Consumption of underground storage organs is associated with improved energetic status in a graminivorous primate.

Early hominin species likely had access to open, grassy habitats where periodic reliance on underground storage organs (USOs) is hypothesized to have played a crucial dietary role. As the only living graminivorous primate today, geladas (Theropithecus gelada) provide a unique perspective for understanding the energetic consequences of seasonal consumption of USOs. Geladas rely heavily on above-ground grasses throughout the year, but when grass is seasonally less available, they feed more on USOs. To assess whether USOs fit the definition of fallback foods (i.e., foods that are difficult to access, less preferred, or both), we examined how foraging effort (measured via time spent feeding and moving) and energetic status (measured via urinary C-peptide) fluctuated during seasonal dietary changes in a population of wild geladas in the Simien Mountains National Park, Ethiopia. If, indeed, USOs are fallback foods, we predicted an increase in foraging effort and a decline in energetic status during the dry season, when geladas rely more heavily on USOs. We collected behavioral and physiological data from 13 adult gelada males across a 13-month period. As expected, we found that male geladas spent more time moving during drier months. However, counter to the hypothesis that USOs are fallback foods in geladas, urinary C-peptide concentrations were significantly higher during the dry season. We suggest that USOs may represent an energy-rich food item for geladas, but it remains unclear why USOs are not consumed year-round. Future work is needed to better understand seasonal variation in the availability, nutrient content, and digestibility of USOs. However, results indicate that exploiting USOs seasonally could have been a valuable dietary strategy for the evolutionary success of early hominins.

The first large-scale record of gelada's spatial distribution and population size in Mountain chains of Tigray, Northern Ethiopia.

Gelada (Theropithecus gelada) is an Ethiopian endemic mammal whose range was previously believed to be limited to the Bale and Simien Mountain national parks. However, knowledge of the range of the species is still not satisfactory. This study was designed to investigate the distribution and population size of the gelada in selected highlands in Tigray. To achieve this, study areas were divided into census tracts identified for a direct field assessment using habitat-based counting approaches. Moreover, informal interviews were conducted parallel to the direct field assessment in different villages. Our large spatial scale survey, the first of its kind for the region, confirmed the presence of T. gelada in three mountain clusters in Tigray for the first time. A total of 223 individual geladas were recorded in Ganta Afeshum, Hawzen and Welkait escarpments. The highest number of individuals (35.7 ± 3.8) was recorded in Hawzen (with 6.99 individuals/km2), followed by Ganta Afeshum (with 4.3 individuals/km2). Agricultural expansion, settlement and a lack of community awareness are the key threats operating against the conservation of the gelada in its current range in Tigray. Further research on the overall ecology, feeding, and spatial distribution of the species should be projected.

A review of Theropithecus oswaldi with the proposal of a new subspecies.

Theropithecus oswaldi darti, as currently understood, is the oldest Theropithecus taxon in the fossil record and the earliest subspecies in the Theropithecusoswaldi lineage. Theropithecus oswaldi darti is typified at the site of Makapansgat in South Africa, and a similar form (T. o. cf. darti) is usually recognized at Hadar, Dikika, some Middle Awash localities, and Woranso-Mille in Ethiopia. This taxon is also tentatively believed to occur in Kenya at Kanam and Koobi Fora and in Member C of the Shungura Formation in Ethiopia. While there is a general consensus that the East African 'darti' specimens are sufficiently similar to each other, there has always been a question of whether they are too distinct from the South African type material of T. o. darti to belong to the same subspecies. Here we conduct a morphological comparison of the different samples previously assigned to T. o. darti and T. o. cf. darti. The results of our analyses overwhelmingly support the hypothesis that the East African samples are distinct from the South African ones, and they are likely distinct in geological age as well. Therefore, we propose a new subspecies designation for the material previously termed T. o. cf. darti from East Africa: Theropithecus (Theropithecus) oswaldi ecki subsp. nov. We also formally recognize Theropithecus (Theropithecus) oswaldi serengetensis (Dietrich, 1942) for specimens from Laetoli, Woranso-Mille, and perhaps Galili.

