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The informed use of scales and units in evolutionary quantitative genetics is often neglected, and naïve standardizations can cause misinterpretations of empirical results. A potentially influential example of such neglect can be found in the recent book by Arnold (2023. Evolutionary quantitative genetics. Oxford University Press). There, Arnold championed the use of heritability over mean-scaled genetic variance as a measure of evolutionary potential arguing that mean-scaled genetic variances are correlated with trait means while heritabilities are not. Here, we show that Arnold's empirical result is an artifact of ignoring the units in which traits are measured. More importantly, Arnold's argument mistakenly assumes that the goal of mean scaling is to remove the relationship between mean and variance. In our view, the purpose of mean scaling is to put traits with different units on a common scale that makes evolutionary changes, or their potential, readily interpretable and comparable in terms of proportions of the mean. [ABSTRACT FROM AUTHOR]

The new foundation for the propensity interpretation of fitness (PIF), developed by Pence and Ramsey (Br J Philos Sci 64:851–881, 2013), describes fitness as a probability distribution that encompasses all possible daughter populations to which the organism may give rise, including daughter populations in which traits might change and the possible environments that members of the daughter populations might encounter. This long-term definition of fitness is general enough to avoid counterexamples faced by previous mathematical conceptions of PIF. However, there seem to be downsides to its generality: the ecological role of fitness involves describing the degree of adaptedness between an organism and the specific environment it inhabits. When all possible changes in traits and all possible environments that a daughter population may encounter are included in the concept, it becomes difficult to see how fitness can fulfill this role. In this paper, we argue that this is a feature of Pence and Ramsey’s view rather than a bug: long-term fitness accommodates evolvability considerations, which concern the role that variation plays in evolutionary processes. Building on the foundations, we show that Pence and Ramsey’s fitness—F—can be partitioned into fourths: adaptedness, robustness of adaptedness, and two facets of evolvability. Conceptualizing these last three components forces us to consider the role played by grains of description of both organisms and the environment when thinking about long-term fitness. They track the possibility that there could be a change in type in a daughter population as a way of responding to environmental challenges, or that the type persists in the face of novel environments. We argue that these components are just as salient as adaptedness for long-term fitness. Together, this decomposition of F provides a more accurate picture of the factors involved in long-term evolutionary success. [ABSTRACT FROM AUTHOR]

Summary: Plants can evolve rapidly after pollinator changes, but the response of different floral traits to novel selection can vary. Floral morphology is often expected to show high integration to maintain pollination accuracy, while nectar traits can be more environmentally sensitive. The relative role of genetic correlations and phenotypic plasticity (PP) in floral evolution remains unclear, particularly for nectar traits, and can be studied in the context of recent pollinator changes.Digitalis purpurea shows rapid recent evolution of corolla morphology but not nectar traits following a range expansion with hummingbirds added as pollinators. We use this species to compare PP, heritability, evolvability and integration of floral morphology and nectar in a common garden.Morphological traits showed higher heritability than nectar traits, and the proximal section of the corolla, which regulates access to nectar and underwent rapid change in introduced populations, presented lower integration than the rest of the floral phenotype. Nectar was more plastic than morphology, driven by highly plastic sugar concentration. Nectar production rate showed high potential to respond to selection.These results explain the differential rapid evolution of floral traits previously observed in this species and show how intrafloral modularity determines variable evolutionary potential in morphological and nectar traits. [ABSTRACT FROM AUTHOR]

The number of multidrug‐resistant strains of bacteria is increasing rapidly, while the number of new antibiotic discoveries has stagnated. This trend has caused a surge in interest in bacteriophages as anti‐bacterial therapeutics, in part because there is near limitless diversity of phages to harness. While this diversity provides an opportunity, it also creates the dilemma of having to decide which criteria to use to select phages. Here we test whether a phage's ability to coevolve with its host (evolvability) should be considered and how this property compares to two previously proposed criteria: fast reproduction and thermostability. To do this, we compared the suppressiveness of three phages that vary by a single amino acid yet differ in these traits such that each strain maximized two of three characteristics. Our studies revealed that both evolvability and reproductive rate are independently important. The phage most able to suppress bacterial populations was the strain with high evolvability and reproductive rate, yet this phage was unstable. Phages varied due to differences in the types of resistance evolved against them and their ability to counteract resistance. When conditions were shifted to exaggerate the importance of thermostability, one of the stable phages was most suppressive in the short‐term, but not over the long‐term. Our results demonstrate the utility of biological therapeutics' capacities to evolve and adjust in action to resolve complications like resistance evolution. Furthermore, evolvability is a property that can be engineered into phage therapeutics to enhance their effectiveness. [ABSTRACT FROM AUTHOR]

This paper delves into the character concept as applied to reproduction. Our argument is that the prevailing functional-adaptationist perspective falls short in explaining the evolution of reproductive traits, and we propose an alternative organismal-relational approach that incorporates the developmental and interactive aspects of reproduction. To begin, we define the functional individuation of reproductive traits as evolutionary strategies aimed at enhancing fitness, and we demonstrate how this perspective influences the classification of reproductive characters and modes, the comprehension of shared traits as resulting from conflicts of evolutionary interest between individuals, and the explanation of reproductive diversity. After outlining the shortcomings of this framework, we introduce an organismal-relational approach grounded in evolutionary developmental studies of reproduction. This view provides a revised classification for reproductive characters and modes and offers a new understanding of interorganismal traits that takes into account their inherently relational nature. Lastly, we present the research agenda that emerges from this approach, which addresses the core explanatory gaps left by the adaptationist perspective, including the explanation of reproductive homologies and homoplasies, the developmental constraints associated with the evolution of reproductive modes, and the evolvability of reproductive characters. [ABSTRACT FROM AUTHOR]

