Mean age at menarche and climate variables on a global scale.

OBJECTIVES: Cross-population variation in age at menarche is related to many factors. The purpose of this study was to examine climate variables in relation to mean age at menarche among 87 modern human populations. We hypothesized a later age at menarche among populations living in areas with high precipitation variability, heavy seasonal rainfall, and high temperatures year-round due to water-borne diseases and periods of resource scarcity. METHODS: Using a comparative dataset, we examined geospatial distribution and climate variables in relation to age at menarche for 87 modern human populations. RESULTS: We found the strongest predictor of a later age at menarche was higher fertility followed by a later mean age at death. In addition, higher annual rainfall, higher precipitation seasonality, and lower annual mean temperature were moderate predictors of age at menarche. CONCLUSIONS: We propose that later ages at menarche in countries with high fertility may be a life-history strategy developed in response to climatic conditions that have resulted in higher immunological load. In these conditions, females may prioritize growth rather than reproduction. Shifts in climate and global population growth may change the future biological landscape of age at menarche.

Geographically divergent evolutionary and ecological legacies shape mammal biodiversity in the global tropics and subtropics.

Studies of the factors governing global patterns of biodiversity are key to predicting community responses to ongoing and future abiotic and biotic changes. Although most research has focused on present-day climate, a growing body of evidence indicates that modern ecological communities may be significantly shaped by paleoclimatic change and past anthropogenic factors. However, the generality of this pattern is unknown, as global analyses are lacking. Here we quantify the phylogenetic and functional trait structure of 515 tropical and subtropical large mammal communities and predict their structure from past and present climatic and anthropogenic factors. We find that the effects of Quaternary paleoclimatic change are strongest in the Afrotropics, with communities in the Indomalayan realm showing mixed effects of modern climate and paleoclimate. Malagasy communities are poorly predicted by any single factor, likely due to the atypical history of the island compared with continental regions. Neotropical communities are mainly codetermined by modern climate and prehistoric and historical human impacts. Overall, our results indicate that the factors governing tropical and subtropical mammalian biodiversity are complex, with the importance of past and present factors varying based on the divergent histories of the world's biogeographic realms and their native biotas. Consideration of the evolutionary and ecological legacies of both the recent and ancient past are key to understanding the forces shaping global patterns of present-day biodiversity and its response to ongoing and future abiotic and biotic changes in the 21st century.

Mid-Cenozoic climate change, extinction, and faunal turnover in Madagascar, and their bearing on the evolution of lemurs.

BACKGROUND: Was there a mid-Cenozoic vertebrate extinction and recovery event in Madagascar and, if so, what are its implications for the evolution of lemurs? The near lack of an early and mid-Cenozoic fossil record on Madagascar has inhibited direct testing of any such hypotheses. We compare the terrestrial vertebrate fauna of Madagascar in the Holocene to that of early Cenozoic continental Africa to shed light on the probability of a major mid-Cenozoic lemur extinction event, followed by an "adaptive radiation" or recovery. We also use multiple analytic approaches to test competing models of lemur diversification and the null hypothesis that no unusual mid-Cenozoic extinction of lemurs occurred. RESULTS: Comparisons of the terrestrial vertebrate faunas of the early Cenozoic on continental Africa and Holocene on Madagascar support the inference that Madagascar suffered a major mid-Cenozoic extinction event. Evolutionary modeling offers some corroboration, although the level of support varies by phylogeny and model used. Using the lemur phylogeny and divergence dates generated by Kistler and colleagues, RPANDA and TESS offer moderate support for the occurrence of unusual extinction at or near the Eocene-Oligocene (E-O) boundary (34 Ma). TreePar, operating under the condition of obligate mass extinction, found peak diversification at 31 Ma, and low probability of survival of prior lineages. Extinction at the E-O boundary received greater support than other candidate extinctions or the null hypothesis of no major extinction. Using the lemur phylogeny and divergence dates generated by Herrera & Dàvalos, evidence for large-scale extinction diminishes and its most likely timing shifts to before 40 Ma, which fails to conform to global expectations. CONCLUSIONS: While support for large-scale mid-Cenozoic lemur extinction on Madagascar based on phylogenetic modeling is inconclusive, the African fossil record does provide indirect support. Furthermore, a major extinction and recovery of lemuriforms during the Eocene-Oligocene transition (EOT) would coincide with other major vertebrate extinctions in North America, Europe, and Africa. It would suggest that Madagascar's lemurs were impacted by the climate shift from "greenhouse" to "ice-house" conditions that occurred at that time. This could, in turn, help to explain some of the peculiar characteristics of the lemuriform clade.

