Annual Review of Ecology, Evolution, and Systematics - Volume 36, 2005

Variation in the subtle differences between right and left sides of bilateral characters, or fluctuating asymmetry (FA), has long been considered to be primarily environmental in origin, and this has promoted its use as a measure of developmental instability (DI) in populations. There is little evidence for specific genes that govern FA per se. Numerous studies show that FA levels in various characters are influenced by dominance and especially epistatic interactions among genes. An epistatic genetic basis for FA may complicate its primary use in comparisons of DI levels in outbred or wild populations subjected or not subjected to various environmental stressors. Although the heritability of FA typically is very low or zero, epistasis can generate additive genetic variation for FA that may allow it to evolve especially in populations subjected to bottlenecks, hybridizations, or periods of rapid environmental changes caused by various stresses.

Two consequences of terrestrial ectothermy (low energy needs and behavioral control of body temperatures) have had major consequences for the evolution of reptile life-history traits. For example, reproducing females can manipulate incubation temperatures and thus phenotypic traits of their offspring by retaining developing eggs in utero. This ability has resulted in multiple evolutionary transitions from oviparity to viviparity in cool-climate reptile populations. The spatial and temporal heterogeneity of operative temperatures in terrestrial habitats also has favored careful nest-site selection and a matching of embryonic reaction norms to thermal regimes during incubation (e.g., via temperature-dependent sex determination). Many of the life-history features in which reptiles differ from endothermic vertebrates—such as their small offspring sizes, large litter sizes, and infrequent reproduction—are direct consequences of ectothermy, reflecting freedom from heat-conserving constraints on body size and energy storage. Ectothermy confers immense flexibility, enabling a dynamic matching of life-history traits to local circumstances. This flexibility has generated massive spatial and temporal variation in life-history traits via phenotypic plasticity as well as adaptation. The diversity of life histories in reptiles can best be interpreted within a conceptual framework that views reptiles as low-energy, variable-temperature systems.

Mixed mating, in which hermaphrodite plant species reproduce by both self- and cross-fertilization, presents a challenging problem for evolutionary biologists. Theory suggests that inbreeding depression, the main selective factor opposing the evolution of selfing, can be purged with self-fertilization, a process that is expected to yield pure strategies of either outcrossing or selfing. Here we present updated evidence suggesting that mixed mating systems are frequent in seed plants. We outline the floral and pollination mechanisms that can lead to intermediate outcrossing, review the theoretical models that address the stability of intermediate outcrossing, and examine relevant empirical evidence. A comparative analysis of estimated inbreeding coefficients and outcrossing rates suggests that mixed mating often evolves despite strong inbreeding depression. The adaptive significance of mixed mating has yet to be fully explained for any species. Recent theoretical and empirical work suggests that future progress will come from a better integration of studies of floral mechanisms, genetics, and ecology, and recognition of how selective pressures vary in space and time.

Although predation has a lethal effect on prey, mature terrestrial plants are rarely killed by herbivores, but herbivory can change plant allelochemistry, cell structure and growth, physiology, morphology, and phenology. This review explores the herbivore-induced indirect effects mediated by such plant responses following herbivory in terrestrial systems. Herbivore-induced indirect effects are ubiquitous in many plant–herbivore systems, and indirect interactions occur among temporally separated, spatially separated, and taxonomically distinct herbivore species. Unlike interspecific competition, herbivores can benefit each other through plant-mediated indirect effects. Herbivore-induced changes in plants occur at low levels of herbivory, which increases the likelihood of plant-mediated indirect interactions between herbivores. The herbivore-induced indirect effects result in interaction linkages, which alter species richness and abundance in arthropod communities. Such interaction linkages should be depicted using indirect interaction webs, which incorporate nontrophic, indirect links. The idea of interaction linkages by herbivore-induced indirect effects that shape community organization and biodiversity is an important revision of the traditional view of plant-based terrestrial food webs.

