African bushpigs exhibit porous species boundaries and appeared in Madagascar concurrently with human arrival.

Several African mammals exhibit a phylogeographic pattern where closely related taxa are split between West/Central and East/Southern Africa, but their evolutionary relationships and histories remain controversial. Bushpigs (Potamochoerus larvatus) and red river hogs (P. porcus) are recognised as separate species due to morphological distinctions, a perceived lack of interbreeding at contact, and putatively old divergence times, but historically, they were considered conspecific. Moreover, the presence of Malagasy bushpigs as the sole large terrestrial mammal shared with the African mainland raises intriguing questions about its origin and arrival in Madagascar. Analyses of 67 whole genomes revealed a genetic continuum between the two species, with putative signatures of historical gene flow, variable FST values, and a recent divergence time (<500,000 years). Thus, our study challenges key arguments for splitting Potamochoerus into two species and suggests their speciation might be incomplete. Our findings also indicate that Malagasy bushpigs diverged from southern African populations and underwent a limited bottleneck 1000-5000 years ago, concurrent with human arrival in Madagascar. These results shed light on the evolutionary history of an iconic and widespread African mammal and provide insight into the longstanding biogeographic puzzle surrounding the bushpig's presence in Madagascar.

Djaffa Mountains guereza (Colobus guereza gallarum) abundance in forests of the Ahmar Mountains, Ethiopia.

The size and density of a population are essential parameters in primate ecology and conservation. Such information, however, is still scarce for many forest primate species. The Djaffa Mountains guereza (Colobus guereza gallarum) is an endemic Ethiopian taxon for which data about its distribution and population size are missing. Therefore, we aimed to estimate the abundance and population size of the Djaffa Mountains guereza in four forests in the Ahmar Mountains southeast of the Ethiopian Rift Valley. We conducted line-transect surveys in the forests. Within an area of 183 km2, we sampled 19 transects covering a distance of 75.9 km. We encountered 73 guereza clusters which most likely represent social groups. Since the detection distances and cluster sizes did not differ among the four forests, we applied a conventional distance sampling (CDS) model and estimated a population density of 20.6 clusters per square kilometer, i.e., 109.6 individuals per square kilometer or 20 061 individuals within the complete study area. This abundance is relatively high compared to other C. guereza taxa. However, given that the habitat and population of C. g. gallarum are already highly fragmented, further monitoring of the population and exploration of the possibilities of reconnecting its habitat should be priorities for the conservation of this taxon.

Potential changes in the extent of suitable habitats for geladas (Theropithecus gelada) in the Anthropocene.

BACKGROUND: Climate change coupled with other anthropogenic pressures may affect the extent of suitable habitat for species and thus their distributions. This is particularly true for species occupying high-altitude habitats such as the gelada (Theropithecus gelada) of the Ethiopian highlands. To explore the impact of climate change on species distributions, Species Distribution Modelling (SDM) has been extensively used. Here we model the current and future extent of sutibale habitat for geladas. Our modelling was based on 285 presence locations of geladas, covering their complete current distribution. We used different techniques to generate pseudoabsence datasets, MaxEnt model complexities, and cut-off thresholds to map the potential distribution of gelada under current and future climates (2050 and 2070). We assembled maps from these techniques to produce a final composite map. We also evaluated the change in the topographic features of gelada over the past 200 years by comparing the topography in current and historical settings. RESULTS: All model runs had high performances, AUC = 0.87-0.96. Under the current climate, the suitable habitat predicted with high certainty was 90,891 km2, but it decreased remarkably under future climates, -36% by 2050 and - 52% by 2070. However, since the habitats of geladas already extend to mountaintop grasslands, no remarkable range shifts across elevation gradients were predicted under future climates. CONCLUSIONS: Our findings indicated that climate change most likely results in a loss of suitable habitat for geladas, particularly south of the Rift Valley. Currently geladas are confined to higher altitudes and steep slopes compared to historical sightings, probably qualifying geladas as refugee species. The difference in topography is potentially associated with anthropogenic pressures that drove niche truncation to higher altitudes, undermining the climatic and topographic niche our models predicted. We recommend protecting the current habitats of geladas even when they are forecasted to become climatically unsuitable in the future, in particular for the population south of the Rift Valley.

