Nongenetic Inheritance and Its Evolutionary Implications
01 Dec 2009-Annual Review of Ecology, Evolution, and Systematics (Annual Reviews)-Vol. 40, Iss: 1, pp 103-125
TL;DR: 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.
Abstract: 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 ...
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TL;DR: The structure, core assumptions and novel predictions of the extended evolutionary synthesis (EES) are spelled out, and it is shown how it can be deployed to stimulate and advance research in those fields that study or use evolutionary biology.
Abstract: 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.
790 citations
TL;DR: The evidence for such effects of epigenetic, ecological and cultural inheritance and parental effects, and methods that quantify the relative contributions of genetic and non-genetic heritability to the transmission of phenotypic variation across generations are reviewed.
Abstract: Many biologists are calling for an 'extended evolutionary synthesis' that would 'modernize the modern synthesis' of evolution. Biological information is typically considered as being transmitted across generations by the DNA sequence alone, but accumulating evidence indicates that both genetic and non-genetic inheritance, and the interactions between them, have important effects on evolutionary outcomes. We review the evidence for such effects of epigenetic, ecological and cultural inheritance and parental effects, and outline methods that quantify the relative contributions of genetic and non-genetic heritability to the transmission of phenotypic variation across generations. These issues have implications for diverse areas, from the question of missing heritability in human complex-trait genetics to the basis of major evolutionary transitions.
620 citations
TL;DR: A general causal theory is presented to explain why human societies gained the capacity to globally alter the patterns, processes, and dynamics of ecology and how these anthropogenic alterations unfold over time and space as societies themselves change over human generational time.
Abstract: Humans, unlike any other multicellular species in Earth's history, have emerged as a global force that is transforming the ecology of an entire planet. It is no longer possible to understand, predict, or successfully manage ecological pattern, process, or change without understanding why and how humans reshape these over the long term. Here, a general causal theory is presented to explain why human societies gained the capacity to globally alter the patterns, processes, and dynamics of ecology and how these anthropogenic alterations unfold over time and space as societies themselves change over human generational time. Building on existing theories of ecosystem engineering, niche construction, inclusive inheritance, cultural evolution, ultrasociality, and social change, this theory of anthroecological change holds that sociocultural evolution of subsistence regimes based on ecosystem engineering, social specialization, and non-kin exchange, or “sociocultural niche construction,” is the main cause of both the long-term upscaling of human societies and their unprecedented transformation of the biosphere. Human sociocultural niche construction can explain, where classic ecological theory cannot, the sustained transformative effects of human societies on biogeography, ecological succession, ecosystem processes, and the ecological patterns and processes of landscapes, biomes, and the biosphere. Anthroecology theory generates empirically testable hypotheses on the forms and trajectories of long-term anthropogenic ecological change that have significant theoretical and practical implications across the subdisciplines of ecology and conservation. Though still at an early stage of development, anthroecology theory aligns with and integrates established theoretical frameworks including social–ecological systems, social metabolism, countryside biogeography, novel ecosystems, and anthromes. The “fluxes of nature” are fast becoming “cultures of nature.” To investigate, understand, and address the ultimate causes of anthropogenic ecological change, not just the consequences, human sociocultural processes must become as much a part of ecological theory and practice as biological and geophysical processes are now. Strategies for achieving this goal and for advancing ecological science and conservation in an increasingly anthropogenic biosphere are presented.
397 citations
TL;DR: It is demonstrated that a tropical reef fish is highly sensitive to small increases in water temperature, but can rapidly acclimate over multiple generations, and highlights the importance of transgenerational acclimation as a mechanism for coping with rapid climate change.
Abstract: Understanding the capacity of species to acclimate and adapt to expected temperature increases is critical for making predictions about the biological impacts of global warming, yet it is one of the least certain aspects of climate change science. Tropical species are considered to be especially sensitive to climate change because they live close to their thermal maximum and exhibit limited capacity for acclimation. Here, we demonstrate that a tropical reef fish is highly sensitive to small increases in water temperature, but can rapidly acclimate over multiple generations. Acute exposure to elevated temperatures (+1.5 °C and +3.0 °C) predicted to occur this century caused a 15% and 30% respective decrease in individual's maximum ability to perform aerobic activities such as swimming or foraging, known as aerobic scope. However, complete compensation in aerobic scope occurred when both parents and offspring were reared throughout their lives at elevated temperature. Such acclimation could reduce the impact of warming temperatures and allow populations to persist across their current range. This study reveals the importance of transgenerational acclimation as a mechanism for coping with rapid climate change and highlights that single generation studies risk underestimating the potential of species to cope.