The predominantly wind-pollinated order Poales includes about one third of all monocot (Angiosperm) species, with c. 20,000 species dominating modern savanna and steppe vegetation. Recent improvements in understanding relationships within the order allow phylogenetic optimizations of habitat preferences and adaptive character states, enabling exploration of the factors that have influenced evolution in this successful order. Poales probably originated in the late Cretaceous in wet nutrient–poor sunny habitats. By the Paleogene the lineage had diversified into swamps, the forest understory, epiphytic habitats, and nutrient-poor heathlands. The Neogene saw major diversifications of the grasses and possibly the sedges into fire-adapted vegetation in seasonal climates and low atmospheric CO2. Diversification into these habitats was facilitated by morphological features such as the sympodial habit and physiological factors that allowed frequent evolution of CO2-concentrating mechanisms.

In contrast to Bateman's principle, there is now increasing evidence that female fitness can depend on the number of mates obtained. A number of genetic benefits have been proposed for the evolution of polyandry. A meta-analysis of available data suggests that polyandry, rather than multiple mating, can have a weak but significant general effect on embryo viability, as indicated by egg hatching success. Although this effect is generally regarded as evidence in favor of the genetic incompatibility hypothesis, appropriate data that test for intrinsic sire effects on embryo viability are generally unavailable. Moreover, maternal effects that could generate the result have not been adequately controlled, and there is little unequivocal evidence to suggest that fertilization is biased toward sperm bearing genotypes that would enhance offspring viability. Greater effort is required in these areas to elucidate the mechanisms underlying observed fitness effects of polyandry.

Individual-based models (IBMs) allow the explicit inclusion of individual variation in greater detail than do classical differential-equation and difference-equation models. Inclusion of such variation is important for continued progress in ecological and evolutionary theory. We provide a conceptual basis for IBMs by describing five major types of individual variation in IBMs: spatial, ontogenetic, phenotypic, cognitive, and genetic. IBMs are now used in almost all subfields of ecology and evolutionary biology. We map those subfields and look more closely at selected key papers on fish recruitment, forest dynamics, sympatric speciation, metapopulation dynamics, maintenance of diversity, and species conservation. Theorists are currently divided on whether IBMs represent only a practical tool for extending classical theory to more complex situations, or whether individual-based theory represents a radically new research program. We feel that the tension between these two poles of thinking can be a source of creativity in ecology and evolutionary theory.

Plant secondary metabolites (PSMs) significantly impact the nutritional ecology of terrestrial vertebrate herbivores. Herbivores have a wide range of mechanisms (herbivore offenses) to mitigate the negative effects of PSMs. We discuss several behavioral and physiological offenses used by terrestrial vertebrates. Several newly recognized herbivore offenses such as regulated absorption and regulation of toxin intake are presented. We give a detailed description of the biotransformation system with respect to PSMs. We also summarize recent findings of plant–animal interactions for lizards, birds, and mammals. Finally, we discuss some new tools that can be applied to long-standing questions of plant–vertebrate interactions.

We explore empirical and theoretical evidence for the functional significance of plant-litter diversity and the extraordinary high diversity of decomposer organisms in the process of litter decomposition and the consequences for biogeochemical cycles. Potential mechanisms for the frequently observed litter-diversity effects on mass loss and nitrogen dynamics include fungi-driven nutrient transfer among litter species, inhibition or stimulation of microorganisms by specific litter compounds, and positive feedback of soil fauna due to greater habitat and food diversity. Theory predicts positive effects of microbial diversity that result from functional niche complementarity, but the few existing experiments provide conflicting results. Microbial succession with shifting enzymatic capabilities enhances decomposition, whereas antagonistic interactions among fungi that compete for similar resources slow litter decay. Soil-fauna diversity manipulations indicate that the number of trophic levels, species identity, and the presence of keystone species have a strong impact on decomposition, whereas the importance of diversity within functional groups is not clear at present. In conclusion, litter species and decomposer diversity can significantly influence carbon and nutrient turnover rates; however, no general or predictable pattern has emerged. Proposed mechanisms for diversity effects need confirmation and a link to functional traits for a comprehensive understanding of how biodiversity interacts with decomposition processes and the consequences of ongoing biodiversity loss for ecosystem functioning.

