Annual Review of Ecology, Evolution, and Systematics - Volume 49, 2018

Behavioral changes, such as those involved in mating, foraging, and migration, can generate reproductive barriers between populations. Birds, in particular, are known for their great diversity in these behaviors, and so behavioral isolation is often proposed to be the major driver of speciation. Here, we review empirical evidence to evaluate the importance of behavioral isolation in the early stages of avian speciation. Experimentally measured mating preferences indicate that changes in mating behavior can result in premating barriers, with their strength depending on the extent of divergence in mating signals. Differences in migratory and foraging behavior also can play important roles in generating reproductive barriers in the early stages of speciation. However, because premating behavioral isolation is imperfect, extrinsic postzygotic barriers, in the form of selection against hybrids having intermediate phenotypes, also play an important role in avian diversification, especially in completing the speciation process.

We review the state of the art of alien plant research with emphasis on conceptual advances and knowledge gains on general patterns and drivers, biotic interactions, and evolution. Major advances include the identification of different invasion stages and invasiveness dimensions (geographic range, habitat specificity, local abundance) and the identification of appropriate comparators while accounting for propagule pressure and year of introduction. Developments in phylogenetic and functional trait research bear great promise for better understanding of the underlying mechanisms. Global patterns are emerging with propagule pressure, disturbance, increased resource availability, and climate matching as major invasion drivers, but species characteristics also play a role. Biotic interactions with resident communities shape invasion outcomes, with major roles for species diversity, enemies, novel weapons, and mutualists. Mounting evidence has been found for rapid evolution of invasive aliens and evolutionary responses of natives, but a mechanistic understanding requires tighter integration of molecular and phenotypic approaches. We hope the open questions identified in this review will stimulate further research on the ecology and evolution of alien plants.

Mesophotic coral reefs, currently defined as deep reefs between 30 and 150 m, are linked physically and biologically to their shallow water counterparts, have the potential to be refuges for shallow coral reef taxa such as coral and sponges, and might be a source of larvae that could contribute to the resiliency of shallow water reefs. Mesophotic coral reefs are found worldwide, but most are undescribed and understudied. Here, we review our current knowledge of mesophotic coral reefs and their functional ecology as it relates to their geomorphology, changes in the abiotic environment along depth gradients, trophic ecology, their reproduction, and their connectivity to shallow depths. Understanding the ecology of mesophotic coral reefs, and the connectivity between them and their shallow water counterparts, is now a primary focus for many reef studies as the worldwide degradation of shallow coral reefs, and the ecosystem services they provide, continues unabated.

Evolutionary conflict occurs when two parties can each affect a joint phenotype, but they gain from pushing it in opposite directions. Conflicts occur across many biological levels and domains but share many features. They are a major source of biological maladaptation. They affect biological diversity, often increasing it, at almost every level. Because opponents create selection that can be strong, persistent, and malevolent, conflict often leads to accelerated evolution and arms races. Conflicts might even drive the majority of adaptation, with pathogens leading the way as selective forces. The evolution of conflicts is complex, with outcomes determined partly by the relative evolvability of each party and partly by the kinds of power that each evolves. Power is a central issue in biology. In addition to physical strength and weapons, it includes strength from numbers and complexity; abilities to bind and block; advantageous timing; and abilities to acquire, use, and distort information.

Many fields of evolutionary biology now depend on stochastic mathematical models. These models are valuable for their ability to formalize predictions in the face of uncertainty and provide a quantitative framework for testing hypotheses. However, no mathematical model will fully capture biological complexity. Instead, these models attempt to capture the important features of biological systems using relatively simple mathematical principles. These simplifications can allow us to focus on differences that are meaningful, while ignoring those that are not. However, simplification also requires assumptions, and to the extent that these are wrong, so is our ability to predict or compare. Here, we discuss approaches for evaluating the performance of evolutionary models in light of their assumptions by comparing them against reality. We highlight general approaches, how they are applied, and remaining opportunities. Absolute tests of fit, even when not explicitly framed as such, are fundamental to progress in understanding evolution.