Vascularization underlies differences in sexually selected skin coloration in a wild primate.

Male reproductive competition can select for condition-dependent, conspicuous traits that signal some aspect of fighting ability and facilitate assessment of potential rivals. However, the underlying mechanisms that link the signal to a male's current condition are difficult to investigate in wild populations, often requiring invasive experimental manipulation. Here, we use digital photographs and chest skin samples to investigate the mechanisms of a visual signal used in male competition in a wild primate, the red chest patch in geladas (Theropithecus gelada). We analysed photographs collected during natural (n = 144) and anaesthetized conditions (n = 38) to understand variability in male and female chest redness, and we used chest skin biopsies (n = 38) to explore sex differences in gene expression. Male and female geladas showed similar average redness, but males exhibited a wider within-individual range in redness under natural conditions. These sex differences were also reflected at the molecular level, with 10.5% of genes exhibiting significant sex differences in expression. Subadult males exhibited intermediate gene expression patterns between adult males and females, pointing to mechanisms underlying the development of the red chest patch. We found that genes more highly expressed in males were associated with blood vessel development and maintenance but not with androgen or oestrogen activity. Together, our results suggest male gelada redness variability is driven by increased blood vessel branching in the chest skin, providing a potential link between male chest redness and current condition as increased blood circulation to exposed skin could lead to heat loss in the cold, high-altitude environment of geladas.

Inter-sexual multimodal communication during mating in wild geladas: the leading role of females.

Female primates can emit vocalizations associated with mating that can function as honest signals of fertility. Here, we investigated the role of mating calls and visual signals in female geladas (Theropithecus gelada). Because females have a central role in the gelada society and seem to solicit sexual interactions, we answered whether they emit vocalizations in conjunction with gazing to increase mating success probability. Before and during copulations, females can emit pre-copulation calls and copulation calls. For the first time, we identified a new female vocalization emitted at the final stage of copulations (end-copulation call), possibly marking the occurrence of ejaculation. We found that longer pre-copulation call sequences were followed by both prolonged copulations and the presence of end-copulation calls, thus suggesting that females use pre-copulation calls to ensure successful copula completion. Moreover, we found that different combinations of female vocal types and gazing had different effects on male vocal behavior and motivation to complete the copula. The analysis of the vocal and visual signals revealed a complex inter-sexual multimodal chattering with the leading role of females in the signal exchange. Such chattering, led by females, modulates male sexual arousal, thus increasing the probability of the copula success.

Biochronology of South African hominin-bearing sites: A reassessment using cercopithecid primates.

Despite recent advances in chronometric techniques (e.g., Uranium-Lead [U-Pb], cosmogenic nuclides, electron spin resonance spectroscopy [ESR]), considerable uncertainty remains regarding the age of many Plio-Pleistocene hominin sites, including several in South Africa. Consequently, biochronology remains important in assessments of Plio-Pleistocene geochronology and provides direct age estimates of the fossils themselves. Historically, cercopithecid monkeys have been among the most useful taxa for biochronology of early hominins because they are widely present and abundant in the African Plio-Pleistocene record. The last major studies using cercopithecids were published over 30 y ago. Since then, new hominin sites have been discovered, radiometric age estimates have been refined, and many changes have occurred in cercopithecid taxonomy and systematics. Thus, a biochronological reassessment using cercopithecids is long overdue. Here, we provide just such a revision based on our recent study of every major cercopithecid collection from African Plio-Pleistocene sites. In addition to correlations based on shared faunal elements, we present an analysis based on the dentition of the abundant cercopithecid Theropithecus oswaldi, which increases in size in a manner that is strongly correlated with geological age (r2 ∼0.83), thereby providing a highly accurate age-estimation tool not previously utilized. In combination with paleomagnetic and U-Pb data, our results provide revised age estimates and suggest that there are no hominin sites in South Africa significantly older than ∼2.8 Ma. Where conflicting age estimates exist, we suggest that additional data are needed and recall that faunal estimates have ultimately proved reliable in the past (e.g., the age of the KBS Tuff).

