All together now: Assessing variation in maternal and nonmaternal handling of wild Colobus vellerosus infants.

Primatologists have a long-standing interest in the study of maternal care and nonmaternal handling (NH) of infants stemming from recognition that early social relationships can have enduring consequences. Though maternal care and NH often include expression of similar behaviors, they are regularly studied in isolation from each other with nonoverlapping terminology, thereby overlooking possible interplay between them and obfuscating potential developmental ramifications that ensue from trade-offs made between maternal (MH) and NH during infancy. To that end, identifying how MH and NH patterns interact and contribute to the total handling (TH) infants receive is a critical first step. We present durational handling data collected from 25 wild Colobus vellerosus infants from 2016 to 2017 and assess the relationships between TH, MH, and NH. Patterns of social affiliation are shaped in part by surrounding context, and therefore, we also assess whether NH and TH differ in their responsivity to various infant and social group characteristics. Ninety-four percent of observed handling was MH, while just 5.5% was NH. Young infants who received more MH (excluding nursing) also received more NH; there was no relationship between the two in older infants. Infants in larger groups participated in more handling of all types. Additionally, NH time was associated with infant sex and group stability. Non-nursing TH time was associated with group stability and infant cohort size. Though NH variation likely confers social-networking advantage, in this population NH is not a major contributor to TH and would not effectively replace reduced MH. The positive association between MH and NH during early infancy suggests that colobus mothers may play a mediating role in shaping infant socialization. This is a first step in elucidating how different forms of handling relate to one another in wild primates and in identifying the impact of handling on infant socialization.

Impact of hindlimb length variation on jumping dynamics in the Longshanks mouse.

Distantly related mammals (e.g. jerboa, tarsiers, kangaroos) have convergently evolved elongated hindlimbs relative to body size. Limb elongation is hypothesized to make these species more effective jumpers by increasing their kinetic energy output (through greater forces or acceleration distances), thereby increasing take-off velocity and jump distance. This hypothesis, however, has rarely been tested at the population level, where natural selection operates. We examined the relationship between limb length, muscular traits and dynamics using Longshanks mice, which were selectively bred over 22 generations for longer tibiae. Longshanks mice have approximately 15% longer tibiae and 10% longer femora compared with random-bred Control mice from the same genetic background. We collected in vivo measures of locomotor kinematics and force production, in combination with behavioral data and muscle morphology, to examine how changes in bone and muscle structure observed in Longshanks mice affect their hindlimb dynamics during jumping and clambering. Longshanks mice achieved higher mean and maximum lunge-jump heights than Control mice. When jumping to a standardized height (14 cm), Longshanks mice had lower maximum ground reaction forces, prolonged contact times and greater impulses, without significant differences in average force, power or whole-body velocity. While Longshanks mice have longer plantarflexor muscle bodies and tendons than Control mice, there were no consistent differences in muscular cross-sectional area or overall muscle volume; improved lunge-jumping performance in Longshanks mice is not accomplished by simply possessing larger muscles. Independent of other morphological or behavioral changes, our results point to the benefit of longer hindlimbs for performing dynamic locomotion.

Oldest evidence of abundant C4 grasses and habitat heterogeneity in eastern Africa.

The assembly of Africa's iconic C4 grassland ecosystems is central to evolutionary interpretations of many mammal lineages, including hominins. C4 grasses are thought to have become ecologically dominant in Africa only after 10 million years ago (Ma). However, paleobotanical records older than 10 Ma are sparse, limiting assessment of the timing and nature of C4 biomass expansion. This study uses a multiproxy design to document vegetation structure from nine Early Miocene mammal site complexes across eastern Africa. Results demonstrate that between ~21 and 16 Ma, C4 grasses were locally abundant, contributing to heterogeneous habitats ranging from forests to wooded grasslands. These data push back the oldest evidence of C4 grass-dominated habitats in Africa-and globally-by more than 10 million years, calling for revised paleoecological interpretations of mammalian evolution.

The evolution of hominoid locomotor versatility: Evidence from Moroto, a 21 Ma site in Uganda.

