Genetic structure correlates with ethnolinguistic diversity in eastern and southern Africa.

African populations are the most diverse in the world yet are sorely underrepresented in medical genetics research. Here, we examine the structure of African populations using genetic and comprehensive multi-generational ethnolinguistic data from the Neuropsychiatric Genetics of African Populations-Psychosis study (NeuroGAP-Psychosis) consisting of 900 individuals from Ethiopia, Kenya, South Africa, and Uganda. We find that self-reported language classifications meaningfully tag underlying genetic variation that would be missed with consideration of geography alone, highlighting the importance of culture in shaping genetic diversity. Leveraging our uniquely rich multi-generational ethnolinguistic metadata, we track language transmission through the pedigree, observing the disappearance of several languages in our cohort as well as notable shifts in frequency over three generations. We find suggestive evidence for the rate of language transmission in matrilineal groups having been higher than that for patrilineal ones. We highlight both the diversity of variation within Africa as well as how within-Africa variation can be informative for broader variant interpretation; many variants that are rare elsewhere are common in parts of Africa. The work presented here improves the understanding of the spectrum of genetic variation in African populations and highlights the enormous and complex genetic and ethnolinguistic diversity across Africa.

A cultural evolutionary model of the interaction between parental beliefs and behaviors, with applications to vaccine hesitancy.

Health perceptions and health-related behaviors can change at the population level as cultures evolve. In the last decade, despite the proven efficacy of vaccines, the developed world has seen a resurgence of vaccine-preventable diseases (VPDs) such as measles, pertussis, and polio. Vaccine hesitancy, which is influenced by historical, political, and socio-cultural forces, is believed to be a primary factor responsible for decreasing vaccine coverage, thereby increasing the risk and occurrence of VPD outbreaks. Behavior change models have been increasingly employed to understand disease dynamics and intervention effectiveness. However, since health behaviors are culturally influenced, it is valuable to examine them within a cultural evolution context. Here, using a mathematical modeling framework, we explore the effects of cultural evolution on vaccine hesitancy and vaccination behavior. With this model, we shed light on facets of cultural evolution (vertical transmission, community influences, homophily, etc.) that promote the spread of vaccine hesitancy, ultimately affecting levels of vaccination coverage and VPD outbreak risk in a population. In addition, we present our model as a generalizable framework for exploring cultural evolution when humans' beliefs influence, but do not strictly dictate, their behaviors. This model offers a means of exploring how parents' potentially conflicting beliefs and cultural traits could affect their children's health and fitness. We show that vaccine confidence and vaccine-conferred benefits can both be driving forces of vaccine coverage. We also demonstrate that an assortative preference among vaccine-hesitant individuals can lead to increased vaccine hesitancy and lower vaccine coverage.

Modelling effects of inter-group contact on links between population size and cultural complexity.

Human populations rely on cultural artefacts for their survival. Populations vary dramatically in the size of their tool repertoires, and the determinants of these cultural repertoire sizes have been the focus of extensive study. A prominent hypothesis, supported by computational models of cultural evolution, asserts that tool repertoire size increases with population size. However, not all empirical studies have found such a correlation, leading to a contentious and ongoing debate. As a possible resolution to this longstanding controversy, we suggest that accounting for even rare cultural migration events that allow sharing of knowledge between different-sized populations may help explain why a population's size might not always predict its cultural repertoire size. Using an agent-based model to test assumptions about the effects of population size and connectivity on tool repertoires, we find that cultural exchange between a focal population and others, particularly with large populations, may significantly boost its tool repertoire size. Thus, two populations of identical size may have drastically different tool repertoire sizes, hinging upon their access to other groups' knowledge. Intermittent contact between populations boosts cultural repertoire size and still allows for the development of unique tool repertoires that have limited overlap between populations.

Cultural dynamics add multiple layers of complexity to behavioural genetics.

