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Molecular evidence suggests that the evolutionary split between hominoids and cercopithecoids occurred between 25 and 30 Myr ago, but fossil evidence for crown-group catarrhines (cercopithecoids and hominoids) before 20 Myr ago has been lacking; newly described fossils of a stem hominoid and a stem cercopithecoid precisely dated to 25.2 Myr ago help to fill this gap in the fossil record. Early coexisting Old World monkeys and apes Molecular evidence suggests that the evolutionary split between hominoids (apes and humans) and cercopithecoids (Old World monkeys) occurred between 25 million and 30 million years ago, but fossil evidence for the catarrhines (cercopithecoids and hominoids) only goes back some 20 million years. Nancy Stevens and colleagues go some way to filling this gap with the discovery of the earliest known evidence of both Old World monkeys and apes. The fossils, of a stem hominoid and a stem-cercopithecoid, were found in a stratum in the East African Rift of Tanzania precisely dated to 25.2 million years. This date, well back in the Oligocene epoch, adds greatly to the time in which both groups are known to have existed. Apes and Old World monkeys are prominent components of modern African and Asian ecosystems, yet the earliest phases of their evolutionary history have remained largely undocumented 1 . The absence of crown catarrhine fossils older than ∼20 million years (Myr) has stood in stark contrast to molecular divergence estimates of ∼25–30 Myr for the split between Cercopithecoidea (Old World monkeys) and Hominoidea (apes), implying long ghost lineages for both clades 2 , 3 , 4 . Here we describe the oldest known fossil ‘ape’, represented by a partial mandible preserving dental features that place it with ‘nyanzapithecine’ stem hominoids. Additionally, we report the oldest stem member of the Old World monkey clade, represented by a lower third molar. Both specimens were recovered from a precisely dated 25.2-Myr-old stratum in the Rukwa Rift, a segment of the western branch of the East African Rift in Tanzania. These finds extend the fossil record of apes and Old World monkeys well into the Oligocene epoch of Africa, suggesting a possible link between diversification of crown catarrhines and changes in the African landscape brought about by previously unrecognized tectonic activity 5 in the East African rift system.

Background Enhancers play an important role in morphological evolution and speciation by controlling the spatiotemporal expression of genes. Previous efforts to understand the evolution of enhancers in primates have typically studied many enhancers at low resolution, or single enhancers at high resolution. Although comparative genomic studies reveal large-scale turnover of enhancers, a specific understanding of the molecular steps by which mammalian or primate enhancers evolve remains elusive. Results We identified candidate hominoid-specific liver enhancers from H3K27ac ChIP-seq data. After locating orthologs in 11 primates spanning around 40 million years, we synthesized all orthologs as well as computational reconstructions of 9 ancestral sequences for 348 active tiles of 233 putative enhancers. We concurrently tested all sequences for regulatory activity with STARR-seq in HepG2 cells. We observe groups of enhancer tiles with coherent trajectories, most of which can be potentially explained by a single gain or loss-of-activity event per tile. We quantify the correlation between the number of mutations along a branch and the magnitude of change in functional activity. Finally, we identify 84 mutations that correlate with functional changes; these are enriched for cytosine deamination events within CpGs. Conclusions We characterized the evolutionary-functional trajectories of hundreds of liver enhancers throughout the primate phylogeny. We observe subsets of regulatory sequences that appear to have gained or lost activity. We use these data to quantify the relationship between sequence and functional divergence, and to identify CpG deamination as a potentially important force in driving changes in enhancer activity during primate evolution.

