Epistasis can accelerate adaptive diversification in haploid asexual populations

A fundamental goal of the biological sciences is to determine processes that facilitate the evolution of diversity. These processes can be separated into ecological, physiological, developmental and genetic. An ecological process that facilitates diversification is frequency-dependent selection caused by competition. Models of frequency-dependent adaptive diversification have generally assumed a genetic basis of phenotype that is non-epistatic. Here, we present a model that indicates diversification is accelerated by an epistatic basis of phenotype in combination with a competition model that invokes frequency-dependent selection. Our model makes use of a genealogical model of epistasis and insights into the effects of balancing selection on the genealogical structure of a population to understand how epistasis can facilitate diversification. The finding that epistasis facilitates diversification may be informative with respect to empirical results that indicate an epistatic basis of phenotype in experimental bacterial populations that experienced adaptive diversification.     

Testing theories of secularization and religious belief in the Czech Republic and Slovakia

Several theoretical approaches have been proposed to explain variation in religiosity, including versions of secularization hypotheses, evolved cognitive biases, and cultural transmission. In this paper we test several theories that aim to explain variation in religiosity and compare them in a representative sample collected in the Czech Republic and Slovakia (N = 2022). These two countries represent a natural experiment in religiosity; despite their high level of historical, institutional and cultural similarity, their populations differ markedly in the rate of religious belief. We examine the predictive power of cognitive biases (anthropomorphism, dualism, teleology, mentalizing, and analytic thinking); institutional insecurity; and exposure to credibility displays of belief in childhood on various factors of religious belief. We find that individual differences in cognitive biases predicted 8% of the variance belief in God, but predicted 21% of the variance in paranormal beliefs and almost no variance in religious participation. Perceived institutional insecurity explains little variance in any of these variables, but cultural transmission, measured as exposure to credibility enhancing displays (CREDs) and church attendance in childhood, predicted 17% of the variance in belief in God and 30% of religious participation, and mediated 70% of the difference between these two countries in belief in God and 80% of the difference in religious practice. These findings suggest cognitive biases may explain the existence of belief in the supernatural generally, but cultural transmission through credible belief displays is a more plausible explanation for why people adopt and maintain a specific set of religious beliefs and practices.     

Endless forms: human behavioural diversity and evolved universals

Human populations have extraordinary capabilities for generating behavioural diversity without corresponding genetic diversity or change. These capabilities and their consequences can be grouped into three categories: strategic (or cognitive), ecological and cultural-evolutionary. Strategic aspects include: (i) a propensity to employ complex conditional strategies, some certainly genetically evolved but others owing to directed invention or to cultural evolution; (ii) situations in which fitness payoffs (or utilities) are frequency-dependent, so that there is no one best strategy; and (iii) the prevalence of multiple equilibria, with history or minor variations in starting conditions (path dependence) playing a crucial role. Ecological aspects refer to the fact that social behaviour and cultural institutions evolve in diverse niches, producing various adaptive radiations and local adaptations. Although environmental change can drive behavioural change, in humans, it is common for behavioural change (especially technological innovation) to drive environmental change (i.e. niche construction). Evolutionary aspects refer to the fact that human capacities for innovation and cultural transmission lead to diversification and cumulative cultural evolution; critical here is institutional design, in which relatively small shifts in incentive structure can produce very different aggregate outcomes. In effect, institutional design can reshape strategic games, bringing us full circle.     

Host-parasite arms races and rapid changes in bird egg appearance

Coevolutionary arms races are a powerful force driving evolution, adaptation, and diversification. They can generate phenotypic polymorphisms that render it harder for a coevolving parasite or predator to exploit any one individual of a given species. In birds, egg polymorphisms should be an effective defense against mimetic brood parasites and are extreme in the African tawny-flanked prinia (Prinia subflava) and its parasite, the cuckoo finch (Anomalospiza imberbis). Here we use models of avian visual perception to analyze the appearance of prinia and cuckoo finch eggs from the same location over 40 years. We show that the two interacting populations have experienced rapid changes in egg traits. Egg colors of both species have diversified over time, expanding into avian color space as expected under negative frequency-dependent selection. Egg pattern showed signatures of both frequency-dependent and directional selection in different traits, which appeared to be evolving independently of one another. Host and parasite appear to be closely tracking one another's evolution, since parasites showed closer color mimicry of contemporaneous hosts. This correlational evidence suggests that hosts and parasites are locked in an ongoing arms race in egg appearance, driven by constant change in the selective advantage of different phenotypes, and that coevolutionary arms races can generate remarkably rapid phenotypic change.     

