Defence mitigation by predators of chemically defended prey integrated over the predation cycle and across biological levels

Abstract

The long-term evolution of species involved in predator-prey interactions has resulted in many examples of specialised prey defences. The methods that predators use to mitigate prey defences has received less attention. The frequent reference to an arms races or coevolution without clear evidence that both strategies evolved under the influence of each other is problematic. In this review, we use the predation sequence approach as a framework to investigate how predators can evolve traits that allow continued interaction with dangerous prey and we evaluate the evidence for an arms race. We synthesise results from 574 records of predation on prey that are protected by cardiotonic steroids (CTS) – defensive compounds that are found in taxa ranging from toads, to fireflies, to numerous plants, and that have a specific physiological target. We find evidence that distinct lineages of predators share generalised mitigation strategies, and in the latter stages of the predation sequence these strategies are more specific and exploitative behavioural, physiological, and molecular adaptations. In most cases the available evidence does not fulfil the theoretical requirements for arms race dynamics. Our review framework helps to direct future research on what kinds of prey defences appear most profitable for predators to overcome, and what kinds of predatory mitigation strategies are best for a given suite of defences.

Constraints on the evolution of toxin-resistant Na,K-ATPases have limited dependence on sequence divergence

“…A number of groups of plants and animals have independently evolved the ability to produce CTS autogenously for use in their defense against herbivory and predation, respectively [4]. Likewise, herbivores and predators that feed on CTS-producing taxa must also evolve mechanisms to circumvent the toxic effects of CTS, and often sequester CTS for use in their own defense [5][6][7][8][9][10][11]. As a result, NKA is often the target of convergent evolution of CTS resistance across widely divergent species.…”

Constraints on the evolution of toxin-resistant Na,K-ATPases have limited dependence on sequence divergence

“…CTS inhibit NKA function by binding to a highly conserved domain of the protein's a-subunit (ATP1A) and blocking the exchange of Na + and K + ions [3]. Thus, NKA is often the target of convergent evolution of CTS resistance across widely divergent species, including insect herbivores that feed on toxic plants [4,5] as well as predators that feed on toxic prey [6][7][8][9][10].…”