Mount Pinatubo, Inflammatory Cytokines, and the Immunological Ecology of Aeta Hunter-Gatherers

Early growth cessation and reproduction are predicted to maximize fitness under conditions of high adult mortality, factors that could explain the pygmy phenotype of many rainforest hunter-gatherers. This life-history hypothesis is elegant but contentious in part because it lacks a clear biological mechanism. One mechanism stems from the field of human immunological ecology and the concept of inflammation memory across the life cycle and into subsequent generations. Maternal exposures to disease can infl uence immunological cues present in breast milk; because maternal provisioning via lactation occurs during critical periods of development, it is plausible that these cues can also mediate early growth cessation and small body size. Such epigenetic hypotheses are difficult to test, but the concept of developmental programming is attractive because it could explain how the stature of a population can change over time, in terms of both secular increases and rapid intergenerational decreases. Here we explore this concept by focusing on the Aeta, a population of former hunter-gatherers, and the Ilocano, a population of rice farmers. We predicted that Aeta mothers would produce breast milk with higher concentrations of four bioactive factors due to high infectious burdens. Further, we predicted that the concentrations of these factors would be highest in the cohort of women born in the early 1990s, when exposure to infectious disease was acute following the eruption of Mount Pinatubo in June 1991. We analyzed levels of adiponectin, C-reactive protein, and epidermal growth factor in the milk of 24 Aeta and 31 Ilocano women and found no detectable differences, whereas levels of transforming growth factor-β2 were elevated among the Aeta, particularly as a function of maternal age. We found no difference between cohorts divided by the volcanic eruption (n = 43 born before, n = 12 born after). We discuss the implications of our findings for the terminal investment hypothesis and we suggest that the historical ecology of the Aeta is a promising model system for testing epigenetic hypotheses focused on the evolution of small body size

Reindeer and the quest for Scottish enlichenment

Funding Information: The authors disclosed receipt of the following financial support for the research, authorship, and/or publication of this article: Data were collected with funding from the Goodman Fund, Dartmouth College and the Global Fellowship Scheme, University of St Andrews.In the hall of animal oddities, the reindeer (Rangifer tarandus) is the only mammal with a color-shifting tapetum lucidum and the only ruminant with a lichen-dominated diet. These puzzling traits coexist with yet another enigma––ocular media that transmit up to 60% of ultraviolet (UV) light, enough to excite the cones responsible for color vision. It is unclear why any day-active circum-Arctic mammal would benefit from UV visual sensitivity, but it could improve detection of UV-absorbing lichens against a background of UV-reflecting snows, especially during the extended twilight hours of winter. To explore this idea and advance our understanding of reindeer visual ecology, we recorded the reflectance spectra of several ground-growing (terricolous), shrubby (fruticose) lichens in the diets of reindeer living in Cairngorms National Park, Scotland.Publisher PDFPeer reviewe

Tree Climbing and Human Evolution

Paleoanthropologists have long argued—often contentiously—about the climbing abilities of early hominins and whether a foot adapted to terrestrial bipedalism constrained regular access to trees. However, some modern humans climb tall trees routinely in pursuit of honey, fruit, and game, often without the aid of tools or support systems. Mortality and morbidity associated with facultative arboreality is expected to favor behaviors and anatomies that facilitate safe and efficient climbing. Here we show that Twa hunter–gatherers use extraordinary ankle dorsiflexion (\u3e45°) during climbing, similar to the degree observed in wild chimpanzees. Although we did not detect a skeletal signature of dorsiflexion in museum specimens of climbing hunter–gatherers from the Ituri forest, we did find that climbing by the Twa is associated with longer fibers in the gastrocnemius muscle relative to those of neighboring, nonclimbing agriculturalists. This result suggests that a more excursive calf muscle facilitates climbing with a bipedally adapted ankle and foot by positioning the climber closer to the tree, and it might be among the mechanisms that allow hunter–gatherers to access the canopy safely. Given that we did not find a skeletal correlate for this observed behavior, our results imply that derived aspects of the hominin ankle associated with bipedalism remain compatible with vertical climbing and arboreal resource acquisition. Our findings challenge the persistent arboreal–terrestrial dichotomy that has informed behavioral reconstructions of fossil hominins and highlight the value of using modern humans as models for inferring the limits of hominin arboreality

Alcohol Discrimination and Preferences in Two Species of Nectar-Feeding Primate

Recent reports suggest that dietary ethanol, or alcohol, is a supplemental source of calories for some primates. For example, slow lorises (Nycticebus coucang) consume fermented nectars with a mean alcohol concentration of 0.6% (range: 0.0–3.8%). A similar behaviour is hypothesized for aye-ayes (Daubentonia madagascariensis) based on a single point mutation (A294V) in the gene that encodes alcohol dehydrogenase class IV (ADH4), the first enzyme to catabolize alcohol during digestion. The mutation increases catalytic efficiency 40-fold and may confer a selective advantage to aye-ayes that consume the nectar of Ravenala madagascariensis. It is uncertain, however, whether alcohol exists in this nectar or whether alcohol is preferred or merely tolerated by nectarivorous primates. Here, we report the results of a multiple-choice food preference experiment with two aye-ayes and a slow loris. We conducted observer-blind trials with randomized, serial dilutions of ethanol (0–5%) in a standard array of nectar- simulating sucrose solutions. We found that both species can discriminate varying concentrations of alcohol; and further, that both species prefer the highest available concentrations. These results bolster the hypothesized adaptive function of the A294V mutation in ADH4, and a connection with fermented foods, both in aye-ayes and the last common ancestor of African apes and humans

