Three epigenetic information channels and their different roles in evolution

There is increasing evidence for epigenetically mediated transgenerational inheritance across taxa. However, the evolutionary implications of such alternative mechanisms of inheritance remain unclear. Herein, we show that epigenetic mechanisms can serve two fundamentally different functions in transgenerational inheritance: (i) selection-based effects, which carry adaptive information in virtue of selection over many generations of reliable transmission; and (ii) detection-based effects, which are a transgenerational form of adaptive phenotypic plasticity. The two functions interact differently with a third form of epigenetic information transmission, namely information about cell state transmitted for somatic cell heredity in multicellular organisms. Selection-based epigenetic information is more likely to conflict with somatic cell inheritance than is detection-based epigenetic information. Consequently, the evolutionary implications of epigenetic mechanisms are different for unicellular and multicellular organisms, which underscores the conceptual and empirical importance of distinguishing between these two different forms of transgenerational epigenetic effect.     

A unified approach to the evolutionary consequences of genetic and nongenetic inheritance

Inheritance-the influence of ancestors on the phenotypes of their descendants-translates natural selection into evolutionary change. For the past century, inheritance has been conceptualized almost exclusively as the transmission of DNA sequence variation from parents to offspring in accordance with Mendelian rules, but advances in cell and developmental biology have now revealed a rich array of inheritance mechanisms. This empirical evidence calls for a unified conception of inheritance that combines genetic and nongenetic mechanisms and encompasses the known range of transgenerational effects, including the transmission of genetic and epigenetic variation, the transmission of plastic phenotypes (acquired traits), and the effects of parental environment and genotype on offspring phenotype. We propose a unified theoretical framework based on the Price equation that can be used to model evolution under an expanded inheritance concept that combines the effects of genetic and nongenetic inheritance. To illustrate the utility and generality of this framework, we show how it can be applied to a variety of scenarios, including nontransmissible environmental noise, maternal effects, indirect genetic effects, transgenerational epigenetic inheritance, RNA-mediated inheritance, and cultural inheritance.     

The extended evolutionary synthesis: its structure,assumptions and predictions

Scientific activities take place within the structured sets of ideas and assumptions that define a field and its practices. The conceptual framework of evolutionary biology emerged with the Modern Synthesis in the early twentieth century and has since expanded into a highly successful research program to explore the processes of diversification and adaptation. Nonetheless, the ability of that framework satisfactorily to accommodate the rapid advances in developmental biology, genomics and ecology has been questioned. We review some of these arguments, focusing on literatures (evo-devo, developmental plasticity, inclusive inheritance and niche construction) whose implications for evolution can be interpreted in two ways—one that preserves the internal structure of contemporary evolutionary theory and one that points towards an alternative conceptual framework. The latter, which we label the ‘extended evolutionary synthesis'' (EES), retains the fundaments of evolutionary theory, but differs in its emphasis on the role of constructive processes in development and evolution, and reciprocal portrayals of causation. In the EES, developmental processes, operating through developmental bias, inclusive inheritance and niche construction, share responsibility for the direction and rate of evolution, the origin of character variation and organism–environment complementarity. We spell out the structure, core assumptions and novel predictions of the EES, and show how it can be deployed to stimulate and advance research in those fields that study or use evolutionary biology.     

Coevolution of slow-fast populations: evolutionary sliding, evolutionary pseudo-equilibria and complex Red Queen dynamics

We study the interplay of ecological and evolutionary dynamics in communities composed of populations with contrasting time-scales. In such communities, genetic variation of individual traits can cause population transitions between stationary and cyclic ecological regimes, hence abrupt variations in fitness. Such abrupt variations raise ridges in the adaptive landscape, where the populations are poised between equilibrium and cyclic coexistence and along which evolutionary trajectories can remain sliding for long times or halt at special points called evolutionary pseudo-equilibria. These novel phenomena should be generic to all systems in which ecological interactions cause fitness to vary discontinuously. They are demonstrated by the analysis of a predator-prey community, with one adaptive trait for each population. The eco-evolutionary dynamics of the system show a number of other distinctive features, including evolutionary extinction and two forms of Red Queen dynamics. One of them is characterized by intermittent bouts of cyclic oscillations of the two populations.     