On the importance of evolving phenotype distributions on evolutionary diversification

Evolutionary branching occurs when a population with a unimodal phenotype distribution diversifies into a multimodally distributed population consisting of two or more strains. Branching results from frequency-dependent selection, which is caused by interactions between individuals. For example, a population performing a social task may diversify into a cooperator strain and a defector strain. Branching can also occur in multi-dimensional phenotype spaces, such as when two tasks are performed simultaneously. In such cases, the strains may diverge in different directions: possible outcomes include division of labor (with each population performing one of the tasks) or the diversification into a strain that performs both tasks and another that performs neither. Here we show that the shape of the population’s phenotypic distribution plays a role in determining the direction of branching. Furthermore, we show that the shape of the distribution is, in turn, contingent on the direction of approach to the evolutionary branching point. This results in a distribution–selection feedback that is not captured in analytical models of evolutionary branching, which assume monomorphic populations. Finally, we show that this feedback can influence long-term evolutionary dynamics and promote the evolution of division of labor.     

Multimodal pattern formation in phenotype distributions of sexual populations

During bouts of evolutionary diversification, such as adaptive radiations, the emerging species cluster around different locations in phenotype space. How such multimodal patterns in phenotype space can emerge from a single ancestral species is a fundamental question in biology. Frequency-dependent competition is one potential mechanism for such pattern formation, as has previously been shown in models based on the theory of adaptive dynamics. Here, we demonstrate that also in models similar to those used in quantitative genetics, phenotype distributions can split into multiple modes under the force of frequency-dependent competition. In sexual populations, this requires assortative mating, and we show that the multimodal splitting of initially unimodal distributions occurs over a range of assortment parameters. In addition, assortative mating can be favoured evolutionarily even if it incurs costs, because it provides a means of alleviating the effects of frequency dependence. Our results reveal that models at both ends of the spectrum between essentially monomorphic (adaptive dynamics) and fully polymorphic (quantitative genetics) yield similar results. This underscores that frequency-dependent selection is a strong agent of pattern formation in phenotype distributions, potentially resulting in adaptive speciation.     

The evolution of costly displays,cooperation and religion: credibility enhancing displays and their implications for cultural evolution

This paper lays out an evolutionary theory for the cognitive foundations and cultural emergence of the extravagant displays (e.g., ritual mutilation, animal sacrifice and martyrdom) that have so tantalized social scientists, as well as more mundane actions that influence cultural learning and historical processes. In Part I, I use the logic of natural selection to build a theory for how and why seemingly costly displays influence the cognitive processes associated with cultural learning — why do “actions speak louder than words?” The core idea is that cultural learners can both avoid being manipulated by their models (those they are inclined to learn from) and more accurately assess their belief commitment by attending to displays or actions by the model that would seem costly to the model if he held beliefs different from those he expresses verbally. Part II examines the implications for cultural evolution of this learning bias in a simple evolutionary model. The model reveals the conditions under which this evolved bias can create stable sets of interlocking beliefs and practices, including quite costly practices. Part III explores how cultural evolution, driven by competition among groups or institutions stabilized at alternative sets of these interlocking belief-practice combinations, has led to the association of costly acts, often in the form of rituals, with deeper commitments to group beneficial ideologies, higher levels of cooperation within groups, and greater success in competition with other groups or institutions. I close by discussing the broader implications of these ideas for understanding various aspects of religious phenomena.     

