Annual Review of Ecology, Evolution, and Systematics - Volume 47, 2016

The surface of plant leaves, or the phyllosphere, harbors hyperdiverse microbial communities. These communities mediate foliar functional traits, influence plant fitness, and contribute to several ecosystem functions, including nutrient and water cycling. In this review, we briefly recall the history of phyllosphere research and present the features of this microbial habitat. Adopting a recent framework for evolutionary community ecology, we then review evidence for each of the four major processes shaping phyllosphere microbial communities: dispersal, evolutionary diversification, selection, and drift. We show how these processes are influenced by the host plant, the surrounding atmospheric conditions, and microbial interactions. Rapidly growing evidence indicates that phyllosphere microbial communities are altered by global change, with potential cascading effects on plant performance, plant evolution, and ecosystem functioning. We propose future avenues for phyllosphere research aimed at improving plant adaptation and ecosystem resilience to environmental changes.

Cancer biology can be better understood by drawing upon methods and concepts from evolutionary genetics. Cancer progression proceeds through somatic evolution, being driven by selection on clonal lineages via the differential survival and proliferation of cell lines. This within-patient evolution can be modeled and analyzed using population genetic and phylogenetic tools to identify mutations and genotypes that are under directional selection during tumor growth, spatial differentiation, and metastasis. Evolutionary genetics can also explain the persistence of cancer within populations. A minority of cancers are associated with inherited risk alleles, which are maintained in populations through genetic drift or antagonistic pleiotropy. Finally, cancer biology can be understood from a macroevolutionary perspective as a case study of evolutionary cooperation and conflict between different levels of biological organization.

Bottlenecks in population size can reduce fitness and evolutionary potential, yet introduced species often become invasive. This poses a dilemma referred to as the genetic paradox of invasion. Three characteristics must hold true for an introduced population to be considered paradoxical in this sense. First, it must pass through a bottleneck that reduces genetic variation. Second, despite the bottleneck, the introduced population must not succumb to the many problems associated with low genetic variation. Third, it must adapt to the novel environment. Some introduced populations are not paradoxical as they do not combine these conditions. In some cases, an apparent paradox is spurious, as seen in introduced populations with low diversity in neutral markers that maintain high genetic variation in ecologically relevant traits. Even when the genetic paradox is genuine, unique aspects of a species' biology can allow a population to thrive. We propose research directions into remaining paradoxical aspects of invasion genetics.

The dog is our oldest domesticate and has experienced a wide variety of demographic histories, including a bottleneck associated with domestication and individual bottlenecks associated with the formation of modern breeds. Admixture with gray wolves, and among dog breeds and populations, has also occurred throughout its history. Likewise, the intensity and focus of selection have varied, from an initial focus on traits enhancing cohabitation with humans, to more directed selection on specific phenotypic characteristics and behaviors. In this review, we summarize and synthesize genetic findings from genome-wide and complete genome studies that document the genomic consequences of demography and selection, including the effects on adaptive and deleterious variation. Consistent with the evolutionary history of the dog, signals of natural and artificial selection are evident in the dog genome. However, conclusions from studies of positive selection are fraught with the problem of false positives given that demographic history is often not taken into account.

Forests regulate climate at local, regional, and global scales through exchanges of momentum, energy, moisture, and chemicals with the atmosphere. The notion that forests affect climate is not new. A vigorous debate about deforestation, land use, and climate change occurred during the colonial settlement of North America and continued through the 1800s, but the arguments of conservationists and foresters for forest–climate influences were dismissed by meteorologists. Modern climate science shows that forests warm climate annually by decreasing surface albedo, cool climate through surface roughness and evapotranspiration and by storing carbon, and have additional effects through atmospheric chemistry. Land use is a key aspect of climate policy, but we lack comprehensive policy recommendations. Like our predecessors, we are seeking a deeper understanding of Earth's climate, its ecosystems, and our uses of those ecosystems, and just as importantly we are still searching for the right interdisciplinary framework in which to find those answers.

