Thomas J. DeWitt

Costs and limits of phenotypic plasticity

The costs and limits of phenotypic plasticity are thought to have important ecological and evolutionary consequences, yet they are not as well understood as the benefits of plasticity. At least nine ideas exist regarding how plasticity may be costly or limited, but these have rarely been discussed together. The most commonly discussed cost is that of maintaining the sensory and regulatory machinery needed for plasticity, which may require energy and material expenses. A frequently considered limit to the benefit of plasticity is that the environmental cues guiding plastic development can be unreliable. Such costs and limits have recently been included in theoretical models and, perhaps more importantly, relevant empirical studies now have emerged. Despite the current interest in costs and limits of plasticity, several lines of reasoning suggest that they might be difficult to demonstrate.

Costs and limits of phenotypic plasticity: Tests with predator-induced morphology and life history in a freshwater snail

Potential constraints on the evolution of phenotypic plasticity were tested using data from a previous study on predator‐induced morphology and life history in the freshwater snail Physa heterostropha. The benefit of plasticity can be reduced if facultative development is associated with energetic costs, developmental instability, or an impaired developmental range. I examined plasticity in two traits for 29 families of P. heterostropha to see if it was associated with growth rate or fecundity, within‐family phenotypic variance, or the potential to produce extreme phenotypes. Support was found for only one of the potential constraints. There was a strong negative selection gradient for growth rate associated with plasticity in shell shape (β = −0.3, P < 0.0001). This result was attributed to a genetic correlation between morphological plasticity and an antipredator behavior that restricts feeding. Thus, reduced growth associated with morphological plasticity may have had unmeasured fitness benefits. The growth reduction, therefore, is equivocal as a cost of plasticity. Using different fitness components (e.g., survival, fecundity, growth) to seek constraints on plasticity will yield different results in selection gradient analyses. Procedural and conceptual issues related to tests for costs and limits of plasticity are discussed, such as whether constraints on plasticity will be evolutionarily ephemeral and difficult to detect in nature.

Shared and unique features of evolutionary diversification

A fundamental question in evolutionary biology asks whether organisms experiencing similar selective pressures will evolve similar solutions or whether historical contingencies dominate the evolutionary process and yield disparate evolutionary outcomes. It is perhaps most likely that both shared selective forces as well as unique histories play key roles in the course of evolution. Consequently, when multiple species face a common environmental gradient, their patterns of divergence might exhibit both shared and unique elements. Here we describe a general framework for investigating and evaluating the relative importance of these contrasting features of diversification. We examined morphological diversification in three species of livebearing fishes across a predation gradient. All species (Gambusia affinis from the United States of America, Brachyrhaphis rhabdophora from Costa Rica, and Poecilia reticulata from Trinidad) exhibited more elongate bodies, a larger caudal peduncle, and a relatively lower position of the eye in predator populations. This shared response suggests that common selective pressures generated parallel outcomes within three different species. However, each species also exhibited unique features of divergence, which might reflect phylogenetic tendencies, chance events, or localized environmental differences. In this system, we found that shared aspects of divergence were of larger magnitude than unique elements, suggesting common natural selective forces have played a greater role than unique histories in producing the observed patterns of morphological diversification. Assessing the nature and relative importance of shared and unique responses should aid in elucidating the relative generality or peculiarity in evolutionary divergence.

PREDATOR-DRIVEN PHENOTYPIC DIVERSIFICATION IN GAMBUSIA AFFINIS

Abstract Predation is heterogeneously distributed across space and time, and is presumed to represent a major source of evolutionary diversification. In fishes, fast‐starts–udden, high‐energy swimmingbursts–are often importan tin avoiding capture during a predator strike. Thus, in the presence of predators, we might expect evolution of morphological features that facilitate increased fast‐start speed. We tested this hypothesis using populations of western mosquitofish (Gambusia affinis) that differed in level of predation by piscivorous fish. Body morphology of G. affinis males, females, and juveniles diverged in a consistent manner between predatory environments. Fish collected from predator populations exhibited a larger caudal region, smaller head, more elongate body, and a posterior, ventral position of the eye relative to fish from predator‐free populations. Divergence in body shape largely matched a priori predictions based on biomechanical principles, and was evident across space (multiple populations) and time (multiple years). We measured maximum burst‐swimming speed for male mosquitofish and found that individuals from predator populations produced faster bursts than fish from predator‐free populations (about 20% faster). Biomechanical models of fish swimming and intrapopulation morphology‐speed correlations suggested that body shape differences were largely responsible for enhanced locomotor performance in fish from predator populations. Morphological differences also persisted in offspring raised in a common laboratory environment, suggesting a heritable component to the observed morphological divergence. Taken together, these results strongly support the hypothesis that divergent selection between predator regimes has produced the observed phenotypic differences among populations of G. affinis. Based on biomechanical principles and recent findings in other species, it appears that the general ecomorphological model described in this paper will apply for many aquatic taxa, and provide insight into the role of predators in shaping the body form of prey organisms.