The multi-gene family that encodes ribosomal RNA (the rDNA) has been the subject of numerous review articles examining its structure and function, as well as its use as a molecular systematic marker. The purpose of this review is to integrate information about structural and functional aspects of rDNA that impact the ecology and evolution of organisms. We examine current understanding of the impact of length heterogeneity and copy number in the rDNA on fitness and the evolutionary ecology of organisms. We also examine the role that elemental ratios (biological stoichiometry) play in mediating the impact of rDNA variation in natural populations and ecosystems. The body of work examined suggests that there are strong reciprocal feedbacks between rDNA and the ecology of all organisms, from microbes to metazoans, mediated through increased phosphorus demand in organisms with high rRNA content.

Plant adaptation to serpentine soil has been a topic of study for many decades, yet investigation of the genetic component of this adaptation has only recently begun. We review the defining properties of serpentine soil and the pioneering work leading to three established physiological and evolutionary mechanisms hypothesized to be responsible for serpentine tolerance: tolerance of a low calcium-to-magnesium ratio, avoidance of Mg toxicity, or a high Mg requirement. In addition, we review recent work in serpentine ecology documenting the high proportion of endemic species present, the adaptive morphologies of serpentine-tolerant plants, and the distinctive structure of serpentine communities. Studies of the physiological mechanisms proposed to confer serpentine tolerance have shown that uptake of particular ions and heavy metals varies between serpentine-tolerant and -intolerant species. Recent studies examining the genetic basis of serpentine adaptation have shown serpentine-adaptive quantitative trait loci (QTL) to have large phenotypic effects, drought tolerance to be as important as metal tolerance, and serpentine adaptation to have evolved independently multiple times within species. Investigations of plant races and species adapted to contrasting soil types have shown disparate flowering times, divergent floral morphologies, and pollen incompatibility to contribute to reproductive isolation. Finally, we propose that future studies involving serpentine systems should merge the fields of ecology, evolution, physiology, and genetics.

It has often been argued that conserving biodiversity is necessary for maintaining ecosystem functioning. We critically evaluate the current evidence for this argument. Although there is substantial evidence that diversity is able to affect function, particularly for plant communities, it is unclear if these patterns will hold for realistic scenarios of extinctions, multitrophic communities, or larger spatial scales. Experiments are conducted at small spatial scales, the very scales at which diversity tends to increase owing to exotics. Stressors may affect function by many pathways, and diversity-mediated effects on function may be a minor pathway, except in the case of multiple-stressor insurance effects. In general, the conservation case is stronger for stability measures of function than stock and flux measures, in part because it is easier to attribute value unambiguously to stability and in part because stock and flux measures of functions are anticipated to be more affected by multitrophic dynamics. Nor is biodiversity-ecosystem function theory likely to help conservation managers in practical decisions, except in the particular case of restoration. We give recommendations for increasing the relevance of this area of research for conservation.

One of the greatest mass extinctions in Earth's history occurred at the end of the Cretaceous era, sixty-five million years (Myr) ago. Considerable evidence indicates that the impact of a large asteroid or comet was the ultimate cause of this extraordinary event. At the time of mass extinction, the organic flux to the deep sea collapsed, and production of calcium carbonate by marine plankton radically declined. These biogeochemical processes did not fully recover for a few million years. The drastic decline and long lag in final recovery of these processes are most simply explained as consequences of open-ocean ecosystem alteration by the mass extinction. If this explanation is correct, the extent and timing of marine biogeochemical recovery from the end-Cretaceous event was ultimately contingent on the extent and timing of open-ocean ecosystem recovery. The biogeochemical recovery may in turn have created new evolutionary opportunities for a diverse array of marine organisms.

Landscape ecology focuses on the reciprocal interactions between spatial pattern and ecological processes, and it is well integrated with ecology. The field has grown rapidly over the past 15 years. The persistent influence of land-use history and natural disturbance on contemporary ecosystems has become apparent. Development of pattern metrics has largely stabilized, and they are widely used to relate landscape pattern to ecological responses. Analyses conducted at multiple scales have demonstrated the importance of landscape pattern for many taxa, and spatially mediated interspecific interactions are receiving increased attention. Disturbance remains prominent in landscape studies, and current research is addressing disturbance interactions. Integration of ecosystem and landscape ecology remains challenging but should enhance understanding of landscape function. Landscape ecology should continue to refine knowledge of when spatial heterogeneity is fundamentally important, rigorously test the generality of its concepts, and develop a more mechanistic understanding of the relationships between pattern and process.

