Complexity and self-organization in the evolution of cell polarization.

Cellular life exhibits order and complexity, which typically increase over the course of evolution. Cell polarization is a well-studied example of an ordering process that breaks the internal symmetry of a cell by establishing a preferential axis. Like many cellular processes, polarization is driven by self-organization, meaning that the macroscopic pattern emerges as a consequence of microscopic molecular interactions at the biophysical level. However, the role of self-organization in the evolution of complex protein networks remains obscure. In this Review, we provide an overview of the evolution of polarization as a self-organizing process, focusing on the model species Saccharomyces cerevisiae and its fungal relatives. Moreover, we use this model system to discuss how self-organization might relate to evolutionary change, offering a shift in perspective on evolution at the microscopic scale.

Evo-devo beyond development: Generalizing evo-devo to all levels of the phenotypic evolution.

A foundational idea of evo-devo is that morphological variation is not isotropic, that is, it does not occur in all directions. Instead, some directions of morphological variation are more likely than others from DNA-level variation and these largely depend on development. We argue that this evo-devo perspective should apply not only to morphology but to evolution at all phenotypic levels. At other phenotypic levels there is no development, but there are processes that can be seen, in analogy to development, as constructing the phenotype (e.g., protein folding, learning for behavior, etc.). We argue that to explain the direction of evolution two types of arguments need to be combined: generative arguments about which phenotypic variation arises in each generation and selective arguments about which of it passes to the next generation. We explain how a full consideration of the two types of arguments improves the explanatory power of evolutionary theory. Also see the video abstract here: https://youtu.be/Egbvma_uaKc.

Developmental Selection and the Perception of Mutation Bias.

The notion that mutations are random relative to their fitness effects is central to the Neo-Darwinian view of evolution. However, a recent interpretation of the patterns of mutation accumulation in the genome of Arabidopsis thaliana has challenged this notion, arguing for the presence of a targeted DNA repair mechanism that causes a nonrandom association of mutation rates and fitness effects. Specifically, this mechanism was suggested to cause a reduction in the rates of mutations on essential genes, thus lowering the rates of deleterious mutations. Central to this argument were attempts to rule out selection at the population level. Here, we offer an alternative and parsimonious interpretation of the patterns of mutation accumulation previously attributed to mutation bias, showing how they can instead or additionally be caused by developmental selection, that is selection occurring at the cellular level during the development of a multicellular organism. Thus, the depletion of deleterious mutations in A. thaliana may indeed be the result of a selective process, rather than a bias in mutation. More broadly, our work highlights the importance of considering development in the interpretation of population-genetic analyses of multicellular organisms, and it emphasizes that efforts to identify mechanisms involved in mutational biases should explicitly account for developmental selection.

On the Decoupling of Evolutionary Changes in mRNA and Protein Levels.

Variation in gene expression across lineages is thought to explain much of the observed phenotypic variation and adaptation. The protein is closer to the target of natural selection but gene expression is typically measured as the amount of mRNA. The broad assumption that mRNA levels are good proxies for protein levels has been undermined by a number of studies reporting moderate or weak correlations between the two measures across species. One biological explanation for this discrepancy is that there has been compensatory evolution between the mRNA level and regulation of translation. However, we do not understand the evolutionary conditions necessary for this to occur nor the expected strength of the correlation between mRNA and protein levels. Here, we develop a theoretical model for the coevolution of mRNA and protein levels and investigate the dynamics of the model over time. We find that compensatory evolution is widespread when there is stabilizing selection on the protein level; this observation held true across a variety of regulatory pathways. When the protein level is under directional selection, the mRNA level of a gene and the translation rate of the same gene were negatively correlated across lineages but positively correlated across genes. These findings help explain results from comparative studies of gene expression and potentially enable researchers to disentangle biological and statistical hypotheses for the mismatch between transcriptomic and proteomic data.

Demographic feedbacks during evolutionary rescue can slow or speed adaptive evolution.