As emphasized in early cultural evolutionary theory, understanding heritability of human traits - especially, behavioural traits - is difficult. The target article describes important ways that culture can enhance, or obscure, signatures of heritability in genetic studies. Here, we discuss the utility of calculating heritability for behavioural traits influenced by cultural evolution and point to conceptual and technical complications to consider in future models.

Functional and evolutionary parallels between birdsong and human musicality.

Here, we compare birdsong and human musicality using insights from songbird neuroethology and evolution. For example, neural recordings during songbird duetting and other coordinated vocal behaviors could inform mechanistic hypotheses regarding human brain function during music-making. Furthermore, considering songbird evolution as a model system suggests that selection favoring certain culturally transmitted behaviors can indirectly select for associated underlying neural functions.

The life history of learning: Demographic structure changes cultural outcomes.

Human populations show rich cultural diversity. Underpinning this diversity of tools, rituals, and cultural norms are complex interactions between cultural evolutionary and demographic processes. Most models of cultural change assume that individuals use the same learning modes and methods throughout their lives. However, empirical data on 'learning life histories'-the balance of dominant modes of learning (for example, learning from parents, peers, or unrelated elders) throughout an individual's lifetime-suggest that age structure may play a crucial role in determining learning modes and cultural evolutionary trajectories. Thus, studied in isolation, demographic and cultural evolutionary models show only part of the picture. This paper describes a mathematical and computational framework that combines demographic and cultural evolutionary methods. Using this general framework, we examine interactions between the ways in which culture is spread throughout an individual's lifetime and cultural change across generations. We show that including demographic structure alongside cultural dynamics can help to explain domain-specific patterns of cultural evolution that are a persistent feature of cultural data, and can shed new light on rare but significant demographic events.

Cultural evolutionary theory: How culture evolves and why it matters.

Human cultural traits-behaviors, ideas, and technologies that can be learned from other individuals-can exhibit complex patterns of transmission and evolution, and researchers have developed theoretical models, both verbal and mathematical, to facilitate our understanding of these patterns. Many of the first quantitative models of cultural evolution were modified from existing concepts in theoretical population genetics because cultural evolution has many parallels with, as well as clear differences from, genetic evolution. Furthermore, cultural and genetic evolution can interact with one another and influence both transmission and selection. This interaction requires theoretical treatments of gene-culture coevolution and dual inheritance, in addition to purely cultural evolution. In addition, cultural evolutionary theory is a natural component of studies in demography, human ecology, and many other disciplines. Here, we review the core concepts in cultural evolutionary theory as they pertain to the extension of biology through culture, focusing on cultural evolutionary applications in population genetics, ecology, and demography. For each of these disciplines, we review the theoretical literature and highlight relevant empirical studies. We also discuss the societal implications of the study of cultural evolution and of the interactions of humans with one another and with their environment.

Structure and evolution of ENTH and VHS/ENTH-like domains in tepsin.

Tepsin is currently the only accessory trafficking protein identified in adaptor-related protein 4 (AP4)-coated vesicles originating at the trans-Golgi network (TGN). The molecular basis for interactions between AP4 subunits and motifs in the tepsin C-terminus have been characterized, but the biological role of tepsin remains unknown. We determined X-ray crystal structures of the tepsin epsin N-terminal homology (ENTH) and VHS/ENTH-like domains. Our data reveal unexpected structural features that suggest key functional differences between these and similar domains in other trafficking proteins. The tepsin ENTH domain lacks helix0, helix8 and a lipid binding pocket found in epsin1/2/3. These results explain why tepsin requires AP4 for its membrane recruitment and further suggest ENTH domains cannot be defined solely as lipid binding modules. The VHS domain lacks helix8 and thus contains fewer helices than other VHS domains. Structural data explain biochemical and biophysical evidence that tepsin VHS does not mediate known VHS functions, including recognition of dileucine-based cargo motifs or ubiquitin. Structural comparisons indicate the domains are very similar to each other, and phylogenetic analysis reveals their evolutionary pattern within the domain superfamily. Phylogenetics and comparative genomics further show tepsin within a monophyletic clade that diverged away from epsins early in evolutionary history (~1500 million years ago). Together, these data provide the first detailed molecular view of tepsin and suggest tepsin structure and function diverged away from other epsins. More broadly, these data highlight the challenges inherent in classifying and understanding protein function based only on sequence and structure.

