Annual Review of Ecology, Evolution, and Systematics - Volume 53, 2022

The ability to reproduce is the key trait that distinguishes living organisms from inorganic matter, and the strategies used to achieve successful reproduction are almost as diverse as the organisms themselves. In animals, the most widespread form of reproduction involves separate male and female sexes: Each sex produces haploid gametes via meiosis, and two gametes fuse to form a new diploid organism. In some cases, both parents contribute equally to the nuclear and cytoplasmic genomes of their offspring. However, such fully symmetric reproduction of both parents represents the extreme end of a continuum toward complete asymmetry, where offspring inherit their nuclear and cytoplasmic genomes from only one of the two parents. Asymmetries also occur with respect to the fate of maternally and paternally inherited genomes and which sex is affected by non-Mendelian inheritance. In this review, we describe the diversity of animal reproductive systems along different axes with a symmetry–asymmetry continuum and suggest evolutionary routes that may have led to increased levels of asymmetry.

We consider the mechanistic basis and functional significance of the pervasive influence of parasitic plants on productivity and diversity, synthesizing recent findings on their responses to drought, heat waves, and fire. Although parasites represent just 1% of all angiosperms, the ecophysiological traits associated with parasitism confer pronounced impacts on their hosts and disproportionate influence upon community structure, composition, and broader ecosystem function. New insights into the roles of their pollinators, seed dispersers, and litter-dependent detritivores have advanced our understanding of how parasitic plants modulate animal communities via their extended and complementary phenology. Direct and indirect impacts of climate change on parasitic plants and their ecological roles are already apparent. Trade-offs between maximizing efficiency at obtaining water from hosts and sensitivity to water stress underlie range shifts and host switching of parasitic plants and increased reliance on these plants by animal communities for food and shelter.

Parasite avoidance is a host defense that reduces an individual's contact rate with parasites. We investigate avoidance as a primary driver of variation among individuals in their risk of parasitism and the evolution of host–parasite interactions. To bridge mechanistic and taxonomic divides, we define and categorize avoidance by its function and position in the sequence of host defenses. We also examine the role of avoidance in limiting epidemics and evaluate evidence for the processes that drive its evolution. Throughout, we highlight important directions in which to advance our conceptual and theoretical understanding of the role of avoidance in host–parasite interactions. We emphasize the need to test assumptions and quantify the effect of avoidance independent of other defenses. Importantly, many open questions may be most tractable in host systems that have not been the focus of traditional behavioral avoidance research, such as plants and invertebrates.

Fungi play key roles in ecosystems and human societies as decomposers, nutrient cyclers, mutualists, and pathogens. Estimates suggest that roughly 3–13 million fungal species exist worldwide, yet considerable knowledge gaps exist regarding the mechanisms and consequences, both ecological and social, of fungal dispersal from local to global scales. In this review, we summarize concepts underlying fungal dispersal, review recent research, and explore how fungi possess unique characteristics that can broaden our understanding of general dispersal ecology. We highlight emerging frontiers in fungal dispersal research that integrate technological advances with trait-based ecology, movement ecology, social–ecological systems, and work in unexplored environments. Outstanding research questions across these themes are presented to stimulate theoretical and empirical research in fungal dispersal ecology. Advances in fungal dispersal will improve our understanding of fungal community assembly and biogeography across a range of spatial scales, with implications for ecosystem functioning, global food security, and human health.

Divergent selection across the landscape can favor the evolution of local adaptation in populations experiencing contrasting conditions. Local adaptation is widely observed in a diversity of taxa, yet we have a surprisingly limited understanding of the mechanisms that give rise to it. For instance, few have experimentally confirmed the biotic and abiotic variables that promote local adaptation, and fewer yet have identified the phenotypic targets of selection that mediate local adaptation. Here, we highlight critical gaps in our understanding of the process of local adaptation and discuss insights emerging from in-depth investigations of the agents of selection that drive local adaptation, the phenotypes they target, and the genetic basis of these phenotypes. We review historical and contemporary methods for assessing local adaptation, explore whether local adaptation manifests differently across life history, and evaluate constraints on local adaptation.

