A intron V nuclear genomic region were evaluated and compared to phylogenies based on mitochondrial DNA sequence variation among spider monkeys (Ateles). Samples of Ateles ranging from Central America throughout the Amazon Basin were sequenced to determine phylogenetic relationships among geographically widely distributed populations. Analysis of nuclear DNA sequences using parsimony, maximum-likelihood, and genetic distance analyses produced similar phylogenies. Four previously proposed monophyletic species of spider monkeys were: (1) Ateles paniscus, composed of haplotypes from the northeastern Amazon Basin; (2) A. belzebuth, found in the western and southern Amazon Basin; (3) A. hybridus, located primarily along the Magdalena River valley of Colombia; and (4) A. geoffroyi, including all haplotypes found in the Choco region of South America and throughout Central America. The nuclear phylograms were analyzed based on associated bootstrap support and confidence probabilities. Support from the nuclear DNA genome was less robust than support from the mitochondrial DNA data, most likely due to a level of sequence variation, which was 90% less than that of the mitochondrial DNA genome. Nuclear DNA congruencies with mitochondrial DNA-based phylogenies, as supported by the incongruence length difference and winning sites tests, provide further support for the suggested revisions in Ateles taxonomy that are contradictory to long-held taxonomies based on pelage variation.     

Chromosomal homologies between Cebus and Ateles (primates) based on ZOO-FISH and G-banding comparisons

ZOO-FISH (Fluorescent "in vitro" hybridization) was used to establish the chromosomal homology between humans (HSA) and Cebus nigrivitatus (CNI) and Ateles belzebuth hybridus (ABH). These two species belong to different New World monkey families (Cebidae and Atelidae, respectively) which differ greatly in chromosome number and in chromosome morphology. The molecular results were followed by a detailed banding analysis. The ancestral karyotype of Cebus was then determined by a comparison of in situ hybridization results, as well as chromosomal morphology and banding in other Platyrrhini species. The karyotypes of the four species belonging to the genus Cebus differ from each other by three inversions and one fusion as well as in the location and amounts of heterochromatin. Results obtained by ZOO-FISH in ABH are in general agreement with previous gene-mapping and in situ hybridization data in Ateles, which show that spider monkeys have highly derived genomes. The chromosomal rearrangements detected between HSA and ABH on a band-to-band basis were 27 fusions/fissions, 12 centromeric shifts, and six pericentric inversions. The ancestral karyotype of Cebus was then compared with that of Ateles. The rearrangements detected were 20 fusions/fissions, nine centromeric shifts, and five inversions. Atelidae species are linked by a fragmentation of chromosome 4 into three segments forming an association of 4/15, while Ateles species are linked by 13 derived associations. The results also helped clarify the content of the ancestral platyrrhine karyotype and the mode of chromosomal evolution in these primates. In particular, associations 2/16 and 5/7 should be included in the ancestral karyotype of New World monkeys.     

Locomotor behavior of Lagothrix lagothricha and Ateles belzebuth in Yasuní National Park, Ecuador: general patterns and nonsuspensory modes.

Field study of the locomotor behavior of sympatric woolly monkeys (Lagothrix lagothricha) and spider monkeys (Ateles belzebuth) in undisturbed rainforest of northern Ecuador revealed similar patterns in use of plant forms (categorized tree and liana structure), and substantial differences in the frequencies of use of different grouped modes (aggregates of kinematically similar specific modes). Lagothrix progressed more than Ateles by leaping/dropping and quadrupedal walking/running, whereas Ateles exhibited more suspensory locomotion. Grouped modes are associated with different plant forms in similar ways in the two species. In contrast, the species differed in use of tree zone (trunk/bole, major branches, intermediate branches, and terminal branches), with Lagothrix using intermediate branches and Ateles terminal branches more. Correlated with this difference was greater use by Lagothrix of quadrupedal movement, especially on intermediate branches, and greater use of suspensory modes by Ateles, especially in the terminal zone. Further research is needed to determine how these patterns are facilitated and constrained by morphological mechanisms. Analysis of specific locomotor modes within groups shows several interspecific differences in relative frequencies.     

