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- Volume 44, 2013
Annual Review of Ecology, Evolution, and Systematics - Volume 44, 2013
Volume 44, 2013
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Introduction to Theme “Genomics in Ecology, Evolution, and Systematics”
Vol. 44 (2013), pp. 1–4More LessThe relationship between genomics and the core disciplines of ecology, evolution, and systematics is rapidly developing, computationally intensive, and changing the ways that our science asks and answers its most fundamental questions. As the six papers under this theme in this volume of AREES demonstrate, comparative and population genomics stand to fundamentally change how we study the nature of adaptation, the tempo and mode of evolution, and the history of life on Earth. Genomics is enabling our understanding of questions ranging from human historical demography to conservation biology of poorly known plants and animals, enhancing the role of organismal biology across basic and applied science.
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Genotype-by-Environment Interaction and Plasticity: Exploring Genomic Responses of Plants to the Abiotic Environment
Vol. 44 (2013), pp. 5–29More LessThere is considerable interest in the occurrence and molecular mechanisms of phenotypic plasticity and genotype-by-environment interactions (G×E) in plant populations. The emergence of genomic tools, including quantitative trait locus (QTL) mapping and transcriptome studies, provides opportunities to identify G×E patterns and mechanisms across a diversity of phenotypes, species, and environments. We review progress in evaluating the presence and characterizing the mechanisms of G×E using genomic studies of abiotic responses in plants. Our review reveals that G×E is common, often caused by changes in the magnitude of genetic effects in response to the environment, and associated with diverse genetic factors and molecular variants. We illustrate this diversity with an examination of transcriptome studies and discussion of cloned genes underlying G×E. We discuss the caveats associated with existing studies and outline future directions for better understanding G×E and its impact on local adaptation and plant improvement.
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Patterns of Selection in Plant Genomes
Vol. 44 (2013), pp. 31–49More LessPlants show a wide range of variation in mating system, ploidy level, and demographic history, allowing for unique opportunities to investigate the evolutionary and genetic factors affecting genome-wide patterns of positive and negative selection. In this review, we highlight recent progress in our understanding of the extent and nature of selection on plant genomes. We discuss differences in selection as they relate to variation in demography, recombination, mating system, and ploidy. We focus on the population genetic consequences of these factors and argue that, although variation in the magnitude of purifying selection is well documented, quantifying rates of positive selection and disentangling the relative importance of recombination, demography, and ploidy are ongoing challenges. Large-scale comparative studies that examine the relative and joint importance of these processes, combined with explicit models of population history and selection, are key and feasible goals for future work.
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Genomics and the Evolution of Phenotypic Traits
Vol. 44 (2013), pp. 51–72More LessEvolutionary genetics has entered an unprecedented era of discovery, catalyzed in large part by the development of technologies that provide information about genome sequence and function. An important benefit is the ability to move beyond a handful of model organisms in lab settings to identify the genetic basis for evolutionarily interesting traits in many organisms in natural settings. Other benefits are the abilities to identify causal mutations and validate their phenotypic consequences more readily and in many more species. Genomic technologies have reinvigorated interest in some of the most fundamental and persistent questions in evolutionary genetics, revealed previously unsuspected evolutionary phenomena, and opened the door to a wide range of new questions.
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Geographic Mode of Speciation and Genomic Divergence
Vol. 44 (2013), pp. 73–97More LessUnderstanding speciation requires determining how inherent barriers to gene flow (reproductive isolation, RI) evolve between populations. The field of population genomics attempts to address this question by characterizing genome-wide patterns of divergence between taxa, often utilizing next-generation sequencing. Here, we focus on a central assumption of such “genome scans”: regions displaying high levels of differentiation contain loci contributing to RI. Three major issues are discussed concerning the relationship between gene flow, genomic divergence, and speciation: (a) patterns expected in the presence versus absence of gene flow; (b) processes, such as direct selection and genetic hitchhiking, allowing for divergence with gene flow; and (c) the consequences of the timing of when gene flow occurs during speciation (e.g., continuous gene flow versus gene flow following secondary contact after a period of initial allopatric divergence). Theory and existing data are presented for each issue, and avenues for future work are highlighted.
