Brenda R. Benefit

On the Relationships and Adaptations of Kenyapithecus, a Large-Bodied Hominoid from the Middle Miocene of Eastern Africa

The phylogenetic relationships and adaptations of Kenyapithecus have been of special interest since Leakey (1962, p. 696) first described the genus as possessing a number of characters exhibiting “a marked tendency in the direction of the Hominidae.” Expectations regarding the hominid affinities of Kenyapithecus influenced the reconstruction of many functionally and phylogenetically significant aspects of its anatomy in the absence of tangible fossil evidence. The type species Kenyapithecus wickeri is represented by four jaw fragments, 11 isolated teeth, and a distal humerus collected from a single site, Fort Ternan (Pickford, 1985). As of 1985, the hypodigm of the referred species Kenyapithecus africanus consisted of the type maxilla together with 46 isolated teeth, four incomplete postcranial pieces, and a poorly preserved mandible collected from the Maboko Formation and an isolated lower molar from Nyakach (Pickford, 1985). Features for which little or no fossil evidence existed, but which Kenyapithecus was said to share with hominids, include: small lower incisors relative to cheek tooth size, reduced incisor procumbency, arcuate dental arcade, short rostrum, and a humerus that is longer than the femur (Simons and Pilbeam, 1972). The supposed reduction in upper canine and lower incisor size, and facial abbreviation, in combination with thickenameled molars in Kenyapithecus was interpreted as being related to an australopithecine-like emphasis on molar grinding resulting from the consumption of hard objects (Andrews and Walker, 1976), with incisors being “relatively unimportant in food preparation” (Simons and Pilbeam, 1978, pp. 149, 152).

Fossil Evidence for the Origins of Terrestriality among Old World Higher Primates

Preference for terrestrial substrates is one of the most significant adaptive differences between some members of the radiation of Old World higher primates and the anthropoids of the Neotropics (Le Gros Clark, 1959; Napier and Napier, 1967, 1985; Fleagle, 1988; Martin, 1990). Adaptations for terrestriality are most conspicuous among savanna baboons (Papio — Rose, 1977), geladas (Theropithecus — Jolly, 1967; Dunbar and Dunbar, 1974), and humans (Napier, 1967). Varying degrees of semi-terrestriality and terrestriality are also present among the African great apes (Gorilla — Remis, 1995 and Pan — Hunt, 1992; Doran, 1993) and some of the Asian colobines (Presbytis entellus — Ripley, 1967 and Rhinopithecus roxellana — Davison, 1982), guenons (Cercopithecus aethiops and Erythrocebus patas — Hall, 1965), mandrills and drills (Mandrillus — Jouventin, 1975), mangabeys (Cercocebus — Waser, 1984), and macaques (e.g., Macaca nemestrina — Caldicott, 1986). In contrast, terrestrial adaptations are notably absent from the otherwise diverse adaptive array of New World anthropoids.

Earliest known Old World monkey skull

Similarities of the skull are commonly used to support hypotheses of ancestor–descendant relationships between fossil and living ape genera, especially between the late Miocene apes Sivapithecus and Dryopithecus from Eurasia and the living orang-utan (Pongo) from Borneo and Sumatra. Yet determining whether craniofacial traits shared by extant and Miocene apes are primitive or derived is severely hampered by the rarity of well-preserved fossil crania, particularly of early members of their closest outgroup, the Old World monkeys (Cercopithecoidea). The discovery of a complete and undistorted skull of Victoriapithecus at middle Miocene deposits from Maboko Island, Kenya, provides evidence of intact cranial-vault and basicranial morphology, brain size and craniofacial hafting for a primate from between 32 and 7 million years ago. Victoriapithecus represents a branch of Old World monkey that is intermediate between extant cercopithecids (Colobinae and Cercopithecinae) and the common ancestor they shared with apes (Hominoidea). The skull preserves traits widely thought to be derived for extant and fossil members of a proposed Sivapithecus/Pongo clade, but which now appear to be primitive features of ancestral Old World higher primates in general.