Living hominoids are distinguished by upright torsos and versatile locomotion. It is hypothesized that these features evolved for feeding on fruit from terminal branches in forests. To investigate the evolutionary context of hominoid adaptive origins, we analyzed multiple paleoenvironmental proxies in conjunction with hominoid fossils from the Moroto II site in Uganda. The data indicate seasonally dry woodlands with the earliest evidence of abundant C4 grasses in Africa based on a confirmed age of 21 million years ago (Ma). We demonstrate that the leaf-eating hominoid Morotopithecus consumed water-stressed vegetation, and postcrania from the site indicate ape-like locomotor adaptations. These findings suggest that the origin of hominoid locomotor versatility is associated with foraging on leaves in heterogeneous, open woodlands rather than forests.

Assessing stress in wild black-and-white colobus monkeys non-invasively.

Analysis of glucocorticoid profiles serves as a valuable, multi-faceted tool for insight into the behavior and physiology of wild populations. Recently, the measurement of fecal glucocorticoid metabolites (FCMs) has exploded in popularity due to its compatibility with noninvasive techniques and remote environments A critical first step is to perform a biological validation to ensure that the assay accurately reflect changes in FCM levels. We use an enzyme immunoassay (EIA) to perform a biological validation on samples collected from two males and six females in a wild population of Colobus vellerosus in response to three naturally occurring potential stressors. We also describe the FCM response pattern in the week following parturition in three females and examine the influence of sex, reproductive state, and time of day on the concentrations of baseline samples collected daily from 13 adult individuals over a period of four months. We validated the assay: FCM levels increase in response to natural stressors with a two-day lag. In the two days surrounding parturition, FMC levels increased. Baseline concentrations were affected by collection time and female reproductive state, with lactating females having lower concentrations than pregnant or cycling females. Thus, we successfully carried out the first validation and characterization of FCMs in a wild African colobine. This will serve as an essential foundation for future studies of C. vellerosus and similar wild primates whose objective is to investigate the role glucocorticoids play in responses to social and ecological challenges.

Fine-scaled climate variation in equatorial Africa revealed by modern and fossil primate teeth.

Variability in resource availability is hypothesized to be a significant driver of primate adaptation and evolution, but most paleoclimate proxies cannot recover environmental seasonality on the scale of an individual lifespan. Oxygen isotope compositions (δ18O values) sampled at high spatial resolution in the dentitions of modern African primates (n = 2,352 near weekly measurements from 26 teeth) track concurrent seasonal precipitation, regional climatic patterns, discrete meteorological events, and niche partitioning. We leverage these data to contextualize the first δ18O values of two 17 Ma Afropithecus turkanensis individuals from Kalodirr, Kenya, from which we infer variably bimodal wet seasons, supported by rainfall reconstructions in a global Earth system model. Afropithecus' δ18O fluctuations are intermediate in magnitude between those measured at high resolution in baboons (Papio spp.) living across a gradient of aridity and modern forest-dwelling chimpanzees (Pan troglodytes verus). This large-bodied Miocene ape consumed seasonally variable food and water sources enriched in 18O compared to contemporaneous terrestrial fauna (n = 66 fossil specimens). Reliance on fallback foods during documented dry seasons potentially contributed to novel dental features long considered adaptations to hard-object feeding. Developmentally informed microsampling recovers greater ecological complexity than conventional isotope sampling; the two Miocene apes (n = 248 near weekly measurements) evince as great a range of seasonal δ18O variation as more time-averaged bulk measurements from 101 eastern African Plio-Pleistocene hominins and 42 papionins spanning 4 million y. These results reveal unprecedented environmental histories in primate teeth and suggest a framework for evaluating climate change and primate paleoecology throughout the Cenozoic.

Additional hominoid fossils from the early Miocene of the Lothidok Formation, Kenya.

