Y-chromosome Data and Tribal Affiliations of Allenopithecus and Miopithecus

The phylogeny of Old World monkeys has remained unresolved in part because of a lack of resolution in the Cercopithecinae. Competing morphological hypotheses have had Allen's swamp monkey (Allenopithecus nigroviridis) and the talapoins (Miopithecus spp.) as basal branches of either the tribe Cercopithecini or the tribe Papionini. Previous molecular analyses have not adequately addressed the issue. To better understand the evolutionary history of these primates, we sequenced and subjected to phylogenetic analysis 3.1 kb of 2 loci (TSPY and SRY) from the non-recombining portion of the Y-chromosome. Individuals from the genera Allenopithecus, Miopithecus, Erythrocebus, Chlorocebus, and Cercopithecus were surveyed and their sequences compared with those previously published for the Papionini and Colobinae. The results suggest Allenopithecus and Miopithecus are more closely related to the Cercopithecini than Papionini. Our data also support the hypothesis that within the Cercopithecini, Erythrocebus and Chlorocebus share a close evolutionary relationship, distinct from the other members of the tribe.     

Sex chromosome phylogenetics indicate a single transition to terrestriality in the guenons (tribe Cercopithecini)

This is the first molecular study to trace the evolutionary transition in substrate preference across a primate radiation. We surveyed 20 guenons (tribe Cercopithecini) and 4 outgroup taxa for two Y-chromosomal genes, TSPY ( approximately 2240 bp) and SRY ( approximately 780 bp), and one X-chromosomal intergenic region ( approximately 1600 bp) homologous to a fragment of human Xq13.3. Parsimony and maximum likelihood analyses of the sex chromosomal datasets consistently cluster the three terrestrial taxa, Cercopithecus aethiops, Cercopithecus lhoesti, and Erythrocebus patas, into a group that is reciprocally monophyletic with a clade of arboreal Cercopithecus spp. Given that the common ancestor of the two clades was most likely an arboreal taxon, this phylogenetic pattern suggests the transition to terrestriality occurred only once among the extant guenons. This pattern also indicates that the genus Cercopithecus is paraphyletic, as presently defined, and calls for taxonomic revision so that the nomen describes a strictly monophyletic group. We outline four acceptable taxonomic schemes and suggest that the most appropriate is to reassign C. aethiops, C. lhoesti, and E. patas to the resurrected genus Chlorocebus. Finally, while the phylogeny and taxonomy of terrestrial guenons were the focus of this study, the X-chromosome sequences presented here represent the first molecular evidence to unambiguously place Allenopithecus nigroviridis as the basal lineage of the tribe Cercopithecini.     

Reciprocal painting between humans, De Brazza's and patas monkeys reveals a major bifurcation in the Cercopithecini phylogenetic tree

We report on reciprocal painting between humans and two Cercopithecini species, Erythrocebus patas (patas monkey) and Cercopithecus neglectus (De Brazza's monkey). Both human and monkeys chromosome-specific probes were made by degenerate oligonucleotide primed PCR (DOP-PCR) from flow sorted chromosomes. Metaphases of both monkey species were first hybridized with human chromosome-specific probes and then human metaphases were hybridized with chromosome paints from each monkey species. The human paint probes detected 34 homologous segments on the C. neglectus karyotype, while the C. neglectus probes, including the Y, revealed 41 homologous segments on the human karyotype. The probes specific for human chromosomes detected 29 homologous segments in the E. patas karyotype, while the patas monkey probes painted 34 segments on the human karyotype. We tested various hypotheses of Cercopithecini phylogeny and taxonomy developed by morphologists, molecular biologists and cytogeneticists. Our hybridization data confirm that fissions (both Robertsonian and non-Robertsonian) are the main mechanism driving the evolutionary trend in Cercopithecini toward higher diploid numbers and strongly suggest an early phylogenetic bifurcation in Cercopithecini. One branch leads to Cercopithecus neglectus/Cercopithecus wolfi while the other line leads to Erythrocebus patas/Chlorocebus aethiops. Allenopithecus nigroviridis may have diverged prior to this major phylogenetic node.     

