Emily W. Ruell

Non-adaptive plasticity potentiates rapid adaptive evolution of gene expression in nature.

Phenotypic plasticity is the capacity for an individual genotype to produce different phenotypes in response to environmental variation. Most traits are plastic, but the degree to which plasticity is adaptive or non-adaptive depends on whether environmentally induced phenotypes are closer or further away from the local optimum. Existing theories make conflicting predictions about whether plasticity constrains or facilitates adaptive evolution. Debate persists because few empirical studies have tested the relationship between initial plasticity and subsequent adaptive evolution in natural populations. Here we show that the direction of plasticity in gene expression is generally opposite to the direction of adaptive evolution. We experimentally transplanted Trinidadian guppies (Poecilia reticulata) adapted to living with cichlid predators to cichlid-free streams, and tested for evolutionary divergence in brain gene expression patterns after three to four generations. We find 135 transcripts that evolved parallel changes in expression within the replicated introduction populations. These changes are in the same direction exhibited in a native cichlid-free population, suggesting rapid adaptive evolution. We find 89% of these transcripts exhibited non-adaptive plastic changes in expression when the source population was reared in the absence of predators, as they are in the opposite direction to the evolved changes. By contrast, the remaining transcripts exhibiting adaptive plasticity show reduced population divergence. Furthermore, the most plastic transcripts in the source population evolved reduced plasticity in the introduction populations, suggesting strong selection against non-adaptive plasticity. These results support models predicting that adaptive plasticity constrains evolution, whereas non-adaptive plasticity potentiates evolution by increasing the strength of directional selection. The role of non-adaptive plasticity in evolution has received relatively little attention; however, our results suggest that it may be an important mechanism that predicts evolutionary responses to new environments.Phenotypic plasticity is the capacity for an individual genotype to produce different phenotypes in response to environmental variation. Most traits are plastic, but the degree to which plasticity is adaptive or non-adaptive depends on whether environmentally induced phenotypes are closer or further away from the local optimum. Existing theories make conflicting predictions about whether plasticity constrains or facilitates adaptive evolution. Debate persists because few empirical studies have tested the relationship between initial plasticity and subsequent adaptive evolution in natural populations. Here we show that the direction of plasticity in gene expression is generally opposite to the direction of adaptive evolution. We experimentally transplanted Trinidadian guppies (Poecilia reticulata) adapted to living with cichlid predators to cichlid-free streams, and tested for evolutionary divergence in brain gene expression patterns after three to four generations. We find 135 transcripts that evolved parallel changes in expression within the replicated introduction populations. These changes are in the same direction exhibited in a native cichlid-free population, suggesting rapid adaptive evolution. We find 89% of these transcripts exhibited non-adaptive plastic changes in expression when the source population was reared in the absence of predators, as they are in the opposite direction to the evolved changes. By contrast, the remaining transcripts exhibiting adaptive plasticity show reduced population divergence. Furthermore, the most plastic transcripts in the source population evolved reduced plasticity in the introduction populations, suggesting strong selection against non-adaptive plasticity. These results support models predicting that adaptive plasticity constrains evolution, whereas non-adaptive plasticity potentiates evolution by increasing the strength of directional selection. The role of non-adaptive plasticity in evolution has received relatively little attention; however, our results suggest that it may be an important mechanism that predicts evolutionary responses to new environments.

ESTIMATING BOBCAT POPULATION SIZES AND DENSITIES IN A FRAGMENTED URBAN LANDSCAPE USING NONINVASIVE CAPTURE-RECAPTURE SAMPLING

Abstract Bobcats (Lynx rufus) are valuable indicators of connectivity in the highly fragmented landscape of coastal southern California, yet their population sizes and densities are largely unknown. Using noninvasive scat sampling in a capture–recapture framework, we estimated population sizes for 2 similar areas of natural habitat with differing levels of isolation by human development in Santa Monica Mountains National Recreation Area, California. We used scat transects with geographic information system land-use layers and home-range sizes of bobcats to estimate effective sampling area and population densities. Estimates of population size in the study area connected to a much larger habitat area (26–31 individuals) were similar to estimates for the area that was completely surrounded by development (25–28 individuals). Bobcat densities for the 2 study areas also were similar (ranging from 0.25 to 0.42 bobcat/km2) and likely represent recent population declines because of notoedric mange likely interacting with toxicants. These methods proved effective despite particularly low densities of bobcats and may be especially useful when study areas are geographically isolated, reducing the uncertainty in size of the sampling area.