Adulis and the transshipment of baboons during classical antiquity.

Adulis, located on the Red Sea coast in present-day Eritrea, was a bustling trading centre between the first and seventh centuries CE. Several classical geographers-Agatharchides of Cnidus, Pliny the Elder, Strabo-noted the value of Adulis to Greco-Roman Egypt, particularly as an emporium for living animals, including baboons (Papio spp.). Though fragmentary, these accounts predict the Adulite origins of mummified baboons in Ptolemaic catacombs, while inviting questions on the geoprovenance of older (Late Period) baboons recovered from Gabbanat el-Qurud ('Valley of the Monkeys'), Egypt. Dated to ca. 800-540 BCE, these animals could extend the antiquity of Egyptian-Adulite trade by as much as five centuries. Previously, Dominy et al. (2020) used stable isotope analysis to show that two New Kingdom specimens of Papio hamadryas originate from the Horn of Africa. Here, we report the complete mitochondrial genomes from a mummified baboon from Gabbanat el-Qurud and 14 museum specimens with known provenance together with published georeferenced mitochondrial sequence data. Phylogenetic assignment connects the mummified baboon to modern populations of P. hamadryas in Eritrea, Ethiopia, and eastern Sudan. This result, assuming geographical stability of phylogenetic clades, corroborates Greco-Roman historiographies by pointing toward present-day Eritrea, and by extension Adulis, as a source of baboons for Late Period Egyptians. It also establishes geographic continuity with baboons from the fabled Land of Punt (Dominy et al., 2020), giving weight to speculation that Punt and Adulis were essentially the same trading centres separated by a thousand years of history.

Genome-wide coancestry reveals details of ancient and recent male-driven reticulation in baboons.

Baboons (genus Papio) are a morphologically and behaviorally diverse clade of catarrhine monkeys that have experienced hybridization between phenotypically and genetically distinct phylogenetic species. We used high-coverage whole-genome sequences from 225 wild baboons representing 19 geographic localities to investigate population genomics and interspecies gene flow. Our analyses provide an expanded picture of evolutionary reticulation among species and reveal patterns of population structure within and among species, including differential admixture among conspecific populations. We describe the first example of a baboon population with a genetic composition that is derived from three distinct lineages. The results reveal processes, both ancient and recent, that produced the observed mismatch between phylogenetic relationships based on matrilineal, patrilineal, and biparental inheritance. We also identified several candidate genes that may contribute to species-specific phenotypes.

Recent Advances in Genetics and Genomics of Snub-Nosed Monkeys (Rhinopithecus) and Their Implications for Phylogeny, Conservation, and Adaptation.

The snub-nosed monkey genus Rhinopithecus (Colobinae) comprises five species (Rhinopithecus roxellana, Rhinopithecus brelichi, Rhinopithecus bieti, Rhinopithecus strykeri, and Rhinopithecus avunculus). They are range-restricted species occurring only in small areas in China, Vietnam, and Myanmar. All extant species are listed as endangered or critically endangered by the International Union for Conservation of Nature (IUCN) Red List, all with decreasing populations. With the development of molecular genetics and the improvement and cost reduction in whole-genome sequencing, knowledge about evolutionary processes has improved largely in recent years. Here, we review recent major advances in snub-nosed monkey genetics and genomics and their impact on our understanding of the phylogeny, phylogeography, population genetic structure, landscape genetics, demographic history, and molecular mechanisms of adaptation to folivory and high altitudes in this primate genus. We further discuss future directions in this research field, in particular how genomic information can contribute to the conservation of snub-nosed monkeys.

Genome-wide coancestry reveals details of ancient and recent male-driven reticulation in baboons.