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High-Throughput Genomic Data in Systematics and Phylogenetics
Vol. 44 (2013), pp. 99–121More LessHigh-throughput genomic sequencing is rapidly changing the field of phylogenetics by decreasing the cost and increasing the quantity and rate of data collection by several orders of magnitude. This deluge of data is exerting tremendous pressure on downstream data-analysis methods providing new opportunities for method development. In this review, we present (a) recent advances in laboratory methods for collection of high-throughput phylogenetic data and (b) challenges and constraints for phylogenetic analysis of these data. We compare the merits of multiple laboratory approaches, compare methods of data analysis, and offer recommendations for the most promising protocols and data-analysis workflows currently available for phylogenetics. We also discuss several strategies for increasing accuracy, with an emphasis on locus selection and proper model choice.
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Population Genomics of Human Adaptation
Vol. 44 (2013), pp. 123–143More LessRecent advances in genotyping technologies have facilitated genome-wide scans for natural selection. Detecting targets of natural selection sheds light on human evolution and it can help identify genetic variants that influence normal human phenotypic variation as well as disease susceptibility. Here we focus on studies of natural selection in modern humans who originated ∼200,000 years ago in Africa and migrated across the globe ∼50,000–100,000 years ago. Movement into new environments, as well as changes in culture and technology, including plant and animal domestication, resulted in local adaptation to diverse environments. We summarize statistical approaches for detecting targets of natural selection and for distinguishing the effects of demographic history from natural selection. On a genome-wide scale, immune-related genes are major targets of positive selection. Genes associated with reproduction and fertility also are fast evolving. Additional examples of recent human adaptation include genes associated with lactase persistence, eccrine glands, and response to hypoxia. Lastly, we emphasize the need to supplement scans of selection with functional studies to demonstrate the physiologic impact of candidate loci.
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Symbiogenesis: Mechanisms, Evolutionary Consequences, and Systematic Implications
Vol. 44 (2013), pp. 145–172More LessSymbiogenesis is the extremely rare, but permanent merger of two organisms from phylogenetically distant lineages into one radically more complex organism. Three examples are exceptionally important: intracellular enslavement by an early eukaryote of an α-proteobacterium by host protein insertion to make mitochondria; later conversion of a cyanobacterium into the first chloroplast, thereby forming kingdom Plantae; and secondary enslavement of a red alga to yield more complex membrane topology in the phagophototrophic kingdom Chromista. Two other cases involved independent acquisition of green-algal chloroplasts by ancestrally phagotrophic lineages, yielding chlorarachnean algae (phylum Cercozoa, within the chromist infrakingdom Rhizaria) and euglenophyte algae (phylum Euglenozoa, within the protozoan subkingdom Eozoa). Less radically, chloroplast replacement occurred within dinoflagellate Chromista by two symbiogeneses: Green-algal or haptophyte chloroplasts replaced ancestral peridinin-containing chloroplasts. These seven lineage mergers were all mediated by the evolution of novel modes of transmembrane protein import into the enslaved cell, allowing massive gene transfer from symbionts to host genomes.
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Cognitive Ecology of Food Hoarding: The Evolution of Spatial Memory and the Hippocampus
Vol. 44 (2013), pp. 173–193More LessMany animals cache food when it is abundant and later rely in part on spatial memory to retrieve those caches. The importance of memory for cache recovery and fitness in food-caching species has been hypothesized to result in selection favoring enhanced spatial memory and an enlarged hippocampus, an area of the brain involved in spatial memory. This review aims to provide an overview of research investigating adaptive variation in memory, the hippocampus, and food hoarding; to identify the pitfalls of previous approaches; and to provide suggestions for future directions. Given the relatively low phylogenetic diversity of scatter-hoarding taxa, we advocate using a single-species, multipopulation approach to track evolutionary changes related to dependence on food caching for survival as a function of differences in the environment. We conclude that existing evidence strongly supports the hypothesis that spatial memory and its underlying neural mechanisms respond to selection pressures associated with scatter-hoarding food.
