Daniel I. Bolnick

The Ecology of Individuals: Incidence and Implications of Individual Specialization

Most empirical and theoretical studies of resource use and population dynamics treat conspecific individuals as ecologically equivalent. This simplification is only justified if interindividual niche variation is rare, weak, or has a trivial effect on ecological processes. This article reviews the incidence, degree, causes, and implications of individual‐level niche variation to challenge these simplifications. Evidence for individual specialization is available for 93 species distributed across a broad range of taxonomic groups. Although few studies have quantified the degree to which individuals are specialized relative to their population, between‐individual variation can sometimes comprise the majority of the population’s niche width. The degree of individual specialization varies widely among species and among populations, reflecting a diverse array of physiological, behavioral, and ecological mechanisms that can generate intrapopulation variation. Finally, individual specialization has potentially important ecological, evolutionary, and conservation implications. Theory suggests that niche variation facilitates frequency‐dependent interactions that can profoundly affect the population’s stability, the amount of intraspecific competition, fitness‐function shapes, and the population’s capacity to diversify and speciate rapidly. Our collection of case studies suggests that individual specialization is a widespread but underappreciated phenomenon that poses many important but unanswered questions.

SCARED TO DEATH? THE EFFECTS OF INTIMIDATION AND CONSUMPTION IN PREDATOR–PREY INTERACTIONS

Predation is a central feature of ecological communities. Most theoretical and empirical studies of predation focus on the consequences of predators consuming their prey. Predators reduce prey population densities through direct consumption (a density- mediated interaction, DMI), a process that may indirectly affect the preys resources, com- petitors, and other predators. However, predators can also affect prey population density by stimulating costly defensive strategies. The costs of these defensive strategies can include reduced energy income, energetic investment in defensive structures, lower mating success, increased vulnerability to other predators, or emigration. Theoretical and empirical studies confirm the existence of these induced costs (trait-mediated interactions, TMIs); however, the relative importance of intimidation (TMI) and consumption (DMI) effects remains an open question. We conducted a meta-analysis assessing the magnitude of both TMIs and DMIs in predator-prey interactions. On average, the impact of intimidation on prey de- mographics was at least as strong as direct consumption (63% and 51% the size of the total predator effect, respectively). This contrast is even more pronounced when we consider the cascading effects of predators on their preys resources: density effects attenuated through food chains, while TMIs remained strong, rising to 85% of the total predator effect. Predators can thus strongly influence resource density even if they consume few prey items. Finally, intimidation was more important in aquatic than terrestrial ecosystems. Our results suggest that the costs of intimidation, traditionally ignored in predator-prey ecology, may actually be the dominant facet of trophic interactions.

Why intraspecific trait variation matters in community ecology

Natural populations consist of phenotypically diverse individuals that exhibit variation in their demographic parameters and intra- and inter-specific interactions. Recent experimental work indicates that such variation can have significant ecological effects. However, ecological models typically disregard this variation and focus instead on trait means and total population density. Under what situations is this simplification appropriate? Why might intraspecific variation alter ecological dynamics? In this review we synthesize recent theory and identify six general mechanisms by which trait variation changes the outcome of ecological interactions. These mechanisms include several direct effects of trait variation per se and indirect effects arising from the role of genetic variation in trait evolution.

Intraspecific competition drives increased resource use diversity within a natural population

Resource competition is thought to play a major role in driving evolutionary diversification. For instance, in ecological character displacement, coexisting species evolve to use different resources, reducing the effects of interspecific competition. It is thought that a similar diversifying effect might occur in response to competition among members of a single species. Individuals may mitigate the effects of intraspecific competition by switching to use alternative resources not used by conspecific competitors. This diversification is the driving force in some models of sympatric speciation, but has not been demonstrated in natural populations. Here, we present experimental evidence confirming that competition drives ecological diversification within natural populations. We manipulated population density of three-spine sticklebacks (Gasterosteus aculeatus) in enclosures in a natural lake. Increased population density led to reduced prey availability, causing individuals to add alternative prey types to their diet. Since phenotypically different individuals added different alternative prey, diet variation among individuals increased relative to low-density control enclosures. Competition also increased the diet–morphology correlations, so that the frequency-dependent interactions were stronger in high competition. These results not only confirm that resource competition promotes niche variation within populations, but also show that this increased diversity can arise via behavioural plasticity alone, without the evolutionary changes commonly assumed by theory.