Molecular phylogeny of Old World monkeys (Cercopithecidae) as inferred from gamma-globin DNA sequences

DNA sequence data of the nuclear-encoded gamma1-gamma2-globin duplication region were used to examine the phylogenetic relationships of 16 cercopithecid (Old World monkey) species representing 12 extant genera. Morphology- and molecular-based hypotheses of Old World monkey branching patterns are generally congruent, except for generic relationships within the subtribe Papionina. The cercopithecids divide into colobines (leaf-eating monkeys) and cercopithecines (cheek-pouched monkeys). The colobines examined by the DNA data divide into an Asian clade (Nasalis, proboscis monkeys; Trachypithecus, langurs) and an African clade (Colobus, colobus monkeys). The cercopithecines divide into tribes Cercopithecini (Erythrocebus, patas monkey; Chlorocebus, green monkeys; Cercopithecus, guenons) and Papionini. Papionins divide into subtribes Macacina (Macaca, macaques) and Papionina (Papio, hamadryas baboons; Mandrillus, drills and mandrills; Theropithecus, gelada baboons; Lophocebus, arboreal mangabeys; Cercocebus, terrestrial mangabeys). In a morphologically based classification, Mandrillus is a subgenus of Papio, whereas Lophocebus is a subgenus of Cercocebus. In contrast, the molecular evidence treats Mandrillus as a subgenus of Cercocebus, and treats both Theropithecus and Lophocebus as subgenera of Papio. Local molecular clock divergence time estimates were used as a yardstick in a "rank equals age" system to propose a reduction in taxonomic rank for most clades within Cercopithecidae.     

X-chromosomal window into the evolutionary history of the guenons (Primates: Cercopithecini)

Molecular studies of the guenons suggest that the arboreal Cercopithecus species form a monophyletic group within the tribe Cercopithecini. However, the evolutionary relationships among these arboreal congeners remain poorly resolved. The present work marks the first attempt to reconstruct the history of this group through the phylogenetic analysis of long nuclear sequences. We surveyed 19 guenons and seven outgroup taxa for a approximately 9.3kb fragment of X-chromosomal DNA homologous to a portion of human Xq13.3. Parsimony and maximum likelihood analyses of these sequences consistently recover two strongly-supported patterns within the arboreal Cercopithecus clade: (1) a clustering of members of the cephus and mitis species groups, and (2) a monophyletic aggregate including the mona, neglectus, and diana species groups. Although guenons occasionally hybridize in the wild, interbreeding forms of different species groups do not cluster together as sister-taxa in the X-chromosomal tree, suggesting that the two clades inferred here are not reticulate patterns due to recent gene flow. These clades are most likely the result of either ancestral hybridization or true phylogenetic history. We advocate the latter explanation because the same two aggregates (cephus/mitis and mona/neglectus/diana) are recovered, albeit with weak support, by a number of earlier analyses. Finally, X-chromosomal divergence dates are estimated for a number of nodes in the guenon radiation. The divergence of guenon and papionin lineages at 11.5 (+/-1.3) MYA appears to be a particularly robust estimate since it is inferred from both mitochondrial and X-chromosomal studies, each using different fossil calibration points.     

Y-Chromosome and Mitochondrial Markers in Macaca fascicularis Indicate Introgression with Indochinese M. mulatta and a Biogeographic Barrier in the Isthmus of Kra

This is the first report of Y-chromosome introgression between primate species. We sequenced 3.1 Kb of Y-chromosome DNA and 1.5 Kb of mtDNA for 27 macaques of Fooden's (Folia Primatol. [1976] 25: 225–236) fascicularis species group and 5 outgroup taxa (Macaca sylvanus, Papio hamadryas, Theropithecus gelada, Allenopithecus nigroviridis, and Cercopithecus mona). Phylogenies constructed separately for the paternal and maternal data sets show a Y-chromosome paraphyly among lineages of Macacafascicularis, but a mitochondrial monophyly for the same individuals. The Y-chromosome topology depicts Indochinese Macaca fascicularis haplotypes joining with those of M. mulatta, followed by M. cyclopis and M. fuscata, before clustering with a clade of lineages of M. fascicularis from peninsular Malaysia, Indonesia, and the Philippines. These contrasting patterns of mitochondrial and Y-chromosome DNA, evaluated in the context of the evolutionary consequences of macaque sex-biased dispersal, present strong evidence for contemporary hybridization between Macaca fascicularis and M. mulatta in Indochina and a biogeographic barrier in the Isthmus of Kra.     

