Geographic distribution of microsatellite alleles in geladas (Primates,Cercopithecidae): Evidence for three evolutionary units

The subspecific taxonomy and distribution of geladas (Theropithecus gelada Rüppell, 1835) remains uncertain. Recent molecular studies based on mitochondrial sequence data revealed a geographically structured, three-deme population, suggesting that there are three evolutionary units of geladas. However, mitochondrial distributions do not always recover population relationships, particularly in taxa with a complex history of isolation and gene flow. We therefore analysed the nuclear genetic population structure of the global gelada population based on 20 microsatellite loci in 43 samples from across its geographic range. F_ST values, a STRUCTURE analysis and a principal coordinate analysis (PCoA) confirmed the three-deme population structure corresponding to the mitochondrial population structure. Therefore, our analyses provide additional support for three evolutionary units in geladas, corresponding to (a) a northern (north of Lake Tana, primarily in the Simien Mountains, previously classified as Theropithecus gelada gelada Rüppell, 1835), (b) a central (between Addis Ababa and the highlands east of Lake Tana, previously classified as Theropithecus gelada obscurus Heuglin, 1863) and (c) a southern (south of the Rift Valley, previously tentatively classified as Theropithecus gelada arsi Shotake et al., 2016, Anthropological Science, 124, 157) population. These results pave the way for future conservation decisions and highlight that the gelada population boundaries need more fine-grained genetic sampling and phenotypic analyses, in particular for their taxonomic ranking.     

Intergeneric Hybrid Baboons

Though belonging to genera that have been distinct for several million years, gelada and common baboons—Theropithecus gelada and Papio hamadryas sensu lato, respectively—interbreed occasionally, even in the wild. A female hamadryas at Bihere Tsige Park, Addis Ababa, Ethiopia, apparently favored a gelada male over eligible conspecifics and produced several offspring with him. The F ₁ hybrids were large but developmentally normal. In skull and tooth form, and to a lesser extent in postcranial proportions, they were intermediate between the parental forms but lacked most of their parents' derived, (sub)species-specific epigamic characters. A female infant born to a subadult F ₁ was sired by a hamadryas. The backcross infant appeared normal and was still flourishing at about 2.5 years. Though perhaps impeded by natural selection against poorly adapted hybrids, theoretically interspecific hybridization could exceed mutation as a source of novel, preadapted genes in the wild.     

Social organization of gelada baboons: Social units and definitions

This paper aims to clarify terminological differences that have arisen between two different field studies of gelada baboons (Theropithecus gelada). First, a comparison of age classifications is made to show the physical correspondences between the two sets of classes. Second, the social system of the gelada baboon is outlined and the terms used to refer to the components of this system are defined and clarified. Attention is drawn to the complex structure of gelada society and to the relationship between the superficially similar social systems of the gelada and the hamadryas baboon.     

Patterns of reconciliation among captive gelada baboons (Theropithecus gelada): A brief report

Animals that live in groups are frequently exposed to conflict situations and must in some way maintain group cohesion. One mechanism that appears to restore social relationships after they have been disrupted by conflict isreconciliation. This study investigated reconciliatory behavior in the gelada baboon,Theropithecus gelada. The subjects were 11 adult geladas, housed in a large outdoor enclosure at the Bronx Zoo/Wildlife Conservation Park, New York. Five-minute focal animal samples following spontaneous aggression were compared with 5-min matched-control samples. The results of this study were: (1) geladas reunited in a friendly way after aggression; (2) former opponents were attracted to one another rather than dispersed from one another after a conflict; (3) most post-conflict reunions occurred within the first 2 min of the post-conflict period; and (4) geladas do not have any specific types of behavior associated with post-conflict reunions as do chimpanzees and macaques. The results of this study support the hypothesis that gelada baboons reconcile after aggression.     

