Microgeographic Adaptation of Wood Frog Tadpoles to an Apex Predator
Rapid adaptation of defenses can alter ecological dynamics following introduction of a new predator. We tested for local adaptation in Wood Frog (Rana sylvatica) populations that face varying selection from an apex predator, the Marbled Salamander (Ambystoma opacum), which is expanding its distribution in the study region. We performed a reciprocal transplant experiment with Wood Frog eggs and tadpoles and tested survival of tadpoles when exposed to Marbled Salamander larvae in experimental predation trials. We also evaluated life history, behavioral, and morphological trait variation with respect to origin and transplant environments. We found that tadpoles from populations exposed to high risk from Marbled Salamanders survived better when raised in high-risk environments than tadpoles from low-risk populations. However, tadpoles from high-risk environments experienced lower survival than those from low-risk environments when raised in low-risk environments. Development rate, activity, and morphology differed among populations and environments. Faster development of high-risk populations in high-risk environments and activity patterns best explained observed survival differences. These results suggest that tadpoles have evolved adaptive plasticity at microgeographic scales in response to a mosaic of varying predation risk. Fine-scaled evolution of prey survival and local gene flow could enhance the resilience of Wood Frogs to this predator expansion. As warming winters allow Marbled Salamanders to increase in abundance and distribution, the rapid and fine-scaled evolution of their prey could mediate predicted changes to temporary pond communities and ecosystems. Rapid prey evolution might often promote ecological resilience to predator introductions.
Landmarks used to evaluate shape variation among Wood Frog tadpoles. We used 16 morphometric landmarks to represent overall tadpole shape. Landmarks included: (1) anteriormost point on snout; (2) posteriormost point on tailfin; (3) junction of tailfin and body; (4) junction of vent and tail muscle; (5) the posterior extreme of the body before tail; (6–7) dorsal and ventral points, respectively, on the body above and below the eye; (8–9) dorsal and ventral points of the upper and lower tailfin, respectively, at the midway point between landmarks 1 and 2; (10–11) dorsal and ventral points at maximum tail muscle depth; (12–13) dorsal and ventral points of the upper and lower tailfin three quarters of the distance from landmark 1 to 2; (14) ventral point on abdomen below landmark 3 where the tail meets the body; and (15–16) dorsal and ventral points at maximum body depth.
Wood Frog tadpoles display adaptive reaction norms in response to Marbled Salamander predation. The survival of Wood Frog tadpoles depended on whether populations came from low-predation risk populations (open circles) or high-risk environments (filled triangles) and whether they were raised in high- or low-predation risk ponds. Error bars indicate SEM.
Wood Frog tadpoles from high-risk populations (filled triangles) developed faster than low-risk populations (open circles) in high-risk environments. Developmental stages follow Gosner (1960). Error bars indicate SEM.
Wood Frog tadpoles from high-risk populations (triangles, complete lines) developed faster than low-risk populations (circles, broken lines) in high-risk environments (red) compared to low-risk environments (white) at a given size (snout–vent length). Error bars indicate SEM for both traits.
Wood Frog tadpoles from low-risk populations (open circles) were more active than high-risk populations (filled triangles) in high-risk environments when exposed to live Marbled Salamander larvae. Error bars indicate SEM.
Wood Frog tadpoles from low-risk populations (open circles) and high-risk populations (filled triangles) differed in lateral morphology. We display the mean scores of each treatment on the first two axes in the canonical variate analyses (CV1 and CV2), which finds the best linear combination of morphological features that explains membership in the four treatment groups. On the left, tadpole landmark diagrams encompass the range of CV scores in our data to illustrate shape changes along these axes: −5 to +6 for CV1 and −5 to +5 for CV2. Error bars indicate SEM.
Contributor Notes
Associate Editor: A. Hendry.
From “Eco-Evolutionary Dynamics in Cold Blood,” an ASIH-sponsored symposium at the 2016 Joint Meeting of Ichthyologists and Herpetologists in New Orleans, Louisiana.