Ever since the first plant secondary metabolites (PSMs) were isolated and identified, questions about their ecological functions and diversity have been raised. Recent advances in analytical chemistry and complex data computation, as well as progress in chemical ecology from mechanistic to functional and evolutionary questions, open a new box of hypotheses. Addressing these hypotheses includes the measurement of complex traits, such as chemodiversity, in a context-dependent manner and allows for a deeper understanding of the multifunctionality and functional redundancy of PSMs. Here we review a hypothesis framework that addresses PSM diversity on multiple ecological levels (α, β, and γ chemodiversity), its variation in space and time, and the potential agents of natural selection. We use the concept of chemical information transfer as mediator of antagonistic and mutualistic interaction to interpret functional and microevolutionary studies and create a hypothesis framework for understanding chemodiversity as a factor driving ecological processes.

Function-valued traits—phenotypes whose expression depends on a continuous index (such as age, temperature, or space)—occur throughout biology and, like any trait, it is important to understand how they vary and evolve. Although methods for analyzing variation and evolution of function-valued traits are well developed, they have been underutilized by evolutionists, especially those who study natural populations. We seek to summarize advances in the study of function-valued traits and to make their analyses more approachable and accessible to biologists who could benefit greatly from their use. To that end, we explain how curve thinking benefits conceptual understanding and statistical analysis of functional data. We provide a detailed guide to the most flexible and statistically powerful methods and include worked examples (with R code) as supplemental material. We review ways to characterize variation in function-valued traits and analyze consequences for evolution, including constraint. We also discuss how selection on function-valued traits can be estimated and combined with estimates of heritable variation to project evolutionary dynamics.

Phenological mismatch results when interacting species change the timing of regularly repeated phases in their life cycles at different rates. We review whether this continuously ongoing phenomenon, also known as trophic asynchrony, is becoming more common under ongoing rapid climate change. In antagonistic trophic interactions, any mismatch will have negative impacts for only one of the species, whereas in mutualistic interactions, both partners are expected to suffer. Trophic mismatch is therefore expected to last for evolutionarily short periods, perhaps only a few seasons, adding to the difficulty of attributing it to climate change, which requires long-term data. So far, the prediction that diverging phenologies linked to climate change will cause mismatch is most clearly met in antagonistic interactions at high latitudes in the Artic. There is limited evidence of phenological mismatch in mutualistic interactions, possibly because of strong selection on mutualists to have co-adapted phenological strategies. The study of individual plasticity, population variation, and the genetic bases for phenological strategies is in its infancy. Recent work on woody plants revealed the large imprint of historic climate change on temperature, chilling, and day-length thresholds used by different species to synchronize their phenophases, which in the Northern Hemisphere has led to biogeographic phenological regions in which long-lived plants have adapted to particular interannual and intermillennial amplitudes of climate change.

Bivalve molluscs are abundant in marine and freshwater ecosystems and perform important ecological functions. Bivalves have epifaunal or infaunal lifestyles but are largely filter feeders that couple the water column and benthos. Bivalve ecology is a large field of study, but few comparisons among aquatic ecosystems or lifestyles have been conducted. Bivalves impact nutrient cycling, create and modify habitat, and affect food webs directly (i.e., prey) and indirectly (i.e., movement of nutrients and energy). Materials accumulated in soft tissue and shells are used as environmental monitors. Freshwater mussel and oyster aggregations in rivers and estuaries are hot spots for biodiversity and biogeochemical transformations. Historically, human use includes food, tools, currency, and ornamentation. Bivalves provide direct benefits to modern cultures as food, building materials, and jewelry and provide indirect benefits by stabilizing shorelines and mitigating nutrient pollution. Research on bivalve-mediated ecological processes is diverse, and future synthesis will require collaboration across conventional disciplinary boundaries.

The study of environmental DNA (eDNA) has the potential to revolutionize biodiversity science and conservation action by enabling the census of species on a global scale in near real time. To achieve this promise, technical challenges must be resolved. In this review, we explore the main uses of eDNA as well as the complexities introduced by its misuse. Current eDNA methods require refinement and improved calibration and validation along the entire workflow to lessen false positives/negatives. Moreover, there is great need for a better understanding of the “natural history” of eDNA—its origins, state, lifetime, and transportation—and for more detailed insights concerning the physical and ecological limitations of eDNA use. Although eDNA analysis can provide powerful information, particularly in freshwater and marine environments, its impact is likely to be less significant in terrestrial settings. The broad adoption of eDNA tools in conservation will largely depend on addressing current uncertainties in data interpretation.