Insectivory, or the consumption of insects and other arthropods, is a significant yet cryptic component of omnivorous primate diets. Here, we used high-throughput DNA sequencing to identify arthropods from fecal DNA and assess variation in insectivory by closely-related sympatric primates. We identified arthropod prey taxa and tested the hypothesis that variation in insectivory facilitates niche differentiation and coexistence among closely-related species with high dietary overlap. We collected 233 fecal samples from redtail (Cercopithecus ascanius; n = 118) and blue monkeys (C. mitis; n = 115) and used a CO1 metabarcoding approach to identify arthropod DNA in each fecal sample. Arthropod DNA was detected in 99% of samples (N = 223 samples), and a total of 68 families (15 orders) were identified. Redtails consumed arthropods from 54 families, of which 12 (21.8%) were absent from blue monkey samples. Blue monkeys consumed arthropods from 56 families, of which 14 (24.6%) were absent from redtail samples. For both species, >97% of taxa present belonged to four orders (Araneae, Diptera, Hymenoptera, Lepidoptera). Redtail samples contained more Lepidoptera taxa (p<0.05), while blue monkey samples contained more Araneae (p<0.05). Blue monkeys consumed a greater diversity of arthropod taxa than redtail monkeys (p<0.05); however, the average number of arthropod families present per fecal sample was greater in the redtail monkey samples (p<0.05). These results indicate that while overlap exists in the arthropod portion of their diets, 20-25% of taxa consumed are unique to each group. Our findings suggest that variation in arthropod intake may help decrease dietary niche overlap and hence facilitate coexistence of closely-related primate species.

Odd-nosed monkeys represent one of the two major groups of Asian colobines. Our knowledge about this primate group is still limited as it is highlighted by the recent discovery of a new species in Northern Myanmar. Although a common origin of the group is now widely accepted, the phylogenetic relationships among its genera and species, and the biogeographic processes leading to their current distribution are largely unknown. To address these issues, we have analyzed complete mitochondrial genomes and 12 nuclear loci, including one X chromosomal, six Y chromosomal and five autosomal loci, from all ten odd-nosed monkey species. The gene tree topologies and divergence age estimates derived from different markers were highly similar, but differed in placing various species or haplogroups within the genera Rhinopithecus and Pygathrix. Based on our data, Rhinopithecus represent the most basal lineage, and Nasalis and Simias form closely related sister taxa, suggesting a Northern origin of odd-nosed monkeys and a later invasion into Indochina and Sundaland. According to our divergence age estimates, the lineages leading to the genera Rhinopithecus, Pygathrix and Nasalis+Simias originated in the late Miocene, while differentiation events within these genera and also the split between Nasalis and Simias occurred in the Pleistocene. Observed gene tree discordances between mitochondrial and nuclear datasets, and paraphylies in the mitochondrial dataset for some species of the genera Rhinopithecus and Pygathrix suggest secondary gene flow after the taxa initially diverged. Most likely such events were triggered by dramatic changes in geology and climate within the region. Overall, our study provides the most comprehensive view on odd-nosed monkey evolution and emphasizes that data from differentially inherited markers are crucial to better understand evolutionary relationships and to trace secondary gene flow.

What do functionally important DNA sites, those scrutinized and shaped by natural selection, tell us about the place of humans in evolution? Here we compare ≈90 kb of coding DNA nucleotide sequence from 97 human genes to their sequenced chimpanzee counterparts and to available sequenced gorilla, orangutan, and Old World monkey counterparts, and, on a more limited basis, to mouse. The nonsynonymous changes (functionally important), like synonymous changes (functionally much less important), show chimpanzees and humans to be most closely related, sharing 99.4% identity at nonsynonymous sites and 98.4% at synonymous sites. On a time scale, the coding DNA divergencies separate the human-chimpanzee clade from the gorilla clade at between 6 and 7 million years ago and place the most recent common ancestor of humans and chimpanzees at between 5 and 6 million years ago. The evolutionary rate of coding DNA in the catarrhine clade (Old World monkey and ape, including human) is much slower than in the lineage to mouse. Among the genes examined, 30 show evidence of positive selection during descent of catarrhines. Nonsynonymous substitutions by themselves, in this subset of positively selected genes, group humans and chimpanzees closest to each other and have chimpanzees diverge about as much from the common human-chimpanzee ancestor as humans do. This functional DNA evidence supports two previously offered taxonomic proposals: family Hominidae should include all extant apes; and genus Homo should include three extant species and two sub-genera, Homo (Homo) sapiens (humankind), Homo (Pan) troglodytes (common chimpanzee), and Homo (Pan) paniscus (bonobo chimpanzee).

