Annual Review of Ecology, Evolution, and Systematics - Volume 43, 2012

Ecologists have long grappled with the problem of scaling up from tractable, small-scale observations and experiments to the prediction of large-scale patterns. Although there are multiple approaches to this formidable task, there is a common underpinning in the formulation, testing, and use of mechanistic response functions to describe how phenomena interact across scales. Here, we review the principles of response functions to illustrate how they provide a means to guide research, extrapolate beyond measured data, and simplify our conceptual grasp of reality. We illustrate these principles with examples of mechanistic approaches ranging from explorations of the ecological niche, random walks, and macrophysiology to theories dealing with scale transition, self-organization, and the prediction of extremes.

There is a growing interest in identifying ecological factors that influence adaptive genetic diversity patterns in both model and nonmodel species. The emergence of large genomic and environmental data sets, as well as the increasing sophistication of population genetics methods, provides an opportunity to characterize these patterns in relation to the environment. Landscape genetics has emerged as a flexible analytical framework that connects patterns of adaptive genetic variation to environmental heterogeneity in a spatially explicit context. Recent growth in this field has led to the development of numerous spatial statistical methods, prompting a discussion of the current benefits and limitations of these approaches. Here we provide a review of the design of landscape genetics studies, the different statistical tools, some important case studies, and perspectives on how future advances in this field are likely to shed light on important processes in evolution and ecology.

The prevailing view that insects lack endogenous enzymes for plant cell wall (PCW) digestion had led to the hypothesis that PCW digestion evolved independently in different insect taxa through the establishment of symbiotic relationships with microorganisms. However, recent studies reporting endogenous PCW-degrading genes and enzymes for several insects, including phylogenetically basal insects and closely related arthropod groups, challenge this hypothesis. Here, we summarize the molecular and biochemical evidence on the mechanisms of PCW digestion in insects to analyze its evolutionary pathways. The evidence reveals that the symbiotic-independent mechanism may be the ancestral mechanism for PCW digestion. We discuss the implications of this alternative hypothesis in the evolution of plant-insect interactions and suggest that changes in the composition of lignocellulolytic complexes were involved in the evolution of feeding habits and diet specializations in insects, playing important roles in the evolution of plant-insect interactions and in the diversification of insects.

Highly pelagic large marine vertebrates have evolved the capability of moving across large expanses of the marine environment; some species routinely move across entire ocean basins. Our understanding of these movements has been enhanced by new technologies that now allow us to follow their movements over great distances and long time periods in great detail. This technology provides not only detailed information on the movements of a wide variety of marine species, but also detailed characteristics of the habitats they use and clues to their navigation abilities. Advances in electronic tracking technologies have been coupled with rapid development of statistical and analytical techniques. With these developments, conservation of highly migratory species has been aided by providing new information on where uncommon or endangered species go, what behaviors they perform and why, which habitats are critical, and where they range, as well as, in many cases, better estimates of their population size and the interconnectedness of subpopulations. Together these tools are providing critical insights into the ecology of highly pelagic marine vertebrates that are key for their conservation and management.

Biologists have long sought to identify and explain patterns in the diverse array of marine life histories. The most famous speculation about such patterns is Gunnar Thorson's suggestion that species producing planktonic larvae are rarer at higher latitudes (Thorson's rule). Although some elements of Thorson's rule have proven incorrect, other elements remain untested. With a wealth of new life-history data, statistical approaches, and remote-sensing technology, new insights into marine reproduction can be generated. We gathered life-history data for more than 1,000 marine invertebrates and examined patterns in the prevalence of different life histories. Systematic patterns in marine life histories exist at a range of scales, some of which support Thorson, whereas others suggest previously unrecognized relationships between the marine environment and the life histories of marine invertebrates. Overall, marine life histories covary strongly with temperature and local ocean productivity, and different regions should be managed accordingly.