Organisms rely on mutations to fuel adaptive evolution. However, many mutations impose a negative effect on fitness. Cells may have therefore evolved mechanisms that affect the phenotypic effects of mutations, thus conferring mutational robustness. Specifically, so-called buffer genes are hypothesized to interact directly or indirectly with genetic variation and reduce its effect on fitness. Environmental or genetic perturbations can change the interaction between buffer genes and genetic variation, thereby unmasking the genetic variation's phenotypic effects and thus providing a source of variation for natural selection to act on. This review provides an overview of our understanding of mutational robustness and buffer genes, with the chaperone gene HSP90 as a key example. It discusses whether buffer genes merely affect standing variation or also interact with de novo mutations, how mutational robustness could influence evolution, and whether mutational robustness might be an evolved trait or rather a mere side-effect of complex genetic interactions. This review uses the example of the chaperone gene HSP90 to outline our current understanding of mutational robustness and the role of buffer genes in evolution. [ABSTRACT FROM AUTHOR]

This article is a Commentary on Huntsman & Leslie (2024), 242: 2301–2311. [ABSTRACT FROM AUTHOR]

We review some of the main goals of theoretical linguistics in the tradition of Generative Grammar: description, evolvability and learnability. We evaluate recent efforts to address these goals, culminating with the Minimalist Program. We suggest that the most prominent versions of the Minimalist Program represent just one possible approach to addressing these goals, and not a particularly illuminating one in many respects. Some desirable features of an alternative minimalist theory are the dissociation between syntax and linear order, the emphasis on representational economy (i.e. Simpler Syntax) and an extra-grammatical account of non-local constraints (e.g. islands). We conclude with the outline of an alternative minimalist perspective that we believe points to more satisfactory accounts of the observed phenomena. [ABSTRACT FROM AUTHOR]

Recent computational modeling of early fruit fly (Drosophila) development has characterized the degree to which gene regulation networks can be robust to natural variability. In the first few hours of development, broad spatial gradients of maternally derived transcription factors activate embryonic gap genes. These gap patterns determine the subsequent segmented insect body plan through pair-rule gene expression. Gap genes are expressed with greater spatial precision than the maternal patterns. Computational modeling of the gap–gap regulatory interactions provides a mechanistic understanding for this robustness to maternal variability in wild-type (WT) patterning. A long-standing question in evolutionary biology has been how a system which is robust, such as the developmental program creating any particular species' body plan, is also evolvable, i.e. how can a system evolve or speciate, if the WT form is strongly buffered and protected? In the present work, we use the WT model to explore the breakdown of such Waddington-type 'canalization'. What levels of variability will push the system out of the WT form; are there particular pathways in the gene regulatory mechanism which are more susceptible to losing the WT form; and when robustness is lost, what types of forms are most likely to occur (i.e. what forms lie near the WT)? Manipulating maternal effects in several different pathways, we find a common gap 'peak-to-step' pattern transition in the loss of WT. We discuss these results in terms of the evolvability of insect segmentation, and in terms of experimental perturbations and mutations which could test the model predictions. We conclude by discussing the prospects for using continuum models of pattern dynamics to investigate a wider range of evo-devo problems. [ABSTRACT FROM AUTHOR]

Because the universe of possible DNA sequences is inconceivably vast, organisms have evolved mechanisms for exploring DNA sequence space while substantially reducing the hazard that would otherwise accrue to any process of random, accidental mutation. One such mechanism is meiotic recombination. Although sexual reproduction imposes a seemingly paradoxical 50% cost to fitness, sex evidently prevails because this cost is outweighed by the advantage of equipping offspring with genetic variation to accommodate environmental vicissitudes. The potential adaptive utility of additional mechanisms for producing genetic variation has long been obscured by a presumption that the vast majority of mutations are deleterious. Perhaps surprisingly, the probability for adaptive variation can be increased by several mechanisms that generate mutations abundantly. Such mechanisms, here called 'mutation protocols', implement implicit 'constraints that deconstrain'. Like meiotic recombination, they produce genetic variation in forms that minimize potential for harm while providing a reasonably high probability for benefit. One example is replication slippage of simple sequence repeats (SSRs); this process yields abundant, reversible mutations, typically with small quantitative effect on phenotype. This enables SSRs to function as adjustable 'tuning knobs'. There exists a clear pathway for SSRs to be shaped through indirect selection favouring their implicit tuning‐knob protocol. Several other molecular mechanisms comprise probable components of additional mutation protocols. Biologists might plausibly regard such mechanisms of mutation not primarily as sources of deleterious genetic mistakes but also as potentially adaptive processes for 'exploring' DNA sequence space. [ABSTRACT FROM AUTHOR]

Understanding the evolution of evolvability—the evolutionary potential of populations—is key to predicting adaptation to novel environments. Despite growing evidence that evolvability structures adaptation, it remains unclear how adaptation to novel environments in turn influences evolvability. Here we address the interplay between adaptation and evolvability in the peacock fly Tephritis conura, which recently underwent an adaptive change in ovipositor length following a host shift. We compared the evolvability of morphological traits, including ovipositor length, between the ancestral and the derived host race. We found that mean evolvability was reduced in females of the derived host race compared to the ancestral host race. However, patterns of multivariate evolvability (considering trait covariances) were very similar in both host races, and populations of the derived host race had diverged from the ancestral host race in directions of greater-than-average evolvability. Exploration of phenotypic integration patterns further revealed relatively high levels of independent variation in ovipositor length compared to other measured traits, allowing some degree of independent divergence. Our findings suggest that adaptation to novel environments can reduce mean evolvability without major changes in patterns of variational constraints, and that trait autonomy helps facilitate divergence of functionally important traits. [ABSTRACT FROM AUTHOR]