Cladistic analysis of cercopithecid relationships

The phyletic relationships of cercopithecid higher taxa are fairly well understood. By reference to the outgroup Hominoidea, character state distributions for a variety of dental, cranial and posteranial features are reviewed and morphotypes are presented for supra-generic taxa. Cercopithecids show 13 derived conditions relative to the eucatarrhine morphotype. Cercopithecines are further derived by eight features while the colobine morphotype shows an additional nine synapomorphies, including three newly identified pedal features. Within Cercopithecinae, the tribes Papionini and Cercopithecini are each characterized by several derived states. In turn, each tribe includes a relatively conservative and a more derived clade, recognized at the subtribal level: Macacina and Papionina (including the previously recognized Theropithecina) for Papionini: and the newly defined Allenopithecina and Cercopithecina among Cercopithecini. The distinctions within Colobinae appear comparable to those defining cercopithecine subtribes, and two taxa are accepted at that rank: the African Colobina, defined by three derived states: and the possibly paraphyletic Asian Presbytina. Piliocolobus shares four synapomorphies with Procolobus and therefore is ranked as a subgenus of that taxon. The hypothesis that Dolichopithecus is the direct descendant of Mesopithecus is weakened on the basis of contrary pedal evidence.     

Local molecular clocks in three nuclear genes: divergence times for rodents and other mammals and incompatibility among fossil calibrations

Reconstructing the chronology of mammalian evolution is a debated issue between molecule- and fossil-based inferences. A methodological limitation of molecules is the evolutionary rate variation among lineages, precluding the application of the global molecular clock. We considered 2422 first and second codon positions of the combined ADRA2B, IRBP, and vWF nuclear genes for a well-documented set of placentals including an extensive sampling of rodents. Using seven independent calibration points and a maximum-likelihood framework, we evaluated whether molecular and paleontological estimates of mammalian divergence dates may be reconciled by the local molecular clocks approach, allowing local constancy of substitution rates with variations at larger phylogenetic scales. To handle the difficulty of choosing among all possible rate assignments for various lineages, local molecular clocks were based on the results of branch-length and two-cluster tests. Extensive lineage-specific variation of evolutionary rates was detected, even among rodents. Cross-calibrations indicated some incompatibilities between divergence dates based on different paleontological references. To decrease the impact of a single calibration point, estimates derived from independent calibrations displaying only slight reciprocal incompatibility were averaged. The divergence dates inferred for the split between mice and rats (approximately 13-19 Myr) was younger than previously published molecular estimates. The most recent common ancestors of rodents, primates and rodents, boreoeutherians, and placentals were estimated to be, respectively, approximately 60, 70, 75, and 78 Myr old. Global clocks, local clocks, and quartet dating analyses suggested a Late Cretaceous origin of the crown placental clades followed by a Tertiary radiation of some placental orders like rodents.     

A computer ethological-pharmacological analysis of the intraspecific behavior of primates

Experiments were performed on primates (Cercopithecus sabeus, Macaca maurus, Cebus apella). Possibility to formalize the structure of normal and pathological monkey behaviour was shown by computerized technique. Rigid dominant-subordinate structures (linear type) were demonstrated on Macaca maurus, Cercopithecus sabeus, Cebus apella. These structures display some variants of normal relationship between monkeys. Raising in isolation from conspecifics determines behavioural disadaptation and pathological behaviour, e.g. "timid-defensive" syndrome. Model of "timid-defensive" syndrome in isolated primates seems to be useful for psycho-pharmacological research, for assessment of anxiolytic and antidepressive properties of drugs.     

Prevalence of antibody reaction with cercopithecine herpesvirus 1 antigen in Macaca cyclopis, Macaca fascicularis, and Papio anubis in Taiwan

BACKGROUND AND METHODS: A total of 284 non-human primate sera were collected between December 2004 and September 2005 and tested by a commercially available dot immunobinding assay for the antibodies to cercopithecine herpesvirus 1, an alphaherpesvirus with high mortality for infected humans. RESULTS: Seropositive rates were 58% among non-human primates from animal shelters and 38% among those from zoos and academic institutes. Positive reactors were found in three species, the Formosan macaque (Macaca cyclopis; 57%), the cynomolgus macaque (Macaca fascicularis; 11%) and the olive baboon (Papio anubis; 68%). CONCLUSIONS: Our results showed that natural infection by cercopithecine herpesvirus 1 in Formosan macaques was highly prevalent, and to a certain extent reflected the situation of the wild populations in Taiwan. The findings raised the issues of zoonotic public health and the occupational health of primate workers. High positive rate in olive baboons was also found, although, it cannot be ruled out that the positivity was due to cross-reactivity between cercopithecine herpesvirus 1 and other herpesviruses.     