378 citations
TL;DR: Why an evolutionary perspective is crucial to understanding climate change impacts in the sea is emphasised and the various experimental approaches that can be used to estimate evolutionary potential are outlined, focusing on molecular tools, quantitative genetics, and experimental evolution.
Abstract: An increasing number of short-term experimental studies show significant effects of projected ocean warming and ocean acidification on the performance on marine organisms. Yet, it remains unclear if we can reliably predict the impact of climate change on marine populations and ecosystems, because we lack sufficient understanding of the capacity for marine organisms to adapt to rapid climate change. In this review, we emphasise why an evolutionary perspective is crucial to understanding climate change impacts in the sea and examine the approaches that may be useful for addressing this challenge. We first consider what the geological record and present-day analogues of future climate conditions can tell us about the potential for adaptation to climate change. We also examine evidence that phenotypic plasticity may assist marine species to persist in a rapidly changing climate. We then outline the various experimental approaches that can be used to estimate evolutionary potential, focusing on molecular tools, quantitative genetics, and experimental evolution, and we describe the benefits of combining different approaches to gain a deeper understanding of evolutionary potential. Our goal is to provide a platform for future research addressing the evolutionary potential for marine organisms to cope with climate change.
368 citations
Cites background from "Nongenetic Inheritance and Its Evol..."
...Diallel designs assume that all of the variance associated with sires is additive genetic variance – an assumption that is increasingly called into question by evidence of nongenetic (epigenetic) inheritance in many taxa (Bonduriansky & Day 2009)....
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...…that the environmental conditions experienced by parents has a significant effect on the performance of the offspring, through the transmission of nutritional, somatic, cytoplasmic or epigenetic material between generations (Bonduriansky & Day 2009; Marshall & Morgan 2011; Klironomos et al. 2012)....
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References
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Book•
01 Jan 1981
TL;DR: The genetic constitution of a population: Hardy-Weinberg equilibrium and changes in gene frequency: migration mutation, changes of variance, and heritability are studied.
Abstract: Part 1 Genetic constitution of a population: Hardy-Weinberg equilibrium. Part 2 Changes in gene frequency: migration mutation. Part 3 Small populations - changes in gene frequency under simplified conditions. Part 4 Small populations - less simplified conditions. Part 5 Small populations - pedigreed populations and close inbreeding. Part 6 Continuous variation. Part 7 Values and means. Part 8 Variance. Part 9 Resemblance between relatives. Part 10 Heritability. Part 11 Selection - the response and its prediction. Part 12 Selection - the results of experiments. Part 13 Selection - information from relatives. Part 14 Inbreeding and crossbreeding - changes of mean value. Part 15 Inbreeding and crossbreeding - changes of variance. Part 16 Inbreeding and crossbreeding - applications. Part 17 Scale. Part 18 Threshold characters. Part 19 Correlated characters. Part 20 Metric characters under natural selection.
20,288 citations
Book•
01 Jan 2003
4,928 citations
"Nongenetic Inheritance and Its Evol..." refers background in this paper
...Although phenotypic plasticity represents purely phenotypic effects rather than evolution, biologists have long recognized its importance in evolution (Baldwin 1896, Lloyd Morgan 1896, Waddington 1942, West-Eberhard 2003)....
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...It has been suggested that phenotypic divergence in plastic traits can facilitate the evolution of reproductive isolation (West-Eberhard 2003)....
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...However, evolutionary change can follow on the heels of phenotypic change though the eventual assimilation and canalization of optimal phenotypes (Waddington 1942, West-Eberhard 2003)....
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TL;DR: Using methods developed by population biologists, a theory of cultural evolution is proposed that is an original and fair-minded alternative to the sociobiology debate.
Abstract: How do biological, psychological, sociological, and cultural factors combine to change societies over the long run? Boyd and Richerson explore how genetic and cultural factors interact, under the influence of evolutionary forces, to produce the diversity we see in human cultures. Using methods developed by population biologists, they propose a theory of cultural evolution that is an original and fair-minded alternative to the sociobiology debate.