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Genetic Draft, Selective Interference, and Population Genetics of Rapid Adaptation
Vol. 44 (2013), pp. 195–215More LessTo learn about the past from a sample of genomic sequences, one needs to understand how evolutionary processes shape genetic diversity. Most population genetics inferences are based on frameworks assuming that adaptive evolution is rare. But if positive selection operates on many loci simultaneously, as has recently been suggested for many species, including animals such as flies, then a different approach is necessary. In this review, I discuss recent progress in characterizing and understanding evolution in rapidly adapting populations, in which random associations of mutations with genetic backgrounds of different fitness, i.e., genetic draft, dominate over genetic drift. As a result, neutral genetic diversity depends weakly on population size but strongly on the rate of adaptation or more generally the variance in fitness. Coalescent processes with multiple mergers, rather than Kingman's coalescent, are appropriate genealogical models for rapidly adapting populations, with important implications for population genetics inference.
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Nothing in Genetics Makes Sense Except in Light of Genomic Conflict
Vol. 44 (2013), pp. 217–237More LessExamples of genomic conflict were apparent soon after the inception of the field of modern genetics. Despite these early discoveries, the relevance of genomic conflict to the core principles of genetics has been largely unappreciated. In this synthetic review I will describe why knowledge of the logic and diverse forms of genomic conflict is essential to understanding all subfields of genetics. Because there are so many ways in which some parts of all prokaryotic and eukaryotic genomes can evolve to gain a reproductive advantage at the expense of other parts, the prevalence of genomic conflict is universal, and it influences all aspects of genetic form and function.
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The Evolutionary Genomics of Birds
Vol. 44 (2013), pp. 239–259More LessRapidly accumulating genome sequence information in birds, which show several unique genomic features, provides novel insights into evolutionary genomics. The avian karyotype with numerous microchromosomes has remained stable during evolution, although frequent intrachromosomal inversions have occurred. Avian sex chromosome evolution, representing the best characterized ZW system to date, follows patterns seen in other organisms but has the notable exception of incomplete dosage compensation. Recombination is unevenly distributed in the avian genome; it occurs at very high rates in microchromosomes, a consequence of an obligate crossing over in even small chromosomes, and has highly elevated rates near chromosome ends. Moreover, a heterogeneous landscape of recombination feeds significant heterogeneity in base composition via GC-biased gene conversion. A uniform molecular clock is not applicable to birds, and ample evidence for substitution rate heterogeneity both among lineages and within genomes exists. Observed genome-wide levels of nucleotide diversity in birds are in the range of 10−2–10−3.
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Community and Ecosystem Responses to Elevational Gradients: Processes, Mechanisms, and Insights for Global Change
Vol. 44 (2013), pp. 261–280More LessCommunity structure and ecosystem processes often vary along elevational gradients. Their responses to elevation are commonly driven by changes in temperature, and many community- and ecosystem-level variables therefore frequently respond similarly to elevation across contrasting gradients. There are also many exceptions, sometimes because other factors such as precipitation can also vary with elevation. Given this complexity, our capacity to predict when and why the same variable responds differently among disparate elevational gradients is often limited. Furthermore, there is utility in using elevational gradients for understanding community and ecosystem responses to global climate change at much larger spatial and temporal scales than is possible through conventional ecological experiments. However, future studies that integrate elevational gradient approaches with experimental manipulations will provide powerful information that can improve predictions of climate change impacts within and across ecosystems.