Many multicellular eukaryotes have reasonably high per-generation mutation rates. Consequently, most populations harbor an abundance of segregating deleterious alleles. These alleles, most of which are of small effect individually, collectively can reduce substantially the fitness of individuals relative to what it would be otherwise; this is mutation load. Mutation load can be lessened by any factor that causes more mutations to be removed per selective death, such as inbreeding, synergistic epistasis, population structure, or harsh environments. The ecological effects of load are not clear-cut because some conditions (such as selection early in life, sexual selection, reproductive compensation, and intraspecific competition) reduce the effects of load on population size and persistence, but other conditions (such as interspecific competition and load on resource use efficiency) can cause small amounts of load to have strong effects on the population, even extinction. We suggest a series of studies to improve our understanding of the effects of mutation load.

The human body is inhabited by billions of microbial cells and these microbial symbionts play critical roles in human health. Human-associated microbial communities are diverse, and the structure of these communities is variable across body habitats, through time, and between individuals. We can apply concepts developed by plant and animal ecologists to better understand and predict the spatial and temporal patterns in these communities. Due to methodological limitations and the largely unknown natural history of most microbial taxa, this integration of ecology into research on the human microbiome is still in its infancy. However, such integration will yield a deeper understanding of the role of the microbiome in human health and an improved ability to test ecological concepts that are more difficult to test in plant and animal systems.

The dynamics of infectious diseases can be affected by genetic diversity within host populations, species diversity within host communities, and diversity among communities. In principle, diversity can either increase or decrease pathogen transmission and disease risk. Theoretical models and laboratory experiments have demonstrated that a dilution effect (decreased disease risk with increasing diversity) can occur under a wide range of conditions. Field studies of plants, aquatic invertebrates, amphibians, birds, and mammals demonstrate that the phenomenon indeed does occur in many natural systems. A dilution effect is expected when (a) hosts differ in quality for pathogens or vectors; (b) higher quality hosts tend to occur in species-poor communities, whereas lower quality hosts tend to occur in more diverse communities; and (c) lower quality hosts regulate abundance of high-quality hosts or of vectors, or reduce encounter rates between these hosts and pathogens or vectors. Although these conditions characterize many disease systems, our ability to predict when and where the dilution effect occurs remains poor. The life-history traits that cause some hosts to be widespread and resilient might be correlated with those that promote infection and transmission by some pathogens, supporting the notion that the dilution effect might be widespread among disease systems. Criticisms of the dilution effect have focused on whether species richness or species composition (both being metrics of biodiversity) drives disease risk. It is well established, however, that changes in species composition correlate with changes in species richness, and this correlation could explain why the dilution effect appears to be a general phenomenon.

The extinction of a single species is rarely an isolated event. Instead, dependent parasites, commensals, and mutualist partners (affiliates) face the risk of coextinction as their hosts or partners decline and fail. Species interactions in ecological networks can transmit the effects of primary extinctions within and between trophic levels, causing secondary extinctions and extinction cascades. Documenting coextinctions is complicated by ignorance of host specificity, limitations of historical collections, incomplete systematics of affiliate taxa, and lack of experimental studies. Host shifts may reduce the rate of coextinctions, but they are poorly understood. In the absence of better empirical records of coextinctions, statistical models estimate the rates of past and future coextinctions, and based on primary extinctions and interactions among species, network models explore extinction cascades. Models predict and historical evidence reveals that the threat of coextinction is influenced by both host and affiliate traits and is exacerbated by other threats, including habitat loss, climate change, and invasive species.

Shifts in phenology and distribution in response to both recent and paleontological climate changes vary markedly in both direction and extent among species. These individualistic shifts are inconsistent with common forecasting techniques based on environmental rather than biological niches. What biological details could enhance forecasts? Organismal characteristics such as thermal and hydric limits, seasonal timing and duration of the life cycle, ecological breadth and dispersal capacity, and fitness and evolutionary potential are expected to influence climate change impacts. We review statistical and mechanistic approaches for incorporating traits in predictive models as well as the potential to use phylogeny as a proxy for traits. Traits generally account for a significant but modest fraction of the variation in phenological and range shifts. Further assembly of phenotypic and phylogenetic data coupled with the development of mechanistic approaches is essential to improved forecasts of the ecological consequences of climate change.