Evolution of locomotion in Anthropoidea: the semicircular canal evidence

Our understanding of locomotor evolution in anthropoid primates has been limited to those taxa for which good postcranial fossil material and appropriate modern analogues are available. We report the results of an analysis of semicircular canal size variation in 16 fossil anthropoid species dating from the Late Eocene to the Late Miocene, and use these data to reconstruct evolutionary changes in locomotor adaptations in anthropoid primates over the last 35 Ma. Phylogenetically informed regression analyses of semicircular canal size reveal three important aspects of anthropoid locomotor evolution: (i) the earliest anthropoid primates engaged in relatively slow locomotor behaviours, suggesting that this was the basal anthropoid pattern; (ii) platyrrhines from the Miocene of South America were relatively agile compared with earlier anthropoids; and (iii) while the last common ancestor of cercopithecoids and hominoids likely was relatively slow like earlier stem catarrhines, the results suggest that the basal crown catarrhine may have been a relatively agile animal. The latter scenario would indicate that hominoids of the later Miocene secondarily derived their relatively slow locomotor repertoires.

Systematics of early and middle Miocene Old World monkeys

New information about the early cercopithecoids Prohylobates tandyi (Wadi Moghra, Egypt) and Prohylobates sp. indet. (Buluk and Nabwal, Kenya) is presented. Comparisons are made among all major collections of Early and Middle Miocene catarrhine monkeys, and a systematic revision of the early Old World monkeys is provided. Previous work involving the systematics of early Old World monkeys (Victoriapithecidae; Cercopithecoidea) has been hampered by a number of factors, including the poor preservation of Prohylobates material from North Africa and lack of comparable anatomical parts across collections. However, it is now shown that basal cercopithecoid species from both northern and eastern Africa can be distinguished from one another on the basis of degree of lower molar bilophodonty, relative lower molar size, occlusal details, symphyseal construction, and mandibular shape. Results of particular interest include: 1) the first identification of features that unambiguously define Prohylobates relative to Victoriapithecus; 2) confirmation that P. tandyi is incompletely bilophodont; and 3) recognition of additional victoriapithecid species.

Cerebral complexity preceded enlarged brain size and reduced olfactory bulbs in Old World monkeys

Analysis of the only complete early cercopithecoid (Old World monkey) endocast currently known, that of 15-million-year (Myr)-old Victoriapithecus, reveals an unexpectedly small endocranial volume (ECV) relative to body size and a large olfactory bulb volume relative to ECV, similar to extant lemurs and Oligocene anthropoids. However, the Victoriapithecus brain has principal and arcuate sulci of the frontal lobe not seen in the stem catarrhine Aegyptopithecus, as well as a distinctive cercopithecoid pattern of gyrification, indicating that cerebral complexity preceded encephalization in cercopithecoids. Since larger ECVs, expanded frontal lobes, and reduced olfactory bulbs are already present in the 17- to 18-Myr-old ape Proconsul these features evolved independently in hominoids (apes) and cercopithecoids and much earlier in the former. Moreover, the order of encephalization and brain reorganization was apparently different in hominoids and cercopithecoids, showing that brain size and cerebral organization evolve independently.

Terrestriality in a Middle Miocene Context: Victoriapithecus from Maboko, Kenya

As possibly the earliest higher primate to eschew the trees and descend to the ground, Victoriapithecus offers several important lessons that may have implications for understanding our own ancestry. First, while paleoenvironment obviously constrains paleoecology, it should not be equated with a species’ paleoecology. Although there is a definite correlate between substrate preference and locomotor mode, evidence from Victoriapithecus suggests there is no a priori relationship between locomotor mode and paleoenvironment; that is, wooded or forested environs do not preclude terrestrial behaviors.

The Lacrimal Fossa of Cercopithecoidea, with Special Reference to Cladistic Analysis of Old World Monkey Relationships

Re-examination of lacrimal fossa patterns in extant cercopithecoids indicates that the last common ancestor of Cercopithecini and Papionini, and hence of Cercopithecinae, probably retained a maxillary contribution to the lacrimal fossa, as did the common ancestor of Colobinae. Consequently, the presence of a maxilla-lacrimal fossa cannot be used to assess the subfamily affinity of Old World monkeys. In addition to being correlated with general facial lengthening, the derived, exclusively lacrimal pattern of Erythrocebus, Mandrillus, Papio, Theropithecus and some (but not all) guenons, macaques and mangabeys may be associated with extreme narrowing of the interorbital septum. Moreover, the derived condition may have evolved in response to independent exploitation of open country habitats as it enhances protection of the lacrimal sac and serves to reduce eye infection in terrestrial species.