Cultural evolution of systematically structured behaviour in a non-human primate

Culture pervades human life and is at the origin of the success of our species. A wide range of other animals have culture too, but often in a limited form that does not complexify through the gradual accumulation of innovations. We developed a new paradigm to study cultural evolution in primates in order to better evaluate our closest relatives'' cultural capacities. Previous studies using transmission chain experimental paradigms, in which the behavioural output of one individual becomes the target behaviour for the next individual in the chain, show that cultural transmission can lead to the progressive emergence of systematically structured behaviours in humans. Inspired by this work, we combined a pattern reproduction task on touch screens with an iterated learning procedure to develop transmission chains of baboons (Papio papio). Using this procedure, we show that baboons can exhibit three fundamental aspects of human cultural evolution: a progressive increase in performance, the emergence of systematic structure and the presence of lineage specificity. Our results shed new light on human uniqueness: we share with our closest relatives essential capacities to produce human-like cultural evolution.     

Memory and Belief in the Transmission of Counterintuitive Content

Cognitive scientists have increasingly turned to cultural transmission to explain the widespread nature of religion. One key hypothesis focuses on memory, proposing that that minimally counterintuitive (MCI) content facilitates the transmission of supernatural beliefs. We propose two caveats to this hypothesis. (1) Memory effects decrease as MCI concepts become commonly used, and (2) people do not believe counterintuitive content readily; therefore additional mechanisms are required to get from memory to belief. In experiments 1–3 (n?=?283), we examined the relationship between MCI, belief, and memory. We found that increased tendencies to anthropomorphize predicted poorer memory for anthropomorphic-MCI content. MCI content was found less believable than intuitive content, suggesting different mechanisms are required to explain belief. In experiment 4 (n?=?70), we examined the non-content-based cultural learning mechanism of credibility-enhancing displays (CREDs) and found that it increased participants’ belief in MCI content, suggesting this type of learning can better explain the transmission of belief.     

Interactions between frequency-dependent and vertical transmission in host-parasite systems.

We investigate host-pathogen dynamics and conditions for coexistence in two models incorporating frequency-dependent horizontal transmission in conjunction with vertical transmission. The first model combines frequency-dependent and uniparental vertical transmission, while the second addresses parasites transmitted vertically via both parents. For the first model, we ask how the addition of vertical transmission changes the coexistence criteria for parasites transmitted by a frequency-dependent horizontal route, and show that vertical transmission significantly broadens the conditions for parasite invasion. Host-parasite coexistence is further affected by the form of density-dependent host regulation. Numerical analyses demonstrate that within a host population, a parasite strain with horizontal frequency-dependent transmission can be driven to extinction by a parasite strain that is additionally transmitted vertically for a wide range of parameters. Although models of asexual host populations predict that vertical transmission alone cannot maintain a parasite over time, analysis of our second model shows that vertical transmission via both male and female parents can maintain a parasite at a stable equilibrium. These results correspond with the frequent co-occurrence of vertical with sexual transmission in nature and suggest that these transmission modes can lead to host-pathogen coexistence for a wide range of systems involving hosts with high reproductive rates.     

Uneven segregation of sporophytic self-incompatibility alleles in Arabidopsis lyrata

Self-incompatibility in Arabidopsis lyrata is sporophytically controlled by the multi-allelic S-locus. Self-incompatibility alleles (S-alleles) are under strong negative frequency dependent selection because pollen carrying common S-alleles have fewer mating opportunities. Population genetics theory predicts that deleterious alleles can accumulate if linked to the S-locus. This was tested by studying segregation of S-alleles in 11 large full sib families in A. lyrata. Significant segregation distortion leading to an up to fourfold difference in transmission rates was found in six families. Differences in transmission rates were not significantly different in reciprocal crosses and the distortions observed were compatible with selection acting at the gametic stage alone. The S-allele with the largest segregation advantage is also the most recessive, and is very common in natural populations concordant with its apparent segregation advantage. These results imply that frequencies of S-alleles in populations of A. lyrata cannot be predicted based on simple models of frequency-dependent selection alone.     