A novel statovirus identified in fecal samples from wild geladas in the Ethiopian highlands.

We present a novel statovirus in geladas (Theropithecus gelada), graminivorous primates endemic to the Ethiopian highlands. Using a high-throughput sequencing approach, we identified contiguous sequences in feces from two adult female geladas in the Simien Mountains National Park, Ethiopia, that share similarities to statoviruses. Our phylogenetic analysis of the whole genome, as well as the RNA-dependent RNA polymerase (RdRp) and capsid protein (CP) amino acid sequences, revealed that the gelada statoviruses cluster with those from other primates (laboratory populations of Macaca nemestrina and Macaca mulatta). As the first report of statovirus in wild primates, this finding contributes to our understanding of the phylogenetic and geographic distribution of statoviruses and their hosts.

Social correlates of androgen levels and dispersal age in juvenile male geladas.

Androgens offer a window into the timing of important male life history events such as maturation. However, when males are the dispersing sex, piecing together normative androgen profiles across development is challenging because dispersing males are difficult to track. Here, we examined the conditions that may be associated with male androgen status (via fecal androgen metabolites, fAMs) and age at dispersal in wild male geladas (Theropithecus gelada). Gelada male life histories are highly variable - dispersal may occur before sexual maturation, dispersal itself can be immediate or drawn out, and, due to their multi-leveled society, social conditions affecting dispersal can vary for juveniles living in different reproductive units within the same band. Using longitudinal data from known natal males, we examined how androgen levels and age at dispersal were associated with: (1) access to maternal resources (i.e., maternal rank, birth of a younger sibling, experiencing maternal loss), and (2) access to male peers (i.e., number of similar-aged males in their unit). We found that androgens were significantly lower in males with high-ranking mothers (in males >2.5 years of age; infant androgens were unrelated) and that having more male peers in their social group and larger groups overall predicted an earlier age at dispersal. Moreover, dispersal in geladas was not preceded or followed by a surge in androgen levels. Taken together, results suggest that social environments can cause individual variation in androgens and dispersal age. Whether this variation leads to differences in male fitness in later life remains to be determined.

Infant handling increases grooming towards mothers in wild geladas (Theropithecus gelada).

Infant handling - involving affiliative behavior from non-mothers to infants - is a phenomenon that is variably present in Old World monkeys and can be granted by mothers to obtain social services, such as grooming. Here we investigated for the first time whether infant handling could influence grooming exchange in wild geladas. We gathered data on the population of Kundi highland (Ethiopia) in 2019/2020. Via sampling on 15 focal mothers from eight different One-Male Units, we video-recorded 55 grooming sessions between focal mothers and non-focal females (mothers or non-mothers). We also recorded the possible occurrence of infant handling performed by non-focal females. We found that grooming sessions were longer between mother and non-mothers and in the presence than in the absence of infant handling. Hence, our results show that infant handling can influence the grooming exchange between wild gelada females. Because grooming is used to establish and reinforce social bonds in primates, infant handling may act as a 'social bridge' in a female bonded society. From an evolutionary perspective, infant handling strategies might represent the stepping stone to more complex forms of infant care, such as allomaternal care and cooperative breeding.

Let's unite in play! Play modality and group membership in wild geladas.

Two of the main hypotheses put forth to explain the function of immature social play are the Social Skill Hypothesis and the Motor Training Hypothesis focussing on whether play can improve social competence to develop cooperative social networks or physical abilities to outcompete others, respectively. Here, we tested these hypotheses on a monkey species, the wild gelada (Theropithecus gelada) from the Kundi plateau, Ethiopia. This species is organized in bands divided in One-Male Units (OMUs), united only via social play. Immatures form 'play units' in which individuals from the same and different OMUs interact. We analysed the potential differences between inter- and intra-OMU play to verify which of the two hypotheses (Social Skill or Motor Training Hypothesis) best explains the function of play in geladas. We analysed 527 video-recorded social play sessions and found mixed support for both hypotheses. In agreement with the Social Skill Hypothesis, we found that play in geladas shows scarce social canalization being similarly distributed across age, sex and group membership. In line with the Motor Training Hypothesis, we detected higher levels of competition (shorter and more unbalanced sessions) in inter-OMU compared to intra-OMU play. Hence, in geladas play can be a tool for both the development of social relationships and the improvement of the physical skills necessary to cope with either future mates or competitors. In conclusion, neither hypothesis can be discarded and both hypotheses concur in explaining why immature geladas peculiarly form 'play units' embracing both ingroup and outgroup members.