Sexual selection in the Kinda baboon.

Due to wide variation in the presence and degree of expression of a diverse suite of sexually-selected traits, the tribe Papionini represents an outstanding model for understanding how variation in sexual selection pressures and mechanisms leads to trait evolution. Here, we discuss the particular value of Papio as a model genus for studies of sexual selection, emphasizing the presence of multiple mating systems, and differences in the expression of sexually-selected traits among closely-related species. We draw particular attention to the Kinda baboon (Papio kindae), a comparatively less-studied baboon species, by providing a primer to Kinda baboon morphology, genetics, physiology, and behavior. Based on observations of large group sizes, combined with low degrees of sexual dimorphism and large relative testis size relative to other baboon species, we test the hypothesis that Kinda baboons have evolved under reduced direct, and increased indirect, male-male competition. We present the first long-term data on wild Kinda baboons in Zambia. Kinda baboon females show seasonal peaks in births and reproductive receptivity, and males exhibit a queing-rather than contest-based dominance acquisition with long alpha-male tenure lengths. We finish by making a number of explicit testable predictions about Kinda baboon sexual signals and behaviors, and suggest that Kinda baboons have potential to offer new insights into the selective environments that may have been experienced during homininization.

Diversity and evolution of human eccrine sweat gland density.

The human eccrine sweat gland is central to the evolution of the human genus, permitting an enormous thermoregulatory sweating capacity that was essential to the human niche of high physical activity in open, hot, semi-arid environments. Despite a century of research inventorying the structure and function of eccrine glands and the physiological responses of human heat acclimation, we do not have a clear understanding of how intraspecific differences in eccrine density affect thermoregulation. Similarly, existing data does not comprehensively catalogue modern human diversity in this trait, nor do we understand the relative influences of evolutionary forces and phenotypic plasticity in shaping this diversity.

The evolution of eccrine sweat glands in human and nonhuman primates.

Sweating is an unusual thermoregulatory strategy for most mammals, yet is critical for humans. This trait is commonly hypothesized to result from human ancestors moving from a forest to a warmer and drier open environment. As soft tissue traits do not typically fossilize, this idea has been difficult to test. Therefore, we used a comparative approach to examine 15 eccrine gland traits from 35 primate species. For each trait we measured phylogenetic signal, tested three evolutionary models to explain trait variation, and used phylogenetic models to examine how traits varied in response to climate variables. Phylogenetic signal in traits varied substantially, with the two traits exhibiting the highest values being gland distribution on the body and percent eccrine vs. apocrine glands on the body. Variation in most traits was best explained by an Ornstein-Uhlenbeck model suggesting the importance of natural selection. Two traits were strongly predicted by climate. First, species with high eccrine gland glycogen content were associated with habitats exhibiting warm temperatures and low rainfall. Second, species with increased capillarization were associated with high temperature. Glycogen is a primary energy substrate powering sweat production and sodium reabsorption in the eccrine gland, and increased capillarization permits greater oxygen, glucose and electrolyte delivery. Thus, our results are evidence of natural selection for increased sweating capacity in primate species with body surface eccrine glands living in hot and dry climates. We suggest that selection for increased glycogen content and capillarization may have been part of initial increases in hominin thermoregulatory sweating capacity.

Ecological niche modeling of the genus Papio.

OBJECTIVE: Ecological niche modeling (ENM) has been used to assess how abiotic variables influence species distributions and diversity. Baboons are broadly distributed throughout Africa, yet the degree of climatic specialization is largely unexplored for individual taxa. Also, the influence of climate on baboon phylogenetic divergence is unknown. In this study, we constructed ENMs to investigate how niches vary across Papio species to understand how climatic variables have influenced their biogeography and mode of speciation. MATERIALS AND METHODS: We used Maxent to generate ENMs by collating locality data for six Papio species and climate information from WorldClim. In addition, we examined the degree of niche overlap among all possible pairs of taxa, which can provide insight into patterns of species diversity. Lastly, we conducted a Mantel test to assess the relationship between niche overlap and estimated time since divergence. RESULTS: Our models performed moderately to extremely well, with a mean area under the curve value of 0.868. The species with the best models include P. papio and P. kindae, whereas P. hamadryas had the poorest models. We found that most species pairs exhibited significantly different niches. Lastly, we found no significant correlation between niche overlap and divergence times. DISCUSSION: Niche models had good predictive power, which indicates Papio species distributions are correlated with climatic variables to varying degrees. Significantly little niche overlap and incomplete geographic boundaries suggests these models generally support a parapatric speciation scenario for the genus Papio.