Baboons (genus Papio ) are a morphologically and behaviorally diverse clade of catarrhine monkeys that have experienced hybridization between phenotypically and genetically distinct phylogenetic species. We used high coverage whole genome sequences from 225 wild baboons representing 19 geographic localities to investigate population genomics and inter-species gene flow. Our analyses provide an expanded picture of evolutionary reticulation among species and reveal novel patterns of population structure within and among species, including differential admixture among conspecific populations. We describe the first example of a baboon population with a genetic composition that is derived from three distinct lineages. The results reveal processes, both ancient and recent, that produced the observed mismatch between phylogenetic relationships based on matrilineal, patrilineal, and biparental inheritance. We also identified several candidate genes that may contribute to species-specific phenotypes. One-Sentence Summary: Genomic data for 225 baboons reveal novel sites of inter-species gene flow and local effects due to differences in admixture.

Host-Parasite Coevolution in Primates.

Organisms adapt to their environment through evolutionary processes. Environments consist of abiotic factors, but also of other organisms. In many cases, two or more species interact over generations and adapt in a reciprocal way to evolutionary changes in the respective other species. Such coevolutionary processes are found in mutualistic and antagonistic systems, such as predator-prey and host-parasite (including pathogens) relationships. Coevolution often results in an "arms race" between pathogens and hosts and can significantly affect the virulence of pathogens and thus the severity of infectious diseases, a process that we are currently witnessing with SARS-CoV-2. Furthermore, it can lead to co-speciation, resulting in congruent phylogenies of, e.g., the host and parasite. Monkeys and other primates are no exception. They are hosts to a large number of pathogens that have shaped not only the primate immune system but also various ecological and behavioral adaptions. These pathogens can cause severe diseases and most likely also infect multiple primate species, including humans. Here, we briefly review general aspects of the coevolutionary process in its strict sense and highlight the value of cophylogenetic analyses as an indicator for coevolution.

A Comprehensive Overview of Baboon Phylogenetic History.

Baboons (genus Papio) are an intriguing study system to investigate complex evolutionary processes and the evolution of social systems. An increasing number of studies over the last 20 years has shown that considerable incongruences exist between phylogenies based on morphology, mitochondrial, and nuclear sequence data of modern baboons, and hybridization and introgression have been suggested as the main drivers of these patterns. Baboons, therefore, present an excellent opportunity to study these phenomena and their impact on speciation. Advances both in geographic and genomic coverage provide increasing details on the complexity of the phylogeography of baboons. Here, we compile the georeferenced genetic data of baboons and review the current knowledge on baboon phylogeny, discuss the evolutionary processes that may have shaped the patterns that we observe today, and propose future avenues for research.

Population dynamics of the Manyara monkey (Cercopithecus mitis manyaraensis) and vervet monkey (Chlorocebus pygerythrus) in Lake Manyara National Park, Tanzania.

Estimating population densities and their trends over time is essential for understanding primate ecology and for guiding conservation efforts. From 2011 through to 2019, we counted two guenon species during seasonal road transect surveys in Lake Manyara National Park: the Tanzania-endemic Manyara monkey Cercopithecus mitis manyaraensis (International Union for Conservation of Nature and Natural Resources, IUCN, Red List category of "endangered") and the vervet monkey Chlorocebus pygerythrus (Red List category of "least concern"). To account for imperfect detectability, we analysed the data in a line distance sampling framework, fitted species-specific detection functions, and subsequently estimated seasonal densities. To test for seasonal differences and yearly trends in the species-specific density estimates, we fitted generalized additive models. Seasonal point density estimates fluctuated considerably during the 9 years (2011-2019) of our study, ranging from 3 to 29 individuals km - 2 for Manyara monkeys and from 19 to 83 individuals km - 2 for vervet monkeys. Densities of both taxa did not differ seasonally, and we did not detect marked directional population trends. Our study illustrates the utility and limitations of line distance sampling for long-term primate monitoring. Beyond informing primate ecology and management, our results highlight the conservation importance of Lake Manyara National Park for primate conservation.