Kinematics of the cercopithecine foot on arboreal and terrestrial substrates with implications for the interpretation of hominid terrestrial adaptations

The stereotyped characterizations of quadrupedal foot postures were tested by examining the kinematics of the cercopithecine foot on arboreal and terrestrial supports. Strictly arboreal species were compared with semi-terrestrial species for Cercopithecus, Cercocebus, Lophocebus, and Papio, in semi-natural or experimental settings. Results indicate that the kinematics of the cercopithecine arboreal quadruped differ in degree from stereotypical expectations for an arboreal quadruped. The relatively extended, adducted limb movements of the cercopithecines and the emphasis on the central digit as the functional axis of the foot suggest convergence with terrestrial mammalian cursors, and differ from the platyrrhine or colobine arboreal quadruped. The characteristics of the quadrupedal terrestrial primate foot contrast with the very unique pattern seen in the hominid foot. These contrasts provide a new perspective from which to interpret the hominid adaptation, in which the functional axis has remained fixed between the first and second digits. This pattern differs from virtually all other terrestrial mammals. The influence of bipedalism on this functional pattern is examined.     

A mobile element-based evolutionary history of guenons (tribe Cercopithecini)

Background  

Guenons (tribe Cercopithecini) are a species-rich group of primates that have attracted considerable attention from both primatologists and evolutionary biologists. The complex speciation pattern has made the elucidation of their relationships a challenging task, and many questions remain unanswered. SINEs are a class of non-autonomous mobile elements and are essentially homoplasy-free characters with known ancestral states, making them useful genetic markers for phylogenetic studies.     

Comparative chromosome banding studies in the family Cercopithecidae

Comparative banding studies in eight species of the family Cercopithecidae, subfamily Cercopithecinae allowed us to identify the chromosomes that have been conserved and those that have undergone structural changes. The results suggest that while the ancestral karyotype of the Cercopithecini was probably similar to that ofCercopithecus aethiops, the ancestral complement of the cercopithecinae was probably of the type now found in the Papionini. Thus, after their divergence, one of the groups maintained an extremely stable chromosomal complement (Papionini 2n=42) while the other underwent extreme chromosomal rearrangements (Cercopithecini 2n=48–72).     

Comparative analysis of the fragments of highly repeated DNA of Homo, Pan, Macaca and Cercopithecus

In the present paper the restriction patterns of Homo, Pan troglodytes, Macaca fascicularis and Cercopithecus aethiops, obtained by digestion with Eco RI endonuclease, were compared. All these species showed two common bands at 0.3 and 0.6 Kb. In this region another band at 0.5 Kb was present in Macaca fascicularis and Cercopithecus aethiops. Furthermore Macaca fascicularis, Cercopithecus aethiops and Pan troglodytes showed a series of bands not present in humans. The distance matrix shows a strong similarity between Homo and Pan and a decreasing similarity with Macaca fascicularis and Cercopithecus aethiops. No intraspecific variability was observed.     

Congenital malformations and twinning in a breeding colony of Old World monkeys

Clinical and necropsy records of malformations in Old World monkeys were compiled. The numbers of malformations and birth incidence rate for each species were: Rhesus macaque (Macaca mulatta) 3 (1.02%); Cynomolgus macaque (Macaca fascicularis) 11 (1.62%); Stumptail macaque (Macaca arctoides) 3 (1.55%); African green monkey (Cercopithecus aethiops) 4 (1.5%). There was one pair of rhesus twins (twinning rate: 0.34%). Cardiovascular and central nervous system lesions accounted for 55% of all malformations. Only two of the malformations were in inbred infants. Nine of twenty-one colony-born malformed infants lived 24 hours or more.     

Blood markers and genetic evolution in Cercopithecinae

Serum proteins and RBC enzymes were surveyed in 16 species (183 animals) of African guenons (tribe Cercopithecini) in order to determine their genetic polymorphism and to establish dendrograms on the basis of their allele frequencies. The molecular data obtained were compared with those of mangabeys (16 animals tested) and discussed in the light of our results inPapio andMacaca. The species surveyed wereCercopithecus neglectus, C. hamlyni, C. l'hoesti (C. l'h. l'hoesti, C. l'h. preussi, andC. l'h. solatus), C. nictitans, C. mitis (C. m. kolbi, C. m. albotorquatus, C. m. stuhlmanni, andC. m. albogularis), C. cephus, C. ascanius, C. erythrotis, C. petaurista, C. mona, C. pogonias, C. wolfi, andC. aethiops, Miopithecus talapoin, Allenopithecus nigroviridis andErythrocebus patas, Lophocebus albigena, andCercocebus torquatus. Eleven loci (ten systems) were studied in red blood cell enzymes and the Gc, Gm, Km, and Bm systems in DBP and immunoglobulin serum proteins. Most of the loci were polymorphic. Similar and different polymorphisms occur in closely related species or subspecies, particularly inCercopithecus. Guenons have phenotypes clearly distinct from mangabeys.     

