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

Photoperiodism is the ability of organisms to assess and use the day length as an anticipatory cue to time seasonal events in their life histories. Photoperiodism is especially important in initiating physiological and developmental processes that are typically irrevocable and that culminate at a future time or at a distant place; the further away in space or time, the more likely a seasonal event is initiated by photoperiod. The pervasiveness of photoperiodism across broad taxa, from rotifers to rodents, and the predictable changes of photoperiodic response with geography identify it as a central component of fitness in temperate and polar seasonal environments. Consequently, the role of day length cannot be disregarded when evaluating the mechanisms underlying life-historical events, range expansions, invasions of novel species, and response to climate change among animals in the temperate and polar regions of the world.

Viruses represent a serious problem faced by human and veterinary medicine and agronomy. New viruses are constantly emerging while old ones evolve and challenge the latest advances in antiviral pharmaceutics, thus generating tremendous social alarm, sanitary problems, and economical losses. However, they constitute very powerful tools for experimental evolution. These two faces of virology are tightly related because future antiviral treatments shall be rationally designed by considering evolutionary principles. Evidence indicates that the evolution of viruses is determined mainly by key features such as their small genomes, enormous population sizes, and short generation times, and at least for RNA viruses, large selection coefficients, antagonistic epistasis, and high mutation rates. We summarize recent advances in the field of experimental virus evolution. Increasing our understanding of the roles of selection, mutation, chance, and historical contingency on the ecology and epidemiology of viral infections could determine our ability to combat them.

Our understanding of the social lives of microbes has been revolutionized over the past 20 years. It used to be assumed that bacteria and other microorganisms lived relatively independent unicellular lives, without the cooperative behaviors that have provoked so much interest in mammals, birds, and insects. However, a rapidly expanding body of research has completely overturned this idea, showing that microbes indulge in a variety of social behaviors involving complex systems of cooperation, communication, and synchronization. Work in this area has already provided some elegant experimental tests of social evolutionary theory, demonstrating the importance of factors such as relatedness, kin discrimination, competition between relatives, and enforcement of cooperation. Our aim here is to review these social behaviors, emphasizing the unique opportunities they offer for testing existing evolutionary theory as well as highlighting the novel theoretical problems that they pose.

Sexual selection has a reputation as a major cause of speciation, one of the most potent forces driving reproductive isolation. This reputation arises from observations that species differ most in traits involved with mating success and from successful models of sexual selection–driven speciation. But how well proven is the case? Models confirm that the process can occur, but is strongest in conjunction with ecological or niche specialization. Some models also show that strong sexual selection can act against speciation. Studies using the comparative method are equivocal and often inconclusive, but some phylogeographic studies are more convincing. Experimental evolution and genetic or genomic analyses are in their infancy, but look particularly promising for resolving the importance of sexual selection. The case for sexual selection is not as strongly supported as, for example, allopatric speciation. Sexual selection probably contributes most effectively alongside ecological selection or selection for species recognition than as a solitary process.

Researchers are increasingly recognizing that social effects influence the evolution of aging. Kin selection theory provides a framework for analyzing such effects because an individual's longevity and mortality schedule may alter its inclusive fitness via effects on the fitness of relatives. Kin-selected effects on aging have been demonstrated both by models of intergenerational transfers of investment by caregivers and by spatially explicit population models with limited dispersal. They also underlie coevolution between the degree and form of sociality and patterns of aging. In this review I critically examine and synthesize theory and data concerning these processes. I propose a classification, stemming from kin selection theory, of social effects on aging and describe a hypothesis for kin-selected conflict over parental time of death in systems with resource inheritance. I conclude that systematically applying kin selection theory to the analysis of the evolution of aging adds considerably to our general understanding of aging.

Benthic communities living in shallow-shelf habitats in Antarctica (<100-m depth) are archaic in structure and function compared to shallow-water communities elsewhere. Modern predators, including fast-moving, durophagous (skeleton-crushing) bony fish, sharks, and crabs, are rare or absent; slow-moving invertebrates are generally the top predators; and epifaunal suspension feeders dominate many soft-substratum communities. Cooling temperatures beginning in the late Eocene excluded durophagous predators, ultimately resulting in the endemic living fauna and its unique food-web structure. Although the Southern Ocean is oceanographically isolated, the barriers to biological invasion are primarily physiological rather than geographic. Cold temperatures impose limits to performance that exclude modern predators. Global warming is now removing those physiological barriers, and crabs are reinvading Antarctica. As sea temperatures continue to rise, the invasion of durophagous predators will modernize the shelf benthos and erode the indigenous character of marine life in Antarctica.