Toxic hydrogen sulfide and dark caves: phenotypic and genetic divergence across two abiotic environmental gradients in Poecilia mexicana.

Abstract Divergent natural selection drives evolutionary diversification. It creates phenotypic diversity by favoring developmental plasticity within populations or genetic differentiation and local adaptation among populations. We investigated phenotypic and genetic divergence in the livebearing fish Poecilia mexicana along two abiotic environmental gradients. These fish typically inhabit nonsulfidic surface rivers, but also colonized sulfidic and cave habitats. We assessed phenotypic variation among a factorial combination of habitat types using geometric and traditional morphometrics, and genetic divergence using quantitative and molecular genetic analyses. Fish in caves (sulfidic or not) exhibited reduced eyes and slender bodies. Fish from sulfidic habitats (surface or cave) exhibited larger heads and longer gill filaments. Common-garden rearing suggested that these morphological differences are partly heritable. Population genetic analyses using microsatellites as well as cytochrome b gene sequences indicate high population differentiation over small spatial scale and very low rates of gene flow, especially among different habitat types. This suggests that divergent environmental conditions constitute barriers to gene flow. Strong molecular divergence over short distances as well as phenotypic and quantitative genetic divergence across habitats in directions classic to fish ecomorphology suggest that divergent selection is structuring phenotypic variation in this system.

Multiple prey traits, multiple predators: keys to understanding complex community dynamics

Natural communities can be complex. Such complexity makes it difficult to discern the mechanisms generating community structure. In this paper we review concepts and issues related to linking functional and community studies while also including greater complexity into the experimental realm. These principles are primarily illustrated with case studies involving predation ecology in a freshwater snail-fish-crayfish model system. The system illustrates how predator impacts on prey are mediated by multiple prey traits, correlations between traits, functional trade-offs in predator defence, interactions between predators, and interactions with other community members. We argue for a pluralistic approach to investigating mechanisms of community structure; that is, an approach that integrates many subdisciplines of ecology and evolution. We discuss four main areas that when used together yield important insights on community structure. First, selection gradient analyses formally link functional and community ecology. This formalisation is shown to help identify targets of selection, estimate environment-specific mortality rates, and identify agents of selection in complex communities. Second, we encourage increased focus on emergent community properties (results not predicted based on pairwise species interactions). Third, we emphasise that a community, rather than a web of species interactions, may more profitably be viewed as a network of trait interactions. This trait-centred view makes clear how indirect community effects arise between species that do not interact physically. This perspective also leads to our fourth topic, the integration of phenotypes. Just as populations evolve co-adapted suites of traits, so too should individuals embody integrated trait correlations, termed ‘trait integration’, rather than randomly assembled collections of phenotypes. All the perspectives mentioned above suggest that investigations should focus on multiple traits and multiple environments simultaneously, rather than singular, atomised components of complex systems. D 2002 Elsevier Science B.V. All rights reserved.

Complex phenotype-environment associations revealed in an East African cyprinid.

Environmental factors influence phenotypes directly, as well as indirectly via trait correlations and interactions with other environmental variables. Using nine populations of the African cyprinid Barbus neumayeri, we employed path analysis to examine direct, indirect and total effects of two environmental variables, water flow (WF) and dissolved oxygen (DO), on several morphological traits. WF and DO directly influenced relative gill size, body shape and caudal fin shape in manners consistent with a priori predictions. Indirect effects also played an important role in the system: (1) strong, oppositely signed direct and indirect effects of WF on body shape resulted in a nonsignificant total effect; (2) DO had no direct effect on body shape, but a strong total effect via indirect effects on gill size; (3) WF indirectly influenced gill size via effects on DO. Only through examination of multiple environmental parameters and multiple traits can we hope to understand complex relationships between environment and phenotype.