Complex statistical methods are continuously developed across the fields of ecology, evolution, and systematics (EES). These fields, however, lack standardized principles for evaluating methods, which has led to high variability in the rigor with which methods are tested, a lack of clarity regarding their limitations, and the potential for misapplication. In this review, we illustrate the common pitfalls of method evaluations in EES, the advantages of testing methods with simulated data, and best practices for method evaluations. We highlight the difference between method evaluation and validation and review how simulations, when appropriately designed, can refine the domain in which a method can be reliably applied. We also discuss the strengths and limitations of different evaluation metrics. The potential for misapplication of methods would be greatly reduced if funding agencies, reviewers, and journals required principled method evaluation.

There is a widespread view that the process of adaptation in complex systems is made difficult due to an evolutionary cost of complexity that is reflected in lower evolvability. This line of reasoning suggests that organisms must have special properties to overcome this cost, such as integration, modularity, and robustness, and that the reduction in the rate of evolution and variational constraints could help explain why organisms might not respond to selection. Here, we discuss the issues that arise from this conviction and highlight an alternative view where complexity represents an opportunity by increasing the evolutionary potential of a population. We highlight the lack of evidence supporting the influence of complexity on evolvability. Empirical data on the patterns of contemporary selection are critical for understanding this relationship.

The study of individual behavioral variation, sometimes called animal personalities or behavioral types, is now a well-established area of research in behavioral ecology and evolution. Considerable theoretical work has developed predictions about its ecological and evolutionary causes and consequences, and studies testing these theories continue to grow. Here, we synthesize the current empirical work to shed light on which theories are well supported and which need further refinement. We find that the major frameworks explaining the existence of individual behavioral variation, the pace-of-life syndrome hypothesis and state-dependent feedbacks models, have mixed support. The consequences of individual behavioral variation are well studied at the individual level but less is known about consequences at higher levels such as among species and communities. The focus of this review is to reevaluate and reestablish the foundation of individual behavioral variation research: What do we know? What questions remain? And where are we going next?

We review transitions between hermaphroditism and dioecy in animals and (mainly flowering) plants. Although hermaphroditism and dioecy represent two end states in a sex-allocation continuum, both vary in major ways among clades. However, drawing on sex-allocation theory and distinguishing between self-fertilization and outcrossing, we recognize five broad paths to dioecy and two broad paths to hermaphroditism. Which path is taken likely depends on the starting state (especially in terms of the mating system), as well as the ecological setting or genetic context of the transition. Androdioecy may have been more important in some transitions to dioecy than current theory would suggest, and gynodioecy may often be an evolutionary end point in itself rather than a step between hermaphroditism and dioecy. Transitions between environmental and genetic sex determination may also play an important role in sexual-system evolution. Further theory is required to address these possibilities. Detailed empirical work is also greatly needed, especially in animal clades that vary in their sexual system.

Fire has been an ecosystem process since plants colonized land over 400 million years ago. Many diverse traits provide a fitness benefit following fires, and these adaptive traits vary with the fire regime. Some of these traits enhance fire survival, while others promote recruitment in the postfire environment. Demonstrating that these traits are fire adaptations is challenging, since many arose early in the paleontological record, although increasingly better fossil records and phylogenetic analysis make timing of these trait origins to fire more certain. Resprouting from the base of stems is the most widely distributed fire-adaptive trait, and it is likely to have evolved under a diversity of disturbance types. The origins of other traits like serotiny, thick bark, fire-stimulated germination, and postfire flowering are more tightly linked to fire. Fire-adaptive traits occur in many environments: boreal and temperate forests, Mediterranean-type climate (MTC) shrublands, savannas, and other grasslands. MTC ecosystems are distinct in that many taxa in different regions have lost the resprouting ability and depend solely on postfire recruitment for postfire recovery. This obligate seeding mode is perhaps the most vulnerable fire-adaptive syndrome in the face of current global change, particularly in light of increasing anthropogenic fire frequency.

