The evolution of teaching

Teaching, alongside imitation, is widely thought to underlie the success of humanity by allowing high-fidelity transmission of information, skills, and technology between individuals, facilitating both cumulative knowledge gain and normative culture. Yet, it remains a mystery why teaching should be widespread in human societies but extremely rare in other animals. We explore the evolution of teaching using simple genetic models in which a single tutor transmits adaptive information to a related pupil at a cost. Teaching is expected to evolve where its costs are outweighed by the inclusive fitness benefits that result from the tutor's relatives being more likely to acquire the valuable information. We find that teaching is not favored where the pupil can easily acquire the information on its own, or through copying others, or for difficult to learn traits, where teachers typically do not possess the information to pass on to relatives. This leads to a narrow range of traits for which teaching would be efficacious, which helps to explain the rarity of teaching in nature, its unusual distribution, and its highly specific nature. Further models that allow for cumulative cultural knowledge gain suggest that teaching evolved in humans because cumulative culture renders otherwise difficult-to-acquire valuable information available to teach.     

Neutral indirect effects of mycorrhizal fungi on a specialist insect herbivore

Arbuscular mycorrhizal (AM) fungi can indirectly affect insect herbivore performance by altering traits in their host plant. Typically, generalist herbivores are negatively affected by AM fungi, whereas specialists are positively affected. This is thought to be caused by differential abilities of specialists and generalists to tolerate and/or exploit plant secondary compounds, the prevalence of which may be related to mycorrhizal colonization. We performed a feeding experiment in which specialist sunflower beetle larvae (Zygogramma exclamationis Fabricius, Chrysomelidae) were fed on mycorrhizal or nonmycorrhizal common annual sunflower plants (Helianthus annuus L., Asteraceae). To determine the indirect effects of AM fungi on the sunflower beetle larvae, we measured insect survival and relative growth rate. We also measured leaf area eaten, which allowed relative growth rate to be broken down into two components: relative consumption rate and efficiency of conversion of ingested food. Contrary to several previous studies, we detected no indirect effects of mycorrhizal fungi on larval survival or on relative growth rate or its components. Small effect sizes suggest that this is nonsignificant biologically, as well as statistically, rather than merely an issue of statistical power. Our results support an emerging view that indirect effects of mycorrhizal fungi on insect herbivores may be complex and idiosyncratic. We suggest that future research should emphasize the effects of mycorrhizal fungi on individual plant traits and how these interact to affect insect performance.     

Field studies reveal strong postmating isolation between ecologically divergent butterfly populations

Gene flow between populations that are adapting to distinct environments may be restricted if hybrids inherit maladaptive, intermediate phenotypes. This phenomenon, called extrinsic postzygotic isolation (EPI), is thought to play a critical role in the early stages of speciation. However, despite its intuitive appeal, we know surprisingly little about the strength and prevalence of EPI in nature, and even less about the specific phenotypes that tend to cause problems for hybrids. In this study, we searched for EPI among allopatric populations of the butterfly Euphydryas editha that have specialized on alternative host plants. These populations recall a situation thought typical of the very early stages of speciation. They lack consistent host-associated genetic differentiation at random nuclear loci and show no signs of reproductive incompatibility in the laboratory. However, they do differ consistently in diverse host-related traits. For each of these traits, we first asked whether hybrids between populations that use different hosts (different-host hybrids) were intermediate to parental populations and to hybrids between populations that use the same host (same-host hybrids). We then conducted field experiments to estimate the effects of intermediacy on fitness in nature. Our results revealed strong EPI under field conditions. Different-host hybrids exhibited an array of intermediate traits that were significantly maladaptive, including four behaviors. Intermediate foraging height slowed the growth of larvae, while intermediate oviposition preference, oviposition site height, and clutch size severely reduced the growth and survival of the offspring of adult females. We used our empirical data to construct a fitness surface on which different-host hybrids can be seen to fall in an adaptive valley between two peaks occupied by same-host hybrids. These findings demonstrate how ecological selection against hybrids can create a strong barrier to gene flow at the early stages of adaptive divergence.     

