Phylogenetic relationships in the genus Cheracebus (Callicebinae, Pitheciidae).

Cheracebus is a new genus of New World primate of the family Pitheciidae, subfamily Callicebinae. Until recently, Cheracebus was classified as the torquatus species group of the genus Callicebus. The genus Cheracebus has six species: C. lucifer, C. lugens, C. regulus, C. medemi, C. torquatus, and C. purinus, which are all endemic to the Amazon biome. Before the present study, there had been no conclusive interpretation of the phylogenetic relationships among most of the Cheracebus species. The present study tests the monophyly of the genus and investigates the relationships among the different Cheracebus species, based on DNA sequencing of 16 mitochondrial and nuclear markers. The phylogenetic analyses were based on Maximum Likelihood, Bayesian Inference, and multispecies coalescent approaches. The divergence times and genetic distances between the Cheracebus taxa were also estimated. The analyses confirmed the monophyly of the genus and a well-supported topology, with the following arrangement: ((C. torquatus, C. lugens), (C. lucifer (C. purinus, C. regulus))). A well-differentiated clade was also identified within part of the geographic range of C. lugens, which warrants further investigation to confirm its taxonomic status.

Initiation of feeding by four sympatric Neotropical primates (Ateles belzebuth, Lagothrix lagotricha poeppigii, Plecturocebus (Callicebus) discolor, and Pithecia aequatorialis) in Amazonian Ecuador: Relationships to photic and ecological factors.

We examined photic and ecological factors related to initiation of feeding by four sympatric primates in the rain forest of Amazonian Ecuador. With rare exceptions, morning activities of all taxa began only after the onset of nautical twilight, which occurred 47-48 min before sunrise. The larger spider and woolly monkeys, Ateles belzebuth and Lagothrix lagotricha poeppigii, left their sleeping trees before sunrise about half the time, while the smaller sakis and titi monkeys, Pithecia aequatorialis and Plecturocebus (formerly Callicebus) discolor, did not emerge until sunrise or later. None of the four taxa routinely began feeding before sunrise. Pithecia began feeding a median 2.17 h after sunrise, at least 0.8 h later than the median feeding times of the other three taxa. The early movement of Ateles and Lagothrix, and late initiation of feeding by Pithecia are consistent with temporal niche partitioning. Among most New World primate species, all males and many females, have dichromatic color vision, with only two cone photopigments, while some females are trichromats with three cone photopigments. Current evidence indicates that the dichromats have a foraging advantage in dim light, which could facilitate utilization of twilight periods and contribute to temporal niche partitioning. However, in our study, dichromatic males did not differentially exploit the dim light of twilight, and times of first feeding bouts of female Ateles and Lagothrix were similar to those of males. First feeding bouts followed a seasonal pattern, occurring latest in May-August, when ripe fruit abundance and ambient temperature were both relatively low. The most frugivorous taxon, Ateles, exhibited the greatest seasonality, initiating feeding 1.4 h later in May-August than in January-April. This pattern may imply a strategy of conserving energy when ripe fruit is scarcer, but starting earlier to compete successfully when fruit is more abundant. Lower temperatures were associated with later feeding of Ateles (by 26 min / °C) and perhaps Pithecia, but not Lagothrix or Plecturocebus. The potential for modification of temporal activity patterns and temporal niche partitioning by relatively small changes in temperature should be considered when predicting the effects of climate change.

On a new species of titi monkey (Primates: Plecturocebus Byrne et al., 2016), from Alta Floresta, southern Amazon, Brazil.

The taxonomy of the titi monkeys (Callicebinae) has recently received considerable attention. It is now recognised that this subfamily is composed of three genera with 33 species, seven of them described since 2002. Here, we describe a new species of titi, Plecturocebus, from the municipality of Alta Floresta, Mato Grosso, Brazil. We adopt an integrative taxonomic approach that includes phylogenomic analyses, pelage characters, and locality records. A reduced representation genome-wide approach was employed to assess phylogenetic relationships among species of the eastern Amazonian clade of the Plecturocebus moloch group. Using existing records, we calculated the Extent of Occurrence (EOO) of the new species and estimated future habitat loss for the region based on predictive models. We then evaluated the species' conservation status using the IUCN Red list categories and criteria. The new species presents a unique combination of morphological characters: (1) grey agouti colouration on the crown and dorsal parts; (2) entirely bright red-brown venter; (3) an almost entirely black tail with a pale tip; and (4) light yellow colouration of the hair on the cheeks contrasting with bright red-brown hair on the sides of the face. Our phylogenetic reconstructions based on maximum-likelihood and Bayesian methods revealed well-supported species relationships, with the Alta Floresta taxon as sister to P. moloch + P. vieirai. The species EOO is 10,166,653 ha and we predict a total habitat loss of 86% of its original forest habitat under a "business as usual" scenario in the next 24 years, making the newly discovered titi monkey a Critically Endangered species under the IUCN A3c criterion. We give the new titi monkey a specific epithet based on: (1) clear monophyly of this lineage revealed by robust genomic and mitochondrial data; (2) distinct and diagnosable pelage morphology; and (3) a well-defined geographical distribution with clear separation from other closely related taxa. Urgent conservation measures are needed to safeguard the future of this newly discovered and already critically endangered primate.