This review of metapopulation biology has a special focus on Professor Ilkka Hanski's (1953–2016) research. Hanski made seminal contributions to both empirical and theoretical metapopulation biology throughout his scientific career. Hanski's early research focused on ecological aspects of metapopulation biology, in particular how the spatial structure of a landscape influences extinction thresholds and how habitat loss and fragmentation can result in extinction debt. Hanski then used the Glanville fritillary system as a natural laboratory within which he studied genetic and evolutionary processes, such as the influence of inbreeding on extinction risk and variation in selection for dispersal traits generated by landscape variation. During the last years of his career, Hanski's work was in the forefront of the rapidly developing field of eco-evolutionary dynamics. Hanski was a pioneer in showing how molecular-level underpinnings of trait variation can explain why evolutionary change can occur rapidly in natural populations and how these changes can subsequently influence ecological dynamics.

Duplication events are regarded as sources of evolutionary novelty, but our understanding of general trends for the long-term trajectory of additional genomic material is still lacking. Organisms with a history of whole genome duplication (WGD) offer a unique opportunity to study potential trends in the context of gene retention and/or loss, gene and network dosage, and changes in gene expression. In this review, we discuss the prevalence of polyploidy across the tree of life, followed by an overview of studies investigating genome evolution and gene expression. We then provide an overview of methods in network biology, phylogenomics, and population genomics that are critical for advancing our understanding of evolution post-WGD, highlighting the need for models that can accommodate polyploids. Finally, we close with a brief note on the importance of random processes in the evolution of polyploids with respect to neutral versus selective forces, ancestral polymorphisms, and the formation of autopolyploids versus allopolyploids.

The Arctic may seem remote, but the unprecedented environmental changes occurring there have important consequences for global society. Of all Arctic system components, changes in permafrost (perennially frozen ground) are one of the least documented. Permafrost is degrading as a result of climate warming, and evidence is mounting that changing permafrost will have significant impacts within and outside the region. This review asks: What are key structural and functional properties of ecosystems that interact with changing permafrost, and how do these ecosystem changes affect local and global society? Here, we look beyond the classic definition of permafrost to include a broadened focus on the composition of frozen ground, including the ice and the soil organic carbon content, and how it is changing. This ecological perspective of permafrost serves to identify areas of both vulnerability and resilience as climate, ecological disturbance regimes, and the human footprint all continue to change in this sensitive and critical region of Earth.

Parallel evolution across replicate populations has provided evolutionary biologists with iconic examples of adaptation. When multiple populations colonize seemingly similar habitats, they may evolve similar genes, traits, or functions. Yet, replicated evolution in nature or in the laboratory often yields inconsistent outcomes: Some replicate populations evolve along highly similar trajectories, whereas other replicate populations evolve to different extents or in distinct directions. To understand these heterogeneous outcomes, biologists are increasingly treating parallel evolution not as a binary phenomenon but rather as a quantitative continuum ranging from parallel to nonparallel. By measuring replicate populations’ positions along this (non)parallel continuum, we can test hypotheses about evolutionary and ecological factors that influence the extent of repeatable evolution. We review evidence regarding the manifestation of (non)parallel evolution in the laboratory, in natural populations, and in applied contexts such as cancer. We enumerate the many genetic, ecological, and evolutionary processes that contribute to variation in the extent of parallel evolution.