Role of primary intrahepatic T-cell activation in the 'liver tolerance effect'

There is accumulating evidence suggesting that hepatic permeability to both naive and activated T lymphocytes may be unique among the solid organs. The possibility that the liver may act as a site of primary activation for CD8+ T lymphocytes is supported by experimental data and may contribute to some of the unique immunological properties of this organ, particularly its ability to induce antigen-specific tolerance. This review discusses the nature of the liver APC inducing primary T-cell activation within the liver: Kupffer cells, liver dendritic cells, liver sinusoidal endothelial cells and hepatocytes are favourably located to allow physical contact with circulating T lymphocytes. Here, we examine the capability of each cell type to act as APC for naive CD4+ or CD8+ T cells and to induce tolerance.     

Genome-Wide Association Study SNPs in the Human Genome Diversity Project Populations: Does Selection Affect Unlinked SNPs with Shared Trait Associations?

Genome-wide association studies (GWAS) have identified more than 2,000 trait-SNP associations, and the number continues to increase. GWAS have focused on traits with potential consequences for human fitness, including many immunological, metabolic, cardiovascular, and behavioral phenotypes. Given the polygenic nature of complex traits, selection may exert its influence on them by altering allele frequencies at many associated loci, a possibility which has yet to be explored empirically. Here we use 38 different measures of allele frequency variation and 8 iHS scores to characterize over 1,300 GWAS SNPs in 53 globally distributed human populations. We apply these same techniques to evaluate SNPs grouped by trait association. We find that groups of SNPs associated with pigmentation, blood pressure, infectious disease, and autoimmune disease traits exhibit unusual allele frequency patterns and elevated iHS scores in certain geographical locations. We also find that GWAS SNPs have generally elevated scores for measures of allele frequency variation and for iHS in Eurasia and East Asia. Overall, we believe that our results provide evidence for selection on several complex traits that has caused changes in allele frequencies and/or elevated iHS scores at a number of associated loci. Since GWAS SNPs collectively exhibit elevated allele frequency measures and iHS scores, selection on complex traits may be quite widespread. Our findings are most consistent with this selection being either positive or negative, although the relative contributions of the two are difficult to discern. Our results also suggest that trait-SNP associations identified in Eurasian samples may not be present in Africa, Oceania, and the Americas, possibly due to differences in linkage disequilibrium patterns. This observation suggests that non-Eurasian and non-East Asian sample populations should be included in future GWAS.     

Correlated evolution and independent contrasts.

The use of the independent contrast method in comparative tests is studied. It is assumed that: (i) the traits under investigation are subject to natural selection; (ii) closely related species are similar because they share many characteristics of their niche, inherited from a common ancestor; and (iii) the current adaptive significance of the traits is the focus of investigation. The main objection to the use of species values in this case is that third variables which are shared by closely related species confound the relationship between the focal traits. In this paper, I argue that third variables are largely not controlled by the contrast methods, which are designed to estimate correlated evolution. To the extent that third variables also show correlated evolution, the true relationship among the traits of interest will remain obscured. Although the independent contrast method does not resolve the influence of third traits it does, in principle, provide a greater resolution than the use of the species mean values. However, its validity depends on the applicability of an evolutionary model which has a substantial stochastic component. To illustrate the consequences of relaxing this assumption I consider an alternative model of an adaptive radiation, where species come to fill a fixed niche space. Under this model, the expected value for the contrast correlation differs from that for the species correlation. The two correlations differ because contrasts reflect the historical pattern of diversification among species, whereas the species values describe the present-day relationships among the species. If the latter is of interest, I suggest that assessing significance based on the species correlations can be justified, providing that attention is paid to the role of potentially confounding third traits. Often, differences between contrast and species correlations may be biologically informative, reflecting changes in correlations between traits as an adaptive radiation proceeds; contrasts may be particularly useful as a means of investigating past history, rather than current utility of traits.     