Geophagy in brown spider monkeys (Ateles hybridus) in a lowland tropical rainforest in Colombia

Spider monkeys and howler monkeys are the only Neotropical primates that eat soil from mineral licks. Not all species within these genera visit mineral licks, and geophagy has been restricted to populations of Ateles belzebuth belzebuth,Ateles belzebuth chamek and Alouatta seniculus in western Amazonian rainforests. With the aid of a camera trap we studied the visitation patterns of a group of brown spider monkeys (Ateles hybridus) to a mineral lick at Serrania de Las Quinchas, in Colombia. Spider monkeys visited the lick frequently throughout the year, with a monthly average of 21.7 ± 7.2 visits per 100 days of camera trapping (n = 14 months). Spider monkeys visited the mineral lick almost always on days with no rain, or very little (<3 mm) rain, suggesting that proximate environmental variables might determine spider monkeys' decisions to come to the ground at the licks. This study expands the geographical occurrence of mineral lick use by spider monkeys providing additional data for future assessments on the biogeographical correlates of mineral lick use by platyrrhines.     

Gene assignment in the spider monkey (Ateles paniscus chamek--APC): APE-MYH7 to 2q; AR-GLA-F8C to the X chromosome.

Comparative gene assignment between the spider monkey species Ateles paniscus chamek (APC) and man (HSA) showed conserved syntenic associations despite extensive karyotypic rearrangement between species. Two HSA 14q genes were allocated to APC 2q, being syntenic to other HSA 14q and HSA 15q markers previously assigned to APC 2q, and to HSA 12q genes previously assigned to APC 2p. These findings were consistent with A. geoffroyi chromosome painting with human whole-chromosome probes, indicating that the genus Ateles is karyotypically very rearranged. On the other hand, three human X-linked markers were assigned to the Ateles X chromosome, indicating that this chromosome is evolutionary stable.     

Phylogenetic Relationships of Spider Monkeys (Ateles) Based on Mitochondrial DNA Variation

Our goal was to determine phylogenetic relationships among geographically and taxonomically distinct haplotypes of spider monkeys (Ateles) based on DNA sequence variation for the mitochondrial DNA control region and cytochrome c oxidase subunit II gene. We obtained samples from most previously recognized subspecies of Ateles, ranging from Central America throughout the Amazon Basin, to determine phylogenetic relationships among racially recognized groups. Comparison of DNA sequences using both parsimony analysis and genetic distance analysis produced phylogenetic relationships that were very similar for each genetic region. We analyzed the phylograms produced, along with associated bootstrap support, confidence probabilities, and genetic distances between taxonomic groups, to identify four monophyletic species of Ateles: Ateles paniscus, composed of haplotypes from the northeastern Amazon Basin; A. belzebuth in the southern Amazon Basin; A. hybridus, located primarily along the Magdalena River valley of Colombia; and A. geoffroyi, which includes two former species: A. geoffroyi and A. fusciceps. This arrangement is contradictory to long-held taxonomies of Ateles based on pelage variation and is similar to a recent analysis based on craniodental variation. Results of this investigation suggest patterns of gene flow, evolutionary relationships, and speciation patterns that are more plausible than previous pelage-based taxonomies, which required seemingly impossible patterns of gene flow. Conservation efforts aimed at protecting Ateles, one of the Neotropics most endangered genera, will also benefit from the findings presented in this paper.     

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.     

Polymorphism of visual pigment genes in the muriqui (Primates, Atelidae)

Colour vision varies within the family Atelidae (Primates, Platyrrhini), which consists of four genera with the following cladistic relationship: {Alouatta[Ateles (Lagothrix and Brachyteles)]}. Spider monkeys (Ateles) and woolly monkeys (Lagothrix) are characteristic of platyrrhine monkeys in possessing a colour vision polymorphism. The polymorphism results from allelic variation of the single-locus middle-to-long wavelength (M/L) cone opsin gene on the X-chromosome. The presence in the population of alleles coding for different M/L photopigments results in a variety of colour vision phenotypes. Such a polymorphism is absent in howling monkeys (Alouatta), which, alone among platyrrhines, acquired uniform trichromatic vision similar to that of Old World monkeys, apes, and humans through opsin gene duplication. Dietary and morphological similarities between howling monkeys and muriquis (Brachyteles) raise the possibility that the two genera share a similar form of colour vision, uniform trichromacy. Yet parsimony predicts that the colour vision of Brachyteles will resemble the polymorphism present in Lagothrix and Ateles. Here we test this assumption. We obtained DNA from the blood or faeces of 18 muriquis and sequenced exons 3 and 5 of the M/L opsin gene. Our results affirm the existence of a single M/L cone opsin gene in the genus Brachyteles. We detected three alleles with predicted lambdamax values of 530, 550, and 562 nm. Two females were heterozygous and are thus predicted to have different types of M/L cone pigment. We discuss the implication of this result towards understanding the evolutionary ecology of trichromatic vision.     