A model of the gelada socio-ecological system

Data from three populations of gelada baboons are used to generate a model of the species' socio-ecology that relates time budget requirements to group size, day journey length, and relevant environmental parameters. The model is used to examine the range of environmental conditions under which gelada could survive. This analysis indicates that a grazing primate like the gelada would run out of available time for foraging at just above and just below the altitudes at which they are now found. This suggests that, contrary to previous supposition, gelada were not driven into a retreat habitat by more competitivePapio baboons, but rather withdrew from lower altitude habitats because they could not survive under these conditions as the climate deteriorated during the Holocene.     

The synchronization of voices by gelada monkeys

Evidence is presented from recordings made from captive gelada monkeys (Theropithecus gelada) that these monkeys are capable of synchronizing the onsets of their own vocal sounds to the anticipated onsets of sounds produced by other gelada voices. The possibility is discussed that in order to synchronize the onsets of their own sounds to the anticipated onsets of sounds made by other voices, such gelada voices have to possess the ability to “figure out” the tempo and rhythm of the vocal strings produced by the other voices and precisely control the timing of their own voices. It is suggested that geladas do synchronize their voices by using precise temporal and rhythmical controls on the outputs of their voices that are analogous to the temporal and rhythmical abilities humans use in many of the supra-segmental aspects of speech.     

A case of infanticide in a recently found gelada population in Arsi, Ethiopia

There have been no reports of infanticide in wild gelada baboons and it has been argued that infanticide is not necessary in geladas, since the birth interval of female gelada can be shortened after takeover of a unit by a new leader male without infanticide. However, we observed an instance of infanticide in a newly-found wild gelada population in the Arsi Region of Ethiopia. After a leader male of the unit was severely wounded by a leopard attack, he was quite weakened. The second male of the unit, a young adult male, became the leader of the unit three weeks later, but the former leader continued to stay in the unit as a second male. After a week, two other adult males joined the unit which, therefore, came to include four adult males. The infanticide took place nine days later. The perpetrator was one of the immigrant males and he showed great interest in the mother of the unweaned victim infant. Although the perpetrator copulated with her after the infanticide, the usurper was found to own all three adult females after two weeks following the infanticide; i.e. the perpetrator could not own any female. The wounded former leader showed conspicuous protective behavior towards the victim's mother and the dead infant. One possible explanation for the occurrence of infanticide in this population of geladas is as follows. Gelada males in this area may be able to join units more easily to form multi-male units but then have shorter tenure in the units. Facing the unstable condition of units, they may sometimes engage in infanticide to increase their breeding opportunities, even before becoming a leader.     

Sociological and demographic characteristics of a recently found arsi gelada population in ethiopia

A new population of gelada baboons isolated from other known gelada populations living on the opposite side of the Rift Valley was found in 1989 in the Arsi region of Ethiopia (Mori &Belay, 1990). Subsequent observations were conducted on the new gelada population in three study periods of 16 to 55 days over three consecutive years, 1994–1996. When we compare this population with other well studied northern populations, densities were lower, band size was smaller and the ratio of juveniles to adult females was lower. Based onOhsawa andDunbar's (1984) criteria these results suggest that this population exploits the harshest environment among known gelada populations. This may be due to the severe effect of the dry season at low altitude in the study site. Band size was small in the study site. Association rates of units were low, and each unit behaved more independently than those of northern populations. Age-sex composition of units changed drastically between consecutive study periods, indicating unstable unit structure. Moreover, there seems to be a tendency in this population whereby several adult males easily invade and are incorporated into a unit but the unit is expected to thereafter divide. The phenomenon can be explained by two factors: (1) Each unit fed rather independently in this area, where units fed intensively on both plateau and the slope of the cliff; and (2) Males may be incorporated in a unit for defense against leopards. As the units were vary small in size and unstable as compared with the Semien gelada units, the traditional concept of a stable gelada unit formed by blood related females, does not seem to fit this population.     