Modes of response to environmental change and the elusive empirical evidence for bet hedging

Uncertainty is a problem not only in human decision-making, but is a prevalent quality of natural environments and thus requires evolutionary response. Unpredictable natural selection is expected to result in the evolution of bet-hedging strategies, which are adaptations to long-term fluctuating selection. Despite a recent surge of interest in bet hedging, its study remains mired in conceptual and practical difficulties, compounded by confusion over what constitutes evidence for its existence. Here, I attempt to resolve misunderstandings about bet hedging and its relationship with other modes of response to environmental change, identify the challenges inherent to its study and assess the state of existing empirical evidence. The variety and distribution of plausible bet-hedging traits found across 16 phyla in over 100 studies suggest their ubiquity. Thus, bet hedging should be considered a specific mode of response to environmental change. However, the distribution of bet-hedging studies across evidence categories-defined according to potential strength-is heavily skewed towards weaker categories, underscoring the need for direct appraisals of the adaptive significance of putative bet-hedging traits in nature.     

Systems analysis of eleven rodent disease models reveals an inflammatome signature and key drivers

Common inflammatome gene signatures as well as disease‐specific signatures were identified by analyzing 12 expression profiling data sets derived from 9 different tissues isolated from 11 rodent inflammatory disease models. The inflammatome signature significantly overlaps with known drug targets and co‐expressed gene modules linked to metabolic disorders and cancer. A large proportion of genes in this signature are tightly connected in tissue‐specific Bayesian networks (BNs) built from multiple independent mouse and human cohorts. Both the inflammatome signature and the corresponding consensus BNs are highly enriched for immune response‐related genes supported as causal for adiposity, adipokine, diabetes, aortic lesion, bone, muscle, and cholesterol traits, suggesting the causal nature of the inflammatome for a variety of diseases. Integration of this inflammatome signature with the BNs uncovered 151 key drivers that appeared to be more biologically important than the non‐drivers in terms of their impact on disease phenotypes. The identification of this inflammatome signature, its network architecture, and key drivers not only highlights the shared etiology but also pinpoints potential targets for intervention of various common diseases.     

Community-wide character displacement in the presence of clines: a test of Holarctic weasel guilds

1. Competition is thought to be a major influence on community assembly, ecology and evolution; presence of competitors may cause divergence in traits related to resource use (character displacement). 2. Such traits, however, often vary clinally, and this phenomenon may be independent of the presence or absence of competing species. 3. The presence of such clines can either obscure the effects of competition, or create an impression that competition is operating when, in fact, it is not. 4. We corrected for clinal variation while testing for character displacement in two well-studied weasel (Mustela) guilds, in the Nearctic and the west Palaearctic. 5. Without accounting for clines, our results agreed with previous studies suggesting character displacement in these guilds. 6. However, when we corrected for clines, predictions of competition theory were not met - and often we obtained evidence for character convergence in sympatry. 7. This may suggest that the nature of the resource base may be more important than interspecific competition in shaping morphology and size in these carnivores. 8. Our results highlight the need to account for geographic variation when studying character displacement and cast some doubt on prevailing ideas regarding the effect of competition on morphological evolution.     

Antipredator Responses by Native Mosquitofish to Non-Native Cichlids: An Examination of the Role of Prey Naiveté

The strong impact of non‐native predators in aquatic systems is thought to relate to the evolutionary naiveté of prey. Due to isolation and limited dispersal, this naiveté may be relatively high in freshwater systems. In this study, we tested this notion by examining the antipredator response of native mosquitofish, Gambusia holbrooki, to two non‐native predators found in the Everglades, the African jewelfish, Hemichromis letourneuxi, and the Mayan cichlid, Cichlasoma urophthalmus. We manipulated prey naiveté by using two mosquitofish populations that varied in their experience with the recent invader, the African jewelfish, but had similar levels of experience with the longer‐established Mayan cichlid. Specifically, we tested these predictions: (1) predator hunting modes differed between the two predators, (2) predation rates would be higher by the novel jewelfish predator, (3) particularly on the naive population living where jewelfish have not invaded yet, (4) antipredator responses would be stronger to Mayan cichlids due to greater experience and weaker and/or ineffective to jewelfish, and (5) especially weakest by the naive population. We assayed prey and predator behavior, and prey mortality in lab aquaria where both predators and prey were free‐ranging. Predator hunting modes and habitat domains differed, with jewelfish being more active search predators that used slightly higher parts of the water column and less of the habitat structure relative to Mayan cichlids. In disagreement with our predictions, predation rates were similar between the two predators, antipredator responses were stronger to African jewelfish (except for predator inspections), and there was no difference in response between jewelfish‐savvy and jewelfish‐naive populations. These results suggest that despite the novelty of introduced predators, prey may be able to respond appropriately if non‐native predator archetypes are similar enough to those of native predators, if prey rely on general antipredator responses or predation cues, and/or show neophobic responses.     