Mathematical modelling Treponema infection in free-ranging Olive baboons (Papio anubis) in Tanzania.

Yaws is a chronic infection caused by the bacterium Treponema pallidum susp. pertenue (TPE) that was thought to be an exclusive human pathogen but was recently found and confirmed in nonhuman primates. In this paper, we develop the first compartmental ODE model for TPE infection with treatment of wild olive baboons. We solve for disease-free and endemic equilibria and give conditions on local and global stability of the disease-free equilibrium. We calibrate the model based on the data from Lake Manyara National Park in Tanzania. We use the model to help the park managers devise an effective strategy for treatment. We show that an increasing treatment rate yields a decrease in disease prevalence. This indicates that TPE can be eliminated through intense management in closed population. Specifically, we show that if the whole population is treated at least once every 5-6 years, a disease-free equilibrium can be reached. Furthermore, we demonstrate that to see a substantial decrease of TPE infection to near-elimination levels within 15 years, the whole population needs to be treated every 2-3 years.

Mito-phylogenetic relationship of the new subspecies of gentle monkey Cercopithecus mitis manyaraensis, Butynski & De Jong, 2020.

In 2020, a new subspecies was described in the Cercopithecus mitis complex, the Manyara monkey C. m. manyaraensis, Butynski & De Jong, 2020. The internal taxonomy of this species complex is still debated, and the phylogenetic relationships among the taxa are unclear. Here we provide the first mitochondrial sequence data for C. m. manyaraensis to determine its position within the mitochondrial phylogeny of C. mitis. This subspecies clusters within the youngest (internal divergences between 1.01 and 0.42 Ma) of three main taxonomic clades of C. mitis. Its sister lineages are C. m. boutourlinii (Ethiopia), C. m. albotorquatus (Kenya and Somalia), C. m. albogularis (Kenya and Tanzania), and C. m. monoides (Tanzania and Mozambique). In general, the phylogenetic tree of C. mitis based on mitochondrial sequence data indicates several paraphyletic relationships within the C. mitis complex. As in other African cercopithecines (e.g. Papio and Chlorocebus), these data are suitable for reconstructing historic biogeographical patterns, but they are only of limited value for delimitating taxa.

Male-male social bonding, coalitionary support and reproductive success in wild Guinea baboons.

Male-male bonds may confer substantial fitness benefits. The adaptive value of these relationships is often attributed to coalitionary support, which aids in rank ascension and female defence, ultimately resulting in greater reproductive success. We investigated the link between male-male sociality and both coalitionary support and reproductive success in wild Guinea baboons. This species lives in a tolerant multi-level society with reproductive units comprising a male and 1-6 females at the core. Males are philopatric, form differentiated, stable and equitable affiliative relationships (strong bonds) with other males, and lack a clear rank hierarchy. Here, we analysed behavioural and paternity data for 30 males and 50 infants collected over 4 years in the Niokolo-Koba National Park, Senegal. Strongly bonded males supported each other more frequently during conflicts, but strong bonds did not promote reproductive success. Instead, males that spent less time socializing with other males were associated with a higher number of females and sired more offspring. Notably, reproductively active males still maintained bonds with other males, but adjusted their social investment in relation to life-history stage. Long-term data will be needed to test if the adaptive value of male bonding lies in longer male tenure and/or in promoting group cohesion.

Road-based line distance surveys overestimate densities of olive baboons.