Impact of global warming on the distribution and survival of the gelada baboon: a modelling approach

The gelada baboon is a graminivorous primate whose ecology is unusually sensitive to ambient temperature. A systems model of the socio-ecology of the gelada is used to predict the impact of global warming on the species’ altitudinal distribution. The species’ lower altitudinal limit will rise by ≈ 500 m for every 2 °C increase in global mean temperature. A 7 °C rise in temperature would be sufficient to result in the species being confined to a small number of isolated mountain peaks, where its chances of survival will be greatly reduced. Changes in local climate are also likely to have significant effects on agricultural practice on the Ethiopian highlands, and this in turn is likely to have repercussions for the distribution patterns of the gelada by further constraining the habitat available to them.     

Blood protein variation of a new population of gelada baboons (Theoropithecus gelada), in the Southern Rift Valley, Arsi Region, Ethiopia

Blood protein polymorphism of gelada baboon (Theropithecus gelada) to the south of the Rift Valley, Arsi Region, were examined for 36 genetic loci using three electrophoresis techniques for 48 blood samples from three localities, and compared with the northern geladas. New variant alleles and genetic markers of Hb-α, PA-2, and TBPA loci were detected. The distribution patterns of the variant alleles of Hb-α, PA-2, TBPA, Pi, Gc, PGM-II, and TBPA loci were localized in the geographic regions of south and north gelada populations, respectively. Genetic variability of southern geladas was estimated as P_poly=0.083 and , which was comparable to northern geladas. A remarkably high genetic differentiation between the two geographic populations was shown byNei's genetic distance=0.071 and G_ST value=0.420. Our results of genetic analysis suggest that the southern and northern gelada populations have been separated for several hundred thousand years, and gene flow between the two geographic populations is severely restricted. The southern gelada baboon may be regarded as a distinct subspecies.     

Adaptation to grass-eating in gelada baboons

Gelada faecal samples were analyzed for nutritional content and for particle size, and compared with similar data forPapio baboons, cattle, and zebra. Particle size in gelada is similar to that for zebra, larger than that for cattle and smaller than that for baboons. Gelada and baboons are less efficient than ungulates at extracting protein from their diet. The data on energy extraction are less easy to interpret and appear to be confounded by dietary and seasonal factors. It is suggested that gelada may be too large to compete effectively with ruminants in low altitude grassland habitats under the climatic conditions that have prevailed in eastern Africa since the late Pleistocene.     

Female philopatry and dominance patterns in wild geladas

Cercopithecines have a highly conserved social structure with strong female bonds and stable, maternally inherited linear dominance hierarchies. This system has been ascribed to the pervasiveness of female philopatry within the typical multi-male, multi-female social groups. We examined the relationship between female philopatry, dominance hierarchies, and reproduction in geladas (Theropithecus gelada), a species with an unusual multi-leveled society. During a 4-year field study on a wild population in the Simien Mountains National Park, Ethiopia, we observed 14 units across two bands of geladas that underwent a number of events, such as male takeovers and female deaths, which could potentially disrupt female relationships and unit structure. First, we corroborate earlier reports that gelada females are natally philopatric: we observed no interunit migrations, and the female mortality rate was comparable to that of philopatric baboons (suggesting all female disappearances were indeed deaths). Second, contrary to previous reports, data from this long-term study show that geladas exhibit the linear and stable dominance hierarchies typical of other Cercopithecines. Moreover, female ranks appear to be maternally inherited. Third, we found no evidence that alpha females aggressively target the lowest ranking individuals, nor did rank confer clear reproductive advantages to dominant females within our 4-year observation period. As such, geladas fit the allostatic load model [Goymann & Wingfield, Animal Behaviour 67:591-602, 2004]. Our study confirms the importance of female philopatry in the kin-based Cercopithecine dominance system.     