Disentangling the Evolution of Early and Late Life History Traits in Humans

Some aspects of human life history are unique among primates. Most notably, humans have a younger weaning age, a later age at first parturition, a shorter female reproductive period, and a longer lifespan than other living hominoid species. Obtaining a better understanding of when and how life history changed during human evolution is important to those studying the evolutionary developmental biology of extinct hominins, as life history traits pace developmental processes. Life history traits are thought to be linked via tradeoffs, such that changes in early life history traits directly affect those that follow later in life, and vice versa. However, it is also worth considering how changes to a single life history trait may indirectly affect other traits by way of modifying selective pressures acting on individuals and groups. For example, because they affect the size and demographic structure of a group, late life history traits (e.g., lifespan) may also affect the evolution of life history traits that occur earlier in life, but by modifying selective pressures acting on juveniles rather than by triggering a physiological tradeoff. This review marks an effort to begin to disentangle the ways in which early and late life history traits may affect each other both directly and indirectly. We concentrate on female life history characteristics. First, we review previous research on the evolution of the postmenopausal lifespan in women. Next we discuss recent findings concerning the relationship between the optimal length of the female reproductive period, mortality, and weaning age that show that selection favors a shorter female reproductive period in the presence of a younger weaning age. We discuss the implications this finding holds for understanding the evolution of life history traits that are of particular interest to developmental biologists.     

Kinetics of human B cell behavior and amplification of proliferative responses following stimulation with IL-21

Although recent studies indicated that IL-21 is an important regulator of human B cell activation, detailed comparison of the effects of IL-21 on distinct B cell subsets have not been performed. Our studies revealed that IL-21R is expressed by naive and germinal center B cells, but not memory or plasma cells. IL-21R was increased on naive and memory B cells following in vitro activation. Investigation into the kinetics and magnitude of responses of human B cells to IL-21 revealed that IL-21 potently augmented proliferation of CD40L-stimulated neonatal, splenic naive, and memory and tonsil germinal center B cells. This response exceeded that induced by IL-4, IL-10, and IL-13, cytokines that also induce B cell proliferation. Remarkably, CD40L/IL-21-stimulated naive B cells underwent the same number of divisions as memory cells and exhibited a greater enhancement in their response compared with CD40L alone than memory B cells. Therefore, IL-21 is a powerful growth factor for naive B cells. This may result from the higher expression of IL-21R on naive, compared with memory, B cells. Stimulation of human B cells with CD40L/IL-21 also induced IL-10 production and activation of STAT3. We propose that IL-21 may have therapeutic application in conditions of immunodeficiency where it could expand naive B cells, the predominant B cell subset in such patients. Conversely, because IL-21 is increased in murine models of lupus, dysregulated IL-21 production may contribute to perturbed B cell homeostasis observed in systemic lupus erythematosus. Thus, antagonizing IL-21 may be a novel strategy for treating Ab-mediated autoimmune diseases.     