Chaos was proposed in the 1970s as an alternative explanation for apparently noisy fluctuations in population size. Although readily demonstrated in models, the search for chaos in nature proved challenging and led many to conclude that chaos is either rare or nigh impossible to detect. However, in the intervening half-century, it has become clear that ecosystems are replete with the enabling conditions for chaos. Chaos has been repeatedly demonstrated under laboratory conditions and has been found in field data using updated detection methods. Together, these developments indicate that the apparent rarity of chaos was an artifact of data limitations and overreliance on low-dimensional population models. We invite readers to reevaluate the relevance of chaos in ecology, and we suggest that chaos is not as rare or undetectable as previously believed.

Over the past decade, a new set of methods for estimating dated trees has emerged. Originally referred to as the fossilized birth–death (FBD) process, this single model has expanded to a family of models that allows researchers to coestimate evolutionary parameters (e.g., diversification, sampling) and patterns alongside divergence times for a variety of applications from paleobiology to real-time epidemiology. We provide an overview of this family of models. We explore the ways in which these models correspond to methods in quantitative paleobiology, as the FBD process provides a framework through which neontological and paleontological approaches to phylogenetics and macroevolution can be unified. We also provide an overview of challenges associated with applying FBD models, particularly with an eye toward the fossil record. We conclude this review by discussing several exciting avenues for the inclusion of fossil data in phylogenetic analyses.

Myriad branches in the tree of life are intertwined through ecological relationships. Biologists have long hypothesized that intimate symbioses between lineages can influence diversification patterns to the extent that it leaves a topological imprint on the phylogenetic trees of interacting clades. Over the past few decades, cophylogenetic methods development has provided a toolkit for identifying such histories of codiversification, yet it is often difficult to determine which tools best suit the task at hand. In this review, we organize currently available cophylogenetic methods into three categories—pattern-based statistics, event-scoring methods, and more recently developed generative model–based methods—and discuss their assumptions and appropriateness for different types of cophylogenetic questions. We classify cophylogenetic systems based on their biological properties to provide a framework for empiricists investigating the macroevolution of symbioses. In addition, we provide recommendations for the next generation of cophylogenetic models that we hope will facilitate further methods development.

The finding that adaptive evolution can often be substantial enough to alter ecological dynamics challenges traditional views of community ecology that ignore evolution. Here, we propose that evolution might commonly alter both local and regional processes of community assembly. We show how adaptation can substantially affect community assembly and that these effects depend on regional (metacommunity) factors, including environmental heterogeneity and its spatial structure. In particular, early colonists can often arrive from a nearby community, adapt to local conditions, and subsequently alter the establishment or abundance of late-arriving species, often producing an evolutionary priority effect. We also discuss how interaction type and relative rates of colonization, evolution, and community interactions determine divergent community outcomes. We describe new conceptual approaches that provide insights into these dynamics and statistical methods that can better evaluate their importance. Overall, we demonstrate that accounting for adaptation during community assembly opens up novel ways for making progress on fundamental questions in community ecology.

Long-term studies of individuals enable incisive investigations of questions across ecology and evolution. Here, we illustrate this claim by reference to our long-term study of red deer on the Isle of Rum, Scotland. This project has established many of the characteristics of social organization, selection, and population ecology typical of large, polygynous, seasonally breeding mammals, with wider implications for our understanding of sexual selection and the evolution of sex differences, as well as for their population dynamics and population management. As molecular genetic techniques have developed, the project has pivoted to investigate evolutionary genetic questions, also breaking new ground in this field. With ongoing advances in genomics and statistical approaches and the development of increasingly sophisticated ways to assay new phenotypic traits, the questions that long-term studies such as the red deer study can answer become both broader and ever more sophisticated. They also offer powerful means of understanding the effects of ongoing climate change on wild populations.

