Rapid evolution of constitutive and inducible defenses against an invasive predator

Abstract

Invasive alien predators can impose strong selection on native prey populations and induce rapid evolutionary change in the invaded communities. However, studies on evolutionary responses to invasive predators are often complicated by the lack of replicate populations differing in coexistence time with the predator, which would allow the determination of how prey traits change during the invasion. The red swamp crayfish Procambarus clarkii has invaded many freshwater areas worldwide, with negative impacts for native fauna. Here, we examined how coexistence time shapes antipredator responses of the Iberian waterfrog (Pelophylax perezi) to the invasive crayfish by raising tadpoles from five populations differing in historical exposure to P. clarkii (30 years, 20 years, or no coexistence). Tadpoles from non-invaded populations responded to the presence of P. clarkii with behavioral plasticity (reduced activity), whereas long-term invaded populations showed canalized antipredator behavior (constant low activity level). Tadpoles from one of the long-term invaded populations responded to the crayfish with inducible morphological defenses (deeper tails), reflecting the use of both constitutive and inducible antipredator defenses against the exotic predator by this population. Our results suggest that, while naive P. perezi populations responded behaviorally to P. clarkii, the strong predation pressure imposed by the crayfish has induced the evolution of qualitatively different antipredator defenses in populations with longer coexistence time. These responses suggest that strong selection by invasive predators may drive rapid evolutionary change in invaded communities. Examining responses of prey species to biological invasions using multiple populations will help us better forecast the impact of invasive predators in natural communities.

KIFC1 is essential for acrosome formation and nuclear shaping during spermiogenesis in the lobster Procambarus clarkii

“…Red swamp lobster ( Procambarus clarkii ), the invasive species all around the world similar to the rusty crayfish ( Orconectes rusticus ) in the US [9] is a good example of Reptantia. On one side, such an invasive animal causes ecological damage to local species [10]. On the other side, the crayfish is becoming popular food in China for its palatable taste thus catalyzes the emergence of farms.…”

Characterizing a novel predator–prey relationship between native Diplonychus esakii (Heteroptera: Belostomatidae) and invasive Gambusia affinis (Teleostei: Poeciliidae) in central China

“…Several studies focused on the question of whether and how invasive predators affect native prey species (Gerard et al 2014;Nunes et al 2014). For example, predation experiments by Błońska et al (2015) demonstrated that the Ponto-Caspian racer goby Babka gymnotrachelus preys more on the native amphipod Gammarus fossarum than invasive Dikerogammarus villosus and Pontogammarus robustoides in its invasive range in Poland.…”

Responses of Aquatic Non-Native Species to Novel Predator Cues and Increased Mortality

“…Even when species do not immediately recognize and respond to novel predators, selective pressures from predators have resulted in the expression of anti-predator behaviors in prey with which they have coexisted for only a few generations (Thompson 1998, Yoshida et al 2003, Nunes et al 2014, Berthon 2015. For example, native blue mussels, Mytilus edulis, from habitats invaded by the Asian shore crab, Hemigrapsus sanguineus, approximately 15 years prior (7-15 generations of M. edulis prior) increased their shell thickness in response to the crab's presence whereas completely naïve mussels from other, uninvaded populations did not respond to its presence (Freeman & Byers 2006, Zagata et al 2008.…”

“…Anti-predator defenses can take many forms, including physically escaping from or avoiding the predator to physical and chemical defenses (Rockwood 2006). While many anti-predator defenses are permanent, constitutive defenses, other possess temporary or plastic inducible defenses (Tollrian & Harvell 1998, Nunes et al 2014.…”

“…However, previous studies were performed using populations of non-native species that had coexisted with established predator species for generations. The expression of anti-predator behaviors in naïve prey can occur within a few generations (Thompson 1998, Yoshida et al 2003, Freeman & Byers 2006, Nunes et al 2014, Berthon 2015, and thus it is highly possible the observed responses of non-native prey do not represent their responses during their initial introduction. It is likely that during this initial introduction, when the introduced population is small, is when biotic resistance from established predators has the greatest chance of preventing the establishment of the introduced species.…”