Dimensionality and Modularity of Adaptive Variation: Divergence in Threespine Stickleback from Diverse Environments.

AbstractPopulations are subjected to diverse environmental conditions that affect fitness and induce evolutionary or plastic responses, resulting in phenotypic divergence. Some authors contend that such divergence is concentrated along a single major axis of trait covariance even if that axis does not lead populations directly toward a fitness optimum. Other authors argue that divergence can occur readily along many phenotype axes at the same time. We use populations of threespine stickleback (Gasterosteus aculeatus) from 14 lakes with contrasting ecological conditions to find some resolution along the continuum between these two extremes. Unlike many previous studies, we included several functional suites of traits (defensive, swimming, trophic) potentially subject to different sources of selection. We find that populations exhibit dimensionality of divergence that is high enough to preclude a history of constraint along a single axis-both for divergence in multivariate mean trait values and for the structure of trait covariances. Dimensionality varied among trait suites and were strongly influenced by the inclusion of specific traits, and integration of trait suites varied between populations. We leverage this variation into new insights about the process of divergence and suggest that similar analyses could increase understanding of other adaptive radiations.

Freshwater fishes maintain multi-trait phenotypic stability across an environmental gradient in aqueous calcium.

Reductions in a limiting nutrient might be expected to necessitate compromises in the functional traits that depend on that nutrient; yet populations existing in locations with low levels of such nutrients often do not show the expected degradation of functional traits. Indeed, logperch (Percina caprodes), pumpkinseed sunfish (Lepomis gibbosus) and yellow perch (Perca flavescens) residing in low-calcium water in the Upper St. Lawrence River were all previously found to maintain levels of scale calcium comparable to those of conspecific populations in high-calcium water. Yet it remains possible that the maintenance of one functional trait (i.e., scale calcium) under nutrient-limited (i.e., low calcium) conditions could come at the expense of maintaining other functional traits that depend on the same nutrient. The present study therefore examines other calcium-dependent traits, specifically skeletal element sizes and bone densities in the same fish species in the same area. Using radiographs of 101 fish from the three species across four locations (two in high-calcium water and two in low-calcium water), this new work documents multi-trait "homeostasis" along the gradient of water calcium. That is, no effect of calcium regime (low-calcium vs. high-calcium) was detected on any of the measured variables. Further, effect sizes for the skeletal traits were very low - lower even than effect sizes previously documented for scale calcium. These results thus show that native fishes maintain phenotypic stability across a suite of functional traits linked to calcium regulation, perhaps pointing to an "organismal-level homeostasis" scenario rather than a "trait-level homeostasis" scenario.

The pace of modern life, revisited.

Wild populations must continuously respond to environmental changes or they risk extinction. Those responses can be measured as phenotypic rates of change, which can allow us to predict contemporary adaptive responses, some of which are evolutionary. About two decades ago, a database of phenotypic rates of change in wild populations was compiled. Since then, researchers have used (and expanded) this database to examine phenotypic responses to specific types of human disturbance. Here, we update the database by adding 5675 new estimates of phenotypic change. Using this newer version of the data base, now containing 7338 estimates of phenotypic change, we revisit the conclusions of four published articles. We then synthesize the expanded database to compare rates of change across different types of human disturbance. Analyses of this expanded database suggest that: (i) a small absolute difference in rates of change exists between human disturbed and natural populations, (ii) harvesting by humans results in higher rates of change than other types of disturbance, (iii) introduced populations have increased rates of change, and (iv) body size does not increase through time. Thus, findings from earlier analyses have largely held-up in analyses of our new database that encompass a much larger breadth of species, traits, and human disturbances. Lastly, we use new analyses to explore how various types of human disturbances affect rates of phenotypic change, and we call for this database to serve as a steppingstone for further analyses to understand patterns of contemporary phenotypic change.

Integration of swimming kinematics and ram suspension feeding in a model American paddlefish, Polyodon spathula.

Ram suspension-feeding fishes swim with an open mouth to force water through the oral cavity and extract prey items that are too small to be pursued individually. Recent research has indicated that, rather than using a dead-end mechanical sieve, American paddlefish (Polyodon spathula) employ vortical cross-step filtration. In this filtration mechanism, vortical flow that is generated posterior to the branchial arches organizes crossflow filtration processes into a spatial structure across the gill rakers. Despite the known impact of locomotor kinematics on fluid flow around the bodies of swimming fish, the effects of locomotor kinematics on filtration mechanisms in ram suspension feeders are unknown. Potential temporal organization of filtration mechanisms in ram suspension-feeding fish has not been studied previously. We investigated the effects of locomotor kinematics associated with undulatory swimming on intra-oral flow patterns and food particle transport. A mechanized model of the oral cavity was used to simulate the swimming kinematics of suspension-feeding paddlefish. We recorded fluctuations of flow speed and pressure within the model, which occurred at a frequency that corresponded with the frequency of the model's strides. Using the mechanized model in a flow tank seeded with Artemia cysts, we also showed that swimming kinematics aided the transport of this simulated food to the posterior margins of the gill slots, although the time scale of this transport is expected to vary with prey parameters such as size and concentration. Dye stream experiments revealed that, although stable vortical flow formed because of flow separation downstream of backward-facing steps in control trials, vortical flow structures in mechanized trials repeatedly formed and shed. These findings suggest strong integration between locomotor and feeding systems in ram suspension-feeding fishes.