General models of multilocus evolution

In 1991, Barton and Turelli developed recursions to describe the evolution of multilocus systems under arbitrary forms of selection. This article generalizes their approach to allow for arbitrary modes of inheritance, including diploidy, polyploidy, sex linkage, cytoplasmic inheritance, and genomic imprinting. The framework is also extended to allow for other deterministic evolutionary forces, including migration and mutation. Exact recursions that fully describe the state of the population are presented; these are implemented in a computer algebra package (available on the Web at http://helios.bto.ed.ac.uk/evolgen). Despite the generality of our framework, it can describe evolutionary dynamics exactly by just two equations. These recursions can be further simplified using a "quasi-linkage equilibrium" (QLE) approximation. We illustrate the methods by finding the effect of natural selection, sexual selection, mutation, and migration on the genetic composition of a population.     

Identifying Linkages among Conceptual Models of Ecosystem Degradation and Restoration: Towards an Integrative Framework

We present an ecological framework for considering ecosystem degradation and restoration, particularly in rangelands and arid environments. The framework is a synthesis of three conceptual models previously developed by several rangeland and restoration ecologists. We focus first on distinctions and connections between structural and functional components of rangeland ecosystems and then on distinctions and connections between biotic and abiotic components of the ecosystem. We next show that the structural/functional and biotic/abiotic distinctions can be integrated with a stepwise, positive feedback model of degradation to help explain degradation processes and restoration approaches. Finally, we relate those concepts to a threshold model of rangeland degradation. By establishing the conceptual links among these different models, this synthesis provides a broader, more integrated framework for thinking about the dynamics involved in rangeland degradation and restoration. We conclude by presenting some approaches to restoration that are motivated by the suite of concepts that are brought together in the framework.     

Selection response in traits with maternal inheritance

Maternal inheritance is the non-Mendelian transmission of traits from mothers to their offspring. Despite its presence in virtually all organisms, acting through a variety of mechanisms, the evolutionary consequences of maternal inheritance are not well understood. Here we review and extend a model of the inheritance and evolution of multiple quantitative characters with complex pathways of maternal effects. Extensions of the earlier model include common family environmental effects not associated with maternal phenotype, sexual dimorphism, and paternal effects (non-Mendelian influence of the father on offspring traits). We find that, in contrast to simple Mendelian inheritance, maternal inheritance produces qualitatively different evolutionary dynamics for two reasons: (1) the response to selection on a set of characters depends not only on their additive genetic variances and covariances, but also on maternal characters that influence them, and (2) time lags in the response to selection create a form of evolutionary momentum. These results have important implications for evolution in natural populations and practical applications in the economic improvement of domesticated species. We derive selection indices that maximize either the economic improvement in a single generation of artificial selection or the asymptotic rate of improvement in long-term selection programmes, based on individual merit or a combination of individual and family merit. Numerical examples show that accounting for maternal inheritance can lead to considerable increases in the efficiency of artificial selection.     

A conceptual framework for understanding thermal constraints on ectotherm activity with implications for predicting responses to global change

Activity budgets influence the expression of life history traits as well as population dynamics. For ectotherms, a major constraint on activity is environmental temperature. Nonetheless, we currently lack a comprehensive conceptual framework for understanding thermal constraints on activity, which hinders our ability to rigorously apply activity data to answer ecological and evolutionary questions. Here, we integrate multiple aspects of temperature‐dependent activity into a single unified framework that has general applicability. We also provide examples of the implementation of this framework to address fundamental questions in ecology relating to climate change vulnerability and species’ distributions using empirical data from a tropical lizard.     

Choosing mates: good genes versus genes that are a good fit

Female choice for male ornamental traits is widely accepted as a mechanism by which females maximize their reproductive success and/or offspring quality. However, there is an increasing empirical literature that shows a fitness benefit of genetic diversity and a tendency for females to use genetic dissimilarity as a criterion for mate choice. This genetic compatibility hypothesis for female mate choice presents a paradox. How can females use both an absolute criterion, such as male ornamentation, and a relative criterion, such as genetic dissimilarity, to choose their mates? Here, we present potential solutions for this dilemma and the empirical evidence supporting them. The interplay between these two contrasting forms of female mate choice presents an exciting empirical and theoretical challenge for evolutionary ecologists.     

