Annual Review of Ecology, Evolution, and Systematics - Volume 38, 2007

Viral pathogens play a prominent role in human health owing to their ability to rapidly evolve creative new ways to exploit their hosts. As elegant and deceptive as many viral adaptations are, humans and their ancestors have repeatedly answered their call with equally impressive adaptations. Here we argue that the coevolutionary arms race between humans and their viral pathogens is one of the most important forces in human molecular evolution, past and present. With a focus on HIV-1 and other RNA viruses, we highlight recent developments in our understanding of the human innate and adaptive immune systems and how the selective pressures exerted by viruses have shaped the human genome. We also discuss how the antiviral function of cellular machinery like RNAi and APOBEC3G blur the lines between innate and adaptive immunity. The remarkable power of natural selection is revealed in each host-pathogen arms race examined.

Tolerance and resistance are two different plant defense strategies against herbivores. Empirical evidence in natural populations reveals that individual plants allocate resources simultaneously to both strategies, thus plants exhibit a mixed pattern of defense. In this review we examine the conditions that promote the evolutionary stability of mixed defense strategies in the light of available empirical and theoretical evidence. Given that plant tolerance and resistance are heritable and subject to environmentally dependent selection and genetic constraints, the joint evolution of tolerance and resistance is analyzed, with consideration of multiple species interactions and the plant mating system. The existence of mixed defense strategies in plants makes it necessary to re-explore the coevolutionary process between plants and herbivores, which centered historically on resistance as the only defensive mechanism. In addition, we recognize briefly the potential use of plant tolerance for pest management. Finally, we highlight unresolved issues for future development in this field of evolutionary ecology.

The mutually beneficial interactions between plants and their animal pollinators and seed dispersers have been paramount in the generation of Earth's biodiversity. These mutualistic interactions often involve dozens or even hundreds of species that form complex networks of interdependences. Understanding how coevolution proceeds in these highly diversified mutualisms among free-living species presents a conceptual challenge. Recent work has led to the unambiguous conclusion that mutualistic networks are very heterogeneous (the bulk of the species have a few interactions, but a few species are much more connected than expected by chance), nested (specialists interact with subsets of the species with which generalists interact), and built on weak and asymmetric links among species. Both ecological variables (e.g., phenology, local abundance, and geographic range) and past evolutionary history may explain such network patterns. Network structure has important implications for the coexistence and stability of species as well as for the coevolutionary process. Mutualistic networks can thus be regarded as the architecture of biodiversity.

Populations are locally adapted when populations have the highest relative fitness at their home sites, and lower fitness in other parts of the range. Results from the extensive experimental plantations of populations of forest trees from different parts of the range show that populations can survive and grow in broad areas outside the home site. However, intra- and interspecific competition limit the distribution of genotypes. For populations from large parts of the range, relative fitness, compared with the local population, is often highest at the home site. At the edges of the range, this local adaptation may break down. The extent of local adaptation is determined by the balance between gene flow and selection. Genetic differentiation and strong natural selection occur over a range of tens or hundreds of kilometers, but reliable measurements of gene flow are available only for much shorter distances. Current models of spatially varying selection could be made more realistic by the incorporation of strong selection and isolation-by-distance characteristic of tree populations. Many studies suggest that most variation in adaptive traits is based on loci with small effects. Association genetics methods and improved genomic resources are useful for the identification of the loci responsible for this variation. The potential for adaptation to current climate change depends on genetic variation and dispersal and establishment rates.

Benefits of increased size and functional specialization of cells have repeatedly promoted the evolution of multicellular organisms from unicellular ancestors. Many requirements for multicellular organization (cell adhesion, cell-cell communication and coordination, programmed cell death) likely evolved in ancestral unicellular organisms. However, the evolution of multicellular organisms from unicellular ancestors may be opposed by genetic conflicts that arise when mutant cell lineages promote their own increase at the expense of the integrity of the multicellular organism. Numerous defenses limit such genetic conflicts, perhaps the most important being development from a unicell, which minimizes conflicts from selection among cell lineages, and redistributes genetic variation arising within multicellular individuals between individuals. With a unicellular bottleneck, defecting cell lineages rarely succeed beyond the life span of the multicellular individual. When multicellularity arises through aggregation of scattered cells or when multicellular organisms fuse to form genetic chimeras, there are more opportunities for propagation of defector cell lineages. Intraorganismal competition may partly explain why multicellular organisms that develop by aggregation generally exhibit less differentiation than organisms that develop clonally.

During the past decade of study in evolutionary developmental biology, we have seen the focus shift away from the stunning conservation of form and function between distantly related taxa toward the causal explanation of differences between closely related species. A number of fish models have emerged at the forefront of this effort to dissect the developmental genetic and molecular basis of evolutionary novelty and adaptation. We review the highlights of this research, concentrating our attention on skeletal morphology (cranial and postcranial), pigmentation patterning, and sex determination. Thus far, the genes involved in adaptation among fishes belong to well-characterized molecular pathways. We synthesize the current state of knowledge to evaluate theories about the interplay between development and evolution. General rules of evolutionary change have not materialized; however, the field is wide open, and fishes will likely continue to contribute insights to this central biological question.

