Evolutionary trajectory of phenological escape in a flowering plant: Mechanistic insights from bidirectional avoidance of butterfly egg‐laying pressure

TL;DR

The study explores how a flowering plant evolves to avoid butterfly egg-laying by adjusting its flowering time, revealing how plant traits and predator behavior shape this evolutionary response.

Contribution

The paper provides mechanistic insights into how phenological escape evolves through differential selection pressures on plant morphologies and flowering times.

Findings

Bimodal flowering patterns evolve due to disruptive selection on high fecundity plants under butterfly egg-laying pressure.

Asynchronous flowering and size-dependent egg-laying constrain phenological escape in plants.

Plant morphology and anti-predator defenses influence the availability of flowering refugia.

Abstract

Phenological escape, whereby species alter the timing of life‐history events to avoid seasonal antagonists, is usually analyzed either as a potential evolutionary outcome given current selection coefficients, or as a realized outcome in response to known enemies. We here gain mechanistic insights into the evolutionary trajectory of phenological escape in the brassicaceous herb Cardamine pratensis, by comparing the flowering schedules of two sympatric ecotypes in different stages of a disruptive response to egg‐laying pressure imposed by the pierid butterfly Anthocharis cardamines, whose larvae are pre‐dispersal seed predators (reducing realized fecundity by ~70%). When the focal point of highest intensity selection (peak egg‐laying) occurs early in the flowering schedule, selection for late flowering dependent on reduced egg‐laying combined with selection for early flowering dependent on reduced predator survival results in a symmetrical bimodal flowering curve; when the focal point occurs late, an asymmetrical flowering curve results with a large early flowering mode due to selection for reduced egg‐laying augmented by selection for infested plants to outrun larval development and dehisce prior to seed‐pod consumption. Unequal selection pressures on high and low fecundity ramets, due to asynchronous flowering and morphologically targeted (size‐dependent) egg‐laying, constrain phenological escape, with bimodal flowering evolving primarily in response to disruptive selection on high fecundity phenotypes. These results emphasize the importance of analyzing variation in selection coefficients among morphological phenotypes over the entire flowering schedule to predict how populations will evolve in response to altered phenologies resulting from climate change.

We gain mechanistic insights into the evolution of phenological escape, whereby organisms alter the timing of life history events to avoid antagonists, by comparing the flowering schedules of two sympatric ecotypes of the same plant species in early and late phases of a disrupted phenological response to butterfly egg‐laying pressure. We provide evidence that plant morphology, anti‐predator defense mechanisms and flowering time interact to determine the availability of alternative flowering refugia and hence direct the evolutionary trajectory of phenological escape.

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