Populations declining toward extinction can persist via genetic adaptation in a process called evolutionary rescue. Predicting evolutionary rescue has applications ranging from conservation biology to medicine, but requires understanding and integrating the multiple effects of a stressful environmental change on population processes. Here we derive a simple expression for how generation time, a key determinant of the rate of evolution, varies with population size during evolutionary rescue. Change in generation time is quantitatively predicted by comparing how intraspecific competition and the source of maladaptation each affect the rates of births and deaths in the population. Depending on the difference between two parameters quantifying these effects, the model predicts that populations may experience substantial changes in their rate of adaptation in both positive and negative directions, or adapt consistently despite severe stress. These predictions were then tested by comparison to the results of individual-based simulations of evolutionary rescue, which validated that the tolerable rate of environmental change varied considerably as described by analytical results. We discuss how these results inform efforts to understand wildlife disease and adaptation to climate change, evolution in managed populations and treatment resistance in pathogens.

The interplay of local adaptation and gene flow may lead to the formation of supergenes.

Supergenes are genetic architectures resulting in the segregation of alternative combinations of alleles underlying complex phenotypes. The co-segregation of alleles at linked loci is often facilitated by polymorphic chromosomal rearrangements suppressing recombination locally. Supergenes are involved in many complex polymorphisms, including sexual, colour or behavioural polymorphisms in numerous plants, fungi, mammals, fish, and insects. Despite a long history of empirical and theoretical research, the formation of supergenes remains poorly understood. Here, using a two-island population genetic model, we explore how gene flow and the evolution of overdominant chromosomal inversions may jointly lead to the formation of supergenes. We show that the evolution of inversions in differentiated populations, both under disruptive selection, leads to an increase in frequency of poorly adapted, immigrant haplotypes. Indeed, rare allelic combinations, such as immigrant haplotypes, are more frequently reshuffled by recombination than common allelic combinations, and therefore benefit from the recombination suppression generated by inversions. When an inversion capturing a locally adapted haplotype spreads but is associated with a fitness cost hampering its fixation (e.g. a recessive mutation load), the maintenance of a non-inverted haplotype in the population is enhanced; under certain conditions, the immigrant haplotype persists alongside the inverted local haplotype, while the standard local haplotype disappears. This establishes a stable, local polymorphism with two non-recombining haplotypes encoding alternative adaptive strategies, that is, a supergene. These results bring new light to the importance of local adaptation, overdominance, and gene flow in the formation of supergenes and inversion polymorphisms in general.

The evolutionary dynamics of hyperparasites.

Evolutionary theory has typically focused on pairwise interactions, such as those between hosts and parasites, with relatively little work having been carried out on more complex interactions including hyperparasites: parasites of parasites. Hyperparasites are common in nature, with the chestnut blight fungus virus CHV-1 a well-known natural example, but also notably include the phages of important human bacterial diseases. We build a general modeling framework for the evolution of hyperparasites that highlights the central role that the ability of a hyperparasite to be transmitted with its parasite plays in their evolution. A key result is that hyperparasites which transmit with their parasite hosts (hitchhike) will be selected for lower virulence, trending towards hypermutualism or hypercommensalism. We examine the impact on the evolution of hyperparasite systems of a wide range of host and parasite traits showing, for example, that high parasite virulence selects for higher hyperparasite virulence resulting in reductions in parasite virulence when hyperparasitized. Furthermore, we show that acute parasite infection will also select for increased hyperparasite virulence. Our results have implications for hyperparasite research, both as biocontrol agents and for their role in shaping community ecology and evolution and moreover emphasize the importance of understanding evolution in the context of multitrophic interactions.

Beyond genotype-phenotype maps: Toward a phenotype-centered perspective on evolution.

Evolutionary biology is paying increasing attention to the mechanisms that enable phenotypic plasticity, evolvability, and extra-genetic inheritance. Yet, there is a concern that these phenomena remain insufficiently integrated within evolutionary theory. Understanding their evolutionary implications would require focusing on phenotypes and their variation, but this does not always fit well with the prevalent genetic representation of evolution that screens off developmental mechanisms. Here, we instead use development as a starting point, and represent it in a way that allows genetic, environmental and epigenetic sources of phenotypic variation to be independent. We show why this representation helps to understand the evolutionary consequences of both genetic and non-genetic phenotype determinants, and discuss how this approach can instigate future areas of empirical and theoretical research.

Specificity of cost and probability biases in social anxiety: Comparing status and belongingness threats.

