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.genetic accommodation | genetic assimilation | gene expression | pigmentation | rapid evolution T he claim that phenotypic plasticity can facilitate adaptation remains controversial following a century of investigation (1-5). According to modern proponents, genetic accommodation (genetic change in the regulation or form of a plastic trait) can channel and accelerate evolutionary divergence (6, 7). This argument centers on the fact that plastic organisms possess the developmental mechanism to form an alternative, induced phenotype. Selection for the stable production of this phenotype can act on regulation of preexisting developmental pathways to effect adaptive change. One hypothesized result is recurrent rapid evolution in the direction of ancestral plasticity (6-9), based on changes in the expression, rather than the structure, of genes (10). A number of artificial selection experiments demonstrate rapid genetic accommodation within lineages (11-13), providing support for the plausibility of this phenomenon in nature. In addition, many studies of natural populations reveal congruent patterns of plasticity and adaptive change at the population and species level (8,9,14). However, the importance of this process remains difficult to assess, due to three factors: it is usually impossible to observe ancestral reaction norms (but see ref. 14); it is difficult to elucidate the developmental details of both plasticity and adaptation; and adaptation through genetic accommodation is thought to proceed rapidly, making it likely that researchers will observe the results of this process rather than capture it in action (8). As a consequence, there is little to no empirical evidence for a significant role of plasticity in facilitating adaptive evolution in natural populations (3)(4)(5)15).In the high UV environment of Sierra Nevada alpine lakes (California), the microcrustacean Daphnia melanica is normally darkly pigmented...

Evolutionary relatedness does not predict competition and co-occurrence in natural or experimental communities of green algae

“…), it is also possible that traits involved in interspecific competitive interactions evolve rapidly. Phenotypic plasticity in algae could also lead to rapid trait evolution [64][65][66][67], further obscuring phylogenetic signal of such traits. Different abiotic variables across lakes could lead to local adaptation, driving rapid evolution at a local scale.…”

Long prereproductive selection and divergence by depth in a Caribbean candelabrum coral

“…This process of habitatrelated divergence without reproductive isolation may therefore be more common than usually appreciated. It can occur whether the contrasting phenotypes are initially genetically cued (51,52) or environmentally induced (13,30,62), for it is the contrast between the different phenotypes and the underlying sets of expressed genes that, under selection, drives divergence-not the cues (genetic or environmental) that govern their expression.…”

The role of developmental plasticity in evolutionary innovation

“…For example, introduction of salmonid predators to alpine lakes inhabited by the zooplankter Daphnia melanica has led to a loss of plasticity in an antipredator defence [34]. Melanin protects D. melanica from UV light but renders them conspicuous to piscine predators.…”