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Cytonuclear Genomic Interactions and Hybrid Breakdown
Vol. 44 (2013), pp. 281–302More LessReduced fitness in interpopulation hybrids can be a first indication of genetic incompatibilities that may ultimately lead to reproductive isolation and speciation. A growing number of cases of hybrid breakdown have been traced to incompatibilities between the nuclear genome and the organellar genomes of the mitochondria and chloroplasts. Although these organellar genomes derive from ancient bacterial endosymbioses, they have been vastly reduced in size and now encode relatively few genes. The remaining genes are necessary but not sufficient for organelle function. In fact, most proteins functioning in the organelles are encoded in the nuclear genome and need to be imported after synthesis in the cytosol. The necessary interactions between organelle and nuclear genomes have resulted in some degree of coadaptation within all natural populations. Hybridization brings together previously untested allelic combinations and can disrupt intergenomic coadaptation, resulting in organelle dysfunction and, consequently, hybrid breakdown.
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How Was the Australian Flora Assembled Over the Last 65 Million Years? A Molecular Phylogenetic Perspective
Vol. 44 (2013), pp. 303–324More LessAustralia has a mostly dry, open, fire-shaped landscape of sclerophyllous and xeromorphic flora dominated by eucalypt and acacia trees, with diverse shrubs from a few families such as Myrtaceae, Proteaceae, and Fabaceae. Using molecular phylogenies to test hypotheses derived from the fossil record, we review the principal forces that transformed the ancestral Gondwanan rainforest through the Cenozoic. Today's vegetation is a mix of ancient radiations that have persisted in Australia through dramatic climate change since before the breakup of Gondwana, and more recent lineages whose ancestors arrived by trans-oceanic dispersal. Signatures in the fossil record of lineage turnover and trait evolutionary change are detected in phylogenies, but often at earlier dates. The Australian biota is a sample of the wider region, with extinction of some taxa and radiation of others (due to chance and opportunity), but biotic and abiotic interactions have resulted in a unique flora and fauna.
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Introgression of Crop Alleles into Wild or Weedy Populations
Vol. 44 (2013), pp. 325–345More LessThe evolutionary significance of introgression has been discussed for decades. Questions about potential impacts of transgene flow into wild and weedy populations brought renewed attention to the introgression of crop alleles into those populations. In the past two decades, the field has advanced with considerable descriptive, experimental, and theoretical activity on the dynamics of crop gene introgression and its consequences. As illustrated by five case studies employing an array of different approaches, introgression of crop alleles has occurred for a wide array of species, sometimes without significant consequence, but on occasion leading to the evolution of increased weediness. A new theoretical context has emerged for analyzing empirical data, identifying factors that influence introgression, and predicting introgression's progress. With emerging molecular techniques and analyses, research on crop allele introgression into wild and weedy populations is positioned to make contributions to both transgene risk assessment and reticulate evolution.
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Plant Facilitation and Phylogenetics
Vol. 44 (2013), pp. 347–366More LessThe relationship between facilitation and evolutionary ecology is poorly understood. We review five issues elucidating how the phylogenetic relatedness of species provides insight into the role of facilitation in community assembly: (a) Are the facilitative interactions more common between species that differ in a regeneration niche? (b) Are facilitative interactions more common between distantly related species? (c) Do communities governed by facilitation (rather than competition) have higher phylogenetic diversity? (d) As facilitated juvenile plants mature, do they compete with their nurses more often if they are closely related to them? (e) How does the phylogenetic signature in a community reveal ecological processes, such as succession, regeneration dynamics, indirect interactions, and coextinction cascades? The evolutionary history of lineages explains the regeneration niche of species, which ultimately determines the facilitation-competition balance and therefore community assembly and dynamics. We apply this framework to the conservation of biodiversity and propose future research avenues.
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Assisted Gene Flow to Facilitate Local Adaptation to Climate Change
Vol. 44 (2013), pp. 367–388More LessAssisted gene flow (AGF) between populations has the potential to mitigate maladaptation due to climate change. However, AGF may cause outbreeding depression (especially if source and recipient populations have been long isolated) and may disrupt local adaptation to nonclimatic factors. Selection should eliminate extrinsic outbreeding depression due to adaptive differences in large populations, and simulations suggest that, within a few generations, evolution should resolve mild intrinsic outbreeding depression due to epistasis. To weigh the risks of AGF against those of maladaptation due to climate change, we need to know the species' extent of local adaptation to climate and other environmental factors, as well as its pattern of gene flow. AGF should be a powerful tool for managing foundation and resource-producing species with large populations and broad ranges that show signs of historical adaptation to local climatic conditions.