Phylogeny, molecular dating and zoogeographic history of the titi monkeys (Callicebus, Pitheciidae) of eastern Brazil.

The titi monkeys belong to a genus of New World primates endemic to South America, which were recently reclassified in three genera (Cheracebus, Plecturocebus and Callicebus). The genus Callicebus, which currently includes five species, is endemic to eastern Brazil, occurring in the Caatinga, Savanna, and Atlantic Forest biomes. In the present study, we investigated the validity of these species and inferred their phylogenetic relationships, divergence times, and biogeographic patterns based on the molecular analysis of a concatenated sequence of 11 mitochondrial and nuclear DNA markers, derived from 13 specimens. We ran Maximum Likelihood (ML) and Bayesian Inference (BI) analyses, and estimated genetic distances, divergence times. Ancestral areas were estimated on BioGeoBears. Our results suggest that at about twelve million years ago, the ancestor of all titi monkeys inhabited a wide area that extended from the Amazon forest to the South of the Atlantic forest. A first vicariant event originated Cheracebus in the West of the Amazon and the ancestor of Callicebus and Plectorocebus which, later were separated by a second one. The diversification of Callicebus occurred during the Plio-Pleistocene (beginning at 5 Ma) probably influenced by climatic fluctuations and geological events. Therefore, the results of the present work confirmed the existence of five species that currently inhabit forested areas under increasing threat from human activities. Thus, a reliable diagnosis of the taxonomic status of species living in endangered environments is extremely important for the development of conservation measures.

Species, subspecies, or color morphs? Reconsidering the taxonomy of Callicebus Thomas, 1903 in the Purus-Madeira interfluvium.

There have been recent disagreements as to how many taxa of titi monkeys, genus Callicebus, occur in the region between the Purus and Madeira rivers in western Brazilian Amazonia. Three parapatric taxa were proposed for the area: Callicebus caligatus, Callicebus stephennashi, and Callicebus dubius, but the latter has recently been considered a synonym of C. caligatus, even though both form monophyletic groups and are morphologically distinct. We analyzed the geographic variation in the pelage of Callicebus occurring between the Madeira and Purus rivers and concluded that the phenotypes attributed to C. caligatus and C. dubius are not individual morphs, but rather well-marked and geographically restricted varieties. For this reason, we classify Callicebus caligatus as a polytypic species with two subspecies: Callicebus caligatus caligatus and Callicebus caligatus dubius. This classification is corroborated by molecular evidence as well. The morphological and distributional data indicate that Callicebus stephennashi is a hybrid form of C. c. caligatus and C. c. dubius, due to the presence of intermediate characters. Therefore, until more precise locality records are provided and further evidence is presented, we consider Callicebus stephennashi to be a homonym of the two parental forms.

Phylogenetic relationships within the Callicebus cupreus species group (Pitheciidae: Primates): Biogeographic and taxonomic implications.

The genus Callicebus (Thomas, 1903) is one of the most diverse of Neotropical primate genera and the only extant member of the Callicebinae subfamily. It has a widespread distribution from Colombia to Brazil, Bolivia, Peru and northern Paraguay. Coat colouring and colour pattern vary substantially within the genus, and this has led to the description of numerous species and subspecies, as well as numerous species groups. However, a lack of molecular phylogenetic analyses on the genus means that phylogenetic relationships and biogeographic history of species are poorly understood. Here, we examined phylogenetic relationships and patterns of diversification within the Callicebus cupreus species Group (sensu Kobayashi, 1995) using complete mitochondrial DNA cytochrome b gene sequence. Analyses indicate that the Callicebus cupreus Group underwent recent and extensive diversification. The common ancestor appears to have emerged some 2.3 million years ago (Ma) from a centre of origin in the western Amazon region, followed by diversification of the group between about 1.5 and 1.2Ma. Phylogenetic analyses were able to recover most previously described species (including the recently described Colombian endemic Callicebus caquetensis). However, there are some notable inconsistences between the obtained phylogeny and current taxonomy. Some previously recognized taxa were not separated by our data (e.g., Callicebus caligatus and Callicebus dubius), while currently unrecognized species diversity was uncovered within C. cupreus in the form of two divergent lineages: one of which exhibited greater phylogenetic similarity to species from the C. moloch Group. Based on the present study, we challenge current taxonomic arrangements for the C. cupreus species Group and call for a thorough taxonomic revision within the genus Callicebus.