Epistasis is often portrayed as unimportant in evolution. While random patterns of epistasis may have limited effects on the response to selection, systematic directional epistasis can have substantial effects on evolutionary dynamics. Directional epistasis occurs when allele substitutions that change a trait also modify the effects of allele substitution at other loci in a systematic direction. In this case, trait evolution may induce correlated changes in allelic effects and additive genetic variance (evolvability) that modify further evolution. Although theory thus suggests a potentially important role for directional epistasis in evolution, we still lack empirical evidence about its prevalence and magnitude. Using a new framework to estimate systematic patterns of epistasis from line-crosses experiments, we quantify its effects on 197 size-related traits from diverging natural populations in 24 animal and 17 plant species. We show that directional epistasis is common and tends to become stronger with increasing morphological divergence. In animals, most traits displayed negative directionality toward larger size, suggesting that epistatic constraints reducing evolvability toward larger size. Dominance was also common but did not systematically alter the effects of epistasis. [ABSTRACT FROM AUTHOR]

Diverse organisms actively manipulate their (sym)biotic and physical environment in ways that feed back on their own development. However, the degree to which these processes affect microevolution remains poorly understood. The gazelle dung beetle both physically modifies its ontogenetic environment and structures its biotic interactions through vertical symbiont transmission. By experimentally eliminating (i) physical environmental modifications and (ii) the vertical inheritance of microbes, we assess how environment modifying behaviour and microbiome transmission shape heritable variation and evolutionary potential. We found that depriving larvae of symbionts and environment modifying behaviours increased additive genetic variance and heritability for development time but not body size. This suggests that larvae's ability to manipulate their environment has the potential to modify heritable variation and to facilitate the accumulation of cryptic genetic variation. This cryptic variation may become released and selectable when organisms encounter environments that are less amenable to organismal manipulation or restructuring. Our findings also suggest that intact microbiomes, which are commonly thought to increase genetic variation of their hosts, may instead reduce and conceal heritable variation. More broadly, our findings highlight that the ability of organisms to actively manipulate their environment may affect the potential of populations to evolve when encountering novel, stressful conditions. [ABSTRACT FROM AUTHOR]

Understanding, predicting, and controlling the phenotypic consequences of genetic and environmental change is essential to many areas of fundamental and applied biology. In evolutionary biology, the generative process of development is a major source of organismal evolvability that constrains or facilitates adaptive change by shaping the distribution of phenotypic variation that selection can act upon. While the complex interactions between genetic and environmental factors during development may appear to make it impossible to infer the consequences of perturbations, the persistent observation that many perturbations result in similar phenotypes indicates that there is a logic to what variation is generated. Here, we show that a general representation of development as a dynamical system can reveal this logic. We build a framework that allows predicting the phenotypic effects of perturbations, and conditions for when the effects of perturbations of different origins are concordant. We find that this concordance is explained by two generic features of development, namely the dynamical dependence of the phenotype on itself and the fact that all perturbations must affect the developmental process to have an effect on the phenotype. We apply our theoretical framework to classical models of development and show that it can be used to predict the evolutionary response to selection using information of plasticity and to accelerate evolution in a desired direction. The framework we introduce provides a way to quantitatively interchange perturbations, opening an avenue of perturbation design to control the generation of variation. [ABSTRACT FROM AUTHOR]

Understanding and predicting the evolutionary responses of complex morphological traits to selection remains a major challenge in evolutionary biology. Because traits are genetically correlated, selection on a particular trait produces both direct effects on the distribution of that trait and indirect effects on other traits in the population. The correlations between traits can strongly impact evolutionary responses to selection and may thus impose constraints on adaptation. Here, we used museum specimens and comparative quantitative genetic approaches to investigate whether the covariation among cranial traits facilitated or constrained the response to selection during the major dietary transitions in one of the world's most ecologically diverse mammalian families—the phyllostomid bats. We reconstructed the set of net selection gradients that would have acted on each cranial trait during the major transitions to feeding specializations and decomposed the selection responses into their direct and indirect components. We found that for all transitions, most traits capturing craniofacial length evolved toward adaptive directions owing to direct selection. Additionally, we showed instances of dietary transitions in which the complex interaction between the patterns of covariation among traits and the strength and direction of selection either constrained or facilitated evolution. Our work highlights the importance of considering the within-species covariation estimates to quantify evolvability and to disentangle the relative contribution of variational constraints versus selective causes for observed patterns. [ABSTRACT FROM AUTHOR]

Group size is an important trait for many ecological and evolutionary processes. However, it is not a trait possessed by individuals but by social groups, and as many genomes contribute to group size understanding its genetic underpinnings and so predicting its evolution is a conceptual challenge. Here I suggest how group size can be modelled as a joint phenotype of multiple individuals, and so how models for evolution accounting for indirect genetic effects are essential for understanding the genetic variance of group size. This approach makes it clear that (a) group size should have a larger genetic variance than initially expected as indirect genetic effects always contribute exactly as much as direct genetic effects and (b) the response to selection of group size should be faster than expected based on direct genetic variance alone as the correlation between direct and indirect effects is always at the maximum positive limit of 1. Group size should therefore show relatively rapid evolved increases and decreases, the consequences of which and evidence for I discuss. [ABSTRACT FROM AUTHOR]

Sexual dimorphism in traits of insects during the developmental stages could potentially be the direct or indirect result of sex-specific selection provided that genetic variation for sexual dimorphism is present. We investigated genetic variation in sexual dimorphism in a set of Drosophila melanogaster inbred lines for 2 traits: egg to adult development time and pupation site preference. We observed considerable genetic variation in sexual dimorphism among lines in both traits. The sexual dimorphic patterns remained relatively consistent across multiple trials, despite both traits being sensitive to environmental conditions. Additionally, we measured 2 sexually dimorphic adult morphological traits in 6 sampled lines and investigated correlations in the sexual dimorphism patterns with the 2 developmental traits. The abundance of genetic variation in sexual dimorphism for D. melanogaster developmental traits demonstrated in this study provides evidence for a high degree of evolvability of sex differences in preadult traits in natural populations. [ABSTRACT FROM AUTHOR]