Much of the information in visual signals is encoded in motion, form, and texture. Current knowledge about the mechanisms underlying visual communication is spread across diverse disciplines. Contemporary perspectives on the physics, psychology, and genetics of visual signal generation and perception can be synthesized into a conceptually integrative approach. Developmental mechanisms of pattern formation suggest that small changes in gene regulation or structure can result in major shifts in signal architecture. Animals in many species have been shown to attend to variation in higher-order stimulus properties. Preferences for these properties can be innately specified or learned, and may also show large shifts or reversals. Perceptual mechanisms, particularly visual attention, associated with spatiotemporal features are likely to be a major force in shaping the design of visual signals.

A biomechanically parsimonious hypothesis for the evolution of flapping flight in terrestrial vertebrates suggests progression within an arboreal context from jumping to directed aerial descent, gliding with control via appendicular motions, and ultimately to powered flight. The more than 30 phylogenetically independent lineages of arboreal vertebrate gliders lend strong indirect support to the ecological feasibility of such a trajectory. Insect flight evolution likely followed a similar sequence, but is unresolved paleontologically. Recently described falling behaviors in arboreal ants provide the first evidence demonstrating the biomechanical capacity for directed aerial descent in the complete absence of wings. Intentional control of body trajectories as animals fall from heights (and usually from vegetation) likely characterizes many more taxa than is currently recognized. Understanding the sensory and biomechanical mechanisms used by extant gliding animals to control and orient their descent is central to deciphering pathways involved in flight evolution.

Recent advances in molecular biology and computation have enabled evolutionary biologists to develop models that explicitly capture molecular structure. By including complex and realistic maps from genotypes to phenotypes, such models are yielding important new insights into evolutionary processes. In particular, computer simulations of evolving RNA structure have inspired a new conceptual framework for thinking about patterns of mutational connectivity and general theories about the nature of evolutionary transitions, the evolutionary ascent of nonoptimal phenotypes, and the origins of mutational robustness and modular structures. Here, we describe this class of RNA models and review the major conceptual contributions they have made to evolutionary biology.

This review proposes ten tentative answers to frequently asked questions about dispersal evolution. I examine methodological issues, model assumptions and predictions, and their relation to empirical data. Study of dispersal evolution points to the many ecological and genetic feedbacks affecting the evolution of this complex trait, which has contributed to our better understanding of life-history evolution in spatially structured populations. Several lines of research are suggested to ameliorate the exchanges between theoretical and empirical studies of dispersal evolution.

Cyanobacterial symbioses with eukaryotes are ancient associations that are widely distributed in aquatic and terrestrial environments. Cyanobacteria are a significant driving force in the evolution of their hosts, providing a range of services including photosynthesis, nitrogen fixation, UV protection, and defensive toxins. Although widespread, cyanobacteria occur in a limited range of hosts. Terrestrial symbioses are typically restricted to lichens and early evolved plants, and aquatic symbioses to sessile or slow-moving organisms. This review examines the underlying evolutionary processes that may have lead to these patterns. It also examines the facts that the degree of integration between symbiont and host, and the mode of transmission of the symbiont, do not appear to be an indication of how old the symbiosis is or how important it is to host well-being. Biparental transmission of symbionts may prolong the survival of gametes that persist in the environment, increasing chances of fertilization.

Pines (genus Pinus) form the dominant tree cover over large parts of the Northern Hemisphere. Human activities have affected the distribution, composition, and structure of pine forests for millennia. Different human-mediated factors have affected different pine species in different ways in different regions. The most important factors affecting pine forests are altered fire regimes, altered grazing/browsing regimes, various harvesting/construction activities, land clearance and abandonment, purposeful planting and other manipulations of natural ecosystems, alteration of biotas through species reshuffling, and pollution. These changes are occurring against a backdrop of natural and anthropogenically driven climate change. We review past and current influence of humans in pine forests, seeking broad generalizations. These insights are combined with perspectives from paleoecology to suggest probable trajectories in the face of escalating human pressure. The immense scale of impacts and the complex synergies between agents of change calls for urgent and multifaceted action.

We examine how aging is influenced by various chemical challenges that organisms face and by the molecular mechanisms that have evolved to modulate life span in response to them. For example, environmental information, which is detected and processed through sensory systems, can modulate life span by providing information about the presence and quality of food as well as presence and density of conspecifics and predators. In addition, the diverse forms of molecular damage that result from constant exposure to toxic chemicals that are generated from the environment and from metabolism pose an informatic and energetic challenge for detoxification systems, which are important in ensuring longevity. Finally, systems of innate immunity are vital for recognizing and combating pathogens but are also increasingly seen as of importance in causing the aging process. Integrating ideas of molecular mechanism with context derived from evolutionary considerations will lead to exciting new insights into the evolution of aging.

We reviewed over 407 global seaweed introduction events and have increased the total number of introduced seaweed species to 277. Using binomial tests we show that several algal families contain more successful invaders than would be expected by chance, highlighting groups that should be targeted for management. Hull-fouling and aquaculture are the most significant sources of seaweed invaders and should be carefully regulated. The ecological effects of introduced seaweeds have been studied in only 6% of the species, but these studies show mostly negative effects or changes to the native biota. Herbivores generally prefer native to introduced seaweeds, and are unlikely to control spread, as they can do in other habitats. Undisturbed marine communities can be at least initially resistant to most introduced seaweeds aside from the siphonous green species; however, disturbances and eutrophication can facilitate invasion. Major research gaps include community-level ecological studies and economic assessments.