A neuroscientific grasp of concepts: from control to representation

Abstraction denotes the cognitive process by means of which general concepts are formed. The dominant view of abstraction considers it not only as a complex and sophisticated cognitive activity, but also as a distinctive hallmark of mankind. The distinctiveness of abstract thought has indeed been closely related to another feature peculiar to our species: language. Following this perspective, the possibility to entertain conceptual representations is thus precluded to animals devoid of full-blown language. I challenge this view and propose that the representational dynamic of the brain is conceivable as a type of self-organization, in which action plays a crucial part. My aim will be to investigate whether, and to what extent, conceptual knowledge can be attributed to non-linguistic animal species, with particular emphasis on nonhuman primates. I therefore introduce the notion of semantic content as a type of 'relational specification'. A review of recent neurophysiological data on the neural underpinnings of action end-states in the macaque monkey brain is presented. On the basis of this evidence, I propose that conceptual representations can be conceived as the expression of a coherent internal world model. This model decomposes the 'outer' space inhabited by things in a meaningful way only to the extent that it accords to biologically constrained, embodied invariance. Finally, I discuss how the 'comparative' neuroscientific approach to abstraction proposed here may shed some light on its nature and its evolutionary origin.     

Multicomponent shell traits are consistent with an individual recognition function of the appearance of common murre (Uria aalge) eggs: A biological replication study

In dense breeding colonies, and despite having no nest structure, common murres (or guillemots: Uria aalge) are still able to identify their own eggs. Each female murre''s egg is thought to be recognized individually by the shell''s avian‐perceivable traits. This is because the eggshells’ visible traits conform to expectations of the identity‐signaling hypothesis in that they show both high intraindividual repeatability and high interindividual variability. Identity signaling also predicts a lack of correlation between each of the putative multicomponent recognition traits, yielding no significant relationships between those eggshell traits that are generated by mutually exclusive physiological factors. Using a multivariate analysis across eggshell size and shape, avian‐perceivable background coloration, spot (maculation) shape, and spot density, we detected no unexpected statistical correlations between Icelandic common murre egg traits lacking known physiological or mathematical relationships with one another. These results biologically replicate the conclusions of a recent eggshell trait study of Canadian common murres using similar methodology. We also demonstrate the use of static correlations to infer identity signaling function without direct behavioral observations, which in turn may also be applied to rare or extinct species and provide valuable insight into otherwise unknown communicative and behavioral functions.     

Presentation of soluble antigens to CD8+ T cells by CpG oligodeoxynucleotide-primed human naive B cells

Naive B lymphocytes are generally thought to be poor APCs, and there is limited knowledge of their role in activation of CD8(+) T cells. In this article, we demonstrate that class I MHC Ag presentation by human naive B cells is enhanced by TLR9 agonists. Purified naive B cells were cultured with or without a TLR9 agonist (CpG oligodeoxynucleotide [ODN] 2006) for 2 d and then assessed for phenotype, endocytic activity, and their ability to induce CD8(+) T cell responses to soluble Ags. CpG ODN enhanced expression of class I MHC and the costimulatory molecule CD86 and increased endocytic activity as determined by uptake of dextran beads. Pretreatment of naive B cells with CpG ODN also enabled presentation of tetanus toxoid to CD8(+) T cells, resulting in CD8(+) T cell cytokine production and granzyme B secretion and proliferation. Likewise, CpG-activated naive B cells showed enhanced ability to cross-present CMV Ag to autologous CD8(+) T cells, resulting in proliferation of CMV-specific CD8(+) T cells. Although resting naive B cells are poor APCs, they can be activated by TLR9 agonists to serve as potent APCs for class I MHC-restricted T cell responses. This novel activity of naive B cells could be exploited for vaccine design.     

The argument from potential: a reappraisal

Several criticisms of the argument from potential are reported. It is noted that such criticisms are inspired by two similarly wrong interpretations of potentiality, one confusing it with possibility and another with probability. A brief analysis of the original Aristotelian context in which the concept emerged shows that potentiality cannot be thought of as indicating the provision of some empirical facts in the future, but must rather be referred to the inherent ontological structure of the being in question. It is then argued that such an Aristotelian concept can be useful to express the dynamic structure of the person, as it must be understood according to contemporary phenomenological personalism. In the light of this philosophical tradition, the embryo can be vieewed as a being already possessing the human nature and actively developing its potential for personhood: it also follows that human nature must not be understood as a static and predetermined essence, but rather as the principle of becoming and movement toward further achievements.     

