James A. Fordyce

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.

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.

Homoploid Hybrid Speciation in an Extreme Habitat

According to theory, homoploid hybrid speciation, which is hybrid speciation without a change in chromosome number, is facilitated by adaptation to a novel or extreme habitat. Using molecular and ecological data, we found that the alpine-adapted butterflies in the genus Lycaeides are the product of hybrid speciation. The alpine populations possess a mosaic genome derived from both L. melissa and L. idas and are differentiated from and younger than their putative parental species. As predicted, adaptive traits may allow for persistence in the environmentally extreme alpine habitat and reproductively isolate these populations from their parental species.

The evolutionary consequences of ecological interactions mediated through phenotypic plasticity

SUMMARY Phenotypic plasticity describes the capacity of a genotype to exhibit a range of phenotypes in response to variation in the environment. Environmental variation encompasses both abiotic and biotic components of the environment, including interactions among organisms. The strength and outcome of many ecological interactions, ranging from antagonism to mutualism, are mediated through the phenotypically plastic responses of one or more players in the interaction. Herein, three broadly defined, non-mutually exclusive, evolutionary consequences of ecological interactions mediated through phenotypic plasticity are discussed. (1) The predictable plastic response of one partner can favor behaviors, physiological responses, and life history traits of an interacting partner that manipulate, circumvent, or ameliorate the response of that partner. (2) Phenotypic plasticity can generate substantial spatial and temporal variation within and among populations. Such phenotypic variation can depend on the density and identity of interacting players in an ecological community, and can ultimately affect the evolutionary outcome of ecological interactions. (3) Phenotypic plasticity affects the strength and direction of natural selection. Ecological interactions mediated through phenotypic plasticity are ubiquitous in nature, and the potential evolutionary consequences of these interactions illustrate the complexity inherent in understanding evolution in a community context.

Compounded effects of climate change and habitat alteration shift patterns of butterfly diversity.

Climate change and habitat destruction have been linked to global declines in vertebrate biodiversity, including mammals, amphibians, birds, and fishes. However, invertebrates make up the vast majority of global species richness, and the combined effects of climate change and land use on invertebrates remain poorly understood. Here we present 35 years of data on 159 species of butterflies from 10 sites along an elevational gradient spanning 0–2,775 m in a biodiversity hotspot, the Sierra Nevada Mountains of Northern California. Species richness has declined at half of the sites, with the most severe reductions at the lowest elevations, where habitat destruction is greatest. At higher elevations, we observed clear upward shifts in the elevational ranges of species, consistent with the influence of global warming. Taken together, these long-term data reveal the interacting negative effects of human-induced changes on both the climate and habitat available to butterfly species in California. Furthermore, the decline of ruderal, disturbance-associated species indicates that the traditional focus of conservation efforts on more specialized and less dispersive species should be broadened to include entire faunas when estimating and predicting the effects of pervasive stressors.

What, if anything, is sympatric speciation?

Sympatric speciation has always fascinated evolutionary biologists, and for good reason; it pits diversifying selection directly against the tendency of sexual reproduction to homogenize populations. However, different investigators have used different definitions of sympatric speciation and different criteria for diagnosing cases of sympatric speciation. Here, we explore some of the definitions that have been used in empirical and theoretical studies. Definitions based on biogeography do not always produce the same conclusions as definitions based on population genetics. The most precise definitions make sympatric speciation an infinitesimal end point of a continuum. Because it is virtually impossible to demonstrate the occurrence of such a theoretical extreme, we argue that testing whether a case fits a particular definition is less informative than evaluating the biological processes affecting divergence. We do not deny the importance of geographical context for understanding divergence. Rather, we believe this context can be better understood by modelling and measuring quantities, such as gene flow and selection, rather than assigning cases to discrete categories like sympatric and allopatric speciation.