Suspensory locomotion of Lagothrix lagothricha and Ateles belzebuth in Yasuní National Park,Ecuador

A comparative field study of the locomotion of woolly monkeys (Lagothrix lagothricha) and spider monkeys (Ateles belzebuth) in undisturbed rainforest of northeastern Ecuador reveals substantial differences in their use of suspensory modes. Ateles performed both more brachiation (by forelimbs and tail, with trunk rotation), and forelimb swing (similar to brachiation, but without trunk rotation) than Lagothrix. In contrast, in Lagothrix 20% of suspensory movement was by pronograde forelimb swing, which resembles forelimb swing except that the body is held in a pronograde orientation due to the tail and/or feet intermittently grasping behind the trailing forelimb. Ateles never exhibited this mode. Both brachiation and forelimb swing by Ateles were more dynamic than in Lagothrix, consisting of higher proportions of full-stride bouts (versus single-step). Both species used smaller supports for suspensory than for quadrupedal locomotion, and Ateles used both smaller and larger supports for suspension than did Lagothrix. Analysis of support inclination shows that both species tended to perform more above-support movement on horizontal supports and more below-support (suspensory) movement from oblique supports. Our attempt to elucidate the aspects of canopy structure that favor suspension suggests the need for additional kinds of observational data, focusing on the "immediate structural context" of positional events.     

Party size and diet of syntopic atelids (Ateles chamek and Lagothrix cana) in Southwestern Brazilian Amazonia.

Syntopic Alouatta seniculus, Ateles chamek and Lagothrix cana (Atelidae) were studied in southwestern Amazonia. Primate populations were first surveyed, and then the party size, diet and vertical spacing were monitored over a 5-month period. Atelids accounted for more than half the survey sightings and Lagothrix was the most abundant. Party sizes recorded for both Alouatta and Lagothrix during monitoring were significantly larger than those recorded during surveys, but no such difference was found for Ateles. Monitored parties were significantly larger in Lagothrix in comparison with either Alouatta or Ateles, as were groups of Ateles in comparison with Alouatta. Mean party size in Ateles decreased progressively during the course of the study, from 8.9 +/- 3.4 in June to 3.9 +/- 2.3 in October. Moraceae was the most important dietary resource for Ateles and Lagothrix, in terms of both feeding records and number of species exploited. There was considerable overlap in the plant taxa exploited, but some notable differences, such as the exclusive use of Hymenaea courbaril (Caesalpinaceae) by Lagothrix and of Euterpe precatoria (Arecaceae) by Ateles. As at other sites in the region, Ateles occupied significantly higher forest strata in comparison with Lagothrix. Despite the preliminary nature of the study, the results indicate a number of ecological differences between species that undoubtedly play an important role in niche separation.     

Synteny of human chromosomes 14 and 15 in the platyrrhines (Primates, Platyrrhini)

In order to study the intra- and interspecific variability of the 14/15 association in Platyrrhini, we analyzed 15 species from 13 genera, including species that had not been described yet. The DNA libraries of human chromosomes 14 and 15 were hybridized to metaphases of Alouatta guariba clamitans, A. caraya, A. sara, Ateles paniscus chamek, Lagothrix lagothricha, Brachyteles arachnoides, Saguinus midas midas, Leontopithecus chrysomelas, Callimico goeldii, Callithrix sp., Cebus apella, Aotus nigriceps, Cacajao melanocephalus,Chiropotes satanas and Callicebus caligatus. The 14/15 hybridization pattern was present in 13 species, but not in Alouatta sara that showed a 14/15/14 pattern and Aotus nigriceps that showed a 15/14/15/14 pattern. In the majority of the species, the HSA 14 homologue retained synteny for the entire chromosome, whereas the HSA 15 homologue displayed fragmented segments. Within primates, the New World monkeys represent the taxon with the highest variability in chromosome number (2n = 16 to 62). The presence of the HSA 14/15 association in all species and subspecies studied herein confirms that this association is the ancestral condition for platyrrhines and that this association has been retained in most platyrrhines, despite the occurrence of extensive inter- and intrachromosomal rearrangements in this infraorder of Primates.     

Immunodiffusion systematics of the primates. Part V. The Platyrrhini.

Evolutionary relationships between New World monkeys and marmoset genera and the place of the Ceboidea within the primates are considered in terms of the immunological specificity of ceboid proteins. Antigenic distances between the New World primates are measured using antisera produced in rabbits to nine ceboid genera: Alouatta, Aotes, Ateles, Callicebus, Cebus, Chiropotes, Lagothrix, Saimiri and Saguinus. A cladogram constructed on the basis of increasing degrees of antigenic distance between branches depicts Ceboidea as a monophyletic assemblage within which Alouatta is grouped with the Atelinae genera, Lagothrix and Ateles, Chiropotes joins Cacajao and Cebus joins Saimiri. The joining of the cebid genera Aotes and Callicebus with callithricid genera Callimico and Saguinus into a single complex lineage suggests that Cebidae is a paraphyletic or polyphyletic taxon. A phylogenetic taxonomy for Platyrrhini is proposed.     