Disease, frequency-dependent selection, and genetic polymorphisms: experiments with stripe rust and wheat

Abstract.— Pathogens have the potential to maintain genetic polymorphisms by creating frequency-dependent selection on their host. This can occur when a rare host genotype is less likely to be attacked by a pathogen (frequency-dependent disease attack) and has higher fitness at low frequency (negative frequency-dependent selection). In this study, we used wheat genotypes that were susceptible to different races of the pathogen Puccinia striiformis to test whether disease created frequency-selection on its host and whether such selection could maintain polymorphisms for resistance genes in the wheat populations. Four different two-way mixtures of wheat genotypes were planted at different frequencies in both the presence and absence of disease. Disease created frequency-dependent selection on its host in some populations. Unknown factors other than disease also created frequency-dependent selection in this system because, in some instances, rare genotype advantage was observed in the absence of disease. Although the pathogen created frequency-dependent selection on its host, this selection was not sufficient to maintain genetic polymorphism in the host populations. In all cases where frequency-dependent selection occurred only in the diseased plots, one of the two genotypes was predicted to dominate in the population and the same genotype was predicted to dominate in both the presence and absence of disease. Only in cases where frequency-dependent selection was not caused by disease was there evidence that genetic polymorphisms would be maintained in the population. The frequency-dependent selection described in this study is a consequence of epidemiological effects of disease and differs from the time-lagged frequency-dependent selection resulting from coevolution between hosts and parasites. The impact of this direct frequency-dependent selection on the maintenance of genetic polymorphisms in the host population is discussed.     

Transmission coupling mechanisms: cultural group selection

The application of phylogenetic methods to cultural variation raises questions about how cultural adaption works and how it is coupled to cultural transmission. Cultural group selection is of particular interest in this context because it depends on the same kinds of mechanisms that lead to tree-like patterns of cultural variation. Here, we review ideas about cultural group selection relevant to cultural phylogenetics. We discuss why group selection among multiple equilibria is not subject to the usual criticisms directed at group selection, why multiple equilibria are a common phenomena, and why selection among multiple equilibria is not likely to be an important force in genetic evolution. We also discuss three forms of group competition and the processes that cause populations to shift from one equilibrium to another and create a mutation-like process at the group level.     

Cultural evolution of cooperation: The interplay between forms of social learning and group selection

The role of cultural group selection in the evolution of human cooperation is hotly debated. It has been argued that group selection is more effective in cultural evolution than in genetic evolution, because some forms of cultural transmission (conformism and/or the tendency to follow a leader) reduce intra-group variation while creating stable cultural variation between groups. This view is supported by some models, while other models lead to contrasting and sometimes opposite conclusions. A consensus view has not yet been achieved, partly because the modelling studies differ in their assumptions on the dynamics of cultural transmission and the mode of group selection. To clarify matters, we created an individual-based model allowing for a systematic comparison of how different social learning rules governing cultural transmission affect the evolution of cooperation in a group-structured population. We consider two modes of group selection (selection by group replacement or by group contagion) and systematically vary the frequency and impact of group-level processes. From our simulations we conclude that the outcome of cultural evolution strongly reflects the interplay of social learning rules and the mode of group selection. For example, conformism hampers or even prevents the evolution of cooperation if group selection acts via contagion; it may facilitate the evolution of cooperation if group selection acts via replacement. In contrast, leader-imitation promotes the evolution of cooperation under a broader range of conditions.     

Evolution of antigen variation in the tick-borne pathogen Anaplasma phagocytophilum

Anaplasma phagocytophilum is an obligately intracellular tick-transmitted bacterial pathogen of humans and other animals. During the course of infection, A. phagocytophilum utilizes gene conversion to shuffle ～100 functional pseudogenes into a single expression cassette of the msp2(p44) gene, which codes for the major surface antigen and major surface protein 2 (MSP2). The role and extent of msp2(p44) recombination, particularly in hosts that only experience acute infections, is not clear. In the present study, we explored patterns of recombination and expression of the msp2(p44) gene of A. phagocytophilum in a serially infected mouse model. Even though the bacterium was passed rapidly among mice, minimizing the opportunities for the host to develop adaptive immunity, we detected the emergence of 34 unique msp2(p44) expression cassette variants. The expression of msp2(p44) pseudogenes did not follow a consistent pattern among different groups of mice, although some pseudogenes were expressed more frequently than others. In addition, among 263 expressed pseudogenes, 3 mosaic sequences each consisting of 2 different pseudogenes were identified. Population genetic analysis showed that genetic diversity and subpopulation differentiation tended to increase over time until stationarity was reached but that the variance that was observed in allele (expressed pseudogene) frequency could occur by drift alone only if a high variance in bacterial reproduction could be assumed. These findings suggest that evolutionary forces influencing antigen variation in A. phagocytophilum may comprise random genetic drift as well as some innate but apparently nonpurifying selection prior to the strong frequency-dependent selection that occurs cyclically after hosts develop strong adaptive immunity.     

