Abstract
Fear of predation can disappear rapidly in the absence of predators, as bolder individuals outcompete vigilant individuals for food and mates. To examine the evolution of fear in a seasonal environment, we exposed Drosophila melanogaster to mantid predators during the breeding season and the non-breeding season, and compared these with a control. We compared three Drosophila lineages that were maintained in captivity for (1) ∼45 years without mantid predators, (2) ∼5 years without mantid predators, and (3) ∼5 years with mantid predators (predator-evolved). The presence of a predator during the non-breeding season caused reduced fecundity in the following breeding season, independent of the evolutionary lineage. However, the presence of a predator during reproduction caused offspring to emerge earlier, and this effect was more pronounced in the predator-evolved lineage. Thus, the fear response was related to evolutionary lineage only during the larval life stage, which is when foraging competition, and hence the cost of fear, may be highest. We present one of the first experimental demonstrations that emotion (fear) can evolve in response to environmental context.
Highlights
Fecundity depended on the treatment (F2,192 = 61.2, p < 0.0001) and evolutionary lineage (F2,192 = 190.5, p < 0.0001) but not their interaction (F3,192 = 0.92, p = 0.43)
Compared with the control, fecundity in all three lineages was reduced with exposure to mantid cues during the non-breeding season
Fecundity was reduced by exposure to mantid cues during the breeding season for the predator-evolved and control-evolved lineages (Fig. 1a)
Summary
Non-consumptive effects of predators, including the effects of fear, can play an important role in animal ecology, influencing offspring development (Lardner 2000; Dahl and Peckarsky 2002; Benard 2004), adult fitness (Roitberg et al 1979; Ylönen 1989; Dixon and Agarwala 1999; Gallagher et al 2016), population dynamics (Lima 1998; Preisser et al 2005; Creel et al 2009), and even ecosystem function (Beckerman et al 1997; Schmitz et al 1997; Suraci et al 2016). Fear of predation diminishes in the absence of predators (Blumstein and Daniel 2005; Binz et al 2014), with riskier individuals outcompeting less risky individuals for food and mates. Darwin’s observation that animals on remote islands were unafraid of people was an impetus for his theory of natural selection, as he posited that escape behaviour was diminished where predators were rare due to the loss of costly escape responses in the absence of strong natural selection to maintain them (Darwin 1839; Cooper et al 2014). We might expect strong selection against fear in wild, but not laboratory, populations
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