On the origin of species by means of assortative mating.

Assortative mating may split a population even in the absence of natural selection. Here, we study when this happens if mating depends on one or two quantitative traits. Not surprisingly, the modes of assortative mating that can cause sympatric speciation without selection are rather strict. However, some of them may occur in nature. Slow elimination of intermediate individuals caused by the gradual tightening of assortative mating, which evolves owing to relatively weak disruptive selection, provides the alternative scenario for sympatric speciation, in addition to fast elimination of intermediate individuals as a result of the direct action of strong disruptive selection under an invariant mode of assortative mating. Even when assortative mating alone cannot split an initially coherent population, it may be able to prevent the merging of species after their secondary contact.     

Developmental success, stability, and plasticity in closely related parthenogenetic and sexual lizards (Heteronotia, Gekkonidae)

The developmental trajectory of an organism is influenced by the interaction between its genes and the environment in which it develops. For example, the phenotypic traits of a hatchling reptile can be influenced by the organism's genotype, by incubation temperature, and by genetically coded norms of reaction for thermally labile traits. The evolution of parthenogenesis provides a unique opportunity to explore such effects: a hybrid origin of this trait in vertebrates modifies important aspects of the genotype (e.g., heterozygosity, polyploidy) and may thus impact not only on the phenotype generally, but also on the ways in which incubation temperature affects expression of the phenotype. The scarcity of vertebrate parthenogenesis has been attributed to developmental disruptions, but previous work has rarely considered reaction norms of embryogenesis in this respect. We used closely related sexual and asexual races of the Australian gecko Heteronotia binoei, which include those with multiple origins of parthenogenesis, to explore the ways in which reproductive modes (sexual, asexual), incubation temperatures (24, 27, and 30 degrees C), and the interaction between these factors affected hatchling phenotypes. The hatchling traits we considered included incubation period, incidence of deformities, hatchling survivorship, body size and shape, scalation (including fluctuating asymmetry), locomotor performance, and growth rate. Developmental success was slightly reduced (higher proportion of abnormal offspring) in parthenogenetic lineages although there was no major difference in hatching success. Incubation temperature affected a suite of traits including incubation period, tail length, body mass relative to egg mass, labial scale counts, running speed, growth rate, and hatchling survival. Our data also reveal an interaction between reproductive modes and thermal regimes, with the phenotypic traits of parthenogenetic lizards less sensitive to incubation temperature than was the case for their sexual relatives. Thus, the evolution of asexual reproduction in this species complex has modified both mean hatchling viability and the norms of reaction linking hatchling phenotypes to incubation temperature. Discussions on the reasons why parthenogenetic organisms are scarce in nature should take into account interactive effects such as these; future work could usefully try to tease apart the roles of parthenogenesis, its hybrid origin (and thus effects on ploidy and heterozygosity, etc.), and clonal selection in generating these divergent embryonic responses.     

The prediction of adaptive evolution: empirical application of the secondary theorem of selection and comparison to the breeder's equation

Adaptive evolution occurs when fitness covaries with genetic merit for a trait (or traits). The breeder's equation (BE), in both its univariate and multivariate forms, allows us to predict this process by combining estimates of selection on phenotype with estimates of genetic (co)variation. However, predictions are only valid if all factors causal for trait-fitness covariance are measured. Although this requirement will rarely (if ever) be met in practice, it can be avoided by applying Robertson's secondary theorem of selection (STS). The STS predicts evolution by directly estimating the genetic basis of trait-fitness covariation without any explicit model of selection. Here we apply the BE and STS to four morphological traits measured in Soay sheep (Ovis aries) from St. Kilda. Despite apparently positive selection on heritable size traits, sheep are not getting larger. However, although the BE predicts increasing size, the STS does not, which is a discrepancy that suggests unmeasured factors are upwardly biasing our estimates of selection on phenotype. We suggest this is likely to be a general issue, and that wider application of the STS could offer at least a partial resolution to the common discrepancy between naive expectations and observed trait dynamics in natural populations.