The evolutionary advantage of cultural memory on heterogeneous contact networks.

Cultural processes, as well as the selection pressures experienced by individuals in a population over time and space, are fundamentally stochastic. Phenotypic variability, together with imperfect phenotypic transmission between parents and offspring, has been previously shown to play an important role in evolutionary rescue and (epi)genetic adaptation of populations to fluctuating temporal environmental pressures. This type of evolutionary bet-hedging does not confer a direct benefit to a single individual, but can instead increase the adaptability of the whole lineage. Here we develop a population-genetic model to explore cultural response strategies to temporally changing selection, as well as the role of local population structure, as exemplified by heterogeneity in the contact network between individuals, in shaping evolutionary dynamics. We use this model to study the evolutionary advantage of cultural bet-hedging, modeling the evolution of a variable cultural trait starting from one copy in a population of individuals with a fixed cultural strategy. We find that the probability of fixation of a cultural bet-hedger is a non-monotonic function of the probability of cultural memory between generations. Moreover, this probability increases for networks of higher mean degree but decreases with increasing heterogeneity of the contact network, tilting the balance of forces toward drift and against selection. These results shed light on the interplay of temporal and spatial stochasticity in shaping cultural evolutionary dynamics and suggest that partly-heritable cultural phenotypic variability may constitute an important evolutionary bet-hedging strategy in response to changing selection pressures.

Some topics in theoretical population genetics: Editorial commentaries on a selection of Marc Feldman's TPB papers.

This article consists of commentaries on a selected group of papers of Marc Feldman published in Theoretical Population Biology from 1970 to the present. The papers describe a diverse set of population-genetic models, covering topics such as cultural evolution, social evolution, and the evolution of recombination. The commentaries highlight Marc Feldman's role in providing mathematically rigorous formulations to explore qualitative hypotheses, in many cases generating surprising conclusions.

Food-seeking behavior has complex evolutionary pressures in songbirds: Linking parental foraging to offspring sexual selection.

The target article addresses increased food-seeking behaviors in times of instability, particularly in passerines. We note that food instability might have intergenerational effects on birds: Nutritional stress during development affects song-learning abilities, associating parental foraging with offspring sexual selection. We explore the implications of these compounding selection pressures on food-seeking motivation during breeding, as well as the hormonal underpinnings of these behaviors.

Are both necessity and opportunity the mothers of innovations?

Baumard's perspective asserts that "opportunity is the mother of innovation," in contrast to the adage ascribing this role to necessity. Drawing on behavioral ecology and cognition, we propose that both extremes - affluence and scarcity - can drive innovation. We suggest that the types of innovations at these two extremes differ and that both rely on mechanisms operating on different time scales.

Evolution in leaps: The punctuated accumulation and loss of cultural innovations.

Archaeological accounts of cultural change reveal a fundamental conflict: Some suggest that change is gradual, accelerating over time, whereas others indicate that it is punctuated, with long periods of stasis interspersed by sudden gains or losses of multiple traits. Existing models of cultural evolution, inspired by models of genetic evolution, lend support to the former and do not generate trajectories that include large-scale punctuated change. We propose a simple model that can give rise to both exponential and punctuated patterns of gain and loss of cultural traits. In it, cultural innovation comprises several realistic interdependent processes that occur at different rates. The model also takes into account two properties intrinsic to cultural evolution: the differential distribution of traits among social groups and the impact of environmental change. In our model, a population may be subdivided into groups with different cultural repertoires leading to increased susceptibility to cultural loss, whereas environmental change may lead to rapid loss of traits that are not useful in a new environment. Taken together, our results suggest the usefulness of a concept of an effective cultural population size.

A comparison of worldwide phonemic and genetic variation in human populations.

