Phenotypic plasticity facilitates recurrent rapid adaptation to introduced predators

Abstract

A central role for phenotypic plasticity in adaptive evolution is often posited yet lacks empirical support. Selection for the stable production of an induced phenotype is hypothesized to modify the regulation of preexisting developmental pathways, producing rapid adaptive change. We examined the role of plasticity in rapid adaptation of the zooplankton Daphnia melanica to novel fish predators. Here we show that plastic up-regulation of the arthropod melanin gene dopa decarboxylase (Ddc) in the absence of UV radiation is associated with reduced pigmentation in D. melanica. Daphnia populations coexisting with recently introduced fish exhibit environmentally invariant up-regulation of Ddc, accompanied by constitutive up-regulation of the interacting arthropod melanin gene ebony. Both changes in regulation are associated with adaptive reduction in the plasticity and mean expression of melanin. Our results provide evidence that the developmental mechanism underlying ancestral plasticity in response to an environmental factor has been repeatedly co-opted to facilitate rapid adaptation to an introduced predator.

Fig. 1.

Evolution of reaction norms. Three theoretical patterns are illustrated. (A) One common form of genetic accommodation: reduction of the magnitude and environmental sensitivity of a trait; (B) genetic assimilation; and (C) constitutive up-regulation. Our results show (D) genetic accommodation in melanin, (E) loss of plasticity in Ddc expression, and (F) constitutive up-regulation in ebony expression. Gene expression is a relative measure, reported in terms of the highest expression level among samples. Data points are laterally offset to aid visualization. Error bars represent a single standard error. Lake I is Puppet, lake II is Evelyn, lake III is Source, and lake IV is Frog.

Fig. 2.

Contour map of expected level of melanin as a function of ebony and Ddc expression. Darker contours indicate greater melanin deposition. Mean levels of gene expression are indicated for fishless populations (circles) and populations with fish (triangle), reported in terms of the highest expression level among samples. Fill color indicates treatment with UV (black) or no UV (white). The solid arrow represents a plastic developmental shift in fishless populations. The dotted arrow represents an adaptive shift due to fish predation. Populations with fish do not significantly change when UV is absent (Table 1).