Male sexual signal predicts phenotypic plasticity in offspring: implications for the evolution of plasticity and local adaptation

Abstract

In a rapidly changing world, understanding the processes that influence a population's ability to respond to natural selection is critical for identifying how to preserve biodiversity. Two such processes are phenotypic plasticity and sexual selection. Whereas plasticity can facilitate local adaptation, sexual selection potentially impedes local adaptation, especially in rapidly changing or variable environments. Here we hypothesize that, when females preferentially choose males that sire plastic offspring, sexual selection can actually facilitate local adaptation to variable or novel environments by promoting the evolution of adaptive plasticity. We tested this hypothesis by evaluating whether male sexual signals could indicate plasticity in their offspring and, concomitantly, their offspring's ability to produce locally adapted phenotypes. Using spadefoot toads ( Spea multiplicata) as our experimental system, we show that a male sexual signal predicts plasticity in his offspring's resource-use morphology. Specifically, faster-calling males (which are preferred by females) produce more plastic offspring; such plasticity, in turn, enables these males' offspring to respond adaptively to the spadefoots' highly variable environment. The association between a preferred male signal and adaptive plasticity in his offspring suggests that female mate choice can favour the evolution and maintenance of phenotypic plasticity and thereby foster adaptation to a variable environment. This article is part of the theme issue 'The role of plasticity in phenotypic adaptation to rapid environmental change'.

Keywords: local adaptation; mate choice; phenotypic plasticity; sexual selection; spadefoot toads.

Figure 1.

(a) How sexual selection (as mediated by female mate choice) impedes local adaptation in rapidly changing environments. Generally, females should possess preferences for males who sire offspring with locally adapted traits. For instance, females that occur in a light environment in which visually oriented predators are present should prefer males that sire light-coloured offspring (‘L’ males) over males that sire dark-coloured offspring (‘D’ males). However, in a rapidly changing environment (in this case, one that changes into a dark environment), a formerly adaptive preference might become maladaptive. Here, the formerly adaptive light-coloured offspring sired by the ‘L’ male are now more likely to be detected by predators. (b) When females preferentially choose males that sire plastic offspring, sexual selection can facilitate local adaptation to rapidly changing environments. In this case, males that sire plastic offspring (‘P’ males) should produce more surviving offspring than either L or D males (who sire non-plastic offspring) across both environments (note that we have assumed here that plastic offspring bear a cost not borne by non-plastic offspring in the environment for which they are adapted; weakening this assumption only increases the advantage to P males).

Figure 2.

Generalized linear model fit with ln call rate (back-transformed) as the predictor and total number of carnivores as the response (Poisson distribution specified).

Figure 3.

Linear regression of plasticity in resource-use morphology (calculated as differences between family-mean MI values on shrimp versus on detritus diets) on ln call rate (back-transformed).

Figure 4.

Reaction norms of family-mean morphological index values when tadpoles were reared on detritus versus shrimp diets. Call rates are shown for sires whose tadpoles exhibited the steepest and shallowest reaction norms. (Online version in colour.)