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Ecological and Evolutionary Misadventures of Spartina
Vol. 44 (2013), pp. 389–410More LessSpartina species of the mid-low intertidal areas are powerful ecological engineers that are highly valued where they are native. Elsewhere, they overgrow native salt marsh and open intertidal mudflats, diminish biota, increase costs of managing wildlife, and interfere with human uses of estuaries. Huge efforts have been mounted to kill some populations of invading Spartina. All large Spartina invasions are by S. densiflora (2n = 7x = 70) or S. alterniflora (2n = 6x = 62) or hybrids between the hexaploid species (2n = 6x). Hybridization is a recurrent theme in Spartina; the allododecaploid S. anglica (2n = 12x = 120) and the hybrid swarm in San Francisco Bay arose through the introductions of S. alterniflora into the range of native Spartina species. The ancient hybrid S. densiflora also hybridized with native Spartina species. Hybridization promotes the evolution of highly invasive populations and hampers control efforts. Whether Spartina, native and not, would protect the shore as sea levels rise depends upon unimpeded areas for upward marsh growth and sufficient sediment, conditions that are often not satisfied.
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Evolutionary Processes of Diversification in a Model Island Archipelago
Vol. 44 (2013), pp. 411–435More LessLong celebrated for its spectacular landscapes and strikingly high levels of endemic biodiversity, the Philippines has been studied intensively by biogeographers for two centuries. Concentration of so many endemic land vertebrates into a small area and shared patterns of distribution in many unrelated forms has inspired a search for common mechanisms of production, partitioning, and maintenance of life in the archipelago. In this review, we (a) characterize an ongoing renaissance of species discovery, (b) discuss the changing way biogeographers conceive of the archipelago, (c) review the role molecular phylogenetic studies play in understanding the evolutionary history of Philippine vertebrates, and (d) describe how a 25-year Pleistocene island connectivity paradigm continues to provide some explanatory power, but has been augmented by increased understanding of the archipelago's geological history and ecological gradients. Finally, we (e) review new insights provided by studies of adaptive versus nonadaptive radiation and phylogenetic perspectives on community ecology.
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Perceptual Biases and Mate Choice
Vol. 44 (2013), pp. 437–459More LessOur view of the evolution of sexually selected traits and preferences was influenced radically in the 1990s by studies that emphasized how signals interact with sensory properties of receivers. Here, twenty-five years later, we review evidence that has accumulated in support of this idea. We replace the term sensory biases with perceptual biases to emphasize the growing knowledge of how cognitive processes generate selection on sexual traits. We show that mating preferences among conspecifics (e.g., sexual selection by mate choice) often are influenced by perceptual adaptations and constraints that have evolved in other contexts. We suggest that these perceptual biases need not be costly to females when they influence mate choice because in many cases they generate direct benefits. Although we do not reject a role for indirect benefits in mate choice, such as good genes, exclusive focus on eugenic mate choice limits our understanding of the evolution of the remarkable diversity of sexually selected traits.
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Thermal Ecology, Environments, Communities, and Global Change: Energy Intake and Expenditure in Endotherms
Vol. 44 (2013), pp. 461–480More LessTo survive, animals must maintain a balance between energy acquisition (foraging) and energy expenditure. This challenge is particularly great for endotherm vertebrates that require high amounts of energy to maintain homeothermy. Many of these endotherms use hibernation or daily torpor as a mechanism to reduce energy expenditure during anticipated or stochastic periods of stress. Although ecological researchers have focused extensively on energy acquisition, physiologists have largely studied thermal ecology and the mechanisms allowing endotherms to regulate energy expenditure, with little research explicitly linking ecology and thermal biology. Nevertheless, theoretical considerations and research conducted so far point to a significant ecological role for torpor in endotherms. Moreover, global-change challenges facing vertebrate endotherms are also considered in view of their ability to regulate their energy expenditure. We review the thermal ecology of endothermic vertebrates and some of its ecological and evolutionary implications.