Seasonal shifts in the gut microbiome indicate plastic responses to diet in wild geladas.

BACKGROUND: Adaptive shifts in gut microbiome composition are one route by which animals adapt to seasonal changes in food availability and diet. However, outside of dietary shifts, other potential environmental drivers of gut microbial composition have rarely been investigated, particularly in organisms living in their natural environments. RESULTS: Here, we generated the largest wild nonhuman primate gut microbiome dataset to date to identify the environmental drivers of gut microbial diversity and function in 758 samples collected from wild Ethiopian geladas (Theropithecus gelada). Because geladas live in a cold, high-altitude environment and have a low-quality grass-based diet, they face extreme thermoregulatory and energetic constraints. We tested how proxies of food availability (rainfall) and thermoregulatory stress (temperature) predicted gut microbiome composition of geladas. The gelada gut microbiome composition covaried with rainfall and temperature in a pattern that suggests distinct responses to dietary and thermoregulatory challenges. Microbial changes were driven by differences in the main components of the diet across seasons: in rainier periods, the gut was dominated by cellulolytic/fermentative bacteria that specialized in digesting grass, while during dry periods the gut was dominated by bacteria that break down starches found in underground plant parts. Temperature had a comparatively smaller, but detectable, effect on the gut microbiome. During cold and dry periods, bacterial genes involved in energy, amino acid, and lipid metabolism increased, suggesting a stimulation of fermentation activity in the gut when thermoregulatory and nutritional stress co-occurred, and potentially helping geladas to maintain energy balance during challenging periods. CONCLUSION: Together, these results shed light on the extent to which gut microbiota plasticity provides dietary and metabolic flexibility to the host, and might be a key factor to thriving in changing environments. On a longer evolutionary timescale, such metabolic flexibility provided by the gut microbiome may have also allowed members of Theropithecus to adopt a specialized diet, and colonize new high-altitude grassland habitats in East Africa. Video abstract.

First evidence of stone handling in geladas: From simple to more complex forms of object play.

Stone Handling (SH) is a solitary object play behaviour that can vary from simple exploratory actions to more complex manipulations. So far, among primates, this behaviour has been exclusively reported in macaques. We collected data on 62 geladas (Theropithecus gelada) housed at the NaturZoo (Rheine, Germany). We found that about 70% of subjects belonging to all age- and sex-classes engaged in SH. Due to their exceptional manipulative skills (the highest opposability index among nonhuman primates) and propensity to play, geladas are a good model species to test hypotheses on the function of this form of object play. While the frequency of SH tended to decrease with age of the player, the duration of each session and its complexity tended to increase in juveniles/subadults and adults compared to infants. This age-related variation in terms of frequency, duration and complexity suggests that, in agreement with the motor training hypothesis, SH could have a role in the neural-motor development of immature subjects and a basic function in stimulating neurogenesis and maintaining the psychological well-being of adults. In all age classes, the frequency of SH did not vary across pre-feeding, feeding and non-feeding conditions. Hence, our data do not support the misdirected foraging hypothesis, which predicts that animals engage in SH to anticipate food provisioning. In conclusion, our study reveals, for the first time, the presence of SH outside the genus Macaca and attempts to delineate possible functions of the behaviour in geladas. Since the hypotheses tested cannot be mutually exclusive, long-term studies of SH across individuals' lifetimes in both captive and wild groups of geladas are needed to clarify the proximate and ultimate functions of the behaviour in this species of Papionini. Finally, long-term studies could also provide some important indications about the cultural nature and social transmission of SH in a taxonomic group outside the Macaca genus.

