Browsing by Subject "Human evolution"

Admixture occurs when previously isolated populations come together to form a new population with genetic ancestry from those sources. Admixture is ubiquitous across the tree of life, including humans, and is often associated with migration and exposure to new environments and selective pressures. Admixed populations provide a unique opportunity to study adaptation on short timescales by introducing beneficial alleles at high frequency. However, admixed populations are often excluded from genomic studies due to lack of applicable methodology. Instead of relying on classical methods confounded by the process of admixture itself, we can detect changes in patterns of genetics ancestry that are informative about selection in admixed populations and at the short timescales often relevant for post-admixture selection. However, we lack theoretical expectations and methods to detect and characterize ancestry-based genomic signals indicative of post-admixture selection and adaptation. Common ancestry outlier approaches discard information about the surrounding genomic context and are prone to false positives due to drift and demography. Here, I present three studies which leverage patterns of genetic ancestry to investigate the evolutionary history of admixed populations. First, I develop a suite of ancestry-based summary statistics and computational methods to detect post-admixture adaptation, and demonstrate their application in a case study of human adaptation to malaria. In particular, these summary statistics incorporate patterns of ancestry beyond the site under selection, such as the length of contiguous ancestry tracts surrounding the locus, and are informative about the strength and timing of selection in admixed populations. I observe one of the strongest signals of recent selection in humans at the malaria protective Duffy-null allele, and show that this mode of strong single-locus selection over 20 generations has impacted genome-wide patterns of ancestry. Next, I move beyond summary statistics to develop a deep learning strategy for localizing regions of the genome under selection. This method takes images of chromosomes painted by ancestry as input to avoid the loss of information and bias that can occur when relying on user-defined summary statistics. I demonstrate this approach on simulated admixture scenarios and find that the method successfully localizes variants under selection 95% percent of the time, outperforms the common ancestry outlier approach, and is robust to demographic misspecification. Lastly, I present the first Illyrian genome sequences available from the Iron Age in a study of the ancestry and genetic relationships of five neonates buried in Korčula, Croatia. I find genetic support for classifying these individuals as Illyrian, and show that patterns of ancestry and genetic variation are consistent with their geographic location between Italy and the mainland Balkans. In the combined work presented here, I advance our ability to study the evolutionary history of admixed populations, which has implications for our understanding of phenotypic variation, disease risk, and conservation genetics across many study systems. Further, these methods tailored to the mosaic ancestry of admixed populations is a step towards expanding the diversity of populations, especially humans, who benefit from discoveries and advancement in genomic research.

Searches for the genetic underpinnings of uniquely human traits have focused on human-specific divergence in conserved genomic regions, which reflects adaptive modifications of existing functional elements. However, the study of conserved regions excludes novel functional elements that descended from previously neutral regions. In this work, I integrate comparative genomic analyses with human population variation data to reveal that rapid divergence rate is associated with positive selection in human evolutionary history. Encouraged by this finding, I identified 1581 Human Ancestor Quickly Evolved Regions (HAQERs), which represent the fastest-evolved regions of the human genome. HAQERs rapidly diverged in an episodic burst of directional positive selection prior to the human-Neanderthal split before transitioning to constraint within hominins. HAQERs are enriched for bivalent chromatin states, particularly in gastrointestinal and neurodevelopmental tissues, and genetic variants linked to neurodevelopmental disease. I led a collaborative effort to develop scSTARR-seq as a multiplex single-cell in vivo enhancer assay to discover that rapid sequence divergence in HAQERs generated hominin-unique enhancers in the developing cerebral cortex. I propose that a lack of pleiotropic constraints and elevated mutation rates poised HAQERs for rapid adaptation and subsequent susceptibility to disease.

A fundamental question in evolutionary anthropology asks how the human brain evolved. Characterized as relatively large and energetically taxing, numerous hypotheses have been proposed to explain how the human brain has evolved to its current size through tradeoffs to improve fitness by increasing behavioral complexity while minimizing caloric costs. The comparative method has been a key approach to testing these hypotheses, but a major hinderance has been the lack of directly measured brain metabolic rates for many comparable species. This dissertation takes an anatomical approach to predict brain metabolic rates from osteological specimens, utilizing the following proposed relationships: 1) that the brain is supplied by arteries (encephalic arteries) which travel through bony canals, 2) the size of the canal reflects the size of the artery within, 3) the size of the artery is proportional to blood flow rate, and 4) encephalic blood flow rate is proportional to brain metabolic rate.