Although research on the role of competitive interactions during community assembly began decades ago, a recent revival of interest has led to new discoveries and research opportunities. Using contemporary coexistence theory that emphasizes stabilizing niche differences and relative fitness differences, we evaluate three empirical approaches for studying community assembly. We show that experimental manipulations of the abiotic or biotic environment, assessments of trait-phylogeny-environment relationships, and investigations of frequency-dependent population growth all suggest strong influences of stabilizing niche differences and fitness differences on the outcome of plant community assembly. Nonetheless, due to the limitations of these approaches applied in isolation, we still have a poor understanding of which niche axes and which traits determine the outcome of competition and community structure. Combining current approaches represents our best chance of achieving this goal, which is fundamental to conceptual ecology and to the management of plant communities under global change.

Avian faunas vary greatly among montane areas; those at high latitudes are biologically impoverished, whereas those of some low-latitude mountains are biologically very complex. Their high level of species richness is caused by the aggregation of many small-ranged species, which has been difficult to explain from purely macroecological models focusing on contemporary ecological processes. Because the individual mountain tracts harbor species that represent different evolutionary trajectories, it seems plausible to relate these species assemblages to high persistence (or absence of extinction) in addition to high levels of speciation. The distribution of small-ranged species is concentrated near tropical coasts, where moderation of the climate in topographically complex areas creates cloud forests and stable local conditions. The stability underpins specialization and resilience of local populations, and thereby the role of these places as cradles of biodiversity.

There are many methods for making evolutionary inferences from phylogenetic trees. Many of these can be divided into three main classes of models: continuous-time Markov chain models with finite state space (CTMC-FSS), multivariate normal models, and birth-death models. Numerous approaches are just restrictions of more general models to focus on particular questions or kinds of data. Methods can be further modified with the addition of tree-stretching algorithms. The recent realization of the effect of correlated trait evolution with diversification rates represents an important advance that is slowly revolutionizing the field. Increased attention to model adequacy may lead to future methodological improvements.

Mathematical models have played an important role in the development of sexual selection theory. These models come in different flavors and they differ in their assumptions, often in a subtle way. Similar questions can be addressed by modeling frameworks from population genetics, quantitative genetics, evolutionary game theory, or adaptive dynamics, or by individual-based simulations. Confronted with such diversity, nonspecialists may have difficulties judging the scope and limitations of the various approaches. Here we review the major modeling frameworks, highlighting their pros and cons when applied to different research questions. We also discuss recent developments, where classical models are enriched by including more detail regarding genetics, behavior, demography, and population dynamics. It turns out that some seemingly well-established conclusions of sexual selection theory are less general than previously thought. Linking sexual selection to other processes such as sex-ratio evolution or speciation also reveals that enriching the theory can lead to surprising new insights.

The net primary production of the biosphere is consumed largely by microorganisms, whose metabolism creates the trophic base for detrital foodwebs, drives element cycles, and mediates atmospheric composition. Biogeochemical constraints on microbial catabolism, relative to primary production, create reserves of detrital organic carbon in soils and sediments that exceed the carbon content of the atmosphere and biomass. The production of organic matter is an intracellular process that generates thousands of compounds from a small number of precursors drawn from intermediary metabolism. Osmotrophs generate growth substrates from the products of biosynthesis and diagenesis by enzyme-catalyzed reactions that occur largely outside cells. These enzymes, which we define as ecoenzymes, enter the environment by secretion and lysis. Enzyme expression is regulated by environmental signals, but once released from the cell, ecoenzymatic activity is determined by environmental interactions, represented as a kinetic cascade, that lead to multiphasic kinetics and large spatiotemporal variation. At the ecosystem level, these interactions can be viewed as an energy landscape that directs the availability and flow of resources. Ecoenzymatic activity and microbial metabolism are integrated on the basis of resource demand relative to environmental availability. Macroecological studies show that the most widely measured ecoenzymatic activities have a similar stoichiometry for all microbial communities. Ecoenzymatic stoichiometry connects the elemental stoichiometry of microbial biomass and detrital organic matter to microbial nutrient assimilation and growth. We present a model that combines the kinetics of enzyme activity and community growth under conditions of multiple resource limitation with elements of metabolic and ecological stoichiometry theory. This biogeochemical equilibrium model provides a framework for comparative studies of microbial community metabolism, the principal driver of biogeochemical cycles.

