Trade‐offs affect the adaptive value of plasticity: stronger cannibal‐induced defenses incur greater costs in toad larvae

Abstract

Adaptive developmental plasticity allows individuals to match their phenotype with their environment, increasing fitness where threats are inconsistently present. However, despite clear advantages of plasticity, adaptive traits are not ubiquitously nor infinitely plastic. Trade‐offs between benefits and costs or limits are therefore theoretically necessary to constrain the evolution of plastic responses. Systems in which extreme risk can be reliably detected are ideal for investigating trade‐offs, as even costly responses may be adaptive where risk is severe. Cane toads (Rhinella marina) are abundant in Australia and produce large clutches (frequently >10,000 eggs), but asynchronous breeding and rapid development result in variable larval densities within breeding pools. In the field, we found that cannibalism by older cohorts often reduces the survival of conspecific eggs and newly hatched pre‐feeding larvae (“hatchlings”) by >99%, as feeding larvae (“tadpoles”) use chemical cues from the relatively immobile hatchlings to locate and consume them. After hatchlings become free‐swimming, however, they cannot be cannibalized. Hatchlings can reduce this period of vulnerability by accelerating development when they detect cannibal cues. However, this developmental acceleration decreases initial tadpole mass, reduces subsequent survival, growth, and development, affects behavior, and compromises feeding structures. Reaction norms differ among clutches, and greater developmental acceleration is followed by greater impairment of larval function in plastic clutches, whereas nonresponsive clutches are unaffected by cue exposure. More plastic clutches ultimately exhibit both poorer performance and greater variation among siblings in exposed and (to a lesser degree) control treatments. Variation among clutches in tadpole viability is driven by differences in plasticity rather than phenotype; fitness reductions are linked to developmental acceleration, not rapid development per se. Clutches with intrinsically slow pre‐feeding developmental rates exhibit stronger acceleration (i.e., steeper reaction norms), but clutches with intrinsically rapid development reach invulnerable stages more quickly than those that accelerate development. As a result, high cannibalism risk may favor canalized rapid development rather than facultative developmental acceleration. Cannibalism plays an important role in the recruitment of this invasive species, and hatchling defenses against this threat demonstrate how the limits and costs associated with an inducible defense can favor canalized defenses over phenotypic plasticity.

Intergenerational effects of manipulating DNA methylation in the early life of an iconic invader

“…To determine whether exposure to +A or +Z affected the potency of the chemical cues produced by cane toad tadpoles, we exposed the tadpoles from each treatment to conspecific hatchlings. Conspecific hatchlings exhibit clear, dose-dependent responses to the cues produced by cane toad tadpoles [26][27][28]. These effects are associated with the induction of defence against cannibalism by older conspecifics, which is a major source of mortality for cane toad eggs and hatchlings.…”

Variation in size and shape of toxin glands among cane toads from native-range and invasive populations

“…A female toad’s investment into toxin stores should incorporate two components: the amount needed for her own defence against predation, and the toxins that she needs to allocate to her eggs 28 . However, the optimal allocation of toxins to eggs is complicated by geographic variation in the incidence of cannibalism, which is frequent in Australian cane toads 46 , 47 but is infrequent in the native range (DeVore et al, unpublished data). Cannibalistic conspecific tadpoles locate eggs by detecting toxins exuded during late stages of egg development 46 ; and thus, a higher investment of toxins into the eggs may render a female’s offspring more vulnerable to cannibalistic attack by conspecifics but less vulnerable to predation by other taxa such as fish and turtles 48 , 49 .…”

Field trials of chemical suppression of embryonic cane toads (Rhinella marina) by older conspecifics

“…The data from our laboratory study on suppressor‐cue concentrations support and extend the conclusions from previous work. That work, showing that suppression can be induced even at low densities of older toad tadpoles (0.004 tadpoles/L), was conducted in small (1 L) containers, with the cue evenly dispersed (Clarke et al., 2016; but see DeVore, Crossland, & Shine, 2020). Our study simulated a more realistic situation, whereby the suppression cue was allowed to disperse naturally after being created by tadpoles inside a mesh container within a large (1,800 L) waterbody.…”