Worldwide patterns of genetic variation are driven by human demographic history. Here, we test whether this demographic history has left similar signatures on phonemes-sound units that distinguish meaning between words in languages-to those it has left on genes. We analyze, jointly and in parallel, phoneme inventories from 2,082 worldwide languages and microsatellite polymorphisms from 246 worldwide populations. On a global scale, both genetic distance and phonemic distance between populations are significantly correlated with geographic distance. Geographically close language pairs share significantly more phonemes than distant language pairs, whether or not the languages are closely related. The regional geographic axes of greatest phonemic differentiation correspond to axes of genetic differentiation, suggesting that there is a relationship between human dispersal and linguistic variation. However, the geographic distribution of phoneme inventory sizes does not follow the predictions of a serial founder effect during human expansion out of Africa. Furthermore, although geographically isolated populations lose genetic diversity via genetic drift, phonemes are not subject to drift in the same way: within a given geographic radius, languages that are relatively isolated exhibit more variance in number of phonemes than languages with many neighbors. This finding suggests that relatively isolated languages are more susceptible to phonemic change than languages with many neighbors. Within a language family, phoneme evolution along genetic, geographic, or cognate-based linguistic trees predicts similar ancestral phoneme states to those predicted from ancient sources. More genetic sampling could further elucidate the relative roles of vertical and horizontal transmission in phoneme evolution.

Game-Changing Innovations: How Culture Can Change the Parameters of Its Own Evolution and Induce Abrupt Cultural Shifts.

One of the most puzzling features of the prehistoric record of hominid stone tools is its apparent punctuation: it consists of abrupt bursts of dramatic change that separate long periods of largely unchanging technology. Within each such period, small punctuated cultural modifications take place. Punctuation on multiple timescales and magnitudes is also found in cultural trajectories from historical times. To explain these sharp cultural bursts, researchers invoke such external factors as sudden environmental change, rapid cognitive or morphological change in the hominids that created the tools, or replacement of one species or population by another. Here we propose a dynamic model of cultural evolution that accommodates empirical observations: without invoking external factors, it gives rise to a pattern of rare, dramatic cultural bursts, interspersed by more frequent, smaller, punctuated cultural modifications. Our model includes interdependent innovation processes that occur at different rates. It also incorporates a realistic aspect of cultural evolution: cultural innovations, such as those that increase food availability or that affect cultural transmission, can change the parameters that affect cultural evolution, thereby altering the population's cultural dynamics and steady state. This steady state can be regarded as a cultural carrying capacity. These parameter-changing cultural innovations occur very rarely, but whenever one occurs, it triggers a dramatic shift towards a new cultural steady state. The smaller and more frequent punctuated cultural changes, on the other hand, are brought about by innovations that spur the invention of further, related, technology, and which occur regardless of whether the population is near its cultural steady state. Our model suggests that common interpretations of cultural shifts as evidence of biological change, for example the appearance of behaviorally modern humans, may be unwarranted.

Complexity in models of cultural niche construction with selection and homophily.

Niche construction is the process by which organisms can alter the ecological environment for themselves, their descendants, and other species. As a result of niche construction, differences in selection pressures may be inherited across generations. Homophily, the tendency of like phenotypes to mate or preferentially associate, influences the evolutionary dynamics of these systems. Here we develop a model that includes selection and homophily as independent culturally transmitted traits that influence the fitness and mate choice determined by another focal cultural trait. We study the joint dynamics of a focal set of beliefs, a behavior that can differentially influence the fitness of those with certain beliefs, and a preference for partnering based on similar beliefs. Cultural transmission, selection, and homophily interact to produce complex evolutionary dynamics, including oscillations, stable polymorphisms of all cultural phenotypes, and simultaneous stability of oscillation and fixation, which have not previously been observed in models of cultural evolution or gene-culture interactions. We discuss applications of this model to the interaction of beliefs and behaviors regarding education, contraception, and animal domestication.

Genome-scale co-evolutionary inference identifies functions and clients of bacterial Hsp90.