Bony fishes are the principal group of backboned animals in contemporary aquatic settings. Extant species are the focus of a vigorous program of macroevolutionary research, but paleontology offers important perspectives. Multiple fossil records bear on the evolution of bony fishes, each with its own strengths and weaknesses. Understanding of the interrelationships among living bony fishes has improved substantially in recent years, but confidence in the phylogenetic placement of fossils is highly variable. This reflects limitations in current understanding of both fossil anatomy and hard-tissue characters for extant clades. Patterns of taxonomic and morphological diversity over bony fish history remain incompletely known, with most studies restricted to particular clades or specific intervals of time. The wealth of anatomical data recorded by the fossil record could make an important addition to a growing body of work examining phenotypic evolution across living species, but incorporating this information requires the placement of fossils within phylogenetic trees.

The interactions between ants and certain sap-feeding insects in the order Hemiptera are classic examples of food-for-protection mutualisms. In these associations, herbivorous hemipterans use a highly specialized, straw-like mouthpart to consume sap directly from plant phloem and xylem and, as a result, excrete a sugar-rich waste product called honeydew. Ant foragers use specialized adaptations to collect and share honeydew with nestmates and, in exchange, protect hemipterans against predators. The two key innovations underlying this interaction—hemipteran sap feeding and ant harvesting of honeydew—have driven the evolutionary success and ecological dominance of ants. These interactions also carry unique costs and benefits for each partner and are highly context dependent. Understanding the factors mediating this mutualism is critical, as these interactions have broader ecological consequences for the natural and agricultural ecosystems in which they are embedded.

We are facing interwoven global threats to public health and ecosystem function that reveal the intrinsic connections between human and wildlife health. These challenges are especially pressing in cities, where social-ecological interactions are pronounced. The One Health concept provides an organizing framework that promotes the health and well-being of urban communities and ecosystems. However, for One Health to be successful, it must incorporate societal inequities in environmental disamenities, exposures, and policy. Such inequities affect all One Health interfaces, including the distribution of ecosystem services and disservices, the nature and frequency ofhuman–wildlife interactions, and legacies of land use. Here, we review the current literature on One Health perspectives, pinpoint areas in which to incorporate an environmental justice lens, and close with recommendations for future work. Intensifying social, political, and environmental unrest underscores a dire need for One Health solutions informed by environmental justice principles to help build healthier, more resilient cities.

Freshwater fish have been widely introduced worldwide, and freshwater ecosystems are among those most affected by biological invasions. Consequently, freshwater fish invasions are one of the most documented invasions among animal taxa, with much information available about invasive species, their characteristics, invaded regions, invasion pathways, impacts, and management. While existing reviews address specific aspects of freshwater fish invasions, there is still a gaping lack of comprehensive assessments of freshwater fish invasions that simultaneously address pivotal and connected elements of the invasion process. Here, we provide a holistic review, together with quantitative assessments, divided into four major parts: (a) introduction pathways, (b) characteristics of nonnative species andinvaded ecosystems that explain successful invasion processes, (c) invasion impacts and their mechanisms, and (d) management. We highlight data gaps and biases in the current databases and highlight a basic lack of understanding of several aspects of freshwater fish invasions. In addition, we provide recommendations for future studies.

Epistasis occurs when the effect of a mutation depends on its carrier's genetic background. Despite increasing evidence that epistasis for fitness is common, its role during evolution is contentious. Fitness landscapes, which are mappings of genotype or phenotype to fitness, capture the full extent and complexity of epistasis. Fitness landscape theory has shown how epistasis affects the course and the outcome of evolution. Moreover, by measuring the competitive fitness of sets of tens to thousands of connected genotypes, empirical fitness landscapes have shown that epistasis is frequent and depends on the fitness measure, the choice of mutations for the landscape, and the environment in which it was measured. In this article, I review fitness landscape theory and experiments and their implications for the role of epistasis in adaptation. I discuss theoretical expectations in the light of empirical fitness landscapes and highlight open challenges and future directions toward integrating theory and data and incorporating ecological factors.