Buccal dental-microwear and feeding ecology of Early Pleistocene Theropithecus oswaldi from Cueva Victoria (Spain).

Despite the scarcity of fossil specimens of Theropithecus oswaldi in Eurasia, its presence out of Africa attests to the great dispersal of this Papionini genus during the Early Pleistocene. In the present study, we analyze the buccal dental microwear of T. oswaldi (T. o. leakeyi) fossil specimens from Cueva Victoria (Southeastern Spain). This analysis is the first characterization of the feeding ecology of T. oswaldi in Europe. The buccal microwear pattern of the molar and premolar teeth of T. oswaldi from Cueva Victoria shows great similarities to that observed for the extant frugivorous forest-dwelling Mandrillus sphinx and mangabeys (Cercocebus sp.)-both species adapted to durophagous dietary habits-while significantly different from that observed for the gramnivorous Theropithecus gelada. These results suggest that T. oswaldi from Cueva Victoria could have exploited both hard-shelled fruits or seeds and succulent fruits from open and forested Mediterranean ecosystems.

Cercopithecid fossils from Kanapoi, West Turkana, Kenya (2007-2015).

Recent fieldwork at Kanapoi has expanded the sample of fossil cercopithecids, facilitating a re-appraisal of their taxonomy. The assemblage now includes at least one species of cercopithecin, two papionins, and two colobines. The guenon Nanopithecus browni is similar in dental size to extant Miopithecus. We tentatively re-affirm the identification of Parapapio cf. ado and confirm the presence of Theropithecus. The colobines include a small form tentatively attributed to Kuseracolobus and a second larger species. The Kanapoi fossils represent the oldest occurrences of guenons in Africa and of the important genus Theropithecus, the most abundant and widespread primate in the Neogene of Africa. In the assemblage, Parapapio cf. ado is the most abundant form, comprising the majority of specimens. All of the other taxa are comparatively rare. Colobines make up a small part of the Kanapoi fossil assemblage compared to most other contemporary sites, including Allia Bay, Kenya, where, like Kanapoi, Australopithecus anamensis has been found. The presence of Theropithecus is consistent with the presence of some relatively open habitat at Kanapoi. While the ecological preferences of the small cercopithecin are unknown, most guenons are associated with relatively wooded habitats, as are most colobines, suggesting the availability of at least some wooded areas.

Alloscardovia theropitheci sp. nov., isolated from the faeces of gelada baboon, the 'bleeding heart' monkey (Theropithecus gelada).

A novel irregularly shaped and slightly curved rod bacterial strain, GLDI4/2T, showing activity of fructose 6-phosphate phosphoketolase was isolated from a faecal sample of an adult gelada baboon (Theropithecus gelada). Phylogenetic analyses based on 16S rRNA genes as well as multilocus sequences (representing fusA, gyrB and xfp genes) and the core genome revealed that GLDI4/2T exhibited phylogenetic relatedness to Alloscardovia omnicolens DSM 21503T and to Alloscardovia macacae DSM 24762T. Comparative analysis of 16S rRNA gene sequences confirmed the phylogenetic results showing the highest gene sequence identity with strain A. omnicolens DSM 21503T (96.0 %). Activities of α- and ß-gluco(galacto)sidases were detected in strain GLDI4/2T, which is characteristic for almost all members of the family Bifidobacteriaceae. Compared to other Alloscardovia species its DNA G+C content (43.8 mol%) was very low. Phylogenetic studies and the evaluation of phenotypic characteristics, including the results of biochemical, physiological and chemotaxonomic analyses, confirmed the novel species status for strain GLDI4/2T, for which the name Alloscardoviatheropitheci sp. nov. is proposed. The type strain is GLDI4/2T (=DSM 106019T=JCM 32430T).

Morphology, diet, and stable carbon isotopes: On the diet of Theropithecus and some limits of uniformitarianism in paleoecology.