Characterizing symbiont inheritance during host–microbiota evolution: Application to the great apes gut microbiota

Microbiota play a central role in the functioning of multicellular life, yet understanding their inheritance during host evolutionary history remains an important challenge. Symbiotic microorganisms are either acquired from the environment during the life of the host (i.e. environmental acquisition), transmitted across generations with a faithful association with their hosts (i.e. strict vertical transmission), or transmitted with occasional host switches (i.e. vertical transmission with horizontal switches). These different modes of inheritance affect microbes’ diversification, which at the two extremes can be independent from that of their associated host or follow host diversification. The few existing quantitative tools for investigating the inheritance of symbiotic organisms rely on cophylogenetic approaches, which require knowledge of both host and symbiont phylogenies, and are therefore often not well adapted to DNA metabarcoding microbial data. Here, we develop a model‐based framework for identifying vertically transmitted microbial taxa. We consider a model for the evolution of microbial sequences on a fixed host phylogeny that includes vertical transmission and horizontal host switches. This model allows estimating the number of host switches and testing for strict vertical transmission and independent evolution. We test our approach using simulations. Finally, we illustrate our framework on gut microbiota high‐throughput sequencing data of the family Hominidae and identify several microbial taxonomic units, including fibrolytic bacteria involved in carbohydrate digestion, that tend to be vertically transmitted.     

Humidity – The overlooked variable in the thermal biology of mosquito-borne disease

Vector-borne diseases cause significant financial and human loss, with billions of dollars spent on control. Arthropod vectors experience a complex suite of environmental factors that affect fitness, population growth and species interactions across multiple spatial and temporal scales. Temperature and water availability are two of the most important abiotic variables influencing their distributions and abundances. While extensive research on temperature exists, the influence of humidity on vector and pathogen parameters affecting disease dynamics are less understood. Humidity is often underemphasized, and when considered, is often treated as independent of temperature even though desiccation likely contributes to declines in trait performance at warmer temperatures. This Perspectives explores how humidity shapes the thermal performance of mosquito-borne pathogen transmission. We summarize what is known about its effects and propose a conceptual model for how temperature and humidity interact to shape the range of temperatures across which mosquitoes persist and achieve high transmission potential. We discuss how failing to account for these interactions hinders efforts to forecast transmission dynamics and respond to epidemics of mosquito-borne infections. We outline future research areas that will ground the effects of humidity on the thermal biology of pathogen transmission in a theoretical and empirical framework to improve spatial and temporal prediction of vector-borne pathogen transmission.     

Population and evolutionary dynamics in spatially structured seasonally varying environments

Increasingly imperative objectives in ecology are to understand and forecast population dynamic and evolutionary responses to seasonal environmental variation and change. Such population and evolutionary dynamics result from immediate and lagged responses of all key life‐history traits, and resulting demographic rates that affect population growth rate, to seasonal environmental conditions and population density. However, existing population dynamic and eco‐evolutionary theory and models have not yet fully encompassed within‐individual and among‐individual variation, covariation, structure and heterogeneity, and ongoing evolution, in a critical life‐history trait that allows individuals to respond to seasonal environmental conditions: seasonal migration. Meanwhile, empirical studies aided by new animal‐tracking technologies are increasingly demonstrating substantial within‐population variation in the occurrence and form of migration versus year‐round residence, generating diverse forms of ‘partial migration’ spanning diverse species, habitats and spatial scales. Such partially migratory systems form a continuum between the extreme scenarios of full migration and full year‐round residence, and are commonplace in nature. Here, we first review basic scenarios of partial migration and associated models designed to identify conditions that facilitate the maintenance of migratory polymorphism. We highlight that such models have been fundamental to the development of partial migration theory, but are spatially and demographically simplistic compared to the rich bodies of population dynamic theory and models that consider spatially structured populations with dispersal but no migration, or consider populations experiencing strong seasonality and full obligate migration. Second, to provide an overarching conceptual framework for spatio‐temporal population dynamics, we define a ‘partially migratory meta‐population’ system as a spatially structured set of locations that can be occupied by different sets of resident and migrant individuals in different seasons, and where locations that can support reproduction can also be linked by dispersal. We outline key forms of within‐individual and among‐individual variation and structure in migration that could arise within such systems and interact with variation in individual survival, reproduction and dispersal to create complex population dynamics and evolutionary responses across locations, seasons, years and generations. Third, we review approaches by which population dynamic and eco‐evolutionary models could be developed to test hypotheses regarding the dynamics and persistence of partially migratory meta‐populations given diverse forms of seasonal environmental variation and change, and to forecast system‐specific dynamics. To demonstrate one such approach, we use an evolutionary individual‐based model to illustrate that multiple forms of partial migration can readily co‐exist in a simple spatially structured landscape. Finally, we summarise recent empirical studies that demonstrate key components of demographic structure in partial migration, and demonstrate diverse associations with reproduction and survival. We thereby identify key theoretical and empirical knowledge gaps that remain, and consider multiple complementary approaches by which these gaps can be filled in order to elucidate population dynamic and eco‐evolutionary responses to spatio‐temporal seasonal environmental variation and change.     