Radii of encephalic arterial canals of a growth series of humans (n= 305 individuals) and of adult mammals (n=329 species) were measured from cadaveric computed tomography scans and osteological specimens, and blood flow rates were predicted using anatomical and physiological equations previously published in the literature. The major goals of this dissertation were to better evaluate the use of encephalic arterial canals in the prediction of brain metabolism and to characterize how mammals vary in their brain size, encephalic blood flow rates, brain metabolism, and whole body metabolism to test hypotheses which have been proposed to explain human and primate brain evolution.

The first research chapter finds that the blood flow rates predicted from the sizes of the encephalic arterial canals tracks the changes in brain metabolism during human growth. The second research chapter finds that patterns of variation in predicted blood flow rate, brain size, and body size across primates and other mammals suggest that predicted blood flow rates are reflecting the metabolic substrate supply needs of the brain. Furthermore, evidence is presented that the relative metabolic rate of the brains of primates is lower than many mammals of comparable brain size. The third research chapter utilizes phylogenetically informed Bayesian methods to predict brain metabolic rates from predicted blood flow rates, and finds that humans devote a high (although not always the highest) proportion of their basal metabolic rate (BMR) and total energy expenditure (TEE) to brain metabolism, even compared to other primates. In turn, primates tend to have elevated predicted brain metabolic rates relative to their BMR and TEE compared to most other mammal groups.

Combined, the evidence presented within this dissertation suggests that 1) osteologically derived predictions of blood flow rates present a viable alternative to understanding patterns of variation in brain metabolic rates during human ontogeny and among mammalian samples, and 2) compared to many other mammals, humans and other primates have evolved physiological mechanisms to reduce the mass-specific metabolic rate of their relatively large, energy-hungry brains.

The neocortex expanded spectacularly during human origins. That expansion is thought to form the foundation for our cognitive faculties underlying abstract reasoning and socialization. The human neocortex differs from that of other great apes in several notable regards including altered cell cycle, prolonged corticogenesis, and massively increased size. However, despite decades of effort, little progress has been made in uncovering the genetic contributions that underlie these differences that distinguish our species from closely related primate, such as chimpanzees. A subset of highly conserved non-coding regions that show rapid sequence changes along the human lineage are candidate loci for the development and evolution of uniquely human traits. Several studies have identified human-accelerated enhancers, but none have linked an expression difference to a organismal traits, such as brain sizes. Here we report the discovery of a human-accelerated regulatory enhancer (HARE5) near the Wnt receptor FRIZZLED-8 (FZD8). Using a variety of approaches, we demonstrate dramatic differences in human and chimpanzee HARE5 activity, with human HARE5 driving significantly strong expression. We show that HARE5 likely regulates FZD8 and that expression differences influence cell cycle kinetics, cortical layers, and brain size. At present, this would provide the first evidence of a human-chimpanzee genetic difference influencing the evolution of brain size.

There has been a trend toward decreasing skeletal robusticity in the genus Homo throughout the Pleistocene, culminating in the gracile postcrania of living modern humans. This change is typically attributed to changing tool technologies and subsistence patterns among human groups. However, other mammalian groups also experience a similar change in their postcranial strength over the same time period. It is proposed in this dissertation that ecological variables are correlated with measures of postcranial strength and may be a better explanation for Holocene skeletal gracilization in humans, as well as in other mammalian genera. This hypothesis is investigated through a close examination of the scaling patterns in two extant genera, Canis and Ursus, and a comparison of scaling patterns and relative strength of different species of Canis, including a fossil species that provides information about temporal change. Measurements of limb length, joint surface area, bone diameter, and strength measurements derived from radiographic images of long bone midshafts of North American specimens of Canis, (including the fossil Canis dirus) and Ursus were collected. Scaling patterns of the cross-sectional variables on limb length and joint surfaces were analyzed for the interspecific and intraspecific samples.

The first hypothesis tested was that Canis scales with geometric similarity of cross-sectional variables on bone length and body mass, and the Ursus scales with elastic similarity. Larger Canis have relatively stronger postcrania than smaller Canis. The primary way in which this strength is achieved in larger individuals is through a relatively shortening of the bone length. The second hypothesis tested was that postcranial strength is correlated with ecological variables. To investigate this hypothesis, scaling patterns of different species of Canis were compared, including the fossil dire wolf. The results show that the dire wolf is relatively stronger than its living congenerics. There is also a strong relationship between the ratio of prey body mass to predator body mass and relative strength for these species. Carnivores that are hunting animals much larger than themselves must have postcranial skeletons that are strong enough to withstand the loading of the skeleton that occurs during hunting, taking down, and processing large herbivores.