Along with the ongoing digitalization of society, we witness a strong movement to make scientific data FAIR, machine-actionable, and available in the form of knowledge graphs. On the other hand, converting machine-actionable data from knowledge graphs back into human-oriented formats, including documents, graphical, or voice user interfaces, poses significant challenges. The solutions often build on various templates tailored to specific platforms on top of the shared underlying data. These templates suffer from limited reusability, making their adaptations difficult. Moreover, the continuous evolution of data or technological advancements requires substantial efforts to maintain these templates over time. In general, these challenges increase software development costs and are error-prone. In this paper, we propose a solution based on Normalized Systems Theory to address this challenge with the aim of achieving evolvability and sustainability in the transformation process of knowledge graphs into human-oriented formats with broad applicability across domains and technologies. We explain the theoretical foundation and design theorems used in our solution and outline the approach and implementation details. We theoretically evaluate our solution by comparing it to the traditional approach, where the systems are crafted manually. The evaluation shows that our solution is more efficient and effective on a large scale, reducing the human labor required to maintain various templates and supported target platforms. Next, we demonstrate the technical feasibility of our solution on a proof-of-concept implementation in a domain of data management planning that may also serve as a basis for future development. [ABSTRACT FROM AUTHOR]

This article reviews the edited volume "Evolvability: A Unifying Concept in Evolutionary Biology?" through biological and philosophical lenses. The book provides diverse angles on evolvability, which is affected by various hierarchical levels, timescales, and types of variation, thus moving beyond a purely genomics perspective. Evolvability is important to biosemiotics because understanding the dynamics of topological genotype spaces could help one better comprehend the phenotypic spaces of meaning, as developmental codes and interrelations can influence the emergence of biological novelty over time. This book is successful in provoking thought on evolvability's role as both a product and a driver of evolutionary innovations and explores the philosophical implications of how evolution has the capacity to generate novel forms of meaning. [ABSTRACT FROM AUTHOR]

Abstract The number of multidrug‐resistant strains of bacteria is increasing rapidly, while the number of new antibiotic discoveries has stagnated. This trend has caused a surge in interest in bacteriophages as anti‐bacterial therapeutics, in part because there is near limitless diversity of phages to harness. While this diversity provides an opportunity, it also creates the dilemma of having to decide which criteria to use to select phages. Here we test whether a phage's ability to coevolve with its host (evolvability) should be considered and how this property compares to two previously proposed criteria: fast reproduction and thermostability. To do this, we compared the suppressiveness of three phages that vary by a single amino acid yet differ in these traits such that each strain maximized two of three characteristics. Our studies revealed that both evolvability and reproductive rate are independently important. The phage most able to suppress bacterial populations was the strain with high evolvability and reproductive rate, yet this phage was unstable. Phages varied due to differences in the types of resistance evolved against them and their ability to counteract resistance. When conditions were shifted to exaggerate the importance of thermostability, one of the stable phages was most suppressive in the short‐term, but not over the long‐term. Our results demonstrate the utility of biological therapeutics' capacities to evolve and adjust in action to resolve complications like resistance evolution. Furthermore, evolvability is a property that can be engineered into phage therapeutics to enhance their effectiveness.

Understanding the causes and limits of population divergence in phenotypic traits is a fundamental aim of evolutionary biology, with the potential to yield predictions of adaptation to environmental change. Reciprocal transplant experiments and the evaluation of optimality models suggest that local adaptation is common but not universal, and some studies suggest that trait divergence is highly constrained by genetic variances and covariances of complex phenotypes. We analyze a large database of population divergence in plants and evaluate whether evolutionary divergence scales positively with standing genetic variation within populations (evolvability), as expected if genetic constraints are evolutionarily important. We further evaluate differences in divergence and evolvability-divergence relationships between reproductive and vegetative traits and between selfing, mixed-mating, and outcrossing species, as these factors are expected to influence both patterns of selection and evolutionary potentials. Evolutionary divergence scaled positively with evolvability. Furthermore, trait divergence was greater for vegetative traits than for floral (reproductive) traits, but largely independent of the mating system. Jointly, these factors explained ~40% of the variance in evolutionary divergence. The consistency of the evolvability-divergence relationships across diverse species suggests substantial predictability of trait divergence. The results are also consistent with genetic constraints playing a role in evolutionary divergence.

Although evolvability of genes and traits may promote specialization during species diversification, how ecology subsequently restricts such variation remains unclear. Chemosensation requires animals to decipher a complex chemical background to locate fitness-related resources, and thus the underlying genomic architecture and morphology must cope with constant exposure to a changing odorant landscape; detecting adaptation amidst extensive chemosensory diversity is an open challenge. In phyllostomid bats, an ecologically diverse clade that evolved plant visiting from a presumed insectivorous ancestor, the evolution of novel food detection mechanisms is suggested to be a key innovation, as plant-visiting species rely strongly on olfaction, supplementarily using echolocation. If this is true, exceptional variation in underlying olfactory genes and phenotypes may have preceded dietary diversification. We compared olfactory receptor (OR) genes sequenced from olfactory epithelium transcriptomes and olfactory epithelium surface area of bats with differing diets. Surprisingly, although OR evolution rates were quite variable and generally high, they are largely independent of diet. Olfactory epithelial surface area, however, is relatively larger in plant-visiting bats and there is an inverse relationship between OR evolution rates and surface area. Relatively larger surface areas suggest greater reliance on olfactory detection and stronger constraint on maintaining an already diverse OR repertoire. Instead of the typical case in which specialization and elaboration are coupled with rapid diversification of associated genes, here the relevant genes are already evolving so quickly that increased reliance on smell has led to stabilizing selection, presumably to maintain the ability to consistently discriminate among specific odorants-a potential ecological constraint on sensory evolution.