Hierarchy Theory of Evolution and the Extended Evolutionary Synthesis: Some Epistemic Bridges,Some Conceptual Rifts

Contemporary evolutionary biology comprises a plural landscape of multiple co-existent conceptual frameworks and strenuous voices that disagree on the nature and scope of evolutionary theory. Since the mid-eighties, some of these conceptual frameworks have denounced the ontologies of the Modern Synthesis and of the updated Standard Theory of Evolution as unfinished or even flawed. In this paper, we analyze and compare two of those conceptual frameworks, namely Niles Eldredge’s Hierarchy Theory of Evolution (with its extended ontology of evolutionary entities) and the Extended Evolutionary Synthesis (with its proposal of an extended ontology of evolutionary processes), in an attempt to map some epistemic bridges (e.g. compatible views of causation; niche construction) and some conceptual rifts (e.g. extra-genetic inheritance; different perspectives on macroevolution; contrasting standpoints held in the “externalism–internalism” debate) that exist between them. This paper seeks to encourage theoretical, philosophical and historiographical discussions about pluralism or the possible unification of contemporary evolutionary biology.     

The Information Value of Non-Genetic Inheritance in Plants and Animals

Parents influence the development of their offspring in many ways beyond the transmission of DNA. This includes transfer of epigenetic states, nutrients, antibodies and hormones, and behavioural interactions after birth. While the evolutionary consequences of such non-genetic inheritance are increasingly well understood, less is known about how inheritance mechanisms evolve. Here, we present a simple but versatile model to explore the adaptive evolution of non-genetic inheritance. Our model is based on a switch mechanism that produces alternative phenotypes in response to different inputs, including genes and non-genetic factors transmitted from parents and the environment experienced during development. This framework shows how genetic and non-genetic inheritance mechanisms and environmental conditions can act as cues by carrying correlational information about future selective conditions. Differential use of these cues is manifested as different degrees of genetic, parental or environmental morph determination. We use this framework to evaluate the conditions favouring non-genetic inheritance, as opposed to genetic determination of phenotype or within-generation plasticity, by applying it to two putative examples of adaptive non-genetic inheritance: maternal effects on seed germination in plants and transgenerational phase shift in desert locusts. Our simulation models show how the adaptive value of non-genetic inheritance depends on its mechanism, the pace of environmental change, and life history characteristics.     

A dimensionless number for understanding the evolutionary dynamics of antigenically variable RNA viruses

Antigenically variable RNA viruses are significant contributors to the burden of infectious disease worldwide. One reason for their ubiquity is their ability to escape herd immunity through rapid antigenic evolution and thereby to reinfect previously infected hosts. However, the ways in which these viruses evolve antigenically are highly diverse. Some have only limited diversity in the long-run, with every emergence of a new antigenic variant coupled with a replacement of the older variant. Other viruses rapidly accumulate antigenic diversity over time. Others still exhibit dynamics that can be considered evolutionary intermediates between these two extremes. Here, we present a theoretical framework that aims to understand these differences in evolutionary patterns by considering a virus's epidemiological dynamics in a given host population. Our framework, based on a dimensionless number, probabilistically anticipates patterns of viral antigenic diversification and thereby quantifies a virus's evolutionary potential. It is therefore similar in spirit to the basic reproduction number, the well-known dimensionless number which quantifies a pathogen's reproductive potential. We further outline how our theoretical framework can be applied to empirical viral systems, using influenza A/H3N2 as a case study. We end with predictions of our framework and work that remains to be done to further integrate viral evolutionary dynamics with disease ecology.     