MEASURING INDIVIDUAL-LEVEL RESOURCE SPECIALIZATION

Many apparently generalized species are in fact composed of individual specialists that use a small subset of the populations resource distribution. Niche variation is usually established by testing the null hypothesis that individuals draw from a common resource distribution. This approach encourages a publication bias in which negative results are rarely reported, and obscures variation in the degree of individual specialization, limiting our ability to carry out comparative studies of the causes or consequences of niche variation. To facilitate studies of the degree of individual specialization, this paper outlines four quantitative indices of intrapopulation variation in resource use. Traditionally, such variation has been measured by partitioning the populations total niche width into within- and between-individual, sex, or phenotype components. We suggest two alternative measures that quantify the mean resource overlap between an individual and its population, and we discuss the advantages and disadvantages of all four measures. The utility of all indices depends on the quality of the empirical data. If resources are measured in a coarse-grained manner, individuals may falsely appear generalized. Alternatively, specialization may be overestimated by cross-sectional sampling schemes where diet variation can reflect a patchy environment. Isotope ratios, parasites, or diet-morphology correlations can complement cross-sectional data to establish temporal consistency of individual specialization.

REVISITING THE CLASSICS: CONSIDERING NONCONSUMPTIVE EFFECTS IN TEXTBOOK EXAMPLES OF PREDATOR-PREY INTERACTIONS

Predator effects on prey dynamics are conventionally studied by measuring changes in prey abundance attributed to consumption by predators. We revisit four classic examples of predator-prey systems often cited in textbooks and incorporate subsequent studies of nonconsumptive effects of predators (NCE), defined as changes in prey traits (e.g., behavior, growth, development) measured on an ecological time scale. Our review revealed that NCE were integral to explaining lynx-hare population dynamics in boreal forests, cascading effects of top predators in Wisconsin lakes, and cascading effects of killer whales and sea otters on kelp forests in nearshore marine habitats. The relative roles of consumption and NCE of wolves on moose and consequent indirect effects on plant communities of Isle Royale depended on climate oscillations. Nonconsumptive effects have not been explicitly tested to explain the link between planktonic alewives and the size structure of the zooplankton, nor have they been invoked to attribute keystone predator status in intertidal communities or elsewhere. We argue that both consumption and intimidation contribute to the total effects of keystone predators, and that characteristics of keystone consumers may differ from those of predators having predominantly NCE. Nonconsumptive effects are often considered as an afterthought to explain observations inconsistent with consumption-based theory. Consequently, NCE with the same sign as consumptive effects may be overlooked, even though they can affect the magnitude, rate, or scale of a prey response to predation and can have important management or conservation implications. Nonconsumptive effects may underlie other classic paradigms in ecology, such as delayed density dependence and predator-mediated prey coexistence. Revisiting classic studies enriches our understanding of predator-prey dynamics and provides compelling rationale for ramping up efforts to consider how NCE affect traditional predator-prey models based on consumption, and to compare the relative magnitude of consumptive and NCE of predators.

Comparative support for the niche variation hypothesis that more generalized populations also are more heterogeneous

There is extensive evidence that some species of ecological generalists, which use a wide diversity of resources, are in fact heterogeneous collections of relatively specialized individuals. This within-population variation, or “individual specialization,” is a key requirement for frequency-dependent interactions that may drive a variety of types of evolutionary diversification and may influence the population dynamics and ecological interactions of species. Consequently, it is important to understand when individual specialization is likely to be strong or weak. The niche variation hypothesis (NVH) suggests that populations tend to become more generalized when they are released from interspecific competition. This niche expansion was proposed to arise via increased variation among individuals rather than increased individual niche breadth. Consequently, we expect ecological generalists to exhibit stronger individual specialization, but this correlation has been repeatedly rejected by empiricists. The drawback with previous empirical tests of the NVH is that they use morphological variation as a proxy for niche variation, ignoring the role of behavior and complex phenotype–function relationships. Here, we used diet data to directly estimate niche variation among individuals. Consistent with the NVH, we show that more generalized populations also exhibit more niche variation. This trend is quite general, appearing in all five case studies examined: three-spine stickleback, Eurasian perch, Anolis lizards, intertidal gastropods, and a community of neotropical frogs. Our results suggest that generalist populations may tend to be more ecologically variable. Whether this translates into greater genetic variation, evolvability, or ecological stability remains to be determined.

