The implications of nongenetic inheritance for evolution in changing environments.
TL;DR: 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 are outlined.
Abstract: 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.
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1,217 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 "The implications of nongenetic inhe..."
...Furthermore, there have been important theoretical advances in understanding the roles of phenotypic plasticity and genetic evolution in species persistence in the face of climate change (e.g. Lande 2009; Chevin et al. 2010; Bonduriansky et al. 2012)....
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...This opens the way to include transgenerational effects into marine climate change studies (see Bonduriansky et al. 2012 for discussion on experimental design)....
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TL;DR: Two key approaches are focused on: measuring standing genetic variation within populations and experimental evolution, which highlight benefits and challenges of each approach and recommend future research directions for understanding the modulating role of evolution in a changing ocean.
Abstract: Ocean acidification poses a global threat to biodiversity, yet species might have the capacity to adapt through evolutionary change. Here we summarize tools available to determine species' capacity for evolutionary adaptation to future ocean change and review the progress made to date with respect to ocean acidification. We focus on two key approaches: measuring standing genetic variation within populations and experimental evolution. We highlight benefits and challenges of each approach and recommend future research directions for understanding the modulating role of evolution in a changing ocean.
343 citations
TL;DR: The extent to which transgenerational induction is predictable, detectable in nature, and subject to manipulation will determine the ability of researchers to decipher its role in plant-herbivore and plant-pathogen interactions.
Abstract: Rapidly accumulating evidence shows that herbivore and pathogen attack of plants can generate particular defense phenotypes across generations. What was once thought to be an oddity of plant defense induction now appears to be a taxonomically widespread phenomenon with strong potential to impact the ecology and evolution of species interactions. DNA methylation, histone modifications, and small RNAs each contribute to transgenerational defense initiation; examples in several species demonstrate that this induction can last for multiple generations. Priming of the offspring generation for more rapid induction following subsequent attack has also been reported. The extent to which transgenerational induction is predictable, detectable in nature, and subject to manipulation will determine the ability of researchers to decipher its role in plant‐herbivore and plant‐pathogen interactions.
322 citations
TL;DR: It is shown that there is only weak evidence for higher offspring performance when parental and offspring environments are matched compared with when they are mismatched, and estimates of heterogeneity among studies suggest that effects, when they occur, are subtle.
Abstract: The evolution of adaptive phenotypic plasticity relies on the presence of cues that enable organisms to adjust their phenotype to match local conditions. Although mostly studied with respect to nonsocial cues, it is also possible that parents transmit information about the environment to their offspring. Such ‘anticipatory parental effects’ or ‘adaptive transgenerational plasticity’ can have important consequences for the dynamics and adaptive potential of populations in heterogeneous environments. Yet, it remains unknown how widespread this form of plasticity is. Using a meta-analysis of experimental studies with a fully factorial design, we show that there is only weak evidence for higher offspring performance when parental and offspring environments are matched compared with when they are mismatched. Estimates of heterogeneity among studies suggest that effects, when they occur, are subtle. Study features, environmental context, life stage and trait categories all failed to explain significant amounts of variation in effect sizes. We discuss theoretical and methodological reasons for the limited evidence for anticipatory parental effects and suggest ways to improve our understanding of the prevalence of this form of plasticity in nature.
313 citations
References
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01 Jan 2004
TL;DR: "Not by Genes Alone" offers a radical interpretation of human evolution, arguing that the authors' ecological dominance and their singular social systems stem from a psychology uniquely adapted to create complex culture.
Abstract: Humans are a striking anomaly in the natural world. While we are similar to other mammals in many ways, our behavior sets us apart. Our unparalleled ability to adapt has allowed us to occupy virtually every habitat on earth, and our societies are larger, more complex, and more cooperative than any other mammal's. In "Not by Genes Alone", Peter J. Richerson and Robert Boyd argue that only a Darwinian theory of cultural evolution can explain these unique characteristics. "Not by Genes Alone" offers a radical interpretation of human evolution, arguing that our ecological dominance and our singular social systems stem from a psychology uniquely adapted to create complex culture. Richerson and Boyd consider culture to be essential to human adaptation, as much a part of human biology as bipedal locomotion. Drawing on work in the fields of anthropology, political science, sociology, and economics - and building their case with such fascinating examples as kayaks, clever knots, and yams that require twelve men to carry them - Richerson and Boyd convincingly demonstrate that culture and biology are inextricably linked. In abandoning the nature-versus-nurture debate as fundamentally misconceived, "Not by Genes Alone" is a truly original and groundbreaking theory of the role of culture in evolution and a book to be reckoned with for generations to come.