Assessing the prospects for a return of organisms in evolutionary biology

An argument has been raised from various perspectives against the Modern Synthesis (MS) in the past two decades: it has forgotten organisms. Niche construction theorists (Odling-Smee et al. 2003), developmental biologists like West-Eberhard (2003) and Evo-Devo elaborated various views which concur on a rehabilitation of the explanatory role of organisms, formerly neglected by an evolutionary science mostly centered on genes. This paper aims at assessing such criticisms by unraveling the specific arguments they use and evaluating how empirical findings may support them. In the first section, I review the usual critiques about the way MS treats organisms and show that the organisms-concerned critique is multifaceted, and I use the controversy about units of selection in order to show that purely conceptual and empirical arguments have been mixed up when organisms were concerned. In the second section, I consider successively the challenges raised to evolutionary MS by structuralist biologists and then the developmentalist challenge mostly raised by Evo-Devo. I distinguish what is purely conceptual among those criticisms and what mostly relies on recent empirical findings about genome activation, inheritance, and epigenetics. The last section discusses another program in MS, namely "evolutionary transitions" research, as enquiry into the emergence of organisms.     

Evolutionary rescue beyond the models

Laboratory model systems and mathematical models have shed considerable light on the fundamental properties and processes of evolutionary rescue. But it remains to determine the extent to which these model-based findings can help biologists predict when evolution will fail or succeed in rescuing natural populations that are facing novel conditions that threaten their persistence. In this article, we present a prospectus for transferring our basic understanding of evolutionary rescue to wild and other non-laboratory populations. Current experimental and theoretical results emphasize how the interplay between inheritance processes and absolute fitness in changed environments drive population dynamics and determine prospects of extinction. We discuss the challenge of inferring these elements of the evolutionary rescue process in field and natural settings. Addressing this challenge will contribute to a more comprehensive understanding of population persistence that combines processes of evolutionary rescue with developmental and ecological mechanisms.     

A generalised approach to the study and understanding of adaptive evolution

Evolutionary theory has made large impacts on our understanding and management of the world, in part because it has been able to incorporate new data and new insights successfully. Nonetheless, there is currently a tension between certain biological phenomena and mainstream evolutionary theory. For example, how does the inheritance of molecular epigenetic changes fit into mainstream evolutionary theory? Is niche construction an evolutionary process? Is local adaptation via habitat choice also adaptive evolution? These examples suggest there is scope (and perhaps even a need) to broaden our views on evolution. We identify three aspects whose incorporation into a single framework would enable a more generalised approach to the understanding and study of adaptive evolution: (i) a broadened view of extended phenotypes; (ii) that traits can respond to each other; and (iii) that inheritance can be non-genetic. We use causal modelling to integrate these three aspects with established views on the variables and mechanisms that drive and allow for adaptive evolution. Our causal model identifies natural selection and non-genetic inheritance of adaptive parental responses as two complementary yet distinct and independent drivers of adaptive evolution. Both drivers are compatible with the Price equation; specifically, non-genetic inheritance of parental responses is captured by an often-neglected component of the Price equation. Our causal model is general and simplified, but can be adjusted flexibly in terms of variables and causal connections, depending on the research question and/or biological system. By revisiting the three examples given above, we show how to use it as a heuristic tool to clarify conceptual issues and to help design empirical research. In contrast to a gene-centric view defining evolution only in terms of genetic change, our generalised approach allows us to see evolution as a change in the whole causal structure, consisting not just of genetic but also of phenotypic and environmental variables.     

The evolution of mate choice and mating biases

We review the current status of three well-established models (direct benefits, indirect benefits and sensory drive) and one newcomer (antagonistic chase-away) of the evolution of mate choice and the biases that are expressed during choice. We highlight the differences and commonalities in the underlying genetics and evolutionary dynamics of these models. We then argue that progress in understanding the evolution of mate choice is currently hampered by spurious distinctions among models and a misguided tendency to test the processes underlying each model as mutually exclusive alternatives. Finally, we suggest potentially fruitful directions for future theoretical and empirical research.     

Disease evolution across a range of spatio-temporal scales

Traditional explorations of infectious disease evolution have considered the competition between two cross-reactive strains within the standard framework of disease models. Such techniques predict that diseases should evolve to be highly transmissible, benign to the host and possess a long infectious period: in general, diseases do not conform to this ideal. Here we consider a more holistic approach, suggesting that evolution is a trade-off between adaptive pressures at different scales: within host, between hosts and at the population level. We present a model combining within-host pathogen dynamics and transmission between individuals governed by an explicit contact network, where transmission dynamics between hosts are a function of the interaction between the pathogen and the hosts' immune system, though ultimately constrained by the contacts each infected host possesses. Our results show how each of the scales places constraints on the evolutionary behavior, and that complex dynamics may emerge due to the feedbacks between epidemiological and evolutionary dynamics. In particular, multiple stable states can occur with switching between them stochastically driven.