Modern evolutionary biology is founded on the Mendelian-genetic model of inheritance, but it is now clear that this model is incomplete. Empirical evidence shows that environment (encompassing all ...external influences on the genome) can impose transgenerational effects and generate heritable variation for a broad array of traits in animals, plants, and other organisms. Such effects can be mediated by the transmission of epigenetic, cytoplasmic, somatic, nutritional, environmental, and behavioral variation. Building on the work of many authors, we outline a general framework for conceptualizing nongenetic inheritance and its evolutionary implications. This framework shows that, by decoupling phenotypic change from the genotype, nongenetic inheritance can circumvent the limitations of genetic inheritance and thereby influence population dynamics and alter the fitness landscape. The weight of theory and empirical evidence indicates that nongenetic inheritance is a potent factor in evolution that can engender outcomes unanticipated under the Mendelian-genetic model.
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.
There is no doubt that the novel coronavirus SARS-CoV-2 that causes COVID-19 is mutating and thus has the potential to adapt during the current pandemic. Whether this evolution will lead to changes ...in the transmission, the duration, or the severity of the disease is not clear. This has led to considerable scientific and media debate, from raising alarms about evolutionary change to dismissing it. Here we review what little is currently known about the evolution of SARS-CoV-2 and extend existing evolutionary theory to consider how selection might be acting upon the virus during the COVID-19 pandemic. Although there is currently no definitive evidence that SARS-CoV-2 is undergoing further adaptation, continued evidence-based analysis of evolutionary change is important so that public health measures can be adjusted in response to substantive changes in the infectivity or severity of COVID-19.
Evolutionary theory predicts that selection favors increased transmission, longer pre-symptomatic periods, fewer asymptomatic cases, and lower disease severity for SARS-CoV-2. However, viral mutations are expected to affect combinations of these traits, making it challenging to predict the direction and disease impact of evolution.
One year into the global COVID-19 pandemic, the focus of attention has shifted to the emergence and spread of SARS-CoV-2 variants of concern (VOCs). After nearly a year of the pandemic with little ...evolutionary change affecting human health, several variants have now been shown to have substantial detrimental effects on transmission and severity of the virus. Public health officials, medical practitioners, scientists, and the broader community have since been scrambling to understand what these variants mean for diagnosis, treatment, and the control of the pandemic through nonpharmaceutical interventions and vaccines. Here we explore the evolutionary processes that are involved in the emergence of new variants, what we can expect in terms of the future emergence of VOCs, and what we can do to minimise their impact.
Otto et al. review the evolutionary processes that have led to the emergence of variants of concern during the COVID-19 pandemic and describe efforts that could limit the future emergence of variants that spread faster, are more severe, or better escape immune responses.
High-dose chemotherapy has long been advocated as a means of controlling drug resistance in infectious diseases but recent empirical studies have begun to challenge this view. We develop a very ...general framework for modeling and understanding resistance emergence based on principles from evolutionary biology. We use this framework to show how high-dose chemotherapy engenders opposing evolutionary processes involving the mutational input of resistant strains and their release from ecological competition. Whether such therapy provides the best approach for controlling resistance therefore depends on the relative strengths of these processes. These opposing processes typically lead to a unimodal relationship between drug pressure and resistance emergence. As a result, the optimal drug dose lies at either end of the therapeutic window of clinically acceptable concentrations. We illustrate our findings with a simple model that shows how a seemingly minor change in parameter values can alter the outcome from one where high-dose chemotherapy is optimal to one where using the smallest clinically effective dose is best. A review of the available empirical evidence provides broad support for these general conclusions. Our analysis opens up treatment options not currently considered as resistance management strategies, and it also simplifies the experiments required to determine the drug doses which best retard resistance emergence in patients.