2,672 citations
TL;DR: The challenges to understand when evolution will occur and to identify potential evolutionary winners as well as losers, such as species lacking adaptive capacity living near physiological limits can be met through realistic models of evolutionary change linked to experimental data across a range of taxa.
Abstract: Evolutionary adaptation can be rapid and potentially help species counter stressful conditions or realize ecological opportunities arising from climate change. The challenges are to understand when evolution will occur and to identify potential evolutionary winners as well as losers, such as species lacking adaptive capacity living near physiological limits. Evolutionary processes also need to be incorporated into management programmes designed to minimize biodiversity loss under rapid climate change. These challenges can be met through realistic models of evolutionary change linked to experimental data across a range of taxa.
2,505 citations
TL;DR: The ability of an environmental factor to reprogram the germ line and to promote a transgenerational disease state has significant implications for evolutionary biology and disease etiology.
Abstract: Transgenerational effects of environmental toxins require either a chromosomal or epigenetic alteration in the germ line. Transient exposure of a gestating female rat during the period of gonadal sex determination to the endocrine disruptors vinclozolin (an antiandrogenic compound) or methoxychlor (an estrogenic compound) induced an adult phenotype in the F1 generation of decreased spermatogenic capacity (cell number and viability) and increased incidence of male infertility. These effects were transferred through the male germ line to nearly all males of all subsequent generations examined (that is, F1 to F4). The effects on reproduction correlate with altered DNA methylation patterns in the germ line. The ability of an environmental factor (for example, endocrine disruptor) to reprogram the germ line and to promote a transgenerational disease state has significant implications for evolutionary biology and disease etiology.
2,280 citations
"The implications of nongenetic inhe..." refers background in this paper
...This is because, although some nongenetically transmitted variants can be stable over many generations (Anway et al. 2005; Richerson and Boyd 2005; Johannes et al. 2009), genetic inheritance is likely to provide greater long-term stability of the optimal phenotype....
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...Exposure of pregnant rats to endocrine disruptors reduced spermatogenic capacity in male descendants, and this low-fertility phenotype was transmitted through the male line (perhaps via transgenerational epigenetic inheritance) for at least four generations (Anway et al. 2005, 2006b)....
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Book•
22 Jul 2003
TL;DR: This book extends evolutionary theory by formally including niche construction and ecological inheritance as additional evolutionary processes, and demonstrates how the theory can resolve long-standing problems in ecology, particularly by advancing the sorely needed synthesis of ecology and evolution.
Abstract: The seemingly innocent observation that the activities of organisms bring about changes in environments is so obvious that it seems an unlikely focus for a new line of thinking about evolution. Yet niche construction - as this process of organism-driven environmental modification is known - has hidden complexities. By transforming biotic and abiotic sources of natural selection in external environments, niche construction generates feedback in evolution on a scale hitherto underestimated - and in a manner that transforms the evolutionary dynamic. It also plays a critical role in ecology, supporting ecosystem engineering and influencing the flow of energy and nutrients through ecosystems. Despite this, niche construction has been given short shrift in theoretical biology, in part because it cannot be fully understood within the framework of standard evolutionary theory. Wedding evolution and ecology, this book extends evolutionary theory by formally including niche construction and ecological inheritance as additional evolutionary processes. The authors support their historic move with empirical data, theoretical population genetics, and conceptual models. They also describe new research methods capable of testing the theory. They demonstrate how their theory can resolve long-standing problems in ecology, particularly by advancing the sorely needed synthesis of ecology and evolution, and how it offers an evolutionary basis for the human sciences. Already hailed as a pioneering work by some of the world's most influential biologists, this is a rare, potentially field-changing contribution to the biological sciences.
2,237 citations
"The implications of nongenetic inhe..." refers background in this paper
...We do not discuss the extensive literature on niche-construction, which encompasses phenomena that extend beyond the purview of inheritance (Laland et al. 1996, 1999; Odling-Smee et al. 2003)....
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