4,592 citations
TL;DR: In this paper, the authors suggest that recent views on the nature of the developmental process make it easier to understand how the genotypes of evolving organisms can respond to the environment in a more co-ordinated fashion.
Abstract: THE battle, which raged for so long between the theories of evolution supported by geneticists on one hand and by naturalists on the other, has in recent years gone strongly in favour of the former. Few biologists now doubt that genetical investigation has revealed at any rate the most important categories of hereditary variation ; and the classical 'naturalist' theory-the inheritance of acquired characters-has been very generally relegated to the background because, in the forms in which it has been put forward, it has required a type of hereditary variation for the existence of which there was no adequate evidence. The long popularity of the theory was based, not on any positive evidence for it, but on its usefulness in accounting for some of the most striking of the results of evolution. Naturalists cannot fail to be continually and deeply impressed by the adaptation of an organism to its surroundings and of the parts of the organism to each other. These adaptive characters are inherited and some explanation of this must be provided. If we are deprived of the hypothesis of the inheritance of the effects of use and disuse, we seem thrown back on an exclusive reliance on the natural selection of merely chance mutations. It is doubtful, however, whether even the most statistically minded geneticists are entirely satisfied that nothing more is involved than the sorting out of random mutations by the natural selective filter. It is the purpose of this short communication to suggest that recent views on the nature of the developmental process make it easier to understand how the genotypes of evolving organisms can respond to the environment in a more co-ordinated fashion.
2,644 citations
Book•
01 Jan 1981
TL;DR: A mathematical theory of the non-genetic transmission of cultural traits is developed that provides a framework for future investigations in quantitative social and anthropological science and concludes that cultural transmission is an essential factor in the study of cultural change.
Abstract: A number of scholars have found that concepts such as mutation, selection, and random drift, which emerged from the theory of biological evolution, may also explain evolutionary phenomena in other disciplines as well. Drawing on these concepts, Professors Cavalli-Sforza and Feldman classify and systematize the various modes of transmitting "culture" and explore their consequences for cultural evolution. In the process, they develop a mathematical theory of the non-genetic transmission of cultural traits that provides a framework for future investigations in quantitative social and anthropological science. The authors use quantitative models that incorporate the various modes of transmission (for example, parent-child, peer-peer, and teacher-student), and evaluate data from sociology, archaeology, and epidemiology in terms of the models. They show that the various modes of transmission in conjunction with cultural and natural selection produce various rates of cultural evolution and various degrees of diversity within and between groups. The same framework can be used for explaining phenomena as apparently unrelated as linguistics, epidemics, social values and customs, and diffusion of innovations. The authors conclude that cultural transmission is an essential factor in the study of cultural change.
2,502 citations
"Nongenetic Inheritance and Its Evol..." refers background in this paper
...At the same time, theoretical analysis of behavioral/cultural transmission (Avital & Jablonka 2000, Boyd & Richerson 1985, Cavalli-Sforza & Feldman 1981, Laland 1994, Richerson & Boyd 2005), transgenerational epigenetic inheritance ( Jablonka & Lamb 1995, 2006; Pál 1998; Pál & Miklós 1999), and…...
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...This is possible because the rate of spread is a function of transmission probability as well as selection (Cavalli-Sforza & Feldman 1981)....
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...…flow from a crucial property of nongenetic inheritance: the partial decoupling of phenotypic change from genotypic change (Avital & Jablonka 2000; Cavalli-Sforza & Feldman 1981; Jablonka et al. 1992, 1995; Kirkpatrick & Lande 1989; Lachmann & Jablonka 1996; Lande & Kirkpatrick 1990; Pál 1998)....
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...A striking consequence of such decoupling is that the response of the mean phenotype to selection need not always be in the direction of selection (Boyd & Richerson 1985, Cavalli-Sforza & Feldman 1981, Kirkpatrick & Lande 1989, Laland et al. 1996, Lande & Kirkpatrick 1990, Odling-Smee et al. 2003)....
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...Cultural variation is especially pronounced in humans (Boyd & Richerson 1985, Cavalli-Sforza & Feldman 1981, Richerson and Boyd 2005) and some other primates (Whiten et al. 1999), but complex behavioral repertoires are transmitted nongenetically to offspring in many mammals and birds (Avital &…...
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