How genes are not the only basis of heredity—and what this means for evolution, human life, and disease For much of the twentieth century it was assumed that genes alone mediate the transmission of ...biological information across generations and provide the raw material for natural selection. In Extended Heredity, leading evolutionary biologists Russell Bonduriansky and Troy Day challenge this premise. Drawing on the latest research, they demonstrate that what happens during our lifetimes--and even our grandparents' and great-grandparents' lifetimes—can influence the features of our descendants. On the basis of these discoveries, Bonduriansky and Day develop an extended concept of heredity that upends ideas about how traits can and cannot be transmitted across generations. By examining the history of the gene-centered view in modern biology and reassessing fundamental tenets of evolutionary theory, Bonduriansky and Day show that nongenetic inheritance—involving epigenetic, environmental, behavioral, and cultural factors—could play an important role in evolution. The discovery of nongenetic inheritance therefore has major implications for key questions in evolutionary biology, as well as human health. Extended Heredity reappraises long-held ideas and opens the door to a new understanding of inheritance and evolution.
A rapidly growing body of literature in several organisms suggests that environmentally-induced adaptive changes in phenotype can be transmitted across multiple generations. Although ...within-generation plasticity has been well documented, multigenerational plasticity represents a significant departure from conventional evolutionary thought. Studies of
have been particularly influential because this species exhibits extensive phenotypic plasticity, it is often essentially isogenic, and it has well-documented molecular and cellular mechanisms through which nongenetic inheritance occurs. However, while experimentalists are eager to claim that nongenetic modes of inheritance characterized in this and other model systems enhance fitness, many biologists remain skeptical given the extraordinary nature of this claim. We establish three criteria to evaluate how compelling the evidence for adaptive multigenerational plasticity is, and we use these criteria to critically examine putative cases of it in
We conclude by suggesting potentially fruitful avenues for future research.
The evolution of drug-resistant pathogens is a major challenge for 21st century medicine. Drug use practices vigorously advocated as resistance management tools by professional bodies, public health ...agencies, and medical schools represent some of humankind's largest attempts to manage evolution. It is our contention that these practices have poor theoretical and empirical justification for a broad spectrum of diseases. For instance, rapid elimination of pathogens can reduce the probability that de novo resistance mutations occur. This idea often motivates the medical orthodoxy that patients should complete drug courses even when they no longer feel sick. Yet "radical pathogen cure" maximizes the evolutionary advantage of any resistant pathogens that are present. It could promote the very evolution it is intended to retard. The guiding principle should be to impose no more selection than is absolutely necessary. We illustrate these arguments in the context of malaria; they likely apply to a wide range of infections as well as cancer and public health insecticides. Intuition is unreliable even in simple evolutionary contexts; in a social milieu where in-host competition can radically alter the fitness costs and benefits of resistance, expert opinion will be insufficient. An evidence-based approach to resistance management is required.
Following the initiation of the unprecedented global vaccination campaign against Severe Acute Respiratory Syndrome Coronavirus 2 (SARS-CoV-2), attention has now turned to the potential impact of ...this large-scale intervention on the evolution of the virus. In this Essay, we summarize what is currently known about pathogen evolution in the context of immune priming (including vaccination) from research on other pathogen species, with an eye towards the future evolution of SARS-CoV-2.
Nongenetic inheritance is a potentially important but poorly understood factor in population responses to rapid environmental change. Accumulating evidence indicates that nongenetic inheritance ...influences a diverse array of traits in all organisms and can allow for the transmission of environmentally induced phenotypic changes (‘acquired traits’), as well as spontaneously arising and highly mutable variants. We review models of adaptation to changing environments under the assumption of a broadened model of inheritance that incorporates nongenetic mechanisms of transmission, and survey relevant empirical examples. Theory suggests that nongenetic inheritance can increase the rate of both phenotypic and genetic change and, in some cases, alter the direction of change. Empirical evidence shows that a diversity of phenotypes – spanning a continuum from adaptive to pathological – can be transmitted nongenetically. The presence of nongenetic inheritance therefore complicates our understanding of evolutionary responses to environmental change. We outline a research program encompassing experimental studies that test for transgenerational effects of a range of environmental factors, followed by theoretical and empirical studies on the population‐level consequences of such effects.
PDF