Nonmarine molluscs are the major animal group with the greatest number of recorded extinctions due to anthropogenic impacts, and that number is certainly a serious underestimate. Land snails, particularly endemic land snails of oceanic islands, are the group of molluscs that have sustained the most extinctions. Understanding their ecology and the evolutionary processes that have led to their extreme vulnerability is crucial if we are to be able to conserve these diverse and important species. Oceanic island snails tend to have low α-diversity and high β-diversity, and divergence of habitat use among related species is known to occur in some radiations of land snails on oceanic islands. Processes of speciation and ecological interaction are possible major drivers of these patterns. The ecological opportunities available at the initial stage of insular evolution and the scarcity of effective predators may have led to divergence of habitat use and high β-diversity in oceanic island snails. Fewer and less diverse predators on oceanic islands lead to the evolution of fewer and less diverse defense traits in oceanic island snails, which results in their high vulnerability to non-native predators. High β-diversity of oceanic island snails also results in great vulnerability to habitat loss. Accordingly, the high susceptibility of oceanic island snails to extinction reflects their evolutionary history.

The niche is generally viewed in terms of species' intrinsic physiological potential and limitations due to competition. Although DNA sequencing has revealed the ubiquity of beneficial microbial symbioses, the role of mutualisms in shaping species niches is not broadly recognized. In this review, I use a widespread terrestrial mutualism, the ectomycorrhizal symbiosis, to help develop the mutualistic niche concept. Using contemporary niche theory, I show how mycorrhizal symbioses expand environmental ranges (requirement niche) and influence resource use (impact niche) for both plants and fungi. Simple niche models for competition between resource specialists and generalists also predict a range of ecological phenomena, from unexpected monodominance by some tropical trees to the functional biogeography of mycorrhizal symbiosis. A niche-based view of mutualism may also help explain stability of mutualisms even in the absence of clear benefits. The niche is a central concept in ecology, and better integration of mutualism will more accurately reflect the positive interactions experienced by nearly all species.

Understanding the processes that generate and maintain genetic variation within populations is a central goal in evolutionary biology. Theory predicts that some of this variation is maintained as a consequence of adapting to variable habitats. Studies in herbivorous insects have played a key role in confirming this prediction. Here, we highlight theoretical and conceptual models for the maintenance of genetic diversity in herbivorous insects, empirical genomic studies testing these models, and pressing questions within the realm of evolutionary and functional genomic studies. To address key gaps, we propose an integrative approach combining population genomic scans for adaptation, genome-wide characterization of targets of selection through experimental manipulations, mapping the genetic architecture of traits influencing fitness, and functional studies. We also stress the importance of studying the maintenance of genetic variation across biological scales—from variation within populations to divergence among populations—to form a comprehensive view of adaptation in herbivorous insects.

With proliferation of molecular phylogenies and advances in statistical modeling, phylogeneticists can now address macroevolutionary questions that had traditionally been the purview of paleontology. Interest has focused on three areas at the intersection of phylogenetic and paleontological research: time-scaling phylogenies, understanding trait evolution, and modeling species diversification. Fossil calibrations have long been crucial for scaling phylogenies to absolute time, but recent advances allow more equal integration of extinct taxa. Simulation and empirical studies have shown that fossil data can markedly improve inferences about trait evolution, especially for models with heterogeneous temporal dynamics and in clades for which the living forms are unrepresentative remnants of their larger clade. Recent years have also seen a productive cross-disciplinary conversation about the nature and uncertainties of inferring diversification dynamics. Challenges remain, but the present time represents a flowering of interest in integrating these two views on the history of life.

Understanding how drylands respond to ongoing environmental change is extremely important for global sustainability. In this review, we discuss how biotic attributes, climate, grazing pressure, land cover change, and nitrogen deposition affect the functioning of drylands at multiple spatial scales. Our synthesis highlights the importance of biotic attributes (e.g., species richness) in maintaining fundamental ecosystem processes such as primary productivity, illustrates how nitrogen deposition and grazing pressure are impacting ecosystem functioning in drylands worldwide, and highlights the importance of the traits of woody species as drivers of their expansion in former grasslands. We also emphasize the role of attributes such as species richness and abundance in controlling the responses of ecosystem functioning to climate change. This knowledge is essential to guide conservation and restoration efforts in drylands, as biotic attributes can be actively managed at the local scale to increase ecosystem resilience to global change.