FORM, FUNCTION, AND FITNESS: PATHWAYS TO SURVIVAL

Abstract Two hypotheses have been considered in the literature regarding how anuran morphology reduces predation risk: by (1) improving escape swimming performance, or (2) using the tail as a lure to draw predator strikes away from the body of the tadpole. We investigated these hypotheses using a modification of the morphology, performance, and fitness path analysis of Arnold (1983, Am. Zool. 23:347–361). Indirect effects of morphology on fitness, as mediated by burst swimming speed, as well as direct paths from morphology to survival with dragonfly larvae were included in the path model. Tadpole morphology did affect burst swimming speed, however, burst swimming speed did not influence survival. Fast tadpoles were larger overall, had long tails, deep tail muscles, and proportionally small bodies. In addition, a shape trait similar to published descriptions of the tail lure morphology had a direct relationship with survival. Thus, only the tail lure effect was supported. This study documents the utility of analyzing multiple trait effects and demonstrates that including direct paths between traits and fitness in the morphology, performance, and fitness path model allows evaluation of alternative hypothesis of selection.

Fused traditional and geometric morphometrics demonstrate pinniped whisker diversity.

Vibrissae (whiskers) are important components of the mammalian tactile sensory system, and primarily function as detectors of vibrotactile information from the environment. Pinnipeds possess the largest vibrissae among mammals and their vibrissal hair shafts demonstrate a diversity of shapes. The vibrissae of most phocid seals exhibit a beaded morphology with repeating sequences of crests and troughs along their length. However, there are few detailed analyses of pinniped vibrissal morphology, and these are limited to a few species. Therefore, we comparatively characterized differences in vibrissal hair shaft morphologies among phocid species with a beaded profile, phocid species with a smooth profile, and otariids with a smooth profile using traditional and geometric morphometric methods. Traditional morphometric measurements (peak-to-peak distance, crest width, trough width and total length) were collected using digital photographs. Elliptic Fourier analysis (geometric morphometrics) was used to quantify the outlines of whole vibrissae. The traditional and geometric morphometric datasets were subsequently combined by mathematically scaling each to true rank, followed by a single eigendecomposition. Quadratic discriminant function analysis demonstrated that 79.3, 97.8 and 100% of individuals could be correctly classified to their species based on vibrissal shape variables in the traditional, geometric and combined morphometric analyses, respectively. Phocids with beaded vibrissae, phocids with smooth vibrissae, and otariids each occupied distinct morphospace in the geometric morphometric and combined data analyses. Otariids split into two groups in the geometric morphometric analysis and gray seals appeared intermediate between beaded- and smooth-whiskered species in the traditional and combined analyses. Vibrissal hair shafts modulate the transduction of environmental stimuli to the mechanoreceptors in the follicle-sinus complex (F-SC), which results in vibrotactile reception, but it is currently unclear how the diversity of shapes affects environmental signal modulation.

Facilitated by nature and agriculture: performance of a specialist herbivore improves with host‑plant life history evolution, domestication, and breeding

Plant defenses against herbivores are predicted to change as plant lineages diversify, and with domestication and subsequent selection and breeding in the case of crop plants. We addressed whether defense against a specialist herbivore declined coincidently with life history evolution, domestication, and breeding within the grass genus Zea (Poaceae). For this, we assessed performance of corn leafhopper (Dalbulus maidis) following colonization of one of four Zea species containing three successive transitions: the evolutionary transition from perennial to annual life cycle, the agricultural transition from wild annual grass to primitive crop cultivar, and the agronomic transition from primitive to modern crop cultivar. Performance of corn leafhopper was measured through seven variables relevant to development speed, survivorship, fecundity, and body size. The plants included in our study were perennial teosinte (Zea diploperennis), Balsas teosinte (Zea mays parviglumis), a landrace maize (Zea mays mays), and a hybrid maize. Perennial teosinte is a perennial, iteroparous species, and is basal in Zea; Balsas teosinte is an annual species, and the progenitor of maize; the landrace maize is a primitive, genetically diverse cultivar, and is ancestral to the hybrid maize; and, the hybrid maize is a highly inbred, modern cultivar. Performance of corn leafhopper was poorest on perennial teosinte, intermediate on Balsas teosinte and landrace maize, and best on hybrid maize, consistent with our expectation of declining defense from perennial teosinte to hybrid maize. Overall, our results indicated that corn leafhopper performance increased most with the agronomic transition, followed by the life history transition, and least with the domestication transition.