Quantitative estimates of the gene complement of the last common ancestor of all extant organisms, that is, the cenancestor, may be hindered by ancient horizontal gene transfer events and polyphyletic gene losses, as well as by biases in genome databases and methodological artifacts. Nevertheless, most reports agree that the last common ancestor resembled extant prokaryotes. A significant number of the highly conserved genes are sequences involved in the synthesis, degradation, and binding of RNA, including transcription and translation. Although the gene complement of the cenancestor includes sequences that may have originated in different epochs, the extraordinary conservation of RNA-related sequences supports the hypothesis that the last common ancestor was an evolutionary outcome of the so-called RNA/protein world. The available evidence suggests that the cenancestor was not a hyperthermophile, but it is currently not possible to assess its ecological niche or its mode of energy acquisition and carbon sources.

Studies of the evolution of phenotypic diversity have gained momentum among neontologists interested in the uneven distribution of diversity across the tree of life. Potential morphological diversity in a lineage is a function of the number of independent parameters required to describe the form, and innovations such as structural duplication and functional decoupling can enhance the potential for diversity in a given clade. The functional properties of organisms are determined by underlying parts, but any property that is determined by three or more parts expresses many-to-one mapping of form to function, in which many morphologies will have the same functional property. This ubiquitous feature of organismal design results in surfaces of morphological variation that are neutral with respect to the functional property, and enhances the potential for simultaneously optimizing two or more functions of the system.

Continuous-trait game theory fills the niche of enabling analytically solvable models of the evolution of biologically realistically complex traits. Game theory provides a mathematical language for understanding evolution by natural selection. Continuous-trait game theory starts with the notion of an evolutionarily stable strategy (ESS) and adds the concept of convergence stability (that the ESS is an evolutionary attractor). With these basic tools in hand, continuous-trait game theory can be easily extended to model evolution under conditions of disruptive selection and speciation, nonequilibrium population dynamics, stochastic environments, coevolution, and more. Many models applying these tools to evolutionary ecology and coevolution have been developed in the past two decades. Going forward we emphasize the communication of the conceptual simplicity and underlying unity of ideas inherent in continuous-trait game theory and the development of new applications to biological questions.

Cleistogamous species present strong evidence for the stability of mixed mating, but are generally not considered in this context. Individuals of cleistogamous species produce both obligately selfing cleistogamous flowers (CL) and potentially outcrossed chasmogamous flowers (CH) with distinct morphologies. Greater energetic economy and reliability of CL relative to CH suggest that forces that maintain selection for outcrossing may be stronger in these species than in mixed maters with monomorphic flowers. We reviewed data from 60 studies of cleistogamous species to evaluate proposed explanations for the evolutionary stability of mixed cleistogamous and chasmogamous reproduction and to quantify the magnitude of selection necessary to account for the maintenance of CH. We found circumstantial support for existing hypotheses for the stability of cleistogamy, and that forces that maintain CH must account for a 15–342% advantage of reproduction via CL. We suggest that heterosis and the effects of mass action pollination should be considered.

Sympatric speciation, the evolution of reproductive isolation without geographic barriers, remains highly contentious. As a result of new empirical examples and theory, it is now generally accepted that sympatric speciation has occurred in at least a few instances, and is theoretically plausible. Instead, debate has shifted to whether sympatric speciation is common, and whether models’ assumptions are generally met in nature. The relative frequency of sympatric speciation will be difficult to resolve, because biogeographic changes have obscured geographical patterns underlying many past speciation events. In contrast, progress is being made on evaluating the empirical validity of key theoretical conditions for sympatric speciation. Disruptive selection and direct selection on mating traits, which should facilitate sympatric speciation, are biologically well supported. Conversely, costs to assortative mating are also widely documented, but inhibit speciation. Evaluating the joint incidence of these key factors may illuminate why sympatric speciation appears to be relatively uncommon.

The development and maintenance of color polymorphism in cryptic prey species is a source of enduring fascination, in part because it appears to result from selective processes operating across multiple levels of analysis, ranging from cognitive psychology to population ecology. Since the 1960s, prey species with diverse phenotypes have been viewed as the evolved reflection of the perceptual and cognitive characteristics of their predators. Because it is harder to search simultaneously for two or more cryptic prey types than to search for only one, visual predators should tend to focus on the most abundant forms and effectively overlook the others. The result should be frequency-dependent, apostatic selection, which will tend to stabilize the prey polymorphism. Validating this elegant hypothesis has been difficult, and many details have been established only relatively recently. This review clarifies the argument for a perceptual selective mechanism and examines the relevant experimental evidence.

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.