Designing eco-evolutionary experiments for restoration projects: Opportunities and constraints revealed during stickleback introductions.

Eco-evolutionary experiments are typically conducted in semi-unnatural controlled settings, such as mesocosms; yet inferences about how evolution and ecology interact in the real world would surely benefit from experiments in natural uncontrolled settings. Opportunities for such experiments are rare but do arise in the context of restoration ecology-where different "types" of a given species can be introduced into different "replicate" locations. Designing such experiments requires wrestling with consequential questions. (Q1) Which specific "types" of a focal species should be introduced to the restoration location? (Q2) How many sources of each type should be used-and should they be mixed together? (Q3) Which specific source populations should be used? (Q4) Which type(s) or population(s) should be introduced into which restoration sites? We recently grappled with these questions when designing an eco-evolutionary experiment with threespine stickleback (Gasterosteus aculeatus) introduced into nine small lakes and ponds on the Kenai Peninsula in Alaska that required restoration. After considering the options at length, we decided to use benthic versus limnetic ecotypes (Q1) to create a mixed group of colonists from four source populations of each ecotype (Q2), where ecotypes were identified based on trophic morphology (Q3), and were then introduced into nine restoration lakes scaled by lake size (Q4). We hope that outlining the alternatives and resulting choices will make the rationales clear for future studies leveraging our experiment, while also proving useful for investigators considering similar experiments in the future.

Adding the third dimension to studies of parallel evolution of morphology and function: An exploration based on parapatric lake-stream stickleback.

Recent methodological advances have led to a rapid expansion of evolutionary studies employing three-dimensional landmark-based geometric morphometrics (GM). GM methods generally enable researchers to capture and compare complex shape phenotypes, and to quantify their relationship to environmental gradients. However, some recent studies have shown that the common, inexpensive, and relatively rapid two-dimensional GM methods can distort important information and produce misleading results because they cannot capture variation in the depth (Z) dimension. We use micro-CT scanned threespine stickleback (Gasterosteus aculeatus Linnaeus, 1758) from six parapatric lake-stream populations on Vancouver Island, British Columbia, to test whether the loss of the depth dimension in 2D GM studies results in misleading interpretations of parallel evolution. Using joint locations described with 2D or 3D landmarks, we compare results from separate 2D and 3D shape spaces, from a combined 2D-3D shape space, and from estimates of biomechanical function. We show that, although shape is distorted enough in 2D projections to strongly influence the interpretation of morphological parallelism, estimates of biomechanical function are relatively robust to the loss of the Z dimension.

Physical modeling of vortical cross-step flow in the American paddlefish, Polyodon spathula.

Vortical cross-step filtration in suspension-feeding fish has been reported recently as a novel mechanism, distinct from other biological and industrial filtration processes. Although crossflow passing over backward-facing steps generates vortices that can suspend, concentrate, and transport particles, the morphological factors affecting this vortical flow have not been identified previously. In our 3D-printed models of the oral cavity for ram suspension-feeding fish, the angle of the backward-facing step with respect to the model's dorsal midline affected vortex parameters significantly, including rotational, tangential, and axial speed. These vortices were comparable to those quantified downstream of the backward-facing steps that were formed by the branchial arches of preserved American paddlefish in a recirculating flow tank. Our data indicate that vortices in cross-step filtration have the characteristics of forced vortices, as the flow of water inside the oral cavity provides the external torque required to sustain forced vortices. Additionally, we quantified a new variable for ram suspension feeding termed the fluid exit ratio. This is defined as the ratio of the total open pore area for water leaving the oral cavity via spaces between branchial arches that are not blocked by gill rakers, divided by the total area for water entering through the gape during ram suspension feeding. Our experiments demonstrated that the fluid exit ratio in preserved paddlefish was a significant predictor of the flow speeds that were quantified anterior of the rostrum, at the gape, directly dorsal of the first ceratobranchial, and in the forced vortex generated by the first ceratobranchial. Physical modeling of vortical cross-step filtration offers future opportunities to explore the complex interactions between structural features of the oral cavity, vortex parameters, motile particle behavior, and particle morphology that determine the suspension, concentration, and transport of particles within the oral cavity of ram suspension-feeding fish.