OBJECTIVES: Hominoid fossils are abundant at early Miocene fossil sites in the Lothidok Range, located directly west of Lake Turkana in northern Kenya. The West Turkana Miocene Project (WTMP) has worked in the Lothidok Range since 2008 with the goal of further elucidating the paleobiology of the hominoids through the recovery of new specimens and detailed documentation of their paleoecological context. To date our research has focused largely on the Kalodirr and Moruorot Site Complexes, both radiometrically dated to ~17.5-16.8 Ma. MATERIALS AND METHODS: Our ongoing fieldwork at the Kalodirr Site Complex resulted in the discovery of new dentognathic specimens of the three previously identified species of fossil hominoids-Turkanapithecus kalakolensis, Simiolus enjiessi, and Afropithecus turkanensis. RESULTS: A new mandible and an isolated M3 of T. kalakolensis from Kalodirr further clarify the lower molar morphology of the species and permit identification of KNM-MO 1 as a mandible of T. kalakolensis. A new mandible of S. enjiessi provides evidence of the relative proportions of the first and second lower molars. A new male specimen of A. turkanensis shows unusual P4 morphology that may be a developmental anomaly or a previously unknown morphological variant. DISCUSSION: An improved understanding of the lower molar morphology of T. kalakolensis further strengthens its identification as a nyanzapithecine. Our new specimens and subsequent re-identification of existing collections makes it clear that all three Lothidok hominoids are known from both the Moruorot and Kalodirr Site Complexes. The Lothidok Range holds great promise for further documenting hominoid evolution.

Evidence for rapid faunal change in the early Miocene of East Africa based on revised biostratigraphic and radiometric dating of Bukwa, Uganda.

Field expeditions to Bukwa in the late 1960s and early 1970s established that the site had a small but diverse early Miocene fauna, including the catarrhine primate Limnopithecus legetet. Initial potassium-argon radiometric dating indicated that Bukwa was 22 Ma, making it the oldest of the East African early Miocene fossil localities known at the time. In contrast, the fauna collected from Bukwa was similar to other fossil localities in the region that were several million years younger. This discrepancy was never resolved, and due to the paucity of primate remains at the site, little subsequent research took place. We have collected new fossils at Bukwa, reanalyzed the existing fossil collections, and provided new radiometric dating. 40Ar/39Ar incremental heating ages on lavas bracketing the site indicate that the Bukwa fossils were deposited ∼19 Ma, roughly 3 Ma younger than the original radiometric age. Our radiometric dating results are corroborated by a thorough reanalysis of the faunal assemblage. Bukwa shares taxa with both stratigraphically older localities (Tinderet, Napak) and with stratigraphically younger localities (Kisingiri, Turkana Basin) perfectly corresponding to our revised radiometric age. This revised age for Bukwa is important because it indicates that significant faunal turnover may have occurred in East Africa between 20 and 19 Ma. Bukwa samples immigrant taxa such as large suids, large ruminants, and ochotonids that are absent from stratigraphically older but well-sampled localities in the region, such as Tinderet (∼20 Ma) and Napak (20 Ma). Further age refinements for Bukwa and the entire East African early Miocene sequence will help to constrain the timing of this faunal turnover event, of particular importance in paleoanthropology since this temporal sequence also provides us with what is currently our best window into the early evolution of cercopithecoid and hominoid primates.

A detailed assessment of the maxillary morphology of Limnopithecus evansi with implications for the taxonomy of the genus.

Limnopithecus is a small-bodied catarrhine genus that is widespread throughout early Miocene sites in East Africa. Although two species of this genus have been described - Limnopithecus legetet (type species) and Limnopithecus evansi - they are poorly known anatomically and their systematic positions remain unresolved. Here, we provide detailed descriptions and comparisons for two well-preserved maxillary specimens that we attribute to L. evansi. These specimens come from the type locality of the species, Songhor in western Kenya, and add greatly to our knowledge of its dentognathic morphology. Together, they preserve the entire unilateral upper dentition, with overlapping elements demonstrating conspecificity, and provide new information about I(2) morphology and aspects of the palate, nasal aperture, and maxillary sinuses. Detailed morphological comparisons suggest that specimens referred to Limnopithecus from Songhor, Koru, and Rusinga share a unique I(2) morphology not found in any other early Miocene catarrhine. This argues in favor of congeneric status for L. evansi and L. legetet. Moreover, features such as a broad palate, premolar morphology, and the relative proportions of the premolars of L. evansi distinguish it from Lomorupithecus harrisoni, another early Miocene catarrhine from Napak, Uganda. This finding challenges a recently proposed taxonomic interpretation that Lomorupithecus and L. evansi are conspecific. Our results underscore the distinctiveness of L. evansi and Lo. harrisoni, thereby reaffirming the validity of the taxon Lo. harrisoni and indicating that the Songhor and Napak catarrhine communities were relatively distinct, despite their apparent contemporaneity.