Phenotypic Plasticity of Climbing-Related Traits in the Ankle Joint of Great Apes and Rainforest Hunter-Gatherers

The negrito and African pygmy phenotypes are predominately exhibited by hunter-gatherers living in rainforest habitats. Foraging within such habitats is associated with a unique set of locomotor behaviors, most notably habitual vertical climbing during the pursuit of honey, fruit, and game. When performed frequently, this behavior is expected to correlate with developmentally plastic skeletal morphologies that respond to mechanical loading. Using six measurements in the distal tibia and talus that discriminate nonhuman primates by vertical climbing frequency, we tested the prediction that intraspecific variation in this behavior is reflected in the morphology of the ankle joint of habitually climbing human populations. First, to explore the plasticity of climbing-linked morphologies, we made comparisons between chimpanzees, gorillas, and orangutans from wild and captive settings. The analysis revealed significant differences in two climbing-linked traits (anterior expansion of the articular surface of the distal tibia and increased degree of talar wedging), indicating that these traits are sensitive to climbing behavior. However, our analyses did not reveal any signatures of climbing behavior in the ankles of habitually climbing hunter-gatherers. These results suggest that the detection of fine-grained differences in human locomotor behaviors at the ankle joint, particularly those associated with arboreality, may be obscured by the functional demands of terrestrial bipedalism. Accordingly, it may be difficult to use population-level characteristics of ankle morphology to make inferences about the climbing behavior of hominins in the fossil record, even when facultative arborealism is associated with key fitness benefits

Collapse of an ecological network in Ancient Egypt

The dynamics of ecosystem collapse are fundamental to determining how and why biological communities change through time, as well as the potential effects of extinctions on ecosystems. Here we integrate depictions of mammals from Egyptian antiquity with direct lines of paleontological and archeological evidence to infer local extinctions and community dynamics over a 6000-year span. The unprecedented temporal resolution of this data set enables examination of how the tandem effects of human population growth and climate change can disrupt mammalian communities. We show that the extinctions of mammals in Egypt were nonrandom, and that destabilizing changes in community composition coincided with abrupt aridification events and the attendant collapses of some complex societies. We also show that the roles of species in a community can change over time, and that persistence is predicted by measures of species sensitivity, a function of local dynamic stability. Our study is the first high-resolution analysis of the ecological impacts of environmental change on predator-prey networks over millennial timescales, and sheds light on the historical events that have shaped modern animal communities

ASPM and the Evolution of Cerebral Cortical Size in a Community of New World Monkeys

The ASPM (abnormal spindle-like microcephaly associated) gene has been proposed as a major determinant of cerebral cortical size among primates, including humans. Yet the specific functions of ASPM and its connection to human intelligence remain controversial. This debate is limited in part by a taxonomic focus on Old World monkeys and apes. Here we expand the comparative context of ASPM sequence analyses with a study of New World monkeys, a radiation of primates in which enlarged brain size has evolved in parallel in spider monkeys (genus Ateles) and capuchins (genus Cebus). The primate community of Costa Rica is perhaps a model system because it allows for independent pairwise comparisons of smaller- and larger-brained species within two taxonomic families. Accordingly, we analyzed the complete sequence of exon 18 of ASPM in Ateles geoffroyi, Alouatta palliata, Cebus capucinus, and Saimiri oerstedii. As the analysis of multiple species in a genus improves phylogenetic reconstruction, we also analyzed eleven published sequences from other New World monkeys. Our exon-wide, lineage-specific analysis of eleven genera and the ratio of rates of nonsynonymous to synonymous substitutions (dN/dS) on ASPM revealed no detectable evidence for positive selection in the lineages leading toAteles or Cebus, as indicated by dN/dS ratios of ,1.0 (0.6502 and 0.4268, respectively). Our results suggest that a multitude of interacting genes have driven the evolution of larger brains among primates, with different genes involved in this process in different encephalized lineages, or at least with evidence for positive selection not readily apparent for the same genes in all lineages. The primate community of Costa Rica may serve as a model system for future studies that aim to elucidate the molecular mechanisms underlying cognitive capacity and cortical size

Euarchontan opsin variation brings new focus to primate origins

Debate on the adaptive origins of primates has long focused on the functional ecology of the primate visual system. For example, it is hypothesized that variable expression of short- (SWS1) and middle-to-long-wavelength sensitive (M/LWS) opsins, which confer color vision, can be used to infer ancestral activity patterns and therefore selective ecological pressures. A problem with this approach is that opsin gene variation is incompletely known in the grandorder Euarchonta, i.e., the orders Scandentia (treeshrews), Dermoptera (colugos), and Primates. The ancestral state of primate color vision is therefore uncertain. Here we report on the genes (OPN1SW and OPN1LW) that encode SWS1 and M/LWS opsins in seven species of treeshrew, including the sole nocturnal scandentian Ptilocercus lowii. In addition, we examined the opsin genes of the Central American woolly opossum (Caluromys derbianus), an enduring ecological analogue in the debate on primate origins. Our results indicate: 1) retention of ultraviolet (UV) sensitivity in C. derbianus and a shift from UV to blue spectral sensitivities at the base of Euarchonta; 2) ancient pseudogenization of OPN1SW in the ancestors of P. lowii, but a signature of purifying selection in those of C. derbianus; and, 3) the absence of OPN1LW polymorphism among diurnal treeshrews. These findings suggest functional variation in color vision of nocturnal mammals and a distinctive visual ecology of early primates, perhaps one that demanded greater spatial resolution under light levels that could support cone-mediated color discrimination