BACKGROUND: Social anxiety (SA) is characterized by concerns about the expected occurrence (probability) and anticipated distress (cost) of social threats. Unclear is whether SA correlates specifically with biased expectations of belongingness or status threats. AIMS: We aimed to discern if SA is uniquely tied to biased expectancies of either belongingness or status threats. MATERIALS AND METHODS: We assessed 757 participants' perceptions of exclusion and put-down scenarios, analysing associations between SA and threat perceptions. DISCUSSION: Our findings support the status-sensitivity hypothesis, suggesting individuals with high SA are particularly attuned to the perceived cost of status threats, potentially informing treatment approaches. CONCLUSION: Understanding SA's link to status concerns enhances therapeutic strategies, emphasizing the need to address status-related situations, cognitions, and emotions in interventions.

Costs of reproduction are present but latent in eusocial bumblebee queens.

BACKGROUND: The standard evolutionary theory of ageing proposes that ageing occurs because of a trade-off between reproduction and longevity. Eusocial insect queens exhibit positive fecundity-longevity associations and so have been suggested to be counter-examples through not expressing costs of reproduction and through remodelling conserved genetic and endocrine networks regulating ageing and reproduction. If so, eusocial evolution from solitary ancestors with negative fecundity-longevity associations must have involved a stage at which costs of reproduction were suppressed and fecundity and longevity became positively associated. Using the bumblebee (Bombus terrestris), we experimentally tested whether queens in annual eusocial insects at an intermediate level of eusocial complexity experience costs of reproduction, and, using mRNA-seq, the extent to which they exhibit a remodelling of relevant genetic and endocrine networks. Specifically, we tested whether costs of reproduction are present but latent, or whether a remodelling of relevant genetic and endocrine networks has already occurred allowing queens to reproduce without costs. RESULTS: We experimentally increased queens' costs of reproduction by removing their eggs, which caused queens to increase their egg-laying rate. Treatment queens had significantly reduced longevity relative to control queens whose egg-laying rate was not increased. Reduced longevity in treatment queens was not caused by increased worker-to-queen aggression or by increased overall activity in queens. In addition, treatment and control queens differed in age-related gene expression based on mRNA-seq in both their overall expression profiles and the expression of ageing-related genes. Remarkably, these differences appeared to occur principally with respect to relative age, not chronological age. CONCLUSIONS: This study represents the first simultaneously phenotypic and transcriptomic experimental test for a longevity cost of reproduction in eusocial insect queens. The results support the occurrence of costs of reproduction in annual eusocial insects of intermediate social complexity and suggest that reproductive costs are present but latent in queens of such species, i.e. that these queens exhibit condition-dependent positive fecundity-longevity associations. They also raise the possibility that a partial remodelling of genetic and endocrine networks underpinning ageing may have occurred in intermediately eusocial species such that, in unmanipulated conditions, age-related gene expression depends more on chronological than relative age.

The book of Matthew 'On naval timber and arboriculture'. Its structure and development.

The book of Patrick Matthew (1790-1874) 'On Naval Timber and Arboriculture' has regularly thwarted readers' attempts of interpretation. The problems seem to extend beyond analysing and interpreting its evolutionary passages. Building upon previous studies, this analysis presents evidence that the book's structure itself may have contributed significantly to its reception by sundry readers as somehow either clear or obscure, consequently leading to a diversity of interpretations. First, the book does not have a consistent literary form. Second, it presents a miscellany of juxtaposed contents. Third, its readers approach it from different contexts. Internal evidence shows that Patrick Matthew added a lot of material, while the manuscript was already in the proof-reading or press stage. This explains why it provides no consistent literary form or integrated content that would have helped interpretation. Hence readers have been left to their own devices, and their interpretation depended more strongly than usual on their own contexts.

Extending eco-evolutionary theory with oligomorphic dynamics.