The molecular chaperone Hsp90 is essential in eukaryotes, in which it facilitates the folding of developmental regulators and signal transduction proteins known as Hsp90 clients. In contrast, Hsp90 is not essential in bacteria, and a broad characterization of its molecular and organismal function is lacking. To enable such characterization, we used a genome-scale phylogenetic analysis to identify genes that co-evolve with bacterial Hsp90. We find that genes whose gain and loss were coordinated with Hsp90 throughout bacterial evolution tended to function in flagellar assembly, chemotaxis, and bacterial secretion, suggesting that Hsp90 may aid assembly of protein complexes. To add to the limited set of known bacterial Hsp90 clients, we further developed a statistical method to predict putative clients. We validated our predictions by demonstrating that the flagellar protein FliN and the chemotaxis kinase CheA behaved as Hsp90 clients in Escherichia coli, confirming the predicted role of Hsp90 in chemotaxis and flagellar assembly. Furthermore, normal Hsp90 function is important for wild-type motility and/or chemotaxis in E. coli. This novel function of bacterial Hsp90 agreed with our subsequent finding that Hsp90 is associated with a preference for multiple habitats and may therefore face a complex selection regime. Taken together, our results reveal previously unknown functions of bacterial Hsp90 and open avenues for future experimental exploration by implicating Hsp90 in the assembly of membrane protein complexes and adaptation to novel environments.

Fine-scale cultural variation reinforces genetic structure in England.

OBJECTIVES: Genes and languages both contain signatures of human evolution, population movement, and demographic history. Cultural traits like language are transmitted by interactions between people, and these traits influence how people interact. In particular, if groups of people differentiate each other based on some qualities of their cultures, and if these qualities are passed to the next generation, then this differentiation can result in barriers to gene flow. Previous work finds such barriers to gene flow between groups that speak different languages, and we explore this phenomenon further: can more subtle cultural differences also produce genetic structure in a population? We focus on whether subtle, dialect-level linguistic differences in England have influenced genetic population structure, likely by affecting mating preferences. MATERIALS AND METHODS: We analyze spatially dense linguistic and genetic data-both of which independently contain spatially structured variation in England-to examine whether the cultural differences represented by variation in English phonology colocalize with higher genetic rates of change. RESULTS: We find that genetic variation and dialect markers have similar spatial distributions on a country-wide scale, and that throughout England, linguistic boundaries colocalize with the boundaries of genetic clusters found using fineSTRUCTURE. DISCUSSION: This gene-language covariation, in the absence of geographic barriers that could coordinate cultural and genetic differentiation, suggests that similar social forces influenced both dialect boundaries and the genetic population structure of England.

Internal and external factors affecting vaccination coverage: Modeling the interactions between vaccine hesitancy, accessibility, and mandates.

Society, culture, and individual motivations affect human decisions regarding their health behaviors and preventative care, and health-related perceptions and behaviors can change at the population level as cultures evolve. An increase in vaccine hesitancy, an individual mindset informed within a cultural context, has resulted in a decrease in vaccination coverage and an increase in vaccine-preventable disease (VPD) outbreaks, particularly in developed countries where vaccination rates are generally high. Understanding local vaccination cultures, which evolve through an interaction between beliefs and behaviors and are influenced by the broader cultural landscape, is critical to fostering public health. Vaccine mandates and vaccine inaccessibility are two external factors that interact with individual beliefs to affect vaccine-related behaviors. To better understand the population dynamics of vaccine hesitancy, it is important to study how these external factors could shape a population's vaccination decisions and affect the broader health culture. Using a mathematical model of cultural evolution, we explore the effects of vaccine mandates, vaccine inaccessibility, and varying cultural selection trajectories on a population's level of vaccine hesitancy and vaccination behavior. We show that vaccine mandates can lead to a phenomenon in which high vaccine hesitancy co-occurs with high vaccination coverage, and that high vaccine confidence can be maintained even in areas where access to vaccines is limited.