The divergence of apes and Old World monkeys The primate fossil record is uneven, and substantial gaps remain. One gap is the divergence of cercopithecoids (Old World monkeys) and hominoids (apes and humans) within Old World higher primates (Catarrhini). This event was previously thought to have occurred sometime during the early Oligocene–early Miocene interval in Afro-Arabia, but the discovery of a new stem catarrhine in western Saudi Arabia narrows that gap. The Saudi specimen, dated to the mid-Oligocene around 29 million to 28 million years ago, shows no crown catarrhine specializations other than the presence of a tubular ectotympanic, suggesting that the divergence of Old World monkeys and apes happened after that date. The size of the cranium indicates a medium-sized primate, between 15 and 20 kilograms in body mass. The fossil record of primates is sparse, and many gaps remain in our knowledge. One gap relates to the divergence within the catarrhines — the ancestors of hominoids (apes and humans) and Old World monkeys. The discovery of a previously unknown catarrhine in Saudi Arabia, dated to 29–28 million years ago, helps to fill in some details. This specimen shows very few catarrhine specializations, suggesting that the divergence between Old World monkeys and hominoids must have occurred after this date. It is widely understood that Hominoidea (apes and humans) and Cercopithecoidea (Old World monkeys) have a common ancestry as Catarrhini deeply rooted in Afro-Arabia 1 , 2 , 3 , 4 . The oldest stem Catarrhini in the fossil record are Propliopithecoidea, known from the late Eocene to early Oligocene epochs (roughly 35–30 Myr ago) of Egypt, Oman and possibly Angola 5 , 6 , 7 , 8 , 9 , 10 . Genome-based estimates for divergence of hominoids and cercopithecoids range into the early Oligocene 11 ; however, the mid-to-late Oligocene interval from 30 to 23 Myr ago has yielded little fossil evidence documenting the morphology of the last common ancestor of hominoids and cercopithecoids, the timing of their divergence, or the relationship of early stem and crown catarrhines. Here we describe the partial cranium of a new medium-sized (about 15–20 kg) fossil catarrhine, Saadanius hijazensis , dated to 29–28 Myr ago. Comparative anatomy and cladistic analysis shows that Saadanius is an advanced stem catarrhine close to the base of the hominoid–cercopithecoid clade. Saadanius is important for assessing competing hypotheses about the ancestral morphotype for crown catarrhines 1 , 12 , 13 , 14 , early catarrhine phylogeny 12 , 15 and the age of hominoid–cercopithecoid divergence 11 . Saadanius has a tubular ectotympanic but lacks synapomorphies of either group of crown Catarrhini, and we infer that the hominoid–cercopithecoid split happened later, between 29–28 and 24 Myr ago.

Background The BLOC1S2 gene encodes the multifunctional protein BLOS2, a shared subunit of two lysosomal trafficking complexes: i) biogenesis of lysosome-related organelles complex-1 and i) BLOC-1-related complex. In our previous study, we identified an intriguing unreported transcript of the BLOC1S2 gene that has a novel exon derived from two transposable elements (TEs), MIR and Alu Sp. To investigate the evolutionary footprint and molecular mechanism of action of this transcript, we performed PCR and RT-PCR experiments and sequencing analyses using genomic DNA and RNA samples from humans and various non-human primates. Results The results showed that the MIR element had integrated into the genome of our common ancestor, specifically in the BLOC1S2 gene region, before the radiation of all primate lineages and that the Alu Sp element had integrated into the genome of our common ancestor, fortunately in the middle of the MIR sequences, after the divergence of Old World monkeys and New World monkeys. The combined MIR and Alu Sp sequences provide a 3′ splice site (AG) and 5′ splice site (GT), respectively, and generate the Old World monkey-specific transcripts. Moreover, branch point sequences for the intron removal process are provided by the MIR and Alu Sp combination. Conclusions We show for the first time that sequential integration into the same location and sequence divergence events of two different TEs generated lineage-specific transcripts through sequence collaboration during primate evolution.