Hydrogen sulfide (H2S) is a respiratory toxicant that creates extreme environments tolerated by few organisms. H2S is also produced endogenously by metazoans and plays a role in cell signaling. The mechanisms of H2S toxicity and its physiological functions serve as a basis to discuss the multifarious strategies that allow animals to survive in H2S-rich environments. Despite their toxicity, H2S-rich environments also provide ecological opportunities, and complex selective regimes of covarying abiotic and biotic factors drive trait evolution in organisms inhabiting H2S-rich environments. Furthermore, adaptation to H2S-rich environments can drive speciation, giving rise to biodiversity hot spots with high levels of endemism in deep-sea hydrothermal vents, cold seeps, and freshwater sulfide springs. The diversity of H2S-rich environments and their inhabitants provides ideal systems for comparative studies of the effects of a clear-cut source of selection across vast geographic and phylogenetic scales, ultimately informing our understanding of how environmental stressors affect ecological and evolutionary processes.

During the past 100 years, studies spanning thousands of taxa across almost all biomes have demonstrated that competition has powerful negative effects on the performance of individuals and can affect the composition of plant communities, the evolution of traits, and the functioning of whole ecosystems. In this review, we highlight new and important developments that have the potential to greatly improve our understanding of how plants compete and the consequences of competition from individuals to communities in the following major areas of research: (a) mechanisms of competition, (b) competitive effect and response, (c) direct and indirect effects of competition, (d) population-level effects of competition, (e) biogeographical differences in competition, and (f) conditionality of competition. Ecologists have discovered much about competition, but the mechanisms of competition and how competition affects the organization of communities in nature still require both theoretical and empirical exploration.

Infectious diseases dynamics are affected by both spatial and temporal heterogeneity in their environments. Our ability to quantify and predict how this heterogeneity impacts risks of infection and disease emergence is the key to successful disease prevention efforts. Here, we review the literature on infectious diseases from human, agricultural, and wildlife ecosystems to describe the rapid ecological and evolutionary responses in pathogens to environmental heterogeneity, with expected impacts on their epidemiology. To date, the underlying network structures through which disease transmission proceeds have been notoriously difficult to quantify because of this variation. We show that with recent advances in statistical methods and genomic approaches, it is now more feasible than ever to trace disease transmission networks, the molecular underpinning of infection, and the environmental variation relevant to disease dynamics. We end by identifying major new opportunities and challenges in understanding disease dynamics in an ever-changing world.

CRISPR (clustered regularly interspaced short palindromic repeats)-Cas (CRISPR-associated) systems are prokaryotic adaptive immune systems that provide protection against infection by parasitic mobile genetic elements, such as viruses and plasmids. CRISPR-Cas systems are found in approximately half of all sequenced bacterial genomes and in nearly all archaeal genomes. In this review, we summarize our current understanding of the evolutionary ecology of CRISPR-Cas systems, highlight their value as model systems to answer fundamental questions concerning host–parasite coevolution, and explain how CRISPR-Cas systems can be useful tools for scientists across virtually all disciplines.

Anthropocene defaunation, the global extinction of faunal species and populations and the decline in abundance of individuals within populations, has been predominantly documented in terrestrial ecosystems, but indicators suggest defaunation has been more severe in freshwater ecosystems. Marine defaunation is in a more incipient stage, yet pronounced effects are already apparent and its rapid acceleration seems likely. Defaunation now impacts the planet's wildlife with profound cascading consequences, ranging from local to global coextinctions of interacting species to the loss of ecological services critical for humanity. Slowing defaunation will require aggressively reducing animal overexploitation and habitat destruction; mitigating climate disruption; and stabilizing the impacts of human population growth and uneven resource consumption. Given its omnipresence, defaunation should receive status of major global environmental change and should be addressed with the same urgency as deforestation, pollution, and climatic change. Global action is needed to prevent defaunation's current trajectory from catalyzing the planet's sixth major extinction.