Morphological and physiological aspects of digestive processes in the graminivorous primate Theropithecus gelada-a preliminary study

Hindgut fermentation has been suggested to contribute significantly to the digestive process in the gelada (Theropithecus gelada). We therefore hypothesized that in an in vitro fermentation test (Hohenheim gas test, using gas production as measure of microbial digestion) inoculum based on fresh gelada feces would degrade grass to a similar degree as zebra (Equus burchelli chapmani) feces and to a higher degree than that of hamadryas baboons (Papio hamadryas). Additionally, morphology of gelada tongue, salivary glands, stomach, and intestine were examined in this study. Gas production was measured between 4 and 96 hr using animal feces incubated with 200 mg of air-dry hay or mixed concentrate sample. For grass hay, 12-hr gas production was as follows: T. gelada (19.9 ml)>Papio (18.4 ml)>Equus (15.7 ml). After 24 hr, gas production changed: Papio (35.1 ml)>T. gelada (31.9 ml)>Equus (27.9 ml). At 96 hr, Papio was unexpectedly the most effective species with the highest gas production (53.1 ml)>zebra (51.2 ml)>gelada (49.4 ml). With a concentrate standard, 12-hr gas production was as follows: T. gelada (38.5 ml)>Equus (36.8 ml) = Papio (36.4 ml). At 24 hr, gas production differed: Papio (51.7 ml)>Equus (47.0 ml) = T. gelada (46.8 ml). At 96 hr, zebra was the most effective species with the highest gas production (63.9 ml)>Papio (60 ml) = T. gelada (59.9 ml). In conclusion, the results show that the microbial population present in gelada feces is able to ferment forage and concentrate substrates in vitro, although this fermentation did not occur with the expected effectiveness. Future studies should therefore focus also on the bacteria species involved.     

The socio‐genetics of a complex society: female gelada relatedness patterns mirror association patterns in a multilevel society

Multilevel societies with fission–fusion dynamics—arguably the most complex animal societies—are defined by two or more nested levels of organization. The core of these societies are modular social units that regularly fission and fuse with one another. Despite convergent evolution in disparate taxa, we know strikingly little about how such societies form and how fitness benefits operate. Understanding the kinship structure of complex societies could inform us about the origins of the social structure as well as about the potential for individuals in these societies to accrue indirect fitness benefits. Here, we combined genetic and behavioural data on geladas (Theropithecus gelada), an Old World Monkey, to complete the most comprehensive socio‐genetic analysis of a multilevel society to date. In geladas, individuals in the core social ‘units’, associate at different frequencies to form ‘teams’, ‘bands’ and, the largest aggregations, ‘communities’. Units were composed of closely related females, and females remained with their close kin during permanent fissions of units. Interestingly, female–female relatedness also significantly predicted between‐unit, between‐team and between‐band association patterns, while male–male relatedness did not. Thus, it is likely that the socio‐genetic structure of gelada society results from females maintaining associations with their female relatives during successive unit fissions—possibly in an attempt to balance the direct and indirect fitness benefits of group living. Overall, the persistence of associations among related females across generations appears to drive the formation of higher levels of gelada society, suggesting that females seek kin for inclusive fitness benefits at multiple levels of gelada society.     

Blood groups of apes and monkeys. VII. The human-type A-B-H factors in gelada monkeys (Therapithecus gelada)

A series of 21 gelada monkeys (Theropithecus gelada) all showed strong reactivity of their saliva for H substance, but no reactivity for either A or B. Tests on their sera in no case showed the simultaneous presence of both the agglutinins anti-A and anti-B; instead some animals had only anti-A, others had only anti-B, while the remainder had neither anti-A nor anti-B. These findings distinguish gelada monkeys from all other species of Old World monkeys tested to date. They also provide further evidence supporting the genetic independence of the H substance and the A-B-O blood groups.     