Aphids and ants are two abundant and highly successful insect groups, which often live in the same habitat and therefore are likely to interact with one another. Whether the outcome of such an interaction is a predator-prey or mutualistic one is dependent on what each partner has to offer relative to the needs of the other. Consequently, understanding why some aphids enter mutualistic interactions with ants is dependent on understanding the physiological, ecological, and evolutionary traits of both partners. This includes an appreciation of the spatial, temporal, and taxonomic context in which mutualistic interactions developed. In this review, we use aphid-ant interactions to illustrate the whole range of interactions from antagonistic to mutualistic as well as to identify the processes affecting the degree of association and in particular the context within which such interactions evolved. The constraints of establishing and maintaining beneficial interactions between aphids and ants is addressed from a cost-benefit perspective. Prospects for future research are identified to further the understanding of the patterns and processes associated with aphid-ant relationships.

Immune responses can cause severe disease, despite the role immunity plays in defending against parasitism. Indeed, immunopathology is a remarkably common cause of disease and has strong impacts upon both host and parasite fitness. Why has immune-mediated disease not been eliminated by natural selection? What constraints might immunopathology impose upon the evolution of resistance? In this review, we explore two major mechanistic causes of immunopathology in mammals and consider how such disease may have influenced immune system design. We then propose hypotheses that could explain the failure of natural selection to eliminate immunopathology. Finally, we suggest how the evolution of strategies for parasite virulence and host resistance may be shaped by this “double-edged sword” of immunity. Future work may reveal whether immunopathology constrains the evolution of resistance in all host taxa.

Most metazoans engage in recombination every generation. In theory this is associated with considerable cost, such as the production of males, so that asexual organisms, which do not pay this cost, should be able to invade populations of sexuals. Some asexuals depend on sperm of sexual males to trigger embryogenesis, a reproductive mode called gynogenesis. The genetic information of males is typically not used. Theory predicts that such mating complexes are short-lived and highly unstable. Sperm dependency is not only the defining feature of the biology of gynogenetic metazoans, it is also a major puzzle in evolutionary biology. Organisms that apparently combine disadvantages of both sexuality and asexuality are a serious challenge to theory. A number of questions about these systems are still unresolved.

Understanding and predicting the dynamics of multispecies systems generally require estimates of interaction strength among species. Measuring interaction strength is difficult because of the large number of interactions in any natural system, long-term feedback, multiple pathways of effects between species pairs, and possible nonlinearities in interaction-strength functions. Presently, the few studies that extensively estimate interaction strength suggest that distributions of interaction strength tend to be skewed toward few strong and many weak interactions. Modeling studies indicate that such skewed patterns tend to promote system stability and arise during assembly of persistent communities. Methods for estimating interaction strength efficiently from traits of organisms, such as allometric relationships, show some promise. Methods for estimating community response to environmental perturbations without an estimate of interaction strength may also be of use. Spatial and temporal scale may affect patterns of interaction strength, but these effects require further investigation and new multispecies modeling frameworks. Future progress will be aided by development of long-term multispecies time series of natural communities, by experimental tests of different methods for estimating interaction strength, and by increased understanding of nonlinear functional forms.

Investigation into model selection has a long history in the statistical literature. As model-based approaches begin dominating systematic biology, increased attention has focused on how models should be selected for distance-based, likelihood, and Bayesian phylogenetics. Here, we review issues that render model-based approaches necessary, briefly review nucleotide-based models that attempt to capture relevant features of evolutionary processes, and review methods that have been applied to model selection in phylogenetics: likelihood-ratio tests, AIC, BIC, and performance-based approaches.

Quantifying the extent to which seed production is limited by the availability of pollen has been an area of intensive empirical study over the past few decades. Whereas theory predicts that pollen augmentation should not increase seed production, numerous empirical studies report significant and strong pollen limitation. Here, we use a variety of approaches to examine the correlates of pollen limitation in an effort to understand its occurrence and importance in plant evolutionary ecology. In particular, we examine the role of recent ecological perturbations in influencing pollen limitation and discuss the relation between pollen limitation and plant traits. We find that the magnitude of pollen limitation observed in natural populations depends on both historical constraints and contemporary ecological factors.