Progress in evolutionary developmental biology (evo‐devo) has deepened our understanding of how intrinsic properties of embryogenesis, along with natural selection and population genetics, shape phenotypic diversity. A focal point of recent empirical and theoretical research is the idea that highly developmentally stable phenotypes are more conserved in evolution. Previously, we demonstrated that in Japanese medaka (Oryzias latipes), embryonic stages and genes with high stability, estimated through whole‐embryo RNA‐seq, are highly conserved in subsequent generations. However, the precise origin of the stability of gene expression levels evaluated at the whole‐embryo level remained unclear. Such stability could be attributed to two distinct sources: stable intracellular expression levels or spatially stable expression patterns. Here we demonstrate that stability observed in whole‐embryo RNA‐seq can be attributed to stability at the cellular level (low variability in gene expression at the cellular levels). We quantified the intercellular variations in expression levels and spatial gene expression patterns for seven key genes involved in patterning dorsoventral and rostrocaudal regions during early development in medaka. We evaluated intracellular variability by counting transcripts and found its significant correlation with variation observed in whole‐embryo RNA‐seq data. Conversely, variation in spatial gene expression patterns, assessed through intraindividual left–right asymmetry, showed no correlation. Given the previously reported correlation between stability and conservation of expression levels throughout embryogenesis, our findings suggest a potential general trend: the stability or instability of developmental systems—and the consequent evolutionary diversity—may be primarily anchored in intrinsic fundamental elements such as the variability of intracellular states. Research highlights: We investigated the precise origins of developmental stability that was previously determined by whole‐embryo RNA‐seq, given its significance in indicating the potential for phenotypic conservation during evolution.Our findings suggest that the developmental stability can be primarily attributed to stability in gene expression at the cellular level, rather than stability in spatial gene expression patterns.The result provides further insight into how embryogenesis introduces bias in phenotypic evolution, and thus paves the way for a deeper understanding of developmental stability that would enable the prediction of phenotypic evolution. [ABSTRACT FROM AUTHOR]

Predicting if, when, and how populations can adapt to climate change constitutes one of the greatest challenges in science today. Here, we build from contributions to the special issue on evolutionary adaptation to climate change, a survey of its authors, and recent literature to explore the limits and opportunities for predicting adaptive responses to climate change. We outline what might be predictable now, in the future, and perhaps never even with our best efforts. More accurate predictions are expected for traits characterized by a well-understood mapping between genotypes and phenotypes and traits experiencing strong, direct selection due to climate change. A meta-analysis revealed an overall moderate trait heritability and evolvability in studies performed under future climate conditions but indicated no significant change between current and future climate conditions, suggesting neither more nor less genetic variation for adapting to future climates. Predicting population persistence and evolutionary rescue remains uncertain, especially for the many species without sufficient ecological data. Still, when polled, authors contributing to this special issue were relatively optimistic about our ability to predict future evolutionary responses to climate change. Predictions will improve as we expand efforts to understand diverse organisms, their ecology, and their adaptive potential. Advancements in functional genomic resources, especially their extension to non-model species and the union of evolutionary experiments and "omics," should also enhance predictions. Although predicting evolutionary responses to climate change remains challenging, even small advances will reduce the substantial uncertainties surrounding future evolutionary responses to climate change. [ABSTRACT FROM AUTHOR]

How did human societies evolve to become a major force of global change? What dynamics can lead societies on a trajectory of global sustainability? The astonishing growth in human population, economic activity and environmental impact has brought these questions to the fore. This theme issue pulls together a variety of traditions that seek to address these questions using different theories and methods. In this Introduction, we review and organize the major strands of work on how the Anthropocene evolved, how evolutionary dynamics are influencing sustainability efforts today, and what principles, strategies and capacities will be important to guide us towards global sustainability in the future. We present a set of synthetic insights and highlight frontiers for future research efforts which could contribute to a consolidated synthesis. This article is part of the theme issue 'Evolution and sustainability: gathering the strands for an Anthropocene synthesis'. [ABSTRACT FROM AUTHOR]

The use of dispositions has been put into question many times in the philosophical literature, especially with regards to how dispositional attributions can be justified. Yet, dispositions are an important part not only of our everyday talk but also of our scientific practices. In this paper, we develop an argument that infers the epistemic justification of dispositional talk from its indispensability for carrying out basic epistemological projects, and we apply it to the use of dispositions in evolutionary biology. For doing this, we first advocate for a function-based strategy for the epistemic justification of dispositional attributions. We next review the functional role of some key dispositional notions in evolutionary biology, such as fitness and evolvability. Then, we show that alternative non-dispositional substitutes of these dispositions fail to fulfill their roles to the same degree. We conclude that the use of dispositions is justified in evolutionary biology [ABSTRACT FROM AUTHOR]

A protein’s genetic architecture – the set of causal rules by which its sequence produces its functions – also determines its possible evolutionary trajectories. Prior research has proposed that the genetic architecture of proteins is very complex, with pervasive epistatic interactions that constrain evolution and make function difficult to predict from sequence. Most of this work has analyzed only the direct paths between two proteins of interest – excluding the vast majority of possible genotypes and evolutionary trajectories – and has considered only a single protein function, leaving unaddressed the genetic architecture of functional specificity and its impact on the evolution of new functions. Here, we develop a new method based on ordinal logistic regression to directly characterize the global genetic determinants of multiple protein functions from 20-state combinatorial deep mutational scanning (DMS) experiments. We use it to dissect the genetic architecture and evolution of a transcription factor’s specificity for DNA, using data from a combinatorial DMS of an ancient steroid hormone receptor’s capacity to activate transcription from two biologically relevant DNA elements. We show that the genetic architecture of DNA recognition consists of a dense set of main and pairwise effects that involve virtually every possible amino acid state in the protein-DNA interface, but higher-order epistasis plays only a tiny role. Pairwise interactions enlarge the set of functional sequences and are the primary determinants of specificity for different DNA elements. They also massively expand the number of opportunities for single-residue mutations to switch specificity from one DNA target to another. By bringing variants with different functions close together in sequence space, pairwise epistasis therefore facilitates rather than constrains the evolution of new functions.

