Predator-induced phenotypic plasticity of shape and behavior: parallel and unique patterns across sexes and species

Abstract

Phenotypic plasticity is often an adaptation of organisms to cope with temporally or spatially heterogenous landscapes. Like other adaptations, one would predict that different species, populations, or sexes might thus show some degree of parallel evolution of plasticity, in the form of parallel reaction norms, when exposed to analogous environmental gradients. Indeed, one might even expect parallelism of plasticity to repeatedly evolve in multiple traits responding to the same gradient, resulting in integrated parallelism of plasticity. In this study, we experimentally tested for parallel patterns of predator-mediated plasticity of size, shape, and behavior of 2 species and sexes of mosquitofish. Examination of behavioral trials indicated that the 2 species showed unique patterns of behavioral plasticity, whereas the 2 sexes in each species showed parallel responses. Fish shape showed parallel patterns of plasticity for both sexes and species, albeit males showed evidence of unique plasticity related to reproductive anatomy. Moreover, patterns of shape plasticity due to predator exposure were broadly parallel to what has been depicted for predator-mediated population divergence in other studies (slender bodies, expanded caudal regions, ventrally located eyes, and reduced male gonopodia). We did not find evidence of phenotypic plasticity in fish size for either species or sex. Hence, our findings support broadly integrated parallelism of plasticity for sexes within species and less integrated parallelism for species. We interpret these findings with respect to their potential broader implications for the interacting roles of adaptation and constraint in the evolutionary origins of parallelism of plasticity in general.

Keywords: boldness; common garden; geometric morphometrics; reaction norm; sexual dimorphism; size at maturity.

Figure 1.

Behavioral assay experimental design. Area (1) is the largemouth bass enclosure, Area (2) is the risk assessment grid, Area (3) is the acclimation tube, and Area (4) is the shoal group. The “danger zone” is represented by the vertical-lined area. The “safe zone” is represented by the diagonal-lined area.

Figure 2.

Behavioral responses for G. affinis (dashed line) and G. holbrooki (solid line). Panel (A) is the time for a fish to leave the “safe zone” the first time. Panel (B) is the percentage of time a fish spent outside of the “safe zone.” Panel (C) is the percentage of time a fish spent near the shoal group. Panel (D) is the percentage of time a fish spent near the bass enclosure. Asterisks represent significant differences with unique interactions (species by predation). Double crosses represent significant effect of species. All error bars are ±1 standard error.

Figure 3.

Frequency distributions of discriminant function scores summarizing geometric morphometric deformations of 26 relative warps. Summary deformations are shown at each end of the function axis using a visualization exaggeration factor of 4. Gray bars are non-exposure populations and black bars are the exposed populations. Panel (A) is female G. affinis, (B) is female G. holbrooki, (C) is male G. affinis, and (D) is male G. holbrooki.

Figure 4.

Superimposition of morphological deformations due to plasticity (this study) and due to population divergence (Langerhans et al. 2004). All panels are of G. affinis. Thin plate spine images of plasticity from the present study are exaggerated by 4 units (shaded, black points). Images are paired with corresponding sex and predator exposure outlines from Langerhans et al. (2004) with 2-unit exaggeration (dashed, gray points). Different point sets from the 2 studies contribute to some differences in shape resolution, but overall deformation patterns are broadly analogous.