Cultural assemblages show nested structure in humans and chimpanzees but not orangutans.

The evolution of hominin culture is well-documented in the archeological and fossil record, but such a record is largely absent for nonhuman primates. An alternative approach to studying cultural evolution is to examine patterns of modern cultural variation. In this article we measure nestedness across human and great ape "cultural repertoires" to gain insight into the accumulation and maintenance of putative cultural diversity in these species. Cultural assemblages are nested if cultures with a small repertoire of traits tend to comprise a proper subset of those traits present in more complex cultures. This nesting will occur if some traits are sequentially gained or lost, which may be because of the differential dispersal or extinction of traits. Here we apply statistical tools from ecology to examine the degree of nestedness in four datasets documenting the presence or absence of specific cultural traits across indigenous human populations in North America and New Guinea. We then compare the human data to patterns observed for putative cultural traits in chimpanzee and orangutan populations. In both humans and chimpanzees, cultural diversity is highly nonrandom, showing significant nested structure for all of the datasets examined. We find no evidence for nestedness in the orangutan cultural data. These findings are consistent with a sequential "layering" of cultural diversity in humans and chimpanzees, but not orangutans. Such an interpretation implies that the traits required for sequential cultural evolution first appeared in the last common ancestor of chimpanzees and humans.

Strong influence of palaeoclimate on the structure of modern African mammal communities.

Ecological research often assumes that species are adapted to their current climatic environments. However, climate fluctuations over geologic timescales have influenced species dispersal and extinction, which in turn may affect community structure. Modern community structure is likely to be the product of both palaeoclimate and modern climate, with the relative degrees of influence of past and present climates unknown. Here, we assessed the influence of climate at different time periods on the phylogenetic and functional trait structure of 203 African mammal communities. We found that the climate of the mid-Holocene (approx. 6000 years ago) and Last Glacial Maximum (approx. 22 000 years ago) were frequently better predictors of community structure than modern climate for mammals overall, carnivorans and ungulates. Primate communities were more strongly influenced by modern climate than palaeoclimate. Overall, community structure of African mammals appears to be related to the ecological flexibility of the groups considered here and the regions of continental Africa that they occupy. Our results indicate that the future redistribution, expansion and contraction of particular biomes due to human activity, such as climate and land-use change, will differentially affect mammal groups that vary in their sensitivity to environmental change.

Transparency, usability, and reproducibility: Guiding principles for improving comparative databases using primates as examples.

Recent decades have seen rapid development of new analytical methods to investigate patterns of interspecific variation. Yet these cutting-edge statistical analyses often rely on data of questionable origin, varying accuracy, and weak comparability, which seem to have reduced the reproducibility of studies. It is time to improve the transparency of comparative data while also making these improved data more widely available. We, the authors, met to discuss how transparency, usability, and reproducibility of comparative data can best be achieved. We propose four guiding principles: 1) data identification with explicit operational definitions and complete descriptions of methods; 2) inclusion of metadata that capture key characteristics of the data, such as sample size, geographic coordinates, and nutrient availability (for example, captive versus wild animals); 3) documentation of the original reference for each datum; and 4) facilitation of effective interactions with the data via user friendly and transparent interfaces. We urge reviewers, editors, publishers, database developers and users, funding agencies, researchers publishing their primary data, and those performing comparative analyses to embrace these standards to increase the transparency, usability, and reproducibility of comparative studies.

Resource seasonality and reproduction predict fission-fusion dynamics in black-and-white ruffed lemurs (Varecia variegata).

Ruffed lemurs (genus Varecia) are often described as having a flexible social organization, such that both cohesive (low fission-fusion dynamics) and fluid (high fission-fusion dynamics) grouping patterns have been observed. In ruffed lemur communities with high fission-fusion dynamics, group members vary in their temporal and spatial dispersion throughout a communally defended territory. These patterns have been likened to those observed in several haplorrhine species that exhibit the most fluid types of fission-fusion social organization (e.g., Pan and Ateles). To substantiate and further refine these claims, we describe the fission-fusion dynamics of a black-and-white ruffed lemur (Varecia variegata) community at Mangevo, an undisturbed primary rainforest site in Ranomafana National Park, Madagascar. We collected instantaneous group scan samples from August 2007-December 2008 (4,044 observation hours) to study and characterize patterns of subgroup size, composition, cohesion, and social association. In 16 consecutive months, we never found all members of the community together. In fact, individuals spent nearly half of their time alone. Subgroups were small, cohesive, and typically of mixed-sex composition. Mixed-sex subgroups were significantly larger, less cohesive, and more common than either male-only or female-only subgroups. Subgroup dynamics were related to shifts in climate, phenology of preferred fruit species, and female reproductive state. On average, association indices were low. Males and females were equally gregarious; however, adult male-male associations were significantly weaker than any other association type. Results presented herein document striking differences in fission-fusion dynamics between black-and-white ruffed lemurs and haplorrhines, while also demonstrating many broad-scale similarities to haplorrhine taxa that possess the most fluid fission-fusion societies.