Gee's golden langur (Trachypithecus geei) is an endangered colobine primate, endemic to the semi-evergreen and mixed-deciduous forests of Indo-Bhutan border. During the last few decades, extensive fragmentation has caused severe population decline and local extinction of golden langur from several fragments. However, no studies are available on the impact of habitat fragmentation and the genetic diversity of golden langur in the fragmented habitats. The present study aimed to estimate the genetic diversity in the Indian population of golden langur. We sequenced and analyzed around 500 bases of the mitochondrial DNA (mtDNA) hypervariable region-I from 59 fecal samples of wild langur collected from nine forest fragments. Overall, genetic diversity was high (h = 0.934, π = 0.0244) and comparable with other colobines. Populations in smaller fragments showed lower nucleotide diversity compared to the larger forest fragments. The median-joining network of haplotypes revealed a genetic structure that corresponded with the geographical distribution. The Aie and Champabati Rivers were found to be a barrier to gene flow between golden langur populations. In addition, it also established that T. geei is monophyletic but revealed possible hybridization with capped langur, T. pileatus, in the wild. It is hoped that these findings would result in a more scientific approach towards managing the fragmented populations of this enigmatic species.

Background The degree to which loud-calls in nonhuman primates can be used as a reliable taxonomic tool is the subject of ongoing debate. A recent study on crested gibbons showed that these species can be well distinguished by their songs; even at the population level the authors found reliable differences. Although there are some further studies on geographic and phylogenetic differences in loud-calls of nonhuman primate species, it is unclear to what extent loud-calls of other species have a similar close relation between acoustic structure, phylogenetic relatedness and geographic distance. We therefore conducted a field survey in 19 locations on Sumatra, Java and the Mentawai islands to record male loud-calls of wild surilis ( Presbytis ), a genus of Asian leaf monkeys (Colobinae) with disputed taxanomy, and compared the structure of their loud-calls with a molecular genetic analysis. Results The acoustic analysis of 100 surili male loud-calls from 68 wild animals confirms the differentiation of P.potenziani, P.comata, P.thomasi and P.melalophos . In a more detailed acoustic analysis of subspecies of P.melalophos , a further separation of the southern P.m.mitrata confirms the proposed paraphyly of this group. In concordance with their geographic distribution we found the highest correlation between call structure and genetic similarity, and lesser significant correlations between call structure and geographic distance, and genetic similarity and geographic distance. Conclusions In this study we show, that as in crested gibbons, the acoustic structure of surili loud-calls is a reliable tool to distinguish between species and to verify phylogenetic relatedness and migration backgrounds of respective taxa. Since vocal production in other nonhuman primates show similar constraints, it is likely that an acoustic analysis of call structure can help to clarify taxonomic and phylogenetic relationships.

To understand the evolutionary processes leading to the diversity of Asian colobines, we report here on a phylogenetic, phylogeographical and population genetic analysis of three closely related langurs, Trachypithecus francoisi, T. poliocephalus and T. leucocephalus, which are all characterized by different pelage coloration predominantly on the head and shoulders. Therefore, we sequenced a 395 bp long fragment of the mitochondrial control region from 178 T. francoisi, 54 T. leucocephalus and 19 T. poliocephalus individuals, representing all extant populations of these three species. We found 29 haplotypes in T. francoisi, 12 haplotypes in T. leucocephalus and three haplotypes in T. poliocephalus. T. leucocephalus and T. poliocephalus form monophyletic clades, which are both nested within T. francoisi, and diverged from T. francoisi recently, 0.46-0.27 (T. leucocephalus) and 0.50-0.25 million years ago (T. poliocephalus). Thus, T. francoisi appears as a polyphyletic group, while T. leucocephalus and T. poliocephalus are most likely independent descendents of T. francoisi that are both physically separated from T. francoisi populations by rivers, open sea or larger habitat gaps. Since T. francoisi populations show no variability in pelage coloration, pelage coloration in T. leucocephalus and T. poliocephalus is most likely the result of new genetic mutations after the split from T. francoisi and not of the fixation of different characters derived from an ancestral polymorphism. This case study highlights that morphological changes for example in pelage coloration can occur in isolated populations in relatively short time periods and it provides a solid basis for studies in related species. Nevertheless, to fully understand the evolutionary history of these three langur species, nuclear loci should be investigated as well.