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Diversity-Dependence, Ecological Speciation, and the Role of Competition in Macroevolution
Vol. 44 (2013), pp. 481–502More LessVariation in the rate of species diversification underlies many large-scale patterns in the organization of biological diversity. Here, I explore the phenomenon of diversity-dependent diversification and its contribution to differential species proliferation in time and space. Diversity-dependence can be a pattern of asymptotic diversity change through time as well as a process by which interspecific competition influences the dynamics of speciation and extinction. I review the evidence for diversity-dependence as revealed by phylogenies and fossils and discuss the close relationship between diversity-dependence and Darwin's proposed mechanism for the origin of species. An emerging body of research suggests that diversity-dependence contributes to the formation and persistence of incipient species and raises new questions about the meaning of ecological speciation. Diversity-dependence provides a conceptual framework for unifying biodiversity patterns across scales that vary by many orders of magnitude, from the dynamics of geographic range evolution to speciation and adaptive radiation.
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Consumer Fronts, Global Change, and Runaway Collapse in Ecosystems
Vol. 44 (2013), pp. 503–538More LessConsumer fronts occur when grazers or predators aggregate in bands along the edges of a resource. Our review reveals that consumer fronts are a common phenomenon in nature, occur in many different ecosystems, and are triggered by universal mechanisms: External forces locally increase top-down control beyond prey carrying and/or renewal capacity, and resource-dependent movement leads to consumer aggregation along the edge of the remaining prey population. Once formed, consumer fronts move through systems as spatially propagating waves, self-reinforced via intense overexploitation and amplified by density-dependent feedbacks. When consumer fronts are spatially restricted, they generate patchiness. In contrast, when consumer fronts are expansive, they can lead to runaway responses that cause large-scale ecosystem degradation and regime shifts. We conceptualize a synergistic stress hypothesis and model that highlight how coupled intensification of physical stress and enhanced consumer pressure can trigger increased occurrence of consumer fronts and decreased system stability and resilience. With escalating climate change and food-web modification, the physical and biological conditions favoring consumer-front formation will likely become a common feature of many ecosystems.
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Implications of Time-Averaged Death Assemblages for Ecology and Conservation Biology
Vol. 44 (2013), pp. 539–563More LessBiologists increasingly appreciate the importance of community-level attributes in the functioning and temporal turnover of ecosystems, but data other than species richness are difficult to acquire over the habitat-to-regional and decadal-to-millennial scales needed to recognize biodiversity change, discriminate between natural and anthropogenic drivers, and inform theoretical and applied ecology. Death assemblages (DAs)—the actively accumulating organic remains encountered in present-day seabeds and landscapes, as distinct from permanently buried fossil assemblages—are an underexploited source of historical information at precisely these scales. Meta-analyses, dynamic modeling, and individual case studies, particularly of mollusks and mammals, reveal that DAs differ from censused living assemblages (LAs) primarily because they are temporally coarse, time-averaged samples, contrary to concerns that postmortem bias dominates. Temporal pooling predictably damps the ability of DAs to detect small-scale variation, but promotes their ability to inventory rare species; estimate the abundance structure of the metacommunity; document range changes; evaluate historic habitat use; and identify now-absent species, community states, and anthropogenically shifted baselines.
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Population Cycles in Forest Lepidoptera Revisited
Vol. 44 (2013), pp. 565–592More LessA quarter century ago, the question was posed of whether a general hypothesis could explain population cycles of forest Lepidoptera. Since then, considerable progress has been made in elucidating mechanisms associated with cyclic dynamics of forest Lepidoptera. Delayed density-related parasitism and reduced fecundity during population peaks are common influences on population dynamics, although why fecundity declines is not understood. The hypothesis that sunspots explain cycles is rejected. The influences of delayed-induced plant defenses on populations are inconsistent, but interactions between plant chemistry, pathogens, and immunity remain rich areas for future study. Population dynamics of forest Lepidoptera can be synchronous over large geographic scales, and repeatable waves of spread of outbreaks occur for some species. Climate warming could modify species distributions and population cycles, but mechanisms have not been elucidated and changes in cyclic dynamics are not generally apparent. Integration of top-down and bottom-up influences on cyclic dynamics and quantification of dispersal are necessary for progress in understanding patterns of insect outbreaks.