Experimental evidence for sympatric ecological diversification due to frequency-dependent competition in Escherichia coli

We investigate adaptive diversification in experimental Escherichia coli populations grown in serial batch cultures on a mixture of glucose and acetate. All 12 experimental lines were started from the same genetically uniform ancestral strain but became highly polymorphic for colony size after 1000 generations. Five populations were clearly dimorphic and thus serve as a model for an adaptive lineage split. We analyzed the ecological basis for this dimorphism by studying bacterial growth curves. All strains exhibit diauxie, that is, sequential growth on the two resources. Thus, they exhibit phenotypic plasticity, using mostly glucose when glucose is abundant, then switching to acetate when glucose concentration is low. However, the coexisting strains differ in their diauxie pattern, with one cluster in the dimorphic populations growing better in the glucose phase, and the other cluster having a much shorter lag when switching to the acetate phase. Using invasion experiments, we show that the dimorphism of these two ecological types is maintained by frequency-dependent selection. Using a mathematical model for the adaptive dynamics of diauxie behavior, we show that evolutionary branching in diauxie behavior is a plausible theoretical scenario. Our results support the hypothesis that, in our experiments, adaptive diversification from a genetically uniform ancestor occurred due to frequency-dependent ecological interactions. Our results have implications for understanding the evolution of cross-feeding polymorphism in microorganisms, as well as adaptive speciation due to frequency-dependent selection on phenotypic plasticity.     

Experimental evolution with a multicellular host causes diversification within and between microbial parasite populations—Differences in emerging phenotypes of two different parasite strains

Host‐parasite coevolution is predicted to have complex evolutionary consequences, potentially leading to the emergence of genetic and phenotypic diversity for both antagonists. However, little is known about variation in phenotypic responses to coevolution between different parasite strains exposed to the same experimental conditions. We infected Caenorhabditis elegans with one of two strains of Bacillus thuringiensis and either allowed the host and the parasite to experimentally coevolve (coevolution treatment) or allowed only the parasite to adapt to the host (one‐sided parasite adaptation). By isolating single parasite clones from evolved populations, we found phenotypic diversification of the ancestral strain into distinct clones, which varied in virulence toward ancestral hosts and competitive ability against other parasite genotypes. Parasite phenotypes differed remarkably not only between the two strains, but also between and within different replicate populations, indicating diversification of the clonal population caused by selection. This study highlights that the evolutionary selection pressure mediated by a multicellular host causes phenotypic diversification, but not necessarily with the same phenotypic outcome for different parasite strains.     

Sexual dimorphism and adaptive speciation: two sides of the same ecological coin

Models of adaptive speciation are typically concerned with demonstrating that it is possible for ecologically driven disruptive selection to lead to the evolution of assortative mating and hence speciation. However, disruptive selection could also lead to other forms of evolutionary diversification, including ecological sexual dimorphisms. Using a model of frequency-dependent intraspecific competition, we show analytically that adaptive speciation and dimorphism require identical ecological conditions. Numerical simulations of individual-based models show that a single ecological model can produce either evolutionary outcome, depending on the genetic independence of male and female traits and the potential strength of assortative mating. Speciation is inhibited when the genetic basis of male and female ecological traits allows the sexes to diverge substantially. This is because sexual dimorphism, which can evolve quickly, can eliminate the frequency-dependent disruptive selection that would have provided the impetus for speciation. Conversely, populations with strong assortative mating based on ecological traits are less likely to evolve a sexual dimorphism because females cannot simultaneously prefer males more similar to themselves while still allowing the males to diverge. This conflict between speciation and dimorphism can be circumvented in two ways. First, we find a novel form of speciation via negative assortative mating, leading to two dimorphic daughter species. Second, if assortative mating is based on a neutral marker trait, trophic dimorphism and speciation by positive assortative mating can occur simultaneously. We conclude that while adaptive speciation and ecological sexual dimorphism may occur simultaneously, allowing for sexual dimorphism restricts the likelihood of adaptive speciation. Thus, it is important to recognize that disruptive selection due to frequency-dependent interactions can lead to more than one form of adaptive splitting.     