Geladas were long supposed to be the only living primates feeding almost entirely on graminoids and accordingly display dramatic dental and manual adaptive traits. A recent study of Theropithecus gelada, the first in a relatively undisturbed habitat, revealed a more diverse diet, also incorporating large quantities of forbs. The peculiar adaptive traits of T. gelada are also observed in extinct Theropithecus as early as 3.7 Ma. Stable carbon isotopic data of extinct Theropithecus from eastern Africa indicate that specimens older than 3 Ma consumed a significant proportion of C3 plants (on average ca. 40% of total food intake) whereas specimens younger than 2 Ma consumed more C4 plants (on average ca. 80%). Recent paleobotanical evidence suggests that C3 herbaceous plants were still present in non-negligible proportions in Plio-Pleistocene lowland tropical ecosystems. Together, the shared morphological adaptive traits of extant and extinct Theropithecus and the varied diets of extant T. gelada suggest that the paleodiets of Theropithecus may have been dominated by herbaceous plants, comprising both C3 forbs and graminoids and C4 graminoids. The changes in stable carbon isotopes could correspond to a replacement of C3 plants by C4 plants within the herbaceous strata rather than a shift from C3 woody vegetation to C4 graminoids. This synthesis highlights the need for a more exhaustive knowledge of the ecology of extant species to achieve meaningful paleodietary and paleoenvironmental reconstructions. A strong selectivity for food resources that are rare in the landscapes (as in T. gelada) should also be considered when interpreting stable carbon isotopes of extinct African mammals (and notably hominids).

Morphoarchitectural variation in South African fossil cercopithecoid endocasts.

Despite the abundance of well-preserved crania and natural endocasts in the South African Plio-Pleistocene cercopithecoid record, which provide direct information relevant to the evolution of their endocranial characteristics, few studies have attempted to characterize patterns of external brain morphology in this highly successful primate Superfamily. The availability of non-destructive penetrating radiation imaging systems, together with recently developed computer-based analytical tools, allow for high resolution virtual imaging and modeling of the endocranial casts and thus disclose new perspectives in comparative paleoneurology. Here, we use X-ray microtomographic-based 3D virtual imaging and quantitative analyses to investigate the endocranial organization of 14 cercopithecoid specimens from the South African sites of Makapansgat, Sterkfontein, Swartkrans, and Taung. We present the first detailed comparative description of the external neuroanatomies that characterize these Plio-Pleistocene primates. Along with reconstruction of endocranial volumes, we combine a semi-automatic technique for extracting the neocortical sulcal pattern together with a landmark-free surface deformation method to investigate topographic differences in morphostructural organization. Besides providing and comparing for the first time endocranial volume estimates of extinct Plio-Pleistocene South African cercopithecoid taxa, we report additional information regarding the variation in the sulcal pattern of Theropithecus oswaldi subspecies, and notably of the central sulcus, and the neuroanatomical condition of the colobine taxon Cercopithecoides williamsi, suggested to be similar for some aspects to the papionin pattern, and discuss potential phylogenetic and taxonomic implications. Further research in virtual paleoneurology, applied to specimens from a wider geographic area, is needed to clarify the polarity, intensity, and timing of cortical surface evolution in cercopithecoid lineages.

Dietary ecology of fossil Theropithecus: Inferences from dental microwear textures of extant geladas from ecologically diverse sites.