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The Structure, Distribution, and Biomass of the World's Forests
Vol. 44 (2013), pp. 593–622More LessForests are the dominant terrestrial ecosystem on Earth. We review the environmental factors controlling their structure and global distribution and evaluate their current and future trajectory. Adaptations of trees to climate and resource gradients, coupled with disturbances and forest dynamics, create complex geographical patterns in forest assemblages and structures. These patterns are increasingly discernible through new satellite and airborne observation systems, improved forest inventories, and global ecosystem models. Forest biomass is a complex property affected by forest distribution, structure, and ecological processes. Since at least 1990, biomass density has consistently increased in global established forests, despite increasing mortality in some regions, suggesting that a global driver such as elevated CO2 may be enhancing biomass gains. Global forests have also apparently become more dynamic. Advanced information about the structure, distribution, and biomass of the world's forests provides critical ecological insights and opportunities for sustainable forest management and enhancing forest conservation and ecosystem services.
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The Epidemiology and Evolution of Symbionts with Mixed-Mode Transmission
Vol. 44 (2013), pp. 623–643More LessVertical and horizontal transmission are terms that describe the transfer of symbionts from parents to offspring and among unrelated hosts, respectively. Many symbionts, including parasites, pathogens, mutualists, and microbiota, use a combination of both strategies, known as mixed-mode transmission (MMT). Here I review what is known about the evolution, ecology, and epidemiology of symbionts with MMT and compare MMT with our expectations for single-mode strategies. Symbionts with MMT are common and, in comparison with single-mode symbionts, show many surprising features. MMT combines the best of two worlds with regard to the ecological conditions required for persistence and plays a role in the evolution of virulence and genome architecture. Even rare transmission by the minority type of these two transmission modes can make a big difference for the system. This review explores the conceptual issues surrounding the dynamics of mixed-mode symbionts by reviewing literature from the entire range of host and symbiont taxa.
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Previous Volumes
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Volume 54 (2023)
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Volume 53 (2022)
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Volume 52 (2021)
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Volume 51 (2020)
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Volume 50 (2019)
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Volume 49 (2018)
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Volume 48 (2017)
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Volume 47 (2016)
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Volume 46 (2015)
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Volume 45 (2014)
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Volume 44 (2013)
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Volume 43 (2012)
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Volume 42 (2011)
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Volume 41 (2010)
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Volume 40 (2009)
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Volume 39 (2008)
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Volume 38 (2007)
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Volume 37 (2006)
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Volume 36 (2005)
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Volume 35 (2004)
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Volume 34 (2003)
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Volume 33 (2002)
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Volume 32 (2001)
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Volume 31 (2000)
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Volume 30 (1999)
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Volume 29 (1998)
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Volume 28 (1997)
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Volume 27 (1996)
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Volume 26 (1995)
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Volume 25 (1994)
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Volume 24 (1993)
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Volume 23 (1992)
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Volume 22 (1991)
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Volume 21 (1990)
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Volume 20 (1989)
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Volume 19 (1988)
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Volume 18 (1987)
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Volume 17 (1986)
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Volume 16 (1985)
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Volume 15 (1984)
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Volume 14 (1983)
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Volume 13 (1982)
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Volume 12 (1981)
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Volume 11 (1980)
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Volume 10 (1979)
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Volume 9 (1978)
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Volume 8 (1977)
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Volume 7 (1976)
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Volume 6 (1975)
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Volume 5 (1974)
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Volume 4 (1973)
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Volume 3 (1972)
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Volume 2 (1971)
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Volume 1 (1970)
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Volume 0 (1932)