Nematode endoparasites do not codiversify with their stick insect hosts

Host–parasite coevolution stems from reciprocal selection on host resistance and parasite infectivity, and can generate some of the strongest selective pressures known in nature. It is widely seen as a major driver of diversification, the most extreme case being parallel speciation in hosts and their associated parasites. Here, we report on endoparasitic nematodes, most likely members of the mermithid family, infecting different Timema stick insect species throughout California. The nematodes develop in the hemolymph of their insect host and kill it upon emergence, completely impeding host reproduction. Given the direct exposure of the endoparasites to the host's immune system in the hemolymph, and the consequences of infection on host fitness, we predicted that divergence among hosts may drive parallel divergence in the endoparasites. Our phylogenetic analyses suggested the presence of two differentiated endoparasite lineages. However, independently of whether the two lineages were considered separately or jointly, we found a complete lack of codivergence between the endoparasitic nematodes and their hosts in spite of extensive genetic variation among hosts and among parasites. Instead, there was strong isolation by distance among the endoparasitic nematodes, indicating that geography plays a more important role than host‐related adaptations in driving parasite diversification in this system. The accumulating evidence for lack of codiversification between parasites and their hosts at macroevolutionary scales contrasts with the overwhelming evidence for coevolution within populations, and calls for studies linking micro‐ versus macroevolutionary dynamics in host–parasite interactions.     

Molecular evidence of host influences on the evolution and spread of human tapeworms

The taeniasis/cysticercosis complex is included in the list of neglected zoonotic diseases by the World Health Organization due to its significant impact on public health in tropical areas. Cysticercosis is still endemic in many regions of Asia, Africa and Latin America. Long absent in Europe and in other developed countries, cysticercosis has recently re-emerged in the United States and Canada, due to immigration, travel and local transmission. This has encouraged the use of molecular data to understand better the influence of animal and human hosts on the emergence and spread of Taenia species. The increasing number of mitochondrial sequences now available from human tapeworms and recent advances in computational tools has enabled reconstruction of the biogeography and evolutionary history of these organisms. New molecular data have provided insights into the biogeography of T. solium, T. asiatica and T. saginata. A Bayesian statistical framework using variable evolutionary rates from lineage to lineage has allowed an improved timescale analysis of human tapeworms. The dates of divergence obtained were compared to the timing of evolutionary events in the history of their hosts, based on the hypothesis that Taenia spp. and their hosts share a common history. Herein, we review changes in the definitive and secondary hosts and human interactions that underlie the differentiation and evolution of tapeworms. Species diversification of Taenia seems to be closely linked with the evolution of intermediate hosts in response to climatic events during the Pleistocene. Different genotypes of T. solium emerged when European and Asian wild boar Sus spp. populations diverged. Taenia saginata emerged when wild cattle Bos primigenius evolved and when zebu Bos indicus and taurine Bos taurus ancestors separated. Humans through migrations and later with the development of farming and animal husbandry may have had a significant impact on the spread and diversification of tapeworms. Migrations of Homo erectus from Africa to Asia and later of Homo sapiens facilitated the diversification and dispersal of T. solium and T. saginata populations. The development of animal husbandry, making Sus scrofa and Bos taurus preferential intermediate hosts, led to the worldwide distribution of parasites. New molecular data combined with an innovative dating method allow us to explain the ways in which ancient human migrations promoted the emergence and spread of taeniasis and cysticercosis around the world. Another intriguing phenomenon explained better by our approach is the influence of human settlement on the spread of these parasites in recently inhabited areas. The diverse nature of T. solium currently observed in Madagascar may correspond to multiple imports of the parasite during Austronesian migrations, while in Mexico a recent influence of humans during the colonial period is more likely. Human activities, especially food preparation and husbandry methods, remain responsible for the transmission and persistence of these parasites.