Behavioral thermoregulation in Lemur catta: The significance of sunning and huddling behaviors.

Regulation of body temperature poses significant problems for organisms that inhabit environments with extreme and seasonally fluctuating ambient temperatures. To help alleviate the energetic costs of autonomic responses, these organisms often thermoregulate through behavioral mechanisms. Among primates, lemurs in Madagascar experience uncharacteristically seasonal and unpredictable climates relative to other primate-rich regions. Malagasy primates are physiologically flexible, but different species use different mechanisms to influence their body temperatures. Lemur catta, the ring-tailed lemur, experiences particularly acute diurnal temperature fluctuations in its mostly open-canopy habitat in south and southwest Madagascar. Ring-tailed lemurs are also atypical among lemurs in that they appear to use both sun basking postures and huddling to maintain body temperature when ambient temperatures are cold. To our knowledge, however, no one has systematically tested whether these behaviors function in thermoregulation. We present evidence that ring-tailed lemurs use these postures as behavioral thermoregulation strategies, and that different environmental variables are associated with the use of each posture. Major predictors of sunning included ambient temperature, time of day, and season. Specifically, L. catta consistently assumed sunning postures early after daybreak when ambient temperatures were <13°C, and ceased sunning around 10:00a.m., after ambient temperatures approached 26°C. Sunning occurred more often during austral winter months. Huddling was associated with time of day, but not with ambient temperature or season. We conclude that L. catta tend to sun, rather than huddle, under cold weather conditions when sunning is possible. However, both sunning and huddling are important behavioral adaptations of L. catta that augment chemical thermoregulation and the absence of a dynamic, insulating pelage. Sunning and huddling help to account for the great ecological flexibility of the species, but these adaptations may be insufficient in the face of future changes in protective vegetation and temperature. Am. J. Primatol. 78:745-754, 2016. © 2016 Wiley Periodicals, Inc.

Long-term biotic homogenization in the East African Rift System over the last 6 million years of hominin evolution.

Eastern Africa preserves the most complete record of human evolution anywhere in the world but we have little knowledge of how long-term biogeographic dynamics in the region influenced hominin diversity and distributions. Here, we use spatial beta diversity analyses of mammal fossil records from the East African Rift System to reveal long-term biotic homogenization (increasing compositional similarity of faunas) over the last 6 Myr. Late Miocene and Pliocene faunas (~6-3 million years ago (Ma)) were largely composed of endemic species, with the shift towards biotic homogenization after ~3 Ma being driven by the loss of endemic species across functional groups and a growing number of shared grazing species. This major biogeographic transition closely tracks the regional expansion of grass-dominated ecosystems. Although grazers exhibit low beta diversity in open environments of the Early Pleistocene, the high beta diversity of Mio-Pliocene browsers and frugivores occurred in the context of extensive woody vegetation. We identify other key aspects of the Late Cenozoic biogeographic development of eastern Africa, their likely drivers and place the hominin fossil record in this context. Because hominins were undoubtedly influenced by many of the same factors as other eastern African mammals, this provides a new perspective on the links between environmental and human evolutionary histories.

Understanding primate communities: recent developments and future directions.

In 1999, the edited volume Primate Communities presented several studies that examined broad-scale patterns of primate diversity. Similar studies were being conducted on nonprimate taxa; advances in data availability and statistical approaches were allowing scientists to investigate a variety of new questions and to reexamine classical questions in novel ways. While such studies on nonprimate taxa have continued at a steady pace, they have only crept forward for primate species (Fig. 1). In the intervening time, the field of macroecology (Box 1) rapidly developed and has resulted in several books and the establishment of new research institutes. We suggest that examining primate communities, especially in a macroecological context, is an important line of research for our field to embrace and an area where biological anthropologists can provide major contributions. We review the current state of research, describe new datasets and research tools, and suggest future research directions.

Did trichromatic color vision and red hair color coevolve in primates?