Understanding the interplay between ecological processes and the evolutionary dynamics of quantitative traits in natural systems remains a major challenge. Two main theoretical frameworks are used to address this question, adaptive dynamics and quantitative genetics, both of which have strengths and limitations and are often used by distinct research communities to address different questions. In order to make progress, new theoretical developments are needed that integrate these approaches and strengthen the link to empirical data. Here, we discuss a novel theoretical framework that bridges the gap between quantitative genetics and adaptive dynamics approaches. 'Oligomorphic dynamics' can be used to analyse eco-evolutionary dynamics across different time scales and extends quantitative genetics theory to account for multimodal trait distributions, the dynamical nature of genetic variance, the potential for disruptive selection due to ecological feedbacks, and the non-normal or skewed trait distributions encountered in nature. Oligomorphic dynamics explicitly takes into account the effect of environmental feedback, such as frequency- and density-dependent selection, on the dynamics of multi-modal trait distributions and we argue it has the potential to facilitate a much tighter integration between eco-evolutionary theory and empirical data.

Can low-quality parents exploit their high-quality partners to gain higher fitness?

An individual's optimal investment in parental care potentially depends on many variables, including its future fitness prospects, the expected costs of providing care and its partner's expected or observed parental behaviour. Previous models suggested that low-quality parents could evolve to exploit their high-quality partners by reducing care, leading to the paradoxical prediction that low-quality parents could have higher fitness than their high-quality partners. However, these studies lacked a complete and consistent life-history model. Here, we challenge this result, developing a consistent analytical model of parental care strategies given individual variation in quality, and checking our results using agent-based simulations. In contrast to previous models, we predict that high-quality individuals always outcompete low-quality individuals in fitness terms. However, care effort may differ between high- and low-quality parents in either direction: low-quality individuals care more than high-quality individuals if their baseline mortality is higher, but less if their mortality increases more steeply with increasing care. We also highlight the ambiguity of the term 'quality' and stress the need for 'genealogical consistency' in evolutionary models.

Open questions in the social lives of viruses.

Social interactions among viruses occur whenever multiple viral genomes infect the same cells, hosts, or populations of hosts. Viral social interactions range from cooperation to conflict, occur throughout the viral world, and affect every stage of the viral lifecycle. The ubiquity of these social interactions means that they can determine the population dynamics, evolutionary trajectory, and clinical progression of viral infections. At the same time, social interactions in viruses raise new questions for evolutionary theory, providing opportunities to test and extend existing frameworks within social evolution. Many opportunities exist at this interface: Insights into the evolution of viral social interactions have immediate implications for our understanding of the fundamental biology and clinical manifestation of viral diseases. However, these opportunities are currently limited because evolutionary biologists only rarely study social evolution in viruses. Here, we bridge this gap by (1) summarizing the ways in which viruses can interact socially, including consequences for social evolution and evolvability; (2) outlining some open questions raised by viruses that could challenge concepts within social evolution theory; and (3) providing some illustrative examples, data sources, and conceptual questions, for studying the natural history of social viruses.

The evolutionary scaling of cellular traits imposed by the drift barrier.

Owing to internal homeostatic mechanisms, cellular traits may experience long periods of stable selective pressures, during which the stochastic forces of drift and mutation conspire to generate variation. However, even in the face of invariant selection, the drift barrier defined by the genetic effective population size, which is negatively associated with organism size, can have a substantial influence on the location and dispersion of the long-term steady-state distribution of mean phenotypes. In addition, for multilocus traits, the multiplicity of alternative, functionally equivalent states can draw mean phenotypes away from selective optima, even in the absence of mutation bias. Using a framework for traits with an additive genetic basis, it is shown that 1) optimal phenotypic states may be only rarely achieved; 2) gradients of mean phenotypes with respect to organism size (i.e., allometric relationships) are likely to be molded by differences in the power of random genetic drift across the tree of life; and 3) for any particular set of population-genetic conditions, significant variation in mean phenotypes may exist among lineages exposed to identical selection pressures. These results provide a potentially useful framework for understanding numerous aspects of cellular diversification and illustrate the risks of interpreting such variation in a purely adaptive framework.

The Adaptive Potential of Nonheritable Somatic Mutations.

AbstractThe adaptive potential of nonheritable somatic mutations has received limited attention in traditional evolutionary theory because heritability is a fundamental pillar of Darwinian evolution. We hypothesized that the ability of a germline genotype to express a novel phenotype via nonheritable somatic mutations can be selectively advantageous and that this advantage will channel evolving populations toward germline genotypes that constitutively express the phenotype. We tested this hypothesis by simulating evolving populations of developing organisms with an impermeable germline-soma separation navigating a minimal fitness landscape. The simulations revealed the conditions under which nonheritable somatic mutations promote adaptation. Specifically, this can occur when the somatic mutation supply is high, when few cells with the advantageous somatic mutation are required to increase organismal fitness, and when the somatic mutation also confers a selective advantage at the cellular level. We therefore provide proof of principle that nonheritable somatic mutations can promote adaptive evolution via a process we call "somatic genotypic exploration." We discuss the biological plausibility of this phenomenon as well as its evolutionary implications.

