Local adaptation in transgenerational responses to predators

Abstract

Environmental signals can induce phenotypic changes that span multiple generations. Along with phenotypic responses that occur during development (i.e. 'within-generation' plasticity), such 'transgenerational plasticity' (TGP) has been documented in a diverse array of taxa spanning many environmental perturbations. New theory predicts that temporal stability is a key driver of the evolution of TGP. We tested this prediction using natural populations of zooplankton from lakes in Connecticut that span a large gradient in the temporal dynamics of predator-induced mortality. We reared more than 120 clones of Daphnia ambigua from nine lakes for multiple generations in the presence/absence of predator cues. We found that temporal variation in mortality selects for within-generation plasticity while consistently strong (or weak) mortality selects for increased TGP. Such results provide us the first evidence for local adaptation in TGP and argue that divergent ecological conditions select for phenotypic responses within and across generations.

Keywords: ecological epigenetics; life-history evolution; maternal effects; phenotypic plasticity.

Figure 1.

Predictions from theory for the evolution of within- and across-generation phenotypic plasticity. The line with closed circles represents expectations for organisms reared in the presence of the environmental cue. The line with open squares represents the expectations for organisms not exposed to the environmental cue. (a) Local co-adaptation: high environmental (temporal) variation is expected to favour increased within- and across-generation plasticity [22,23]. (b) Antagonistic adaptation: divergent conditions select for within- versus across-generation plasticity [–27]. Low temporal variation favours increased transgenerational plasticity.

Figure 2.

TGP in development rate depends upon predation regime. (a) Anadromous lakes, (b) landlocked lakes, and (c) no alewife lakes. P, predator treatment; NP, non-predator treatment. Exposure to predator cues in generation 1 yielded strong transgenerational responses in Daphnia from landlocked and no alewife lakes (acceleration in development across generations) but weak or absent TGP in Daphnia from anadromous lakes (delayed development across generations). The lake type × generation × predator treatment interaction was significant (p < 0.01). Error bars =±1 standard error (s.e.).

Figure 3.

Transgenerational responses for size at maturation (a–c) and clutch size (d–f). (a,d) Anadromous lakes, (b,e) landlocked lakes, (c,f) no alewife lakes. P, predator treatment; NP, non-predator treatment. The lake type × generation × predator treatment interaction was not significant for either trait (p > 0.05). Error bars = ±1 s.e.

Figure 4.

Contrasting transgenerational patterns for intrinsic rates of increase. (a) Anadromous lakes, (b) landlocked lakes, and (c) no alewife lakes. P, predator treatment; NP, non-predator treatment. The lake type × generation × predator treatment interaction was marginally non-significant (p = 0.052). Error bars =±1 s.e.