Estimating population density and population dynamics is essential for understanding primate ecology and relies on robust methods. While distance sampling theory provides a robust framework for estimating animal abundance, implementing a constrained, non-systematic transect design could bias density estimates. Here, we assessed potential bias associated with line distance sampling surveys along roads based on a case study with olive baboons (Papio anubis) in Lake Manyara National Park (Tanzania). This was achieved by comparing density estimates of olive baboons derived from road transect surveys with density estimates derived from estimating the maximum number of social groups (via sleeping site counts) and multiplying this metric with the estimated average size of social groups. From 2011 to 2019, we counted olive baboons along road transects, estimated survey-specific densities in a distance sampling framework, and assessed temporal population trends. Based on the fitted half-normal detection function, the mean density was 132.5 baboons km-2 (95% CI: 110.4-159.2), however, detection models did not fit well due to heaping of sightings on and near the transects. Density estimates were associated with relatively wide confidence intervals that were mostly caused by encounter rate variance. Based on a generalized additive model, baboon densities were greater during the rainy seasons compared to the dry seasons but did not show marked annual trends. Compared to estimates derived from the alternative method (sleeping site survey), distance sampling along road transects overestimated the abundance of baboons more than threefold. Possibly, this overestimation was caused by the preferred use of roads by baboons. While being a frequently used technique (due to its relative ease of implementation compared to spatially randomized survey techniques), inferring population density of baboons (and possibly other species) based on road transects should be treated with caution. Beyond these methodological concerns and considering only the most conservative estimates, baboon densities in LMNP are among the highest across their geographic distribution range.

Female post-copulatory behavior in a group of olive baboons (Papio anubis) infected by Treponema pallidum.

Pathogens exert a profound and pervasive cost on various aspects of primate sociality and reproduction. In olive baboons (Papio anubis) at Lake Manyara National Park, Tanzania, genital skin ulcers, caused by the bacterium Treponema pallidum subsp. pertenue, are associated with increased female mating avoidance and altered male mating patterns at a pre-copulatory and copulatory level. Beyond this, mating is also comprised of post-copulatory interactions among sexual partners (i.e., copulation calls, darting [post-copulatory sprint away from the male], and post-copulatory grooming). In baboons, female post-copulatory behavior is hypothesized to incite male-male competition, promote subsequent copulations, and/or strengthen the bonds between the mating pairs. Due to a higher reproductive burden (i.e. pregnancy, lactation, infant rearing), females should avoid proceptive behavior after mating to decrease further exposure to potential pathogens. To investigate whether the presence of genital skin ulcers has an impact at the post-copulatory level, we analyzed 517 copulation events of 33 cycling females and 29 males with and without genital skin ulcers. The occurrence of female post-copulatory behaviors was not altered by genital skin ulcerations in males. Similar to other baboon populations, females in our study group were more likely to utter copulation calls after an ejaculatory copulation. The likelihood of darting was higher after ejaculatory copulations and with the presence of copulation calls. Post-copulatory grooming (i.e., occurring within 15 seconds after a copulation) was not frequently observed. Our results indicate that despite the presence of conspicuous signs of disease, female post-copulatory behavior was not affected by the genital health status of the males. This indicates that in our study group, infection cues caused by T. pallidum subsp. pertenue play a major role before and during mating, but not after mating. The post-copulatory behavior of females is most likely affected by physiological or evolutionary constraints other than sexually transmitted infections.

Coordination during group departures and progressions in the tolerant multi-level society of wild Guinea baboons (Papio papio).

Collective movement of social groups requires coordination between individuals. When cohesion is imperative, consensus must be reached, and specific individuals may exert disproportionate influence during decision-making. Animals living in multi-level societies, however, often split into consistent social subunits during travel, which may impact group coordination processes. We studied collective movement in the socially tolerant multi-level society of Guinea baboons (Papio papio). Using 146 group departures and 100 group progressions from 131 Guinea baboons ranging in Senegal's Niokolo-Koba National Park, we examined individual success at initiating group departures and position within progressions. Two-thirds of attempted departures were initiated by adult males and one third by adult females. Both sexes were equally successful at initiating departures (> 80% of initiations). During group progressions, bachelor males were predominantly found in front, while reproductively active 'primary' males and females were observed with similar frequency across the whole group. The pattern of collective movement in Guinea baboons was more similar to those described for baboons living in uni-level societies than to hamadryas baboons, the only other multi-level baboon species, where males initiate and decide almost all group departures. Social organization alone therefore does not determine which category of individuals influence group coordination.

Genomic skimming and nanopore sequencing uncover cryptic hybridization in one of world's most threatened primates.