The need for evolutionary theory in cancer research.

Sir Richard Peto is well known for proposing puzzling paradoxes in cancer biology-some more well-known than others. In a 1984 piece, Peto proposed that after decades of molecular biology in cancer research, we are still ignorant of the biology underpinning cancer. Cancer is a product of somatic mutations. How do these mutations arise and what are the mechanisms? As an epidemiologist, Peto asked if we really need to understand mechanisms in order to prevent cancer? Four decades after Peto's proposed ignorance in cancer research, we can simply ask, are we still ignorant? Did the great pursuit to uncover mechanisms of cancer eclipse our understanding of causes and preventions? Or can we get closer to treating and preventing cancer by understanding the underlying mechanisms that make us most vulnerable to this disease?

Environment-to-phenotype mapping and adaptation strategies in varying environments.

Biological organisms exhibit diverse strategies for adapting to varying environments. For example, a population of organisms may express the same phenotype in all environments ("unvarying strategy") or follow environmental cues and express alternative phenotypes to match the environment ("tracking strategy"), or diversify into coexisting phenotypes to cope with environmental uncertainty ("bet-hedging strategy"). We introduce a general framework for studying how organisms respond to environmental variations, which models an adaptation strategy by an abstract mapping from environmental cues to phenotypic traits. Depending on the accuracy of environmental cues and the strength of natural selection, we find different adaptation strategies represented by mappings that maximize the long-term growth rate of a population. The previously studied strategies emerge as special cases of our model: The tracking strategy is favorable when environmental cues are accurate, whereas when cues are noisy, organisms can either use an unvarying strategy or, remarkably, use the uninformative cue as a source of randomness to bet hedge. Our model of the environment-to-phenotype mapping is based on a network with hidden units; the performance of the strategies is shown to rely on having a high-dimensional internal representation, which can even be random.

Fluctuating selection and global change: a synthesis and review on disentangling the roles of climate amplitude, predictability and novelty.

A formidable challenge for global change biologists is to predict how natural populations will respond to the emergence of conditions not observed at present, termed novel climates. Popular approaches to predict population vulnerability are based on the expected degree of novelty relative to the amplitude of historical climate fluctuations experienced by a population. Here, we argue that predictions focused on amplitude may be inaccurate because they ignore the predictability of environmental fluctuations in driving patterns of evolution and responses to climate change. To address this disconnect, we review major findings of evolutionary theory demonstrating the conditions under which phenotypic plasticity is likely to evolve in natural populations, and how plasticity decreases population vulnerability to novel environments. We outline key criteria that experimental studies should aim for to effectively test theoretical predictions, while controlling for the degree of climate novelty. We show that such targeted tests of evolutionary theory are rare, with marine systems being overall underrepresented in this venture despite exhibiting unique opportunities to test theory. We conclude that with more robust experimental designs that manipulate both the amplitude and predictability of fluctuations, while controlling for the degree of novelty, we may better predict population vulnerability to climate change.

The challenges of documenting coevolution and niche construction: The example of domestic spaces.

This essay delves into some of the challenges of studying the coevolution of humans and domestic spaces. These constructed arenas center on food preparation, and as part of the heritable niche they can shift the opportunities for, and constraints on, social interaction and cooperation in evolutionary time. Domestic spaces are widely evidenced in the archeological record, but investigators have made little progress in demonstrating causal links between proposed feedback spirals and constructed spaces of any sort. Bridging fine-scale and large-scale processes in coevolutionary systems is a complex problem that must engage higher levels of generative evolutionary theory. Archaeology nonetheless stands to offer a great deal to larger research programs by documenting and analyzing the pathways of change based on site formation processes along with evidence from subsistence refuse and technology. Choice models remain valuable tools for investigating aspects of the fine-scale feedback processes involved.