1.32 ± 0.11 Ma age for underwater remains constrain antiquity and longevity of the Dominican primate Antillothrix bernensis.

Endemic New World monkeys are an important element of the extinct mammal faunas of the Caribbean's Greater Antilles. Here we report the first geochronometric evidence that the primate Antillothrix bernensis existed in the Dominican Republic during the Pleistocene, based on the uranium-series age of carbonate speleothem that encased a tibia when it was collected in a flooded cave. Three-dimensional geometric morphometrics of laser-scanned living and extinct samples provide evidence to support the hypothesis that this specimen and other Dominican primate tibial remains belong to that same species. U-Th dating of the host cave carbonate returns ages consistently at the 600 ka upper limit of the technique. However, U-Pb, capable of resolving ages of greater antiquity, is more robust in this context, returning a secure age of 1.32 ± 0.11 Ma, which is the oldest chronometric age recorded for a Hispaniolan mammal. While its origins and manner and time of arrival are obscure, the morphometric studies are consistent with phylogenetic analyses that place A. bernensis within the pitheciid clade of the platyrrhines. The species apparently endured for over 1 million years during the climatic perturbations of the Pleistocene, as a frugivorous climbing quadruped, one of two known primate species occupying the hazard prone island of Hispaniola.

Reconsidering the taxonomy of the Black-Faced Uacaris, Cacajao melanocephalus group (Mammalia: Pitheciidae), from the northern Amazon Basin.

The black-faced uacaris are a poorly known group of platyrrhine monkeys from the Rio Negro basin in northwestern Amazonia. Originally described as two distinct species-Cacajao melanocephalus (Humboldt 1812) and Cacajao ouakary (Spix 1823)-from opposite banks of the Negro, they were treated as a single species until the end of the twentieth century, when molecular studies reconfirmed their status as true species. One of these studies not only nominated a third (northern) species, Cacajao ayresi Boubli et al. 2008, but also identified C. ouakary as a junior synonym of C. melanocephalus, resulting in the introduction of a new nomen, Cacajao hosomi Boubli et al. 2008. In the present study, additional evidence on morphological and zoogeographic variables is analyzed, which indicates that C. ouakary should be reinstated, and supports the nomination of a neotype of C. melanocephalus. The molecular and zoogeographic data on the species status of the ayresi form are also re-assessed, leading to the conclusion that, on the basis of the evidence available at the present time, this form should be considered a subspecies of C. melanocephalus. A new taxonomic arrangement is proposed, which recognizes two species, C. ouakary and C. melanocephalus, the latter with two subspecies, C. m. melanocephalus and C. m. ayresi.

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.

Population parameters of the endangered titi monkey, Callicebus coimbrai Kobayashi and Langguth, 1999, in the fragmented landscape of southern Sergipe, Brazil.

The recently-discovered titi, Callicebus coimbrai, is endemic to the coastal Brazilian Atlantic Forest south of the São Francisco River, a region with a long tradition of deforestation. While a number of C. coimbrai populations have now been identified, little is known about basic population parameters. Considering the importance of this information for conservation planning, the population of a site in southern Sergipe (with a total area of forest of approximately 500 ha) was surveyed between April and October 2008. Standard line transect procedures were used in the four largest fragments, and additional monitoring included the use of playback broadcasts for the observation of titi groups. The presence of titis was confirmed in all the forest fragments at the site, including one of only five hectares. Two other primates - Callithrix jacchus and Cebus xanthosternos - were also recorded at the site, but were less abundant than titis. A total transect walk of 476 km provided 164 sightings of primates, the majority of which (104) were of Callicebus coimbrai. Titi groups ranged in size between two and five individuals. The most reliable estimate of overall population density, derived from the combined data set, was 12.6 individuals per km²;, although density was much higher in smaller (more disturbed) fragments. The total population of Callicebus coimbrai at the site was estimated to be at least 50 individuals, which may represent a considerable proportion of the population of the species remaining in the wild. In addition to its apparent tolerance of habitat fragmentation, densities of C. coimbrai recorded at the site compare favourably with those of other Atlantic Forest titi species.