Predator-Induced Phenotypic Plasticity in Metabolism and Rate of Growth: Rapid Adaptation to a Novel Environment

Novel environments often impose directional selection for a new phenotypic optimum. Novel environments, however, can also change the distribution of phenotypes exposed to selection by inducing phenotypic plasticity. Plasticity can produce phenotypes that either align with or oppose the direction of selection. When plasticity and selection are parallel, plasticity is considered adaptive because it provides a better pairing between the phenotype and the environment. If the plastic response is incomplete and falls short of producing the optimum phenotype, synergistic selection can lead to genetic divergence and bring the phenotype closer to the optimum. In contrast, non-adaptive plasticity should increase the strength of selection, because phenotypes will be further from the local optimum, requiring antagonistic selection to overcome the phenotype-environment mismatch and facilitate adaptive divergence. We test these ideas by documenting predator-induced plasticity for resting metabolic rate and growth rate in populations of the Trinidadian guppy (Poecilia reticulata) adapted to high and low predation. We find reduced metabolic rates and growth rates when cues from a predator are present during development, a pattern suggestive of adaptive and non-adaptive plasticity, respectively. When we compared populations recently transplanted from a high-predation environment into four streams lacking predators, we found evidence for rapid adaptive evolution both in metabolism and growth rate. We discuss the implications for predicting how traits will respond to selection, depending on the type of plasticity they exhibit.

Evaluation of Noninvasive Genetic Sampling Methods for Felid and Canid Populations

Abstract Noninvasive sampling methods provide a means for studying species such as large mammalian carnivores that are difficult to survey using traditional techniques. Focusing on bobcat (Lynx rufus), we compared the effectiveness of noninvasive hair and scat genetic sampling in terms of field sample collection, species identification, and individual identification. We describe a novel hair-snare design and sampling protocol that successfully sampled 4 sympatric carnivore species, bobcat, mountain lion (Felis concolor), coyote (Canis latrans), and gray fox (Urocyon cinereoargenteus), in 3 habitat blocks in coastal southern California, USA. Scat surveys were also successful at sampling bobcats and other carnivores in the area. Hair and scat sampling methods had similar species identification success (81% and 87%, respectively) using mitochondrial DNA amplification and restriction enzyme digestion patterns. Therefore, for studies focused on the distribution and activity of a suite of carnivore species, we recommend a combination of noninvasive methodologies, for example, targeting hair and scat surveys toward species and sites where they are most effective. Because of a higher success rate for scat (85%) than for hair samples (10%) when using 4 microsatellite loci and a multiple-tubes approach to verify individual genotypes, we suggest scat sampling is a better choice for studies that require individual identification of bobcats.

Gene flow and pathogen transmission among bobcats (Lynx rufus) in a fragmented urban landscape.

Urbanization can result in the fragmentation of once contiguous natural landscapes into a patchy habitat interspersed within a growing urban matrix. Animals living in fragmented landscapes often have reduced movement among habitat patches because of avoidance of intervening human development, which potentially leads to both reduced gene flow and pathogen transmission between patches. Mammalian carnivores with large home ranges, such as bobcats (Lynx rufus), may be particularly sensitive to habitat fragmentation. We performed genetic analyses on bobcats and their directly transmitted viral pathogen, feline immunodeficiency virus (FIV), to investigate the effects of urbanization on bobcat movement. We predicted that urban development, including major freeways, would limit bobcat movement and result in genetically structured host and pathogen populations. We analysed molecular markers from 106 bobcats and 19 FIV isolates from seropositive animals in urban southern California. Our findings indicate that reduced gene flow between two primary habitat patches has resulted in genetically distinct bobcat subpopulations separated by urban development including a major highway. However, the distribution of genetic diversity among FIV isolates determined through phylogenetic analyses indicates that pathogen genotypes are less spatially structured—exhibiting a more even distribution between habitat fragments. We conclude that the types of movement and contact sufficient for disease transmission occur with enough frequency to preclude structuring among the viral population, but that the bobcat population is structured owing to low levels of effective bobcat migration resulting in gene flow. We illustrate the utility in using multiple molecular markers that differentially detect movement and gene flow between subpopulations when assessing connectivity.

Fear, food and sexual ornamentation: plasticity of colour development in Trinidadian guppies

The evolution of male ornamentation often reflects compromises between sexual and natural selection, but it may also be influenced by phenotypic plasticity. We investigated the developmental plasticity of male colour ornamentation in Trinidadian guppies in response to two environmental variables that covary in nature: predation risk and food availability. We found that exposure to chemical predator cues delayed the development of pigment-based colour elements, which are conspicuous to visual-oriented predators. Predator cues also reduced the size of colour elements at the time of maturity and caused adult males to be less colourful. To the best of our knowledge, these findings provide the first example of a plastic reduction in the development of a sexually selected male ornament in response to predator cues. The influence of predator cues on ornamentation probably affects individual fitness by reducing conspicuousness to predators, but could reduce attractiveness to females. Reduced food availability during development caused males to delay the development of colour elements and mature later, probably reflecting a physiological constraint, but their coloration at maturity and later in adulthood was largely unaffected, suggesting that variation in food quantity without variation in quality does not contribute to condition dependence of the trait.