The relatively stiff gait of modern humans minimizes the muscular work done to move the lower limbs and the center of mass. Nonhuman primates, and perhaps our earliest ancestors, use a form of bipedalism in which the hip and knee are held in a flexed position. This thesis follows up on other studies examining loading and energetic costs of these compliant walking gaits by examining the effects of increased hip and knee flexion on kinetic, kinematic, and energy exchange variables. The bipedal gait of twelve human subjects using normal and bent hip and bent knee gait were compared. The subjects walked along force plates embedded in the ground while 3D kinematic data was simultaneously gathered. The data was then processed using EvaRT, Orthotrak, and Matlab to evaluate the variables used. During the bent hip and bent knee bipedal locomotion subjects demonstrated lower peak vertical and parallel ground reaction forces, much higher ankle flexion, less hip extension, and less energy recovery during a full stride. These data provide novel insight into the nature and costs of locomotion in bipedal primates and the earliest human ancestors.

Language and morality are two of the most striking manifestations of human social cognition. Each has been investigated in depth individually, but relatively little research has examined how they are related. To help address this gap, the present dissertation outlines key ways in which language and morality co-evolved during human evolution and co-develop during human ontogeny.To begin, Chapter 2 provides a theoretical framework for viewing language and morality as interrelated forms of cooperative social action. Both evolved as adaptations for contexts in which collaboration was necessary for survival, and both stem from the more general social cognitive capacity to engage in shared intentionality (i.e., to align, exchange, and interact with others’ mental states). Furthermore, language is used for many moral functions (e.g., to initiate, preserve, revise, and act on aspects of morality), which are operative even in young children. Building on the theoretical foundations established in Chapter 2, the next two chapters describe novel empirical studies into specific moral functions of language. Highlighting the function of language as a means of signaling normativity, Chapter 3 reports that young children conform more to the choices of another person when those choices are framed as socially normative. In this study, 3.5-year-old children helped set up items for a tea party. A confederate, who was either an adult female or a 6-year-old girl, endorsed various items in terms of either conventional norms (e.g., “For tea parties at Duke, we always use this kind of plate”) or personal preferences (e.g., “For my tea party today, I feel like using this cup”). Children conformed more to the model’s choices when the choices were framed as norms, as opposed to preferences. Highlighting the influence of linguistically mediated social interactions on children’s moral development, Chapter 4 identifies features of social experiences that are conducive to development. In this study, children from 4 to 5.5 years of age discussed simple moral decisions (how to allocate things between different recipients) with a puppet interlocutor. The puppet (i) either agreed or disagreed with the child’s ideas and (ii) either asked the child to justify themselves or not. Experiences of being disagreed with and experiences of being asked for justification both encouraged children to make fair decisions. Overall, the chapters illustrate the interconnectedness of language and morality in human development. This work may serve as a helpful basis for further research into how language and morality shape each other.

Humans are champions of prosociality. Across different cultures and early in life, humans routinely engage in prosocial behaviors that benefit others. Perhaps most strikingly, humans are even prosocial toward strangers (i.e. xenophilic). This is an evolutionary puzzle because it cannot be explained by kinship theory, reciprocal altruism or reputation. The parochialism hypothesis proposes that this extreme prosociality is unique to humans, is motivated by unselfish motivation and evolved through group selection made possible by human culture and warfare. The first impression hypothesis, on the other hand, proposes that xenophilia can evolve to promote the selfish benefits that accrue from extending one's social network. It predicts that 1) nonhuman species can evolve prosociality toward strangers when the benefit of forming new relations is higher than the cost, 2) the motivation for prosociality can be selfish, and 3) encounters with strangers can be a positive social event since strangers represent potential social partners. This dissertation presents three sets of experiments designed to test these predictions with bonobos (Pan paniscus), a species known for reduced xenophobia. These experiments showed, first, that bonobos voluntarily shared monopolizable food with a stranger and helped the stranger to obtain out-of-reach food. Second, the observed prosociality was driven by a selfish motivation to initiate an interaction with the stranger in close proximity and an other-regarding motivation to benefit the stranger. Third, an involuntary yawning task and a voluntary choice task show converging results that bonobos attribute positive valence to completely unknown strangers by default. These experiments support the three core predictions of the first impression hypothesis and challenge the view that intergroup competition is crucial to the origin of prosociality toward strangers in our species. Instead, the first impression hypothesis proposes that xenophilia in bonobos is probably an adaptation to initiating non-kin cooperation. Because female bonobos are highly cooperative even though they are the dispersing sex, xenophilia might function to quickly establish cooperative relationships with new immigrants. This suggests that xenophilia and reciprocity are likely two complementary aspects of non-kin cooperation: the former explains its initiation while the latter explains its maintenance. Similarly, xenophilia in humans is likely a result of the increasing need for cooperation among non-kin due to enhanced fission-fusion dynamics, population expansion, obligate cooperative foraging and greater dependence on cultural knowledge.