Abstract Background Conventional wisdom in evolutionary theory considers aging as a non-selected byproduct of natural selection. Based on this, conviction aging was regarded as an inevitable phenomenon. It was also thought that in the wild organisms tend to die from diseases, predation and other accidents before they could reach the time when senescence takes its course. Evidence has accumulated, however, that aging is not inevitable and there are organisms that show negative aging even. Furthermore, old age does play a role in the deaths of many different organisms in the wild also. The hypothesis of programmed aging posits that a limited lifespan can evolve as an adaptation (i.e., positively selected for) in its own right, partly because it can enhance evolvability by eliminating “outdated” genotypes. A major shortcoming of this idea is that non-aging sexual individuals that fail to pay the demographic cost of aging would be able to steal good genes by recombination from aging ones. Results Here, we show by a spatially explicit, individual-based simulation model that aging can positively be selected for if a sufficient degree of kin selection complements directional selection. Under such conditions, senescence enhances evolvability because the rate of aging and the rate of recombination play complementary roles. The selected aging rate is highest at zero recombination (clonal reproduction). In our model, increasing extrinsic mortality favors evolved aging by making up free space, thereby decreasing competition and increasing drift, even when selection is stabilizing and the level of aging is set by mutation-selection balance. Importantly, higher extrinsic mortality is not a substitute for evolved aging under directional selection either. Reduction of relatedness decreases the evolved level of aging; chance relatedness favors non-aging genotypes. The applicability of our results depends on empirical values of directional and kin selection in the wild. Conclusions We found that aging can positively be selected for in a spatially explicit population model when sufficiently strong directional and kin selection prevail, even if reproduction is sexual. The view that there is a conceptual link between giving up clonal reproduction and evolving an aging genotype is supported by computational results.

Evolvability refers to the capacity, ability, or potential of an organism to generate heritable variation. Under this view, much extragenetic inheritance is regarded not as noise, fine-tuning, or a luxury add-on to genetic inheritance but as an essential tool for short-term adaptation. With respect to humans, the cultural contribution to evolvability is key to understanding evolution. In many instances, cultural inheritance directs genetic inheritance, not the other way around. Culture, being relatively free from the genetic leash, can produce change that genetic inheritance cannot. Soft inheritance—the view that heredity can be changed by an organism's experiences—has been disdained for over a century, but in light of the recent outpouring of data demonstrating extragenetic inheritance, defining evolution only in terms of genetic change ignores half the adaptive process, discarding much of what is interesting and relevant. Archaeologists can play a key role in evolvability research, given their contributions to topics such as niche construction, modularity, mosaic evolution, and developmental bias. [ABSTRACT FROM AUTHOR]

Evolutionary adaptation through genetic change requires genetic variation and is a key mechanism enabling species to persist in changing environments. Although a substantial body of work has focused on understanding how and why additive genetic variance (VA) differs among traits within species, we still know little about how they vary among species. Here we make a first attempt at testing for interspecific variation in two complementary measures of VA and the role of phylogeny in shaping this variation. To this end, we performed a phylogenetic comparative analysis using 1822 narrow‐sense heritability (h2) for 68 species of birds and mammals and 378 coefficients of additive genetic variance (CVA) estimates for 23 species. Controlling for within‐species variation attributable to estimation method and trait type, we found some interspecific variation in h2 (~15%) but not CVA. Although suggestive of interspecific variation in the importance of non‐(additive) genetic sources of variance, sample sizes were insufficient to test this hypothesis directly. Additionally, although power was low, no phylogenetic signal was detected for either measure. Hence, while this suggests interspecific variation in VA is probably small, our understanding of interspecific variation in the adaptive potential of wild vertebrate populations is currently hampered by data limitations, a scarcity of CVA estimates and a measure of their uncertainty in particular. [ABSTRACT FROM AUTHOR]

The development of an individual must be capable of resisting the harmful effects of internal and external perturbations. This capacity, called robustness, can make the difference between normal variation and disease. Some systems and organs are more resilient in their capacity to correct the effects of internal disturbances such as mutations. Similarly, organs and organisms differ in their capacity to be resilient against external disturbances, such as changes in temperature. Furthermore, all developmental systems must be somewhat flexible to permit evolutionary change, and understanding robustness requires a comparative framework. Over the last decades, most research on developmental robustness has been focusing on specific model systems and organs. Hence, we lack tools that would allow cross‐species and cross‐organ comparisons. Here, we emphasize the need for a uniform framework to experimentally test and quantify robustness across study systems and suggest that the analysis of fluctuating asymmetry might be a powerful proxy to do so. Such a comparative framework will ultimately help to resolve why and how organs of the same and different species differ in their sensitivity to internal (e.g., mutations) and external (e.g., temperature) perturbations and at what level of biological organization buffering capacities exist and therefore create robustness of the developmental system. [ABSTRACT FROM AUTHOR]

An agent‐based perspective in the study of complex systems is well established in diverse disciplines, yet is only beginning to be applied to evolutionary developmental biology. In this essay, we begin by defining agency and associated terminology formally. We then explore the assumptions and predictions of an agency perspective, apply these to select processes and key concept areas relevant to practitioners of evolutionary developmental biology, and consider the potential epistemic roles that an agency perspective might play in evo devo. Throughout, we discuss evidence supportive of agential dynamics in biological systems relevant to evo devo and explore where agency thinking may enrich the explanatory reach of research efforts in evolutionary developmental biology. [ABSTRACT FROM AUTHOR]

Maternal effects are an important source of phenotypic variation with potentially large fitness consequences, but how their importance varies with the quality of the environment across an individual's ontogeny is poorly understood. We bred Japanese quail (Coturnix japonica) of known pedigree and experimentally manipulated the quality of the offspring diet, to estimate the importance of prenatal maternal effects in shaping variation in body mass from hatching to adulthood. Maternal genetic effects on body mass at hatching were strong, and largely caused by variation in egg mass, but their importance rapidly declined with age. Whereas there was a large effect of diet on growth, this did not affect the decline of maternal effects variance. The importance of additive genetic and residual variance increased with age, with the latter being considerably larger in the poor diet treatment. Hence, we found no evidence for prenatal maternal effect by postnatal environment interactions and that prenatal maternal effects are rapidly replaced by direct additive genetic and residual effects when offspring start to develop outside the egg. Thereby these results shed new light on the dynamics of the role of maternal versus offspring genes across ontogeny and environments. [ABSTRACT FROM AUTHOR]