Reddish pelage and red hair ornaments have evolved many times, independently, during primate evolution. It is generally assumed that these red-coat phenotypes, like red skin phenotypes, play a role in sociosexual signaling and, thus evolved in tandem with conspecific color vision. This study examines the phylogenetic distribution of color vision and pelage coloration across the primate order to ask: (1) did red pelage and trichromacy coevolve; or (2) did trichromacy evolve first, and then subsequently red pelage evolved as an exaptation? We collected quantitative, color-corrected photographic color data for 142 museum research skins from 92 species representing 41 genera spanning all major primate lineages. For each species, we quantified the ratio of Red/Green values (from a RGB color model) at 20 anatomical landmarks. For these same species, we compiled data on color vision type (routine trichromatic, polymorphic, routine dichromatic, monochromatic) and data on variables that potentially covary with visual system (VS) and coloration, including activity pattern and body mass dimorphism (proxy for sexual selection). We also considered whether the long-term storage of research skins might influence coloration. Therefore, we included the time since the specimen was collected as an additional predictor. Analyzing the data with phylogenetic generalized least squares models, we found that the amount of red hair present in primates is associated with differences in VSs, but not in the direction expected. Surprisingly, trichromatic primate species generally exhibited less red hair compared to red-green colorblind species. Thus, our results do not support the general assumption that color vision and red pelage coloration are a coevolutionary product of sociosexual signaling in primates. In addition, we did not find an effect of activity pattern, body mass dimorphism, or time since collection on the redness of primate hair. Our results have important implications for the evolution of primate coloration and visual systems.

Variation in human functional eccrine gland density and its implications for the evolution of human sweating.

OBJECTIVES: We aim to test three questions regarding human eccrine sweat gland density, which is highly derived yet poorly understood. First, is variation in functional eccrine gland density ("FED") explained by childhood climate, suggesting phenotypic plasticity? Second, is variation in FED explained by genetic similarity (a proxy for "geographic ancestry"), implying divergent evolutionary pathways in this trait of ancestral populations? Third, what is the relationship between FED and sweat production? MATERIALS AND METHODS: To test questions one and two, we measured FED in 68 volunteers aged 18-39 with varied childhood climate regimes and geographic ancestries. To test question three, we compared sweat production to FED in our n = 68 sample. In addition, we examined the relationship between FED and whole-body sweat loss during cycling in warm conditions using a sample of eight heat-acclimated endurance athletes. RESULTS: Interindividual variation in six-site FED was more than twofold, ranging from 60.9 to 132.7 glands/cm2 . Variation in FED was best explained by body surface area and limb circumferences (negative associations) and poorly explained by childhood climatic conditions and genetic similarity. Pilocarpine-induced sweat production was unrelated to FED while whole-body sweat loss during cycling was significantly, though modestly, associated with FED. DISCUSSION: We hypothesize that gland-level phenotypic plasticity, rather than changes in eccrine gland density, was sufficient to permit thermal adaptation to novel environments as humans colonized the globe. Future research should measure effects of FED in dehydrated states and the relationship between FED and salt loss, and control for effects of microclimate to rule out phenotypic plasticity effects.

RUNX2 tandem repeats and the evolution of facial length in placental mammals.

BACKGROUND: When simple sequence repeats are integrated into functional genes, they can potentially act as evolutionary 'tuning knobs', supplying abundant genetic variation with minimal risk of pleiotropic deleterious effects. The genetic basis of variation in facial shape and length represents a possible example of this phenomenon. Runt-related transcription factor 2 (RUNX2), which is involved in osteoblast differentiation, contains a functionally-important tandem repeat of glutamine and alanine amino acids. The ratio of glutamines to alanines (the QA ratio) in this protein seemingly influences the regulation of bone development. Notably, in domestic breeds of dog, and in carnivorans in general, the ratio of glutamines to alanines is strongly correlated with facial length. RESULTS: In this study we examine whether this correlation holds true across placental mammals, particularly those mammals for which facial length is highly variable and related to adaptive behavior and lifestyle (e.g., primates, afrotherians, xenarthrans). We obtained relative facial length measurements and RUNX2 sequences for 41 mammalian species representing 12 orders. Using both a phylogenetic generalized least squares model and a recently-developed Bayesian comparative method, we tested for a correlation between genetic and morphometric data while controlling for phylogeny, evolutionary rates, and divergence times. Non-carnivoran taxa generally had substantially lower glutamine-alanine ratios than carnivorans (primates and xenarthrans with means of 1.34 and 1.25, respectively, compared to a mean of 3.1 for carnivorans), and we found no correlation between RUNX2 sequence and face length across placental mammals. CONCLUSIONS: Results of our diverse comparative phylogenetic analyses indicate that QA ratio does not consistently correlate with face length across the 41 mammalian taxa considered. Thus, although RUNX2 might function as a 'tuning knob' modifying face length in carnivorans, this relationship is not conserved across mammals in general.