As the only extant graminivorous primate, gelada monkeys (Theropithecus gelada) offer unique insights into how hominins and other extinct primates with strong C4 isotopic signatures may have subsisted on graminoid-rich diets. Fossil Theropithecus species sharing a strong C4 signal (i.e., Theropithecus brumpti, Theropithecus darti, and Theropithecus oswaldi) have been reconstructed as predominantly graminivorous and potentially in ecological competition with contemporaneous hominins. However, inferring the breadth and variation of diet in these species (and therefore hominins) has proven problematic. Understanding how ecological variation within extant geladas impacts microwear and isotopic signatures may contribute to reconstructions of diet in fossil Theropithecus. Here, we build on a recent study at an ecologically intact tall grass ecosystem (Guassa, Ethiopia) that expanded the known diversity of gelada diets by demonstrating lower reliance on graminoids, greater consumption of forbs, and greater dietary species richness than previously described at disturbed sites. We used dental microwear texture analysis to explore how dietary variation among extant geladas may inform our understanding of the diets of fossil Theropithecus. First, we compared the dental microwear textures of geladas at Guassa to those of geladas from other sites. The microwear textures of geladas at Guassa exhibited more complexity, less anisotropy, and more variance in anisotropy and heterogeneity, reflecting the greater dietary diversity of Guassa geladas. Comparing microwear texture variables among this expanded gelada sample to those for T. brumpti, T. oswaldi, and T. darti yielded no significant differences. These results raise the intriguing possibility that data on how ecological variation and diet impact dental microwear and (possibly) isotopic signatures in extant geladas can be used to reconstruct the diets of extinct theropiths and, more broadly, hominins with strong C4 isotopic signatures. We conclude that extant gelada populations offer a powerful analog for inferring dietary variation among predominantly graminivorous fossil primates.

Chronology for the Cueva Victoria fossil site (SE Spain): Evidence for Early Pleistocene Afro-Iberian dispersals.

Cueva Victoria has provided remains of more than 90 species of fossil vertebrates, including a hominin phalanx, and the only specimens of the African cercopithecid Theropithecus oswaldi in Europe. To constrain the age of the vertebrate remains we used paleomagnetism, vertebrate biostratigraphy and (230)Th/U dating. Normal polarity was identified in the non-fossiliferous lowest and highest stratigraphic units (red clay and capping flowstones) while reverse polarity was found in the intermediate stratigraphic unit (fossiliferous breccia). A lower polarity change occurred during the deposition of the decalcification clay, when the cave was closed and karstification was active. A second polarity change occurred during the capping flowstone formation, when the upper galleries were filled with breccia. The mammal association indicates a post-Jaramillo age, which allows us to correlate this upper reversal with the Brunhes-Matuyama boundary (0.78 Ma). Consequently, the lower reversal (N-R) is interpreted as the end of the Jaramillo magnetochron (0.99 Ma). These ages bracket the age of the fossiliferous breccia between 0.99 and 0.78 Ma, suggesting that the capping flowstone was formed during the wet Marine Isotopic Stage 19, which includes the Brunhes-Matuyama boundary. Fossil remains of Theropithecus have been only found in situ ∼1 m below the B/M boundary, which allows us to place the arrival of Theropithecus to Cueva Victoria at ∼0.9-0.85 Ma. The fauna of Cueva Victoria lived during a period of important climatic change, known as the Early-Middle Pleistocene Climatic Transition. The occurrence of the oldest European Acheulean tools at the contemporaneous nearby site of Cueva Negra suggest an African dispersal into SE Iberia through the Strait of Gibraltar during MIS 22, when sea-level was ∼100 m below its present position, allowing the passage into Europe of, at least, Theropithecus and Homo bearing Acheulean technology.

Dietary change among hominins and cercopithecids in Ethiopia during the early Pliocene.

The incorporation of C4 resources into hominin diet signifies increased dietary breadth within hominins and divergence from the dietary patterns of other great apes. Morphological evidence indicates that hominin diet became increasingly diverse by 4.2 million years ago but may not have included large proportions of C4 foods until 800 thousand years later, given the available isotopic evidence. Here we use carbon isotope data from early to mid Pliocene hominin and cercopithecid fossils from Woranso-Mille (central Afar, Ethiopia) to constrain the timing of this dietary change and its ecological context. We show that both hominins and some papionins expanded their diets to include C4 resources as early as 3.76 Ma. Among hominins, this dietary expansion postdates the major dentognathic morphological changes that distinguish Australopithecus from Ardipithecus, but it occurs amid a continuum of adaptations to diets of tougher, harder foods and to committed terrestrial bipedality. In contrast, carbon isotope data from cercopithecids indicate that C4-dominated diets of the earliest members of the Theropithecus oswaldi lineage preceded the dental specialization for grazing but occurred after they were fully terrestrial. The combined data indicate that the inclusion of C4 foods in hominin diet occurred as part of broader ecological changes in African primate communities.