The coupled carbon-climate models reported in the literature all demonstrate a positive feedback between terrestrial carbon cycles and climate warming. A primary mechanism underlying the modeled positive feedback is the kinetic sensitivity of photosynthesis and respiration to temperature. Field experiments, however, suggest much richer mechanisms driving ecosystem responses to climate warming, including extended growing seasons, enhanced nutrient availability, shifted species composition, and altered ecosystem-water dynamics. The diverse mechanisms likely define more possibilities of carbon-climate feedbacks than projected by the kinetics-based models. Nonetheless, experimental results are so variable that we have not generated the necessary insights on ecosystem responses to effectively improve global models. To constrain model projections of carbon-climate feedbacks, we need more empirical data from whole-ecosystem warming experiments across a wide range of biomes, particularly in tropic regions, and closer interactions between models and experiments.

Biodiversity is not completely known anywhere, so conservation planning is always based on surrogates for which data are available and, hence, assumed effective for the conservation of unknown biodiversity. We review the literature on the effectiveness of surrogates for conservation planning based on complementary representation. We apply a standardized approach based on a Species Accumulation Index of surrogate effectiveness to compare results from 575 tests in 27 studies. Overall, we find positive, but relatively weak, surrogacy power. Cross-taxon surrogates are substantially more effective than surrogates based on environmental data. Within cross-taxon tests, surrogacy was higher for tests within the same realm (terrestrial, marine, freshwater). Surrogacy was higher when extrapolated (rather than field) data were used. Our results suggest that practical conservation planning based on data for well-known taxonomic groups can cautiously proceed under the assumption that it captures species in less well-known taxa, at least within the same realm.

There is growing interest in the effects of changing marine biodiversity on a variety of community properties and ecosystem processes such as nutrient use and cycling, productivity, stability, and trophic transfer. We review published marine experiments that manipulated the number of species, genotypes, or functional groups. This research reveals several emerging generalities. In studies of primary producers and sessile animals, diversity often has a weak effect on production or biomass, especially relative to the strong effect exerted by individual species. However, sessile taxon richness did consistently decrease variability in community properties, and increased resistance to, or recovery from disturbance or invasion. Multitrophic-level studies indicate that, relative to depauperate assemblages of prey species, diverse ones (a) are more resistant to top-down control, (b) use their own resources more completely, and (c) increase consumer fitness. In contrast, predator diversity can either increase or decrease the strength of top-down control because of omnivory and because interactions among predators can have positive and negative effects on herbivores. Recognizing that marine and terrestrial approaches to understanding diversity-function relationships are converging, we close with suggestions for future research that apply across habitats.

Describing water flow from soil through plants to the atmosphere remains a formidable scientific challenge despite years of research. This challenge is not surprising given the high dimensionality and degree of nonlinearity of the soil-plant system, which evolves in space and time according to complex internal physical, chemical, and biological laws forced by external hydroclimatic variability. Although rigorous microscopic laws for this system still await development, some progress can be made on the formulation of macroscopic laws that upscale known submacroscopic processes and use surrogate stochasticity to preserve the probabilistic and spectral information content of the high dimensional system. The external hydroclimatic forcing is inherently intermittent with variability across all scales, thereby precluding the use of standard approximations employed in analysis of stochastic processes (e.g., small noise perturbations). Examples are provided to show how superposition of stochasticity at multiple space-time scales shapes plant-water interactions.

A productive synthesis of endocrinology and evolutionary genetics has occurred during the past two decades, resulting in the first direct documentation of genetic variation and correlation for endocrine regulators in nondomesticated animals. In a number of insect genetic polymorphisms (dispersal polymorphism in crickets, butterfly wing-pattern polymorphism), blood levels of ecdysteroids and juvenile hormone covary with morphology, development, and life history. Genetic variation in insulin signaling may underlie life history trade-offs in Drosophila. Vertebrate studies identified variation in brain neurohormones, bone-regulating hormones, and hormone receptor gene sequences that underlie ecologically important genetic polymorphisms. Most work to date has focused on genetically variable titers (concentrations) of circulating hormones and the activities of titer regulators. Continued progress will require greater integration among (a) traditional comparative endocrine approaches (e.g., titer measures); (b) molecular studies of hormone receptors and intracellular signaling pathways; and (c) fitness studies of genetically variable endocrine traits in ecologically appropriate conditions.

Spiders’ silks and webs have made it possible for this diverse taxon to occupy a unique niche as the main predator for another, even more diverse taxon, the insects. Indeed, it might well be that the spiders, which are older, were a major force driving the insects into their diversity in a coevolutionary arms race. The spiders’ weapons were their silks and here we explore the evidence for the evolution of silk production and web building as traits in spider phylogeny.

Flow cytometry, a method of rapidly characterizing optical properties of cells and cell components within individuals, populations, and communities, is advancing research in several areas of ecology, systematics, and evolutionary biology. Measuring the light emitted or scattered from cells or cell components, often in combination with specific stains, allows a multitude of physical and genetic attributes to be evaluated simultaneously and the resulting information to be rapidly processed. As a result, the technique has enabled large-scale comparative analyses of genome-size evolution, taxonomic identification and delineation, and studies of polyploids, reproductive biology, and experimental evolution. It is also being used to characterize the structure and composition of microbial communities. Here, we outline the nature of these contributions, as well as future applications, and provide an online summary of protocols and sampling methods.