Population genetic structure of black-tailed prairie dogs, a highly interactive species, in fragmented urban habitat

Abstract Fragmentation of wildlife populations can have detrimental effects, including genetic differentiation of populations, loss of genetic diversity, and inbreeding depression. We evaluated the genetic structure among isolated colonies of black-tailed prairie dogs (Cynomys ludovicianus) along an urban gradient in southern Denver, Colorado. Urban colonies are important ecologically and for educational purposes, and they serve as source populations for relocation efforts. Levels of genetic differentiation between colonies were high relative to colonies in natural habitat at comparable or greater distances. Prairie dog colonies depend on dispersal among colonies for long-term persistence, and we found evidence for reduced but measurable rates of movement of individual prairie dogs among urban fragments. We observed a trend for smaller and more isolated colonies to exhibit lower genetic diversity, but we did not detect inbreeding in any of the colonies sampled. Isolation-by-distance measures, including measures based on permeability of various features of urban habitat such as roads and development, did not explain genetic differences. Our system represents a possible end point in the genetic consequences of continued loss and isolation of prairie dog colonies as fragmentation increases in both urban and natural landscapes. Urban development could affect dispersal in unexpected and complex ways and requires further study, but prairie dog colonies and their associated wildlife communities in urban areas have the potential for long-term persistence if not extirpated by human activity.

Urban Habitat Fragmentation and Genetic Population Structure of Bobcats in Coastal Southern California

Abstract Although habitat fragmentation is recognized as a primary threat to biodiversity, the effects of urban development on genetic population structure vary among species and landscapes and are not yet well understood. Here we use non-invasive genetic sampling to compare the effects of fragmentation by major roads and urban development on levels of dispersal, genetic diversity, and relatedness between paired bobcat populations in replicate landscapes in coastal southern California. We hypothesized that bobcat populations in sites surrounded by urbanization would experience reduced functional connectivity relative to less isolated nearby populations. Our results show that bobcat genetic population structure is affected by roads and development but not always as predicted by the degree that these landscape features surround fragments. Instead, we suggest that urban development may affect functional connectivity between bobcat populations more by limiting the number and genetic diversity of source populations of migrants than by creating impermeable barriers to dispersal.

Phenotypic plasticity changes correlations of traits following experimental introductions of Trinidadian guppies (Poecilia reticulata).

Colonization of novel environments can alter selective pressures and act as a catalyst for rapid evolution in nature. Theory and empirical studies suggest that the ability of a population to exhibit an adaptive evolutionary response to novel selection pressures should reflect the presence of sufficient additive genetic variance and covariance for individual and correlated traits. As correlated traits should not respond to selection independently, the structure of correlations of traits can bias or constrain adaptive evolution. Models of how multiple correlated traits respond to selection often assume spatial and temporal stability of trait-correlations within populations. Yet, trait-correlations can also be plastic in response to environmental variation. Phenotypic plasticity, the ability of a single genotype to produce different phenotypes across environments, is of particular interest because it can induce population-wide changes in the combination of traits exposed to selection and change the trajectory of evolutionary divergence. We tested the ability of phenotypic plasticity to modify trait-correlations by comparing phenotypic variance and covariance in the body-shapes of four experimental populations of Trinidadian guppies (Poecilia reticulata) to their ancestral population. We found that phenotypic plasticity produced both adaptive and novel aspects of body-shape, which was repeated in all four experimental populations. Further, phenotypic plasticity changed patterns of covariance among morphological characters. These findings suggest our ability to make inferences about patterns of divergence based on correlations of traits in extant populations may be limited if novel environments not only induce plasticity in multiple traits, but also change the correlations among the traits.

Gene Flow Constrains and Facilitates Genetically Based Divergence in Quantitative Traits

Theory predicts that gene flow will decrease phenotypic differences among populations. Correlational studies have in some cases documented constraining effects of gene flow on phenotypic divergence and/or have also provided evidence for local differentiation despite high gene flow. However, correlative studies are unable to evaluate how gene flow affects genetically based phenotypic divergence or the extent to which gene flow constrains adaptive divergence. Translocation experiments using Trinidadian guppies provided an opportunity to test the effects of new gene flow on quantitative traits in native recipient populations. We measured a suite of traits in guppies reared in common garden environments before and multiple generations following gene flow from guppies that originated from a different environment. We interpreted our results in light of a priori predictions based on evolutionary theory and extensive background information about guppies and our focal populations. Although we could not include a spatiotemporal control that would allow us to be certain that the observed changes were directly caused by gene flow, we found that post-gene flow populations showed genetically based shifts in most traits. Whether traits shifted in predicted adaptive directions or whether they became more or less similar to the source population depended on the trait and initial conditions of the population. Our study provided a rare opportunity to test how recent gene flow affects genetically based changes in traits with known adaptive significance, and our results attest to the complex interactions between gene flow and selection.