Population parameters of the endangered titi monkey, Callicebus coimbrai Kobayashi and Langguth, 1999, in the fragmented landscape of southern Sergipe, Brazil / Parâmetros populacionais do guigó ameaçado, Callicebus coimbrai Kobayashi and Langguth, 1999, na paisagem fragmentada do sul de Sergipe, Brasil

The recently-discovered titi, Callicebus coimbrai, is endemic to the coastal Brazilian Atlantic Forest south of the São Francisco River, a region with a long tradition of deforestation. While a number of C. coimbrai populations have now been identified, little is known about basic population parameters. Considering the importance of this information for conservation planning, the population of a site in southern Sergipe (with a total area of forest of approximately 500 ha) was surveyed between April and October 2008. Standard line transect procedures were used in the four largest fragments, and additional monitoring included the use of playback broadcasts for the observation of titi groups. The presence of titis was confirmed in all the forest fragments at the site, including one of only five hectares. Two other primates - Callithrix jacchus and Cebus xanthosternos - were also recorded at the site, but were less abundant than titis. A total transect walk of 476 km provided 164 sightings of primates, the majority of which (104) were of Callicebus coimbrai. Titi groups ranged in size between two and five individuals. The most reliable estimate of overall population density, derived from the combined data set, was 12.6 individuals per km²;, although density was much higher in smaller (more disturbed) fragments. The total population of Callicebus coimbrai at the site was estimated to be at least 50 individuals, which may represent a considerable proportion of the population of the species remaining in the wild. In addition to its apparent tolerance of habitat fragmentation, densities of C. coimbrai recorded at the site compare favourably with those of other Atlantic Forest titi species.

O guigó-de-Coimbra-Filho recém descoberto, Callicebus coimbrai, é endêmico da Mata Atlântica do litoral brasileiro ao sul do rio São Francisco, uma região marcada pelo desmatamento. Enquanto um número de populações de C. coimbrai já foram identificadas, pouco se sabe sobre os parâmetros populacionais básicos. Considerando a importância dessas informações para o planejamento da conservação, foi feito um levantamento da população de um local no sul de Sergipe (com uma área total de floresta de cerca de 500 ha) entre abril e outubro de 2008. Procedimentos de transecção linear foram utilizados nos quatro maiores fragmentos e monitoramento adicional incluiu o uso da técnica de playback para a observação de grupos de guigós. A presença de guigós foi confirmada em todos os fragmentos de floresta no local, incluindo um de apenas cinco hectares. Outros dois primatas - Callithrix jacchus e Cebus xanthosternos - também foram registrados no local, mas foram menos abundantes do que o guigó-de-Coimbra-Filho. Um total de 476 km percorridos proveram 164 avistamentos de primatas, a maioria (104) de Callicebus coimbrai. O tamanho dos grupos desta espécie variou entre dois e cinco indivíduos. A estimativa mais confiável da densidade populacional geral, derivada do conjunto de dados combinados, foi de 12,6 indivíduos por km²;, embora a densidade tenha sido muito maior nos fragmentos menores (mais perturbados). A população total de Callicebus coimbrai no local foi estimada em pelo menos 50 indivíduos, que pode representar uma parte considerável da população remanescente da espécie na natureza. Além da sua aparente tolerância à fragmentação de habitat, a densidade de C. coimbrai registrada no local é comparada favoravelmente com a de outras espécies de guigós da Mata Atlântica.

Retropositional events consolidate the branching order among New World monkey genera.

Due to contradicting relationships obtained from various morphological and genetic studies, phylogenetic relationships among New World monkey genera are highly disputed. In the present study, we analyzed the presence/absence pattern of 128 SINE integrations in all New World monkey genera. Among them, 70 were specific for only a single genus, whereas another 18 were present in all New World monkey genera. The 40 remaining insertions were informative to elucidate phylogenetic relationships among genera. Several of them confirmed the monophyly of the three families Cebidae, Atelidae and Pitheciidae as well as of the subfamily Callithrichinae. Further markers provided evidence for a sister grouping of Cebidae and Atelidae to the exclusion of Pitheciidae as well as for relationships among genera belonging to Callithrichinae and Atelidae. Although a close affiliation of Saimiri, Aotus and Cebus to Callithrichinae was shown, the relationships among the three genera remained unresolved due to three contradicting insertions.