Comparison of Y chromosome and mtDNA phylogenies leads to unique inferences of macaque evolutionary history

We report here the results of one of the first analyses to use male-specific nuclear markers in elucidating primate phylogenetic relationships at the intrageneric level. Two closely linked Y chromosome markers, TSPY and SRY, were sequenced for a total of 3100 bases. Forty-four macaques, representing 18 of the 19 recognized species, were sequenced for the full 3.1 kb, as was 1 individual from each of the following outgroup genera: Papio, Theropithecus, Mandrillus, Allenopithecus,Cercopithecus, Trachypithecus, Presbytis, and Homo. In contrast to recent mtDNA phylogenies, Y chromosome loci support four monophyletic species groups, including a sinica group containing M. arctoides-a classification largely congruent with those of Fooden and Delson. Comparison of mtDNA and Y chromosome phylogenies highlight (1) a potential hybrid origin of Macaca arctoides from M. fascicularis and proto-M. assamensis/thibetana and (2) cases of mitochondrial paraphyly in macaque species whose Y chromosome lineages are monophyletic-a probable evolutionary consequence of philopatric females vs dispersing males. These results raise the question of whether a phylogenetic tree should be a topology of species origins or a depiction of more current species relationships, including subsequent episodes of introgression.     

AluI and HaeIII restriction enzyme banding patterns of Macaca fuscata and Cercopithecus aethiops sabaeus chromosomes

AluI and HaeIII restriction endonuclease banding patterns were analyzed in Macaca fuscata and Cercopithecus aethiops sabaeus chromosomes. AluI produced C-negative bands in both species of monkeys, while HaeIII induced the appearance of C-negative bands on Macaca chromosomes and of simultaneous G + C bands on Cercopithecus metaphases.     

The numbers of vertebrae in three African cercopithecine species.

The number of precaudal vertebrae in the three African cercopithecine species are analyzed, with two definitions for thoracic and lumbar vertebrae compared. It is found that generic averages obscure some rather substantial differences at the species level for both Cercopithecus and Cercocebus. Further, when zygapophysis structure is used to define vertebral type, rather than presence or absence of rib facets, there is a substantial change in thoracic and lumbar averages that may be important from a functional (locomotion) standpoint.     

Forest monkeys and Pleistocene refugia: a phylogeographic window onto the disjunct distribution of the Chlorocebus lhoesti species group

The reconstruction of evolutionary relationships among a group of closely‐related taxa provides a valuable window onto their biogeographic history. This is the first such molecular phylogenetic study to survey all three taxa of the Chlorocebus lhoesti species group, a group of Old World monkeys that includes C. lhoesti, Chlorocebus preussi, and Chlorocebus solatus. Representatives of each species were surveyed for two Y‐chromosomal genes, TSPY (～2240 bp) and SRY (～780 bp), and one X‐chromosomal intergenic region (～9300 bp) homologous to a portion of human Xq13.3. Maximum likelihood topologies inferred from these sequences confirm that the lhoesti group is monophyletic within the tribe Cercopithecini, as suggested by earlier karyotype studies. Within this group, C. lhoesti (Albertine region) and C. preussi (Cameroon, Nigeria, Bioko) cluster to the exclusion of C. solatus (Gabon). This phylogeographic pattern, evaluated in the context of Pleistocene glacial cycles and lhoesti group ecology, suggests: (1) the common ancestor of the group probably arose in west central Africa, (2) dispersal to the Albertine region is likely to have occurred during a glacial maximum, rather than an interglacial pluvial, and (3) this dispersal probably occurred via a path north of the Congo Basin. Divergence date calculations suggest C. solatus separated from the ancestral stock at ～2.1 Ma, whereas C. preussi and C. lhoesti bifurcated later, at ～0.5 Ma. Taken together, these evolutionary analyses draw attention to one period in the Pleistocene (～0.5 MYA) when a dispersal corridor suitable to montane taxa is likely to have connected the highlands of east central and west central Africa. © 2008 The Linnean Society of London, Zoological Journal of the Linnean Society, 2008, 154 , 408–418.