Evolutionary disruptions of human syntenic groups 3, 12, 14, and 15 in Ateles paniscus chamek (Platyrrhini, primates)

Comparative gene assignments of 18 markers, based on analyses of somatic cell hybrids and previous data in the literature, indicated that human (HSA) syntenic groups 3, 12, 14, and 15 are dissociated in the spider monkey species Ateles paniscus chamek (APC). Markers present in HSA 3p were allocated to APC 3 and APC 9. The HSA 12 cluster was split into two syntenic groups, one mainly including HSA 12p markers in APC 16 and the other, including HSA 12q markers, in APC 2p. The HSA 14q cluster split into three syntenic groups, corresponding to APC 2q, APC 6, and APC 12. Finally, the HSA 15 cluster split into two syntenic groups, APC 2q and APC 3. Comparisons with previous gene assignments and human SROs led to the tentative postulation of rearrangements having occurred during the evolutionary divergence of man and A. paniscus chamek. Chromosome painting data in the congeneric species A. geoffroyi, other New World and Old World primates, and several representative non-primate animals were compared in an attempt to delineate the ancestral and derived conditions underlying the evolutionary rearrangement of syntenic groups in mammals.     

Qualitative analysis of constitutive heterochromatin and primate evolution

The results of qualitative heterochromatin analysis in 16 species of primates: Homo sapiens , Pan troglodytes and Gorilla gorilla (F. Hominidae), Hylobates syndactilus (F. Hylobatidae), Macaca fascicularis , M. tibetana , Mandrillus sphinx , M. leucophaeus , Cercopithecus aethiops , C. sabaeus and C. albogularis (F. Cercopithecidae), Cebus apella , Ateles belzebuth hybridus , Aotus azarae , Saimiri sciureus and Lagothrix lagothricha (F. Cebidae) are presented in this work. We characterized heterochromatin using: (a) in situ digestion with restriction enzymes AluI, HaeIII, RsaI and Sau3A, and (b) chromosome staining with DA/DAPI on unbanded chromosomes, on C-banded chromosomes and on sequentially G-C-banded chromosomes. The aim of this work was to relate the qualitative characteristics of constitutive heterochromatin observed with the cytogenetic evolutive processes in the primate group. Results obtained show that (1) in the family Cercopithecidae, Papionini species do not present chromosomal rearrangements when their karyotypes are compared and the heterochromatin characteristics are uniform, while Cercopithecini species show a high number of chromosomal reorganizations, but they have the same heterochromatic characteristics; (2) the Platyrrhini species analysed show variability in their karyological and heterochromatic characteristics; (3) the Hominoidea present two different situations: Pan , Gorilla and Homo with few chromosomal reorganizations among their karyotypes but with a high variability in their heterochromatin characteristics, and Hylobates with low heterochromatin variability and a highly derived karyotype. Speciation processes related to chromosome changes and heterochromatin variations in different groups of primates are discussed.  © 2003 The Linnean Society of London, Biological Journal of the Linnean Society , 2003, 80 , 107–124.     

Contribution of genetic distances studies to the taxonomy ofAteles,particularlyAteles paniscus paniscus andAteles paniscus chamek

We studied 20 electrophoretic loci in two populations ofAteles (Ateles paniscus paniscus andAteles paniscus chamek). We observed intrapopulational variation at the following loci: esterase D, glyoxalase 1, adenosine deaminase (A. p. chamek) and carbonic anhydrase 2 (A. p. paniscus). The two populations share the most frequent alleles at 17 loci, but we noted great differences in glyoxalase 1, adenosine deaminase and phosphoglucomutase 1.A. p. paniscus is monomorphic for theGLO1 ^*1 allele, which has a frequency of 6% inA. p.chamek. They did not share alleles in relation to the ADA and PGM1 loci. We found a CA2 allele, named hereCA2 ^*1, which has not been described previously in other neotropical primates (Sampaio et al., 1991a), inA. p. paniscus. The present results suggest that the geographical isolation represented by the Rio Amazonas has lasted long enough to support this level of divergence. These observations taken together with chromosomal findings, led us to endorse the proposal of two distinct species:Ateles paniscus andAteles chamek.