Many-to-One Mapping of Form to Function: A General Principle in Organismal Design? 1

Abstract We introduce the concept of many-to-one mapping of form to function and suggest that this emergent property of complex systems promotes the evolution of physiological diversity. Our work has focused on a 4-bar linkage found in labrid fish jaws that transmits muscular force and motion from the lower jaw to skeletal elements in the upper jaws. Many different 4-bar shapes produce the same amount of output rotation in the upper jaw per degree of lower jaw rotation, a mechanical property termed Maxillary KT. We illustrate three consequences of many-to-one mapping of 4-bar shape to Maxillary KT. First, many-to-one mapping can partially decouple morphological and mechanical diversity within clades. We found with simulations of 4-bars evolving on phylogenies of 500 taxa that morphological and mechanical diversity were only loosely correlated (R2 = 0.25). Second, redundant mapping permits the simultaneous optimization of more than one mechanical property of the 4-bar. Labrid fishes have capitalized on this flexibility, as illustrated by several species that have Maxillary KT = 0.8 but have different values of a second property, Nasal KT. Finally, many-to-one mapping may increase the influence of historical factors in determining the evolution of morphology. Using a genetic model of 4-bar evolution we exerted convergent selection on three different starting 4-bar shapes and found that mechanical convergence only created morphological convergence in simulations where the starting forms were similar. Many-to-one mapping is widespread in physiological systems and operates at levels ranging from the redundant mapping of genotypes to phenotypes, up to the morphological basis of whole-organism performance. This phenomenon may be involved in the uneven distribution of functional diversity seen among animal lineages.

Ecological release from interspecific competition leads to decoupled changes in population and individual niche width

A speciess niche width reflects a balance between the diversifying effects of intraspecific competition and the constraining effects of interspecific competition. This balance shifts when a species from a competitive environment invades a depauperate habitat where interspecific competition is reduced. The resulting ecological release permits population niche expansion, via increased individual niche widths and/or increased among-individual variation. We report an experimental test of the theory of ecological release in three-spine stickleback (Gasterosteus aculeatus). We factorially manipulated the presence or absence of two interspecific competitors: juvenile cut-throat trout (Oncorhynchus clarki) and prickly sculpin (Cottus asper). Consistent with the classic niche variation hypothesis, release from trout competition increased stickleback population niche width via increased among-individual variation, while individual niche widths remained unchanged. In contrast, release from sculpin competition had no effect on population niche width, because increased individual niche widths were offset by decreased between-individual variation. Our results confirm that ecological release from interspecific competition can lead to increases in niche width, and that these changes can occur on behavioural time scales. Importantly, we find that changes in population niche width are decoupled from changes in the niche widths of individuals within the population.

Microgeographic adaptation and the spatial scale of evolution

Local adaptation has been a major focus of evolutionary ecologists working across diverse systems for decades. However, little of this research has explored variation at microgeographic scales because it has often been assumed that high rates of gene flow will prevent adaptive divergence at fine spatial scales. Here, we establish a quantitative definition of microgeographic adaptation based on Wrights dispersal neighborhood that standardizes dispersal abilities, enabling this measure to be compared across species. We use this definition to evaluate growing evidence of evolutionary divergence at fine spatial scales. We identify the main mechanisms known to facilitate this adaptation and highlight illustrative examples of microgeographic evolution in nature. Collectively, this evidence requires that we revisit our understanding of the spatial scale of adaptation and consider how microgeographic adaptation and its driving mechanisms can fundamentally alter ecological and evolutionary dynamics in nature.