The Brazilian buffy-tufted-ear marmoset (Callithrix aurita), one of the world's most endangered primates, is threatened by anthropogenic hybridization with exotic, invasive marmoset species. As there are few genetic data available for C. aurita, we developed a PCR-free protocol with minimal technical requirements to rapidly generate genomic data with genomic skimming and portable nanopore sequencing. With this direct DNA sequencing approach, we successfully determined the complete mitogenome of a marmoset that we initially identified as C. aurita. The obtained nanopore-assembled sequence was highly concordant with a Sanger sequenced version of the same mitogenome. Phylogenetic analyses unexpectedly revealed that our specimen was a cryptic hybrid, with a C. aurita phenotype and C. penicillata mitogenome lineage. We also used publicly available mitogenome data to determine diversity estimates for C. aurita and three other marmoset species. Mitogenomics holds great potential to address deficiencies in genomic data for endangered, non-model species such as C. aurita. However, we discuss why mitogenomic approaches should be used in conjunction with other data for marmoset species identification. Finally, we discuss the utility and implications of our results and genomic skimming/nanopore approach for conservation and evolutionary studies of C. aurita and other marmosets.

Mitogenomes of historical type specimens unravel the taxonomy of sportive lemurs (Lepilemur spp.) in Northwest Madagascar.

Accurate information on name-bearing types, including corresponding type localities, is essential for proper taxonomy. However, such geographic information is often missing or unreliable. The localities of type specimens collected 100-200 years ago can be difficult to trace due to changes in local names or simple inaccuracies. Such a case can be found for the gray-backed sportive lemur (Lepilemur dorsalis), with its type locality imprecisely fixed as Northwest Madagascar. In recent years, eight species have been newly described for the Inter-River-Systems (IRSs) of this region, however the designation of L. dorsalis remains controversial due to a lack of a precise type locality. Here, we sequenced the complete mitochondrial genomes (mitogenomes) of type specimens of L. dorsalis and L. grandidieri, which is currently recognized as a synonym of L. dorsalis and compared their sequences with those of samples of known provenance from different IRSs. Results showed that the two type specimens of L. dorsalis and L. grandidieri had identical mitogenome sequences and clustered closely with samples collected in IRS V, indicating that the type locality could be fixed to IRS V. Consequently, L. dorsalis occurs in IRS V, and L. grandidieri and L. mittermeieri are junior synonyms of L. dorsalis. This finding demonstrates the value of type specimens for clarifying phylogeographic and taxonomic questions and clarifies the taxonomy of sportive lemurs in Northwest Madagascar.

Comparative ecology of Guinea baboons (Papio papio).

Thorough knowledge of the ecology of a species or population is an essential prerequisite for understanding the impact of ecology on the evolution of their respective social systems. Because of their diversity of social organizations, baboons (Papio spp.) are a useful model for comparative studies. Comparative ecological information was missing for Guinea baboons (Papio papio), however. Here we provide data on the ecology of Guinea baboons in a comparative analysis on two geographical scales. First, we compare climate variables and land cover among areas of occurrence of all six baboon species. Second, we describe home range size, habitat use, ranging behaviour, and diet from a local population of Guinea baboons ranging near the Centre de Recherche de Primatologie (CRP) Simenti in the Niokolo-Koba National Park, Senegal. Home ranges and daily travel distances at Simenti varied seasonally, yet the seasonal patterns in their daily travel distance did not follow a simple dry vs. rainy season pattern. Chemical food composition falls within the range of other baboon species. Compared to other baboon species, areas occupied by Guinea baboons experience the highest variation in precipitation and the highest seasonality in precipitation. Although the Guinea baboons' multi-level social organization is superficially similar to that of hamadryas baboons (P. hamadryas), the ecologies of the two species differ markedly. Most Guinea baboon populations, including the one at Simenti, live in more productive habitats than hamadryas baboons. This difference in the ecology of the two species contradicts a simple evolutionary relation between ecology and social system and suggests that other factors have played an additional role here.