Factor in Fear: Interference Competition in Polymorphic Spadefoot Toad Tadpoles and Its Potential Role in Disruptive Selection

SIMPLE SUMMARY: Disruptive selection occurs when extreme phenotypes have a fitness advantage over intermediate phenotypes, thereby favoring the evolution and maintenance of diversity within populations. Resource competition within populations is an important cause of disruptive selection. Individuals can compete in two distinct ways: either by depleting resources (exploitative/indirect competition) or by impeding a competitor’s access to resources (interference/direct competition). However, it is generally assumed that exploitative competition is of greater importance for disruptive selection, while interference competition is rarely considered. Here, we experimentally explored the role of interference competition using a well-known example of disruptive selection, the Mexican spadefoot toad (Spea multiplicata), whose tadpoles develop into alternative resource-use specialists (omnivores and carnivores) while generalist, intermediate tadpoles are disfavored by disruptive selection. Our behavioral experiments revealed that intermediate tadpoles decreased their foraging in the presence of carnivores, while our competition experiment showed that interference competition with carnivores, but not omnivores, significantly lowered growth rates in intermediate tadpoles. Therefore, interference competition may be important in causing disruptive selection. Furthermore, we found that ‘fear’ (phenotypic responses to perceived predation risk) could mediate interference competition as carnivores (who are also cannibalistic) were responsible for both behavioral alterations and a decreased growth rate when direct interaction was possible. ABSTRACT: Disruptive selection arises when extreme phenotypes have a fitness advantage compared to more-intermediate phenotypes. Theory and evidence suggest that intraspecific resource competition is a key driver of disruptive selection. However, while competition can be indirect (exploitative) or direct (interference), the role of interference competition in disruptive selection has not been tested, and most models of disruptive selection assume exploitative competition. We experimentally investigated whether the type of competition affects the outcome of competitive interactions using a system where disruptive selection is common: Mexican spadefoot toads (Spea multiplicata). Spea tadpoles develop into alternative resource-use phenotypes: carnivores, which consume fairy shrimp and other tadpoles, and omnivores, which feed on algae and detritus. Tadpoles intermediate in phenotype have low fitness when competition is intense, as they are outcompeted by the specialized tadpoles. Our experiments revealed that the presence of carnivores significantly decreased foraging behavior in intermediate tadpoles, and that intermediate tadpoles had significantly lower growth rates in interference competition treatments with carnivores but not with omnivores. Interference competition may therefore be important in driving disruptive selection. As carnivore tadpoles are also cannibalistic, the ‘fear’ effect may have a greater impact on intermediate tadpoles than exploitative competition alone, similarly to non-consumptive effects in predator–prey or intraguild relationships.