Adaptive phenotypic plasticity provides a mechanism of developmental rescue in novel and rapidly changing environments. Understanding the underlying mechanism of plasticity is important for predicting both the likelihood that a developmental response is adaptive and associated life-history trade-offs that could influence patterns of subsequent evolutionary rescue. Although evolved developmental switches may move organisms toward a new adaptive peak in a novel environment, such mechanisms often result in maladaptive responses. The induction of generalized physiological mechanisms in new environments is relatively more likely to result in adaptive responses to factors such as novel toxins, heat stress, or pathogens. Developmental selection forms of plasticity, which rely on within-individual selective processes, such as shaping of tissue architecture, trial-and-error learning, or acquired immunity, are particularly likely to result in adaptive plasticity in a novel environment. However, both the induction of plastic responses and the ability to be plastic through developmental selection come with significant costs, resulting in delays in reproduction, increased individual investment, and reduced fecundity. Thus, we might expect complex interactions between plastic responses that allow survival in novel environments and subsequent evolutionary responses at the population level.

Antarctica is enormous, cold, remote, and particularly sensitive to climate change. Most biological research below 60°S has focused on the isolated nature of the biota and how organisms have adapted to the cold and ice. However, biogeographic patterns in Antarctica and the Southern Ocean, and the processes explaining how those patterns came about, still await adequate explanation. Both terrestrial and marine organisms have been influenced by climatic change (e.g., glaciation), physical phenomena (e.g., oceanic currents), and/or potential barriers to gene flow (e.g., steep thermal gradients). Whereas the Antarctic region contains diverse and complex marine communities, terrestrial systems tend to be comparatively simple with limited diversity. Here, we challenge the current dogma used to explain the diversity and biogeographic patterns present in the Antarctic. We assert that relatively modern processes within the last few million years, rather than geo-logical events that occurred in the Eocene and Miocene, account for present patterns of biodiversity in the region. Additionally, reproductive life history stages appear to have little influence in structuring genetic patterns in the Antarctic, as currents and glacial patterns are noted to be more important drivers of organismal patterns of distribution. Finally, we highlight the need for additional sampling, high-throughput genomic approaches, and broad, multinational cooperation for addressing outstanding questions of Antarctic biogeography and biodiversity.

Dinosaurs were large-bodied land animals of the Mesozoic that gave rise to birds. They played a fundamental role in structuring Jurassic–Cretaceous ecosystems and had physiology, growth, and reproductive biology unlike those of extant animals. These features have made them targets of theoretical macroecology. Dinosaurs achieved substantial structural diversity, and their fossil record documents the evolutionary assembly of the avian body plan. Phylogeny-based research has allowed new insights into dinosaur macroevolution, including the adaptive landscape of their body size evolution, patterns of species diversification, and the origins of birds and bird-like traits. Nevertheless, much remains unknown due to incompleteness of the fossil record at both local and global scales. This presents major challenges at the frontier of paleobiological research regarding tests of macroecological hypotheses and the effects of dinosaur biology, ecology, and life history on their macroevolution.

Throughout Earth's history, drought has been a common crisis in terrestrial ecosystems; in human societies, it can cause famine, one of the Four Horsemen of the apocalypse. As the global hydrological cycle intensifies with global warming, deeper droughts and rewetting will alter, and possibly transform, ecosystems. Soil communities, however, seem more tolerant than plants or animals are to water stress—the main effects, in fact, on soil processes appear to be limited diffusion and the limited supply of resources to soil organisms. Thus, the rains that end a drought not only release soil microbes from stress but also create a resource pulse that fuels soil microbial activity. It remains unclear whether the effects of drought on soil processes result from drying or rewetting. It is also unclear whether the flush of activity on rewetting is driven by microbial growth or by the physical/chemical processes that mobilize organic matter. In this review, I discuss how soil water, and the lack of it, regulates microbial life and biogeochemical processes. I first focus on organismal-level responses and then consider how these influence whole-soil organic matter dynamics. A final focus is on how to incorporate these effects into Earth System models that can effectively capture dry–wet cycling.

Genome sequence data are now being routinely obtained from many nonmodel organisms. These data contain a wealth of information about the demographic history of the populations from which they originate. Many sophisticated statistical inference procedures have been developed to infer the demographic history of populations from this type of genomic data. In this review, we discuss the different statistical methods available for inference of demography, providing an overview of the underlying theory and logic behind each approach. We also discuss the types of data required and the pros and cons of each method. We then discuss how these methods have been applied to a variety of nonmodel organisms. We conclude by presenting some recommendations for researchers looking to use genomic data to infer demographic history.