Background: Conventional wisdom in evolutionary theory considers aging as a non-selected byproduct of natural selection. Based on this, conviction aging was regarded as an inevitable phenomenon. It was also thought that in the wild organisms tend to die from diseases, predation and other accidents before they could reach the time when senescence takes its course. Evidence has accumulated, however, that aging is not inevitable and there are organisms that show negative aging even. Furthermore, old age does play a role in the deaths of many different organisms in the wild also. The hypothesis of programmed aging posits that a limited lifespan can evolve as an adaptation (i.e., positively selected for) in its own right, partly because it can enhance evolvability by eliminating "outdated" genotypes. A major shortcoming of this idea is that non-aging sexual individuals that fail to pay the demographic cost of aging would be able to steal good genes by recombination from aging ones. Results: Here, we show by a spatially explicit, individual-based simulation model that aging can positively be selected for if a sufficient degree of kin selection complements directional selection. Under such conditions, senescence enhances evolvability because the rate of aging and the rate of recombination play complementary roles. The selected aging rate is highest at zero recombination (clonal reproduction). In our model, increasing extrinsic mortality favors evolved aging by making up free space, thereby decreasing competition and increasing drift, even when selection is stabilizing and the level of aging is set by mutation-selection balance. Importantly, higher extrinsic mortality is not a substitute for evolved aging under directional selection either. Reduction of relatedness decreases the evolved level of aging; chance relatedness favors non-aging genotypes. The applicability of our results depends on empirical values of directional and kin selection in the wild. Conclusions: We found that aging can positively be selected for in a spatially explicit population model when sufficiently strong directional and kin selection prevail, even if reproduction is sexual. The view that there is a conceptual link between giving up clonal reproduction and evolving an aging genotype is supported by computational results. [ABSTRACT FROM AUTHOR]

Evolvability is the capacity of a population to generate heritable variation that can be acted upon by natural selection. This ability influences the adaptations and fitness of individual organisms. By viewing this capacity as a trait, evolvability is subject to natural selection and thus plays a critical role in eco‐evolutionary dynamics. Understanding this role provides insight into how species respond to changes in their environment and how species coexistence can arise and be maintained. Here, we create a G‐function model of competing species, each with a different evolvability. We analyze population and strategy (= heritable phenotype) dynamics of the two populations under clade initiation (when species are introduced into a population), evolutionary tracking (constant, small changes in the environment), adaptive radiation (availability of multiple ecological niches), and evolutionary rescue (extreme environmental disturbances). We find that when species are far from an eco‐evolutionary equilibrium, faster‐evolving species reach higher population sizes, and when species are close to an equilibrium, slower‐evolving species are more successful. Frequent, minor environmental changes promote the extinction of species with small population sizes, regardless of their evolvability. When several niches are available for a species to occupy, coexistence is possible, though slower‐evolving species perform slightly better than faster‐evolving ones due to the well‐recognized inherent cost of evolvability. Finally, disrupting the environment at intermediate frequencies can result in coexistence with cyclical population dynamics of species with different rates of evolution. [ABSTRACT FROM AUTHOR]

Abstract As organisms evolve, the effects of mutations change as a result of epistatic interactions with other mutations accumulated along the line of descent. This can lead to shifts in adaptability or robustness that ultimately shape subsequent evolution. Here, we review recent advances in measuring, modeling, and predicting epistasis along evolutionary trajectories, both in microbial cells and single proteins. We focus on simple patterns of global epistasis that emerge in this data, in which the effects of mutations can be predicted by a small number of variables. The emergence of these patterns offers promise for efforts to model epistasis and predict evolution.

Abstract Evolutionary adaptation through genetic change requires genetic variation and is a key mechanism enabling species to persist in changing environments. Although a substantial body of work has focused on understanding how and why additive genetic variance (VA) differs among traits within species, we still know little about how they vary among species. Here we make a first attempt at testing for interspecific variation in two complementary measures of VA and the role of phylogeny in shaping this variation. To this end, we performed a phylogenetic comparative analysis using 1822 narrow‐sense heritability (h2) for 68 species of birds and mammals and 378 coefficients of additive genetic variance (CVA) estimates for 23 species. Controlling for within‐species variation attributable to estimation method and trait type, we found some interspecific variation in h2 (~15%) but not CVA. Although suggestive of interspecific variation in the importance of non‐(additive) genetic sources of variance, sample sizes were insufficient to test this hypothesis directly. Additionally, although power was low, no phylogenetic signal was detected for either measure. Hence, while this suggests interspecific variation in VA is probably small, our understanding of interspecific variation in the adaptive potential of wild vertebrate populations is currently hampered by data limitations, a scarcity of CVA estimates and a measure of their uncertainty in particular.

The evolvability of proteins stems from their underlying biochemical, biophysical, and genetic properties. Initial states appear to drive the adaptability of proteins. There is mounting evidence, from evolutionary trajectories, that the availability of adaptive mutations is greatly influenced by epistasis. The underlying molecular mechanisms remain largely unexplored, however. Emerging techniques in single-molecule studies are revolutionizing the exploration of molecular heterogeneity in protein ensembles, a cryptic determinant of evolvability, providing a better understanding of this phenomenon. The plethora of biological functions that sustain life is rooted in the remarkable evolvability of proteins. An emerging view highlights the importance of a protein's initial state in dictating evolutionary success. A deeper comprehension of the mechanisms that govern the evolvability of these initial states can provide invaluable insights into protein evolution. In this review, we describe several molecular determinants of protein evolvability, unveiled by experimental evolution and ancestral sequence reconstruction studies. We further discuss how genetic variation and epistasis can promote or constrain functional innovation and suggest putative underlying mechanisms. By establishing a clear framework for these determinants, we provide potential indicators enabling the forecast of suitable evolutionary starting points and delineate molecular mechanisms in need of deeper exploration. [ABSTRACT FROM AUTHOR]