Leopard predation on gelada monkeys at Guassa,Ethiopia

Predation is widely believed to exert strong selective pressure on primate behavior and ecology but is difficult to study and rarely observed. In this study, we describe seven encounters between lone wild leopards (Panthera pardus) and herds of geladas (Theropithecus gelada) over a 6-year period in an intact Afroalpine grassland ecosystem at the Guassa Community Conservation Area, Ethiopia. Three encounters consisted of attempted predation on geladas by leopards, one of which was successful. All three attacks occurred in low-visibility microhabitats (dominated by tussock graminoids, mima mounds, or tall shrubs) that provided leopards with hidden viewsheds from which to ambush geladas. An additional four encounters did not result in an attempted attack but still document the consistently fearful responses of geladas to leopards. In encounters with leopards, geladas typically gave alarm calls (n = 7 of 7 encounters), reduced interindividual distances (n = 5), and collectively fled towards or remained at their sleeping cliffs (n = 7), the only significant refugia in the open-country habitat at Guassa. Geladas did not engage in mobbing behavior towards leopards. Encounters with leopards tended to occur on days when gelada herd sizes were small, raising the possibility that leopards, as ambush hunters, might stalk geladas on days when fewer eyes and ears make them less likely to be detected. We compare the behavioral responses of geladas to leopards at Guassa with those previously reported at Arsi and the Simien Mountains and discuss how gelada vulnerability and responses to leopards compare with those of other primate species living in habitats containing more refugia. Lastly, we briefly consider how living in multilevel societies may represent an adaptive response by geladas and other open-country primates to predation pressure from leopards and other large carnivores.     

Anti-predator behavior of gelada baboons

The anti-predator behavior of gelada baboons has been observed to consist of simple flight (i.e. they flee to cliffs after becoming alarmed by potential predators). However, active antipredator behavior was observed in a recently found gelada population in Arsi, Ethiopia. This population showed frequent active counter-attacks and severe mobbing at predators. Males fought domestic dogs on the plain and exhibited a systematic mobbing behavior towards a leopard on the cliff face to chase it off. These active anti-predator behaviors are the first confirmed reports on gelada baboons and may provide a useful insight for the understanding of the process of evolutionary adaptation to highland habitats by gelada baboons, as well as for the origin of this small southern population.     

Defining Higher Levels in the Multilevel Societies of Geladas (Theropithecus gelada)

Multilevel societies, identified by two or more nested levels (or modules) of organization, have been touted as some of the most complex social systems. However, few empirical studies have effectively quantified the association patterns that delineate the various levels in such societies. In particular, the multiple levels of gelada society were first described >3 decades ago, yet no operational definitions exist for the higher levels, i.e., levels above the one-male unit. In geladas, multiple units form aggregations that fission and fuse throughout the day, and throughout the year, blurring the distinctions between previously described higher social levels: teams, bands, and communities. Here we use 5?yr of data on the daily composition of a population of geladas living in the Simien Mountains National Park, Ethiopia to test the hypothesis that higher levels of gelada organization are discrete entities. If gelada aggregations are nothing more than a group of units that share a home range, then we expect a continuous distribution of unit association. If, however, gelada aggregations are indeed discrete organizational levels, then we expect discontinuity in the patterns of association. We found significant discontinuity at the 50% association level, indicating a sharp distinction between members of the same band (>50% association) and members of the same community (<50% association). We also found evidence that recently fissioned units form teams that associate significantly more than other band members. Thus, despite their extremely fluid social organization, gelada social levels are nevertheless clearly identifiable and quantifiable. Based on these results, we suggest that gelada society is an extremely flexible, multilevel society with fission–fusion dynamics, and as such gelada society presents an unusual example for understanding the evolution of modular societies.     

Coalitions among gelada baboons

Geladas spend an unusually large amount of time in quiet, mutual grooming in this captive sample, part of which is presumably due to the effects of captivity and part is a reflection of the gelada pattern of social interactions. The most frequent signals associated with threat or displacement (lid) occurs only at a rate of 5.3 times per hour. Herding and displacement activities are important, but infrequent.One-male bisexual units are extremely cohesive. A male does not tolerate the positioning of another male between himself and any of his females, and the adults of the groups react antagonistically to each other's proximity.The solitary male is not groomed by other adults, but stays withChief's group and backsChief in interactions with the other group.Chief's group is a two-male unit in some ways, but withDemon being excluded from any activity or location which interferes withChief's interactions with his group.The females inEcho's group exhibit a dominance hierarchy, as measured in displacement, or denial of desirable social space. Interactions between individuals ofEcho's group reflect strong preferences between individuals, prohibitions toward certain relationships by more dominant individuals, and the ability to enlist the support of others in coalitions. Coalitions are simply another expression of social relationships that are more frequently expressed in grooming, proximity, and displacement.