GENOMIC REGIONS WITH A HISTORY OF DIVERGENT SELECTION AFFECT FITNESS OF HYBRIDS BETWEEN TWO BUTTERFLY SPECIES

Speciation is the process by which reproductively isolated lineages arise, and is one of the fundamental means by which the diversity of life increases. Whereas numerous studies have documented an association between ecological divergence and reproductive isolation, relatively little is known about the role of natural selection in genome divergence during the process of speciation. Here, we use genome‐wide DNA sequences and Bayesian models to test the hypothesis that loci under divergent selection between two butterfly species (Lycaeides idas and L. melissa) also affect fitness in an admixed population. Locus‐specific measures of genetic differentiation between L. idas and L. melissa and genomic introgression in hybrids varied across the genome. The most differentiated genetic regions were characterized by elevated L. idas ancestry in the admixed population, which occurs in L. idas‐like habitat, consistent with the hypothesis that local adaptation contributes to speciation. Moreover, locus‐specific measures of genetic differentiation (a metric of divergent selection) were positively associated with extreme genomic introgression (a metric of hybrid fitness). Interestingly, concordance of differentiation and introgression was only partial. We discuss multiple, complementary explanations for this partial concordance.

Host shifts and evolutionary radiations of butterflies

Ehrlich and Raven proposed a model of coevolution where major host plant shifts of butterflies facilitate a burst of diversification driven by their arrival to a new adaptive zone. One prediction of this model is that reconstructions of historical diversification of butterflies should indicate an increase in diversification rate following major host shifts. Using reconstructed histories of 15 butterfly groups, I tested this prediction and found general agreement with Ehrlich and Ravens model. Butterfly lineages with an inferred major historical host shift showed evidence of diversification rate variation, with a significant acceleration following the host shift. Lineages without an inferred major host shift generally agreed with a constant-rate model of diversification. These results are consistent with the view that host plant associations have played a profound role in the evolutionary history of butterflies, and show that major shifts to chemically distinct plant groups leave a historical footprint that remains detectable today.

Bayesian analysis of molecular variance in pyrosequences quantifies population genetic structure across the genome of Lycaeides butterflies.

The distribution of genetic variation within and among populations is commonly used to infer their demographic and evolutionary histories. This endeavour has the potential to benefit substantially from high‐throughput next‐generation sequencing technologies through a rapid increase in the amount of data available and a corresponding increase in the precision of parameter estimation. Here we report the results of a phylogeographic study of the North American butterfly genus Lycaeides using 454 sequence data. This study serves the dual purpose of demonstrating novel molecular and analytical methods for population genetic analyses with 454 sequence data and expanding our knowledge of the phylogeographic history of Lycaeides. We obtained 341 045 sequence reads from 12 populations that we were able to assemble into 15 262 contigs (most of which were variable), representing one of the largest population genetic data sets for a non‐model organism to date. We examined patterns of genetic variation using a hierarchical Bayesian analysis of molecular variance model, which provides precise estimates of genome‐level φST while appropriately modelling uncertainty in locus‐specific φST. We found that approximately 36% of sequence variation was partitioned among populations, suggesting historical or current isolation among the sampled populations. Estimates of pairwise genome‐level φST were largely consistent with a previous phylogeographic model for Lycaeides, suggesting fragmentation into two to three refugia during Pleistocene glacial cycles followed by post‐Pleistocene range expansion and secondary contact leading to introgressive hybridization. This study demonstrates the potential of using genome‐level data to better understand the phylogeographic history of populations.

What can DNA tell us about biological invasions

It is often hoped that population genetics can answer questions about the demographic and geographic dynamics of recent biological invasions. Conversely, invasions with well-known histories are sometimes billed as opportunities to test methods of population genetic inference. In both cases, underappreciated limitations constrain the usefulness of genetic methods. The most significant is that human-caused invasions have occurred on historical timescales that are orders of magnitude smaller than the timescales of mutation and genetic drift for most multicellular organisms. Analyses based on the neutral theory of molecular evolution cannot resolve such rapid dynamics. Invasion histories cannot be reconstructed in the same way as biogeographic changes occurring over millenia. Analyses assuming equilibrium between mutation, drift, gene flow, and selection will rarely be applicable, and even methods designed for explicitly non-equilibrium questions often require longer timescales than the few generations of most invasions of current concern. We identified only a few population genetic questions that are tractable over such short timescales. These include comparison of alternative hypotheses for the geographic origin of an invasion, testing for bottlenecks, and hybridization between native and invasive species. When proposing population genetic analysis of a biological invasion, we recommend that biologists ask (i) whether the questions to be addressed will materially affect management practice or policy, and (ii) whether the proposed analyses can really be expected to address important population genetic questions. Despite our own enthusiasm for population genetic research, we conclude that genetic analysis of biological invasions is justified only under exceptional circumstances.