The origination of novel genes is an important process during the evolution of organisms because it provides critical sources for evolutionary innovation. Addressing how novel genes emerged and acquired novel and adaptive functions is of fundamental importance. Here we summarize the newest advances in our understanding of the molecular mechanisms and genome-wide patterns of new gene origination and new gene functions. We pay special attention to the origins of noncoding RNA genes and de novo genes, whose processes had been previously overlooked but are gaining increasingly visible importance. We then introduce recent findings that have opened a path to the study of the evolution of novel functions and pathways via novel genes. We also discuss the important issues and potential developments in the field.

Changes in climate, land use, fire incidence, and ecological connections all may contribute to current species' range shifts. Species shift range individually, and not all species shift range at the same time and rate. This variation causes community reorganization in both the old and new ranges. In terrestrial ecosystems, range shifts alter aboveground-belowground interactions, influencing species abundance, community composition, ecosystem processes and services, and feedbacks within communities and ecosystems. Thus, range shifts may result in no-analog communities where foundation species and community genetics play unprecedented roles, possibly leading to novel ecosystems. Long-distance dispersal can enhance the disruption of aboveground-belowground interactions of plants, herbivores, pathogens, symbiotic mutualists, and decomposer organisms. These effects are most likely stronger for latitudinal than for altitudinal range shifts. Disrupted aboveground-belowground interactions may have influenced historical postglacial range shifts as well. Assisted migration without considering aboveground-belowground interactions could enhance risks of such range shift–induced invasions.

Inflammation is a pervasive phenomenon that operates during severe perturbations of homeostasis, such as infection, injury, and exposure to contaminants, and is triggered by innate immune receptors that recognize pathogens and damaged cells. Among vertebrates, the inflammatory cascade is a complex network of immunological, physiological, and behavioral events that are coordinated by cytokines, immune signaling molecules. Although the molecular basis of inflammation is well studied, its role in mediating the outcome of host-parasite interactions has received minimal attention by ecologists. This review provides a synopsis of vertebrate inflammation, its life-history modulation, and its effects upon host-pathogen dynamics as well as host-commensal microbiota interactions in the gut. What emerges is evidence for phenotypic plasticity of inflammatory responses despite the apparently invariant and redundant nature of the immunoregulatory networks that regulate them.

Our understanding of the players and pathways of the global nitrogen cycle has advanced substantially over recent years with discoveries of several new groups of organisms and new types of metabolism. This review focuses on recently discovered processes that add new functionality to the nitrogen cycle and on the organisms that perform these functions. The processes include denitrification and other dissimilatory nitrogen transformations in eukaryotes, anaerobic ammonium oxidation, and anaerobic methane oxidation with nitrite. Of these, anaerobic ammonium oxidation coupled to nitrite reduction by anammox bacteria has been well documented in natural environments and constitutes an important sink for fixed nitrogen. Benthic foraminifera also contribute substantially to denitrification in some sediments, in what potentially represents an ancestral eukaryotic metabolism. The ecophysiology of the novel organisms and their interactions with classical types of nitrogen metabolism are important for understanding the nitrogen cycle and its tight links to the cycling of carbon today, in the past, and in the future.

The seasonal succession of plankton is an annually repeated process of community assembly during which all major external factors and internal interactions shaping communities can be studied. A quarter of a century ago, the state of this understanding was described by the verbal plankton ecology group (PEG) model. It emphasized the role of physical factors, grazing and nutrient limitation for phytoplankton, and the role of food limitation and fish predation for zooplankton. Although originally targeted at lake ecosystems, it was also adopted by marine plankton ecologists. Since then, a suite of ecological interactions previously underestimated in importance have become research foci: overwintering of key organisms, the microbial food web, parasitism, and food quality as a limiting factor and an extended role of higher order predators. A review of the impact of these novel interactions on plankton seasonal succession reveals limited effects on gross seasonal biomass patterns, but strong effects on species replacements.