Understanding coexistence of closely related species lies at the nexus of disentangling how historical and ecological factors govern patterns of biodiversity. The criteria determining local coexistence in close relatives have typically been, for ecologists, whether these species meet conditions of stable coexistence when competing for resources; in contrast, evolutionists often consider coexistence of close relatives from the perspective of complete reproductive isolation. Clearly, both of these conditions must be met, but for coexistence in ecologically and phenotypically similar close relatives to occur, species must overcome a diverse suite of challenges beyond just these. The goal of this review is to present a more holistic, eco-evolutionary view of the factors governing successful coexistence of close relatives, expanding our consideration to recent clade mates, not just sister taxa, and drawing on new technologies and approaches to explore more deeply this classic conundrum. We review the major concepts explaining patterns of coexistence in close relatives, distinguishing between forces related to (a) history, speciation, and extinction; (b) divergence, dispersal, and drivers of range overlap; and (c) successful ecological coexistence of species once in contact. We end by highlighting major gaps and ways forward, including moving beyond the strict dichotomy of local and regional scales and scrutinizing non-native introductions as analogs of secondary contact to tease apart factors contributing to coexistence in real time. By reviewing literature from both ecological and evolutionary perspectives, we hope to illustrate the multifaceted factors that drive coexistence of close relatives and to highlight new questions and approaches that might expand this age-old topic to nonsister close relatives, which often face similar challenges to coexistence as those faced by sister taxa.

Mediterranean-type ecosystems (MTEs) are located today in southwestern Australia, the Cape Region of South Africa, the Mediterranean Basin, California, and central Chile. These MTEs possess the highest levels of plant species richness in the world outside of the wet tropics. These ecosystems include a variety of vegetation structures that range from the iconic mediterranean-type shrublands to deciduous and evergreen woodlands, evergreen forests, and herblands and grasslands. Sclerophyll vegetation similar to today's mediterranean-type shrublands was already present on oligotrophic soils in the wet and humid climate of the Cretaceous, with fire-adapted Paleogene lineages in southwestern Australia and the Cape Region. The novel mediterranean-type climate (MTC) seasonality present since the middle Miocene has allowed colonization of MTEs from a regional species pool with associated diversification. Fire persistence has been a primary driving factor for speciation in four of the five regions. Understanding the regional patterns of plant species diversity among the MTEs involves complex interactions of geologic and climatic histories for each region as well as ecological factors that have promoted diversification in the Neogene and Quaternary. A critical element of species richness for many MTE lineages has been their ability to speciate and persist at fine spatial scales, with low rates of extinction.

The community matrix is among ecology's most important mathematical abstractions, formally encapsulating the interconnected network of effects that species have on one another's populations. Despite its importance, the term “community matrix” has been applied to multiple types of matrices that have differing interpretations. This has hindered the application of theory for understanding community structure and perturbation responses. Here, we clarify the correspondence and distinctions among the Interaction matrix, the Alpha matrix, and the Jacobian matrix, terms that are frequently used interchangeably as well as synonymously with the term “community matrix.” We illustrate how these matrices correspond to different ways of characterizing interaction strengths, how they permit insights regarding different types of press perturbations, and how these are related by a simple scaling relationship. Connections to additional interaction strength characterizations encapsulated by the Beta matrix, the Gamma matrix, and the Removal matrix are also discussed. Our synthesis highlights the empirical challenges that remain in using these tools to understand actual communities.

Biogeographic origins of plant lineages are often reflected in species functional traits, with consequences for community assembly, diversity, and ecosystem function. The climatic and environmental conditions in which species evolved have lasting influence (legacy effects) through phylogenetic conservatism of traits that underlie community assembly and drive ecosystem processes. Legacy effects that influence community assembly may have direct consequences for ecosystem function or may be linked, owing to lineage history, to traits that impact ecosystems. Evolutionary priority effects, driven by the order of colonization and lineage diversification, as well as migration barriers and historical environmental changes, have shaped the diversity and composition of regional floras and their ecosystem functions. We examine the likely consequences of biogeographic history for plant responses to global change and consider how understanding linkages between biogeographic origins, functional traits, and ecosystem consequences can aid the management and restoration of ecosystems globally in the face of rapid environmental change.