Since Washburn's New Physical Anthropology, researchers have sought to understand the complexities of morphological evolution among anatomical regions in human and non‐human primates. Researchers continue, however, to preferentially use comparative and functional approaches to examine complex traits, but these methods cannot address questions about evolutionary process and often conflate function with fitness. Moreover, researchers also tend to examine anatomical elements in isolation, which implicitly assumes independent evolution among different body regions. In this paper, we argue that questions asked in primate evolution are best examined using multiple anatomical regions subjected to model‐bound methods built from an understanding of evolutionary quantitative genetics. A nascent but expanding number of studies over the last two decades use this approach, examining morphological integration, evolvability, and selection modeling. To help readers learn how to use these methods, we review fundamentals of evolutionary processes within a quantitative genetic framework, explore the importance of neutral evolutionary theory, and explain the basics of evolutionary quantitative genetics, namely the calculation of evolutionary potential for multiple traits in response to selection. Leveraging these methods, we demonstrate their use to understand non‐independence in possible evolutionary responses across the limbs, limb girdles, and basicranium of humans. Our results show that model‐bound quantitative genetic methods can reveal unexpected genetic covariances among traits that create a novel but measurable understanding of evolutionary complexity among multiple traits. We advocate for evolutionary quantitative genetic methods to be a standard whenever appropriate to keep studies of primate morphological evolution relevant for the next seventy years and beyond. [ABSTRACT FROM AUTHOR]

Meiotic recombination is one of the main sources of genetic variation, a fundamental factor in the evolutionary adaptation of sexual eukaryotes. Yet, the role of variation in recombination rate and other recombination features remains underexplored. In this review, we focus on the sensitivity of recombination rates to different extrinsic and intrinsic factors. We briefly present the empirical evidence for recombination plasticity in response to environmental perturbations and/or poor genetic background and discuss theoretical models developed to explain how such plasticity could have evolved and how it can affect important population characteristics. We highlight a gap between the evidence, which comes mostly from experiments with diploids, and theory, which typically assumes haploid selection. Finally, we formulate open questions whose solving would help to outline conditions favoring recombination plasticity. This will contribute to answering the long‐standing question of why sexual recombination exists despite its costs, since plastic recombination may be evolutionary advantageous even in selection regimes rejecting any non‐zero constant recombination. [ABSTRACT FROM AUTHOR]

The origin of novel complex traits constitutes a central yet largely unresolved challenge in evolutionary biology. Intriguingly, many of the most promising breakthroughs in understanding the genesis of evolutionary novelty in recent years have occurred not in evolutionary biology itself, but through the comparative study of development and, more recently, the interface of developmental biology and ecology. Here, I discuss how these insights are changing our understanding of what matters in the origin of novel, complex traits in ontogeny and evolution. Specifically, my essay has two major objectives. First, I discuss how the nature of developmental systems biases the production of phenotypic variation in the face of novel or stressful environments toward functional, integrated and, possibly, adaptive variants. This, in turn, allows the production of novel phenotypes to precede (rather than follow) changes in genotype and allows developmental processes that are the product of past evolution to shape evolutionary change that has yet to occur. Second, I explore how this nature of developmental systems has itself evolved over time, increasing the repertoire of ontogenies to pursue a wider range of objectives across an expanding range of conditions, thereby creating an increasingly extensive affordance landscape in development and developmental evolution. Developmental systems and their evolution can thus be viewed as dynamic processes that modify their own means across ontogeny and phylogeny. The study of these dynamics necessitates more than the strict reductionist approach that currently dominates the fields of developmental and evolutionary developmental biology. [ABSTRACT FROM AUTHOR]

The major transitions in evolution include events and processes that result in the emergence of new levels of biological individuality. For collectives to undergo Darwinian evolution, their traits must be heritable, but the emergence of higher-level heritability is poorly understood and has long been considered a stumbling block for nascent evolutionary transitions. Using analytical models, synthetic biology, and biologically-informed simulations, we explored the emergence of trait heritability during the evolution of multicellularity. Prior work on the evolution of multicellularity has asserted that substantial collective-level trait heritability either emerges only late in the transition or requires some evolutionary change subsequent to the formation of clonal multicellular groups. In a prior analytical model, we showed that collective-level heritability not only exists but is usually more heritable than the underlying cell-level trait upon which it is based, as soon as multicellular groups form. Here, we show that key assumptions and predictions of that model are borne out in a real engineered biological system, with important implications for the emergence of collective-level heritability. [ABSTRACT FROM AUTHOR]

Abstract Evolvability is the capacity of a population to generate heritable variation that can be acted upon by natural selection. This ability influences the adaptations and fitness of individual organisms. By viewing this capacity as a trait, evolvability is subject to natural selection and thus plays a critical role in eco‐evolutionary dynamics. Understanding this role provides insight into how species respond to changes in their environment and how species coexistence can arise and be maintained. Here, we create a G‐function model of competing species, each with a different evolvability. We analyze population and strategy (= heritable phenotype) dynamics of the two populations under clade initiation (when species are introduced into a population), evolutionary tracking (constant, small changes in the environment), adaptive radiation (availability of multiple ecological niches), and evolutionary rescue (extreme environmental disturbances). We find that when species are far from an eco‐evolutionary equilibrium, faster‐evolving species reach higher population sizes, and when species are close to an equilibrium, slower‐evolving species are more successful. Frequent, minor environmental changes promote the extinction of species with small population sizes, regardless of their evolvability. When several niches are available for a species to occupy, coexistence is possible, though slower‐evolving species perform slightly better than faster‐evolving ones due to the well‐recognized inherent cost of evolvability. Finally, disrupting the environment at intermediate frequencies can result in coexistence with cyclical population dynamics of species with different rates of evolution.