Spatially heterogeneous selection in nature favors phenotypic plasticity in anuran larvae

Abstract

Theory holds that adaptive phenotypic plasticity evolves under spatial or temporal variation in natural selection. I tested this prediction in a classic system of predator-induced plasticity: frog tadpoles (Rana temporaria) reacting to predaceous aquatic insects. An outdoor mesocosm experiment manipulating exposure to Aeshna dragonfly larvae revealed plasticity in most characters: growth, development, behavior, and external morphology. I measured selection by placing 1927 tadpoles into enclosures within natural ponds; photographs permitted identification of the survivors six to nine days later. Fitness was defined as a linear combination of growth, development, and survival that correlates with survival to age 2 in another anuran species. In enclosures with many predators, selection-favored character values similar to those induced by exposure to Aeshna in mesocosms. The shift in selection along the predation gradient was strongest for characters that exhibited high predator-induced plasticity. A field survey of 50 ponds revealed that predator density changes over a spatial scale relevant for movement of individual adults and larvae: 17% of variation in predation risk was among ponds separated by tens to thousands of meters and 81% was among sites ≤10 m apart within ponds. These results on heterogeneity in the selection regime confirm a key tenant of the standard model for the evolution of plasticity.

Intraspecific developmental variation in the life cycle of the Andean Treefrog (Boana riojana): A temporal analysis

“…Kishida and Nishimura () described morphs in Rana pirica , similar to both different morphologies we observed here for B. riojana , with tadpoles exhibiting a bulgy bodied morphology with a rounded tail tip, that is, a higher tail height and relative size of the maximum body height, when threatened with predation. In R. temporaria , Van Buskirk () described that when predators were common, individuals were favored if they had short and deep tail fins and a narrow head/body whereas in sites with few or no predators, selection favored tadpoles with a shallow tail and head/body, a more anterior mouth, and a larger visceral cavity extending farther forward. Although, we did not test for a relationship, the presence of small predatory fishes from the families Anablepidae and Characidae together with tadpoles of B. riojana could account for such a variation; a hypothesis that needs to be tested in future.…”

“…Phenotypic plasticity is the ability of a single genotype to cope with environmental variation through different phenotypes (West‐Eberhard, ). Amphibians might exhibit plasticity in the timing and age of metamorphosis (e.g., Pintar and Resetarits, ; Ruthsatz, Peck, Dausmann, Sabatino & Glos, ), morphology (e.g., Van Buskirk, ; Levis & Pfennig, ), behavior or life history (e.g., Gazzola, Balestrieri, Ghitti, Paganelli & Galeotti, ), but plasticity is not always advantageous, because it comes with costs as it occasionally results in reduced size and fitness (Snell‐Rood, Van Dyken, Cruickshank, Wade & Moczek, ; Pelster & Burggren ). B. riojana tadpoles altered larval growth and development rates between both generations through the onset of the breeding season.…”

The evolution of phenotypic plasticity when environments fluctuate in time and space

“…It remains the focus of much empirical work and studies continue to be published that give new insights and provide pivotal tests of key ideas (Dey et al. ; Huang and Agrawal ; van Buskirk ). This empirical work is supported by a large body of theoretical work that has either considered scenarios where the environment fluctuates in time in a single population, or in space across multiple populations connected by migration.…”

Matriline effects on metamorphic traits in a natural system in the European common frog (Rana temporaria)

“…In natural amphibian populations, the metamorphic traits of individuals (e.g., size, body condition, age at metamorphosis, and developmental time) can differ profoundly within and between populations (Grözinger, Thein, Feldhaar, & Rödel, ; Loman, ). Factors known to influence these traits under laboratory conditions are temperature, food availability, intra‐ and interspecific competition, presence of predators, and seasonal time constraints (Drakulić et al, ; Laugen, Laurila, Räsänen, & Merilä, ; Laurila & Kujasalo, ; Merilä, Laurila, Pahkala, Räsänen, & Laugen, ; Pakkasmaa & Aikio, ; Smith‐Gill & Berven, ; Van Buskirk, ). Little is known of the interacting effects in natural environments (Loman, ), where environmental variables often seem to counteract the genetic effects.…”