Role of monkeys in the sylvatic cycle of chikungunya virus in Senegal

Arboviruses spillover into humans either as a one-step jump from a reservoir host species into humans or as a two-step jump from the reservoir to an amplification host species and thence to humans. Little is known about arbovirus transmission dynamics in reservoir and amplification hosts. Here we elucidate the role of monkeys in the sylvatic, enzootic cycle of chikungunya virus (CHIKV) in the region around Kédougou, Senegal. Over 3 years, 737 monkeys were captured, aged using anthropometry and dentition, and tested for exposure to CHIKV by detection of neutralizing antibodies. Infant monkeys were positive for CHIKV even when the virus was not detected in a concurrent survey of mosquitoes and when population immunity was too high for monkeys alone to support continuous transmission. We conclude that monkeys in this region serve as amplification hosts of CHIKV. Additional efforts are needed to identify other hosts capable of supporting continuous circulation.The authors examine the role of monkey populations in the sylvatic cycle of chikungunya virus in the Kédougou region, Senegal. The authors show that monkeys are amplification hosts, as opposed to reservoir hosts for infection. These findings expand our knowledge of the transmission dynamics of chikungunya virus in this region of Senegal.

Monkey in the middle: monkeys serve as amplification hosts but not reservoir hosts of sylvatic chikungunya virus

Background Novel pathogens can emerge into humans via one-step transmission from a reservoir host, an animal species in which the pathogen is maintained, or a two-step process in which the pathogen is transmitted from the reservoir host into a different amplification host species and thence to humans. Here we use serosurveillance and mathematical modeling to discover whether monkeys serve as reservoir or amplification hosts for mosquito-borne chikungunya virus (CHIKV). CHIKV invaded the Americas in 2013, and our study provides key data for predicting whether and where CHIKV will establish enzootic transmission among animal hosts in the New World. Results Over three years we captured 219 African green monkeys, 78 patas monkeys, and 440 Guinea baboons, the three monkey species near Kédougou, Senegal. Monkey age was determined by anthropometry and dentition, and exposure of each animal to CHIKV was determined via detection of neutralizing antibodies. Age and exposure were used to estimate age-specific CHIKV seroprevalence, force of infection (FoI), and basic reproductive number (R0) in each species. CHIKV FoI were extremely high, ranging from 0.13 (95% CI, 0.07–0.22) in patas in 2012 to 1.12 (95% CI, 0.81–2.28) in African greens in 2011. R0 ranged from 1.5 (95% CI, 1.3–1.9) in patas in 2012, to 6.6 (95% CI, 5.1–10.4) in baboons in 2011. Conclusions These findings demonstrate that monkeys in this region are constantly exposed to CHIKV transmission, even when population seropositivity, and therefore immunity, was too high for monkeys themselves to support continuous CHIKV transmission. We therefore conclude that monkeys in this system serve as amplification rather than reservoir hosts of CHIKV. Considering the potential for CHIKV to spill back in to monkeys in the Americas and elsewhere, improved understanding of its sylvatic cycle is essential to understanding and perhaps controlling the spread of this virus.Athropod-borne viruses (arboviruses) pose the greatest risk of spillover into humans of any class of pathogens. Such spillover may occur as a one-step jump from a reservoir host species into humans or as a two-step jump from the reservoir to a different amplification host species and thence to humans. Despite the widespread havoc wreaked by emerging arboviruses, little is known about their transmission dynamics in reservoir and amplification hosts. Here we used serosurveillance and mathematical modeling to elucidate the role of monkeys in the sylvatic, enzootic cycle of chikungunya virus (CHIKV). Over three years, 219 African green monkeys, 78 patas monkeys, and 440 Guinea baboons were captured in the region surrounding Kedougou, Senegal. The age of each animal was determined by anthropometry and dentition, and exposure to CHIKV was determined by detection of neutralizing antibodies. We estimate age-specific CHIKV seroprevalence, force of infection (FoI), and basic reproductive number (R0) in each species. Among the different species, CHIKV FoI ranged from 0.13 to 1.12 (95% CI, 0.81-2.28) and R0 ranged from 1.5 (95% CI, 1.3-1.9) to 6.6 (95% CI, 5.1-10.4). CHIKV infection of infant monkeys was detected even when the virus was not detected in a concurrent survey of primatophilic mosquitoes and when population seropositivity, and therefore immunity, was too high for monkeys themselves to support continuous CHIKV transmission. We therefore conclude that monkeys in this region serve primarily as amplification rather than reservoir hosts of CHIKV. Additional efforts are needed to identify other vertebrate hosts capable of supporting continuous circulation.