Additional mandibles of Rangwapithecus gordoni, an early Miocene catarrhine from the Tinderet localities of Western Kenya.

Two catarrhine mandibles and five isolated teeth have been discovered from Early Miocene localities in Western Kenya. One mandible comes from the well-known locality of Songhor whereas the other is from a newly discovered locality, Lower Kapurtay, located near Songhor. The mandibles both can clearly be assigned to the species Rangwapithecus gordoni based on molar morphology, which is unique among Early Miocene catarrhines. The isolated specimens can be assigned to Rangwapithecus based on their similarities in morphology to the homologues preserved in the two mandibles. These specimens provide important new information about the dentognathic morphology of Rangwapithecus, which is described in detail. The mandible from Songhor (KNM-SO 22228) represents the first definitive female mandible of Rangwapithecus. The Lower Kapurtay mandible (KNM-KT 31234) appears to be male but is much smaller than another recently described male mandible of this species (KNM-SO 17500) and the type maxilla (KNM-SO 700). These specimens enable a reassessment of the attributions of all other mandibles and isolated lower teeth of Rangwapithecus, and we present a complete hypodigm of the mandibular and lower dental material for the species. Finally, we provide some additions to the diagnosis of Rangwapithecus gordoni based on previously unknown morphology.

Stratigraphic interpretation of the Kulu Formation (Early Miocene, Rusinga Island, Kenya) and its implications for primate evolution.

Early Miocene fossils from Rusinga Island, Kenya, provide some of the best evidence for catarrhine evolution and diversification, and, together with more than eighty-five other mammalian species, form an important comparative reference for understanding faunal succession in East Africa. While there is consensus over the stratigraphic position of most of Rusinga's volcaniclastic deposits, the lacustrine Kulu Formation has been placed in various parts of the geological sequence by different researchers. To resolve this discrepancy, we conducted detailed geological analyses which indicate that the Kulu Formation was formed in the Early Miocene during a period of volcanic inactivity and subsidence following the early, mainly explosive hyper-alkaline phase of the Kisingiri complex and prior to the final eruptions of nephelinitic lavas. The underlying Hiwegi and older formations were locally deformed and deeply eroded before sedimentation began in the Kulu basin, so that the Kulu sediments may be significantly younger than the 17.8 Ma Hiwegi Formation and not much older than the overlying Kiangata Agglomerata-Lunene Lava series, loosely dated to ca. 15 Ma. The overall similarities between Kulu and Hiwegi faunas imply long-term ecological stability in this region. Our stratigraphic interpretation suggests that the Kulu fauna is contemporaneous with faunas from West Turkana, implying that differences between these assemblages-particularly in the primate communities--reflect paleobiogeographic and/or paleocological differences. Finally, the position of the Kulu Formation restricts the time frame during which the substantial faunal turnover seen in the differences between the primate and mammalian communities of Rusinga and Maboko Islands could have occurred.

Additional material of the enigmatic Early Miocene mammal Kelba and its relationship to the order Ptolemaiida.

Kelba quadeemae, a fossil mammal from the Early Miocene of East Africa, was originally named on the basis of three isolated upper molars. Kelba has previously been interpreted as a creodont, a pantolestid, an insectivoran, and a hemigaline viverrid. The true affinities of this taxon have remained unclear because of the limited material and its unique morphology relative to other Miocene African mammals. New material of Kelba from several East African Miocene localities, most notably a skull from the Early Miocene locality of Songhor in Western Kenya, permits analysis of the affinities of Kelba and documents the lower dentition of this taxon. Morphological comparison of this new material clearly demonstrates that Kelba is a member of the order Ptolemaiida, a poorly understood group whose fossil record was previously restricted to the Oligocene Fayum deposits of northern Egypt. Phylogenetic analysis supports the monophyly of the Ptolemaiida, including Kelba, and recovers two monophyletic clades within the order. We provide new family names for these groups and an emended diagnosis for the order. The discovery of ptolemaiidans from the Miocene of East Africa is significant because it extends the known temporal range of the order by >10 million years and the geographic range by >3,200 km. Although the higher-level affinities of the Ptolemaiida remain obscure, their unique morphology and distribution through a larger area of Africa (and exclusively Africa) lend support to the idea that Ptolemaiida may have an ancient African origin.