The large-bodied, terrestrial primates in the tribe Papionini are among the most intensely studied animals in the world, yet for some members of this tribe we know comparatively little about their evolutionary history and phylogeography. Geladas (Theropithecus gelada Rüppell, 1835), endemic primates of the Ethiopian highlands, are largely unstudied both in genetic diversity and intrageneric phylogeny. Currently, a northern and central subspecies and one isolated southern population are recognized, of which the central is classified as Least Concern, the northern as Vulnerable, and the southern is not yet assessed. The distribution and taxonomy of the subspecies remain poorly defined. Here, we estimate the mitochondrial DNA (mtDNA) diversity and phylogenetic relationships among gelada mtDNA lineages based on samples across the entire species range. We analysed 1.7 kb-long sequences of the mtDNA genome, spanning the cytochrome b gene and the hypervariable region I of the D-loop, derived from 162 faecal samples. We detected five major haplogroups or clades (south, central-1, central-2, north-1, north-2) which diverged between 0.67 and 0.43 million years ago, thus suggesting a rapid radiation, resulting in largely unresolved intrageneric phylogenetic relationships. Both, the northern and central demes contain two similarly valid haplogroups, each with little or no geographic segregation among respective haplogroups. Effective population sizes of the northern and central demes decreased during and after the last glacial maximum but remained stable for the southern deme, although on a very low level. The distribution of haplogroups within the geographic ranges of the putative gelada subspecies indicates that mtDNA sequence information does not allow reliable taxonomic inferences and thus is not sufficient for solving the taxonomic rank of the three demic populations, with the possible exception of the southern population. Nevertheless, due to the genetic differences all three populations deserve conservation efforts, in particular the smallest southern population.
Pair living and pair bonding are rare in mammals, and the mechanisms of their maintenance remain a puzzle. Titi monkeys, a ‘textbook example’ for ‘monogamous’ primates, have strong pair bonds and extensive male care. To investigate mechanisms of pair-bond maintenance, we studied seven wild groups of red titis ( Plecturocebus cupreus ) in Peruvian Amazonia over a period of 14 months. We analysed pair bonds by measuring proximity, grooming and approaches/leaves within pairs, and collected data on intergroup encounters. Females contributed to grooming more than males, especially during infant dependency, when most of the grooming within pairs was done by females. Females were also more active in controlling proximity between pair mates, making most of the approaches and leaves. Males, on the other hand, invested more in territorial defences. They participated in more intergroup encounters than females and were more active during these encounters. Our data is most consistent with the ‘male-services’ hypothesis for pair-bond maintenance, where a female contributes more to the proximity and affiliation maintenance while a male provides beneficial services.
Abstract. Due to their inconspicuous behaviour and colouration, it has been assumed that titi monkeys' main anti-predator behaviour is passive crypsis and hiding. So far, active predator mobbing has been documented only for black-fronted titi monkeys, Callicebus nigrifrons. Here we report for the first time mobbing behaviour of red titi monkeys, Plecturocebus cupreus (previously Callicebus cupreus), as reaction to an ocelot (Leopardus pardalis) and a Boa constrictor. We also report other active anti-predator behaviours, such as alarm calling and approaching, as reactions to tayras (Eira barbara) and raptors. Our observations provide additional evidence for sex differences in anti-predator behaviour, possibly related to the evolution and maintenance of social monogamy.
In pair-living mammals, genetic monogamy is extremely rare. One possible reason is that in socially monogamous animals, mate choice can be severely constrained, increasing the risk of inbreeding or pairing with an incompatible or low-quality partner. To escape these constraints, individuals might engage in extra-pair copulations. Alternatively, inbreeding can be avoided by dispersal. However, little is known about the interactions between mating system, mate choice, and dispersal in pair-living mammals. Here we genotyped 41 wild individuals from 14 groups of coppery titi monkeys (Plecturocebus cupreus) in Peruvian Amazon using 18 microsatellite loci. Parentage analyses of 18 young revealed no cases of extra-pair paternity, indicating that the study population is mostly genetically monogamous. We did not find evidence for relatedness- or heterozygosity-based mate choice. Despite the lack of evidence for active inbreeding avoidance via mate choice, mating partners were on average not related. We further found that dispersal was not sex-biased, with both sexes dispersing opportunistically over varying distances. Our findings suggest that even opportunistic dispersal, as long as it is not constrained, can generate sufficient genetic diversity to prevent inbreeding. This, in turn, can render active inbreeding avoidance via mate choice and extra-pair copulations less necessary, helping to maintain genetic monogamy.
Complete mitochondrial (mtDNA) genomes have proved to be useful in reconstructing primate phylogenies with higher resolution and confidence compared to reconstructions based on partial mtDNA sequences. Here, we analyse complete mtDNA genomes of African green monkeys (genus Chlorocebus), a widely distributed primate genus in Africa representing an interesting phylogeographical model for the evolution of savannah species. Previous studies on partial mtDNA sequences revealed nine major clades, suggesting several cases of para- and polyphyly among Chlorocebus species. However, in these studies, phylogenetic relationships among several clades were not resolved, and divergence times were not estimated. We analysed complete mtDNA genomes for ten Chlorocebus samples representing major mtDNA clades to find stronger statistical support in the phylogenetic reconstruction than in the previous studies and to estimate divergence times. Our results confirmed para- and polyphyletic relationships of most Chlorocebus species, while the support for the phylogenetic relationships between the mtDNA clades increased compared to the previous studies. Our results indicate an initial west–east division in the northern part of the Chlorocebus range with subsequent divergence into north-eastern and southern clades. This phylogeographic scenario contrasts with that for another widespread African savannah primate genus, the baboons (Papio), for which a dispersal from southern Africa into East and West Africa was suggested.
Coordinated singing, performed as duets by mated pairs and often joined by offspring to form choruses, is a distinctive behavioral attribute of the social system of pair-living and pair-bonded Neotropical titi monkeys. Duets and choruses are presumed to be associated with mate or territorial defense, but no consensus has yet been reached regarding their function. Here, we examined temporal and spatial patterns of coordinated singing in eight wild groups of coppery titi monkeys, Plecturocebus cupreus, in Peruvian Amazonia to test predictions of the joint resource and mate defense. We investigated singing rates in relation to female reproductive state, fruit consumption and demographic context using a dataset based on 227 observation days and analyzed temporal and spatial distribution of songs using a dataset based on 150 songs, collected between June 2017 and September 2021. Titi monkeys sang least frequently when females were likely to be sexually receptive and most frequently when females were likely to be pregnant. Groups also sang slightly more often when fruits were consumed more intensively, although this association did not reach statistical significance. The duration of songs was not associated with female reproductive state or fruit consumption, but songs were longer during inter-group encounters compared to non-encounter contexts. Songs were not concentrated in the core areas of home ranges; rather, they were distributed throughout the home ranges in concordance with its use. Finally, songs were concentrated around dawn. Our results provide support for a function in joint resource defense and inter-group communication of coordinated songs in coppery titi monkeys. The function of coordinated songs for mate defense in the form of paternity guarding, on the other hand, was not supported by our findings.
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