Cuckoos versus hosts in insects and birds: adaptations, counter-adaptations and outcomes

Abstract

Avian parents and social insect colonies are victimized by interspecific brood parasites-cheats that procure costly care for their dependent offspring by leaving them in another species' nursery. Birds and insects defend themselves from attack by brood parasites; their defences in turn select counter-strategies in the parasite, thus setting in motion antagonistic co-evolution between the two parties. Despite their considerable taxonomic disparity, here we show striking parallels in the way that co-evolution between brood parasites and their hosts proceeds in insects and birds. First, we identify five types of co-evolutionary arms race from the empirical literature, which are common to both systems. These are: (a) directional co-evolution of weaponry and armoury; (b) furtiveness in the parasite countered by strategies in the host to expose the parasite; (c) specialist parasites mimicking hosts who escape by diversifying their genetic signatures; (d) generalist parasites mimicking hosts who escape by favouring signatures that force specialization in the parasite; and (e) parasites using crypsis to evade recognition by hosts who then simplify their signatures to make the parasite more detectable. Arms races a and c are well characterized in the theoretical literature on co-evolution, but the other types have received little or no formal theoretical attention. Empirical work suggests that hosts are doomed to lose arms races b and e to the parasite, in the sense that parasites typically evade host defences and successfully parasitize the nest. Nevertheless hosts may win when the co-evolutionary trajectory follows arms race a, c or d. Next, we show that there are four common outcomes of the co-evolutionary arms race for hosts. These are: (1) successful resistance; (2) the evolution of defence portfolios (or multiple lines of resistance); (3) acceptance of the parasite; and (4) tolerance of the parasite. The particular outcome is not determined by the type of preceding arms race but depends more on whether hosts or parasites control the co-evolutionary trajectory: tolerance is an outcome that parasites inflict on hosts, whereas the other three outcomes are more dependent on properties intrinsic to the host species. Finally, our review highlights considerable interspecific variation in the complexity and depth of host defence portfolios. Whether this variation is adaptive or merely reflects evolutionary lag is unclear. We propose an adaptive explanation, which centres on the relative strength of two opposing processes: strategy-facilitation, in which one line of host defence promotes the evolution of another form of resistance, and strategy-blocking, in which one line of defence may relax selection on another so completely that it causes it to decay. We suggest that when strategy-facilitation outweighs strategy-blocking, hosts will possess complex defence portfolios and we identify selective conditions in which this is likely to be the case.

Coevolution is linked with phenotypic diversification but not speciation in avian brood parasites

“…Avian brood parasitism is one of the best examples of coevolution in the animal kingdom, and has been shown to lead to adaptations in both hosts and parasites [4,37]. In theory, coevolution of brood parasites and hosts should lead to increased rates of diversification and increased phenotypic diversity [2,19].…”

Collective defence portfolios of ant hosts shift with social parasite pressure

“…Theory suggests that once the first line of defence is breached by exploiters, selection favours victims that mount further defences. This could result in complex defence portfolios, deployed in hierarchical sequence [3,4]. Consequently, in host-parasite systems, the evolution of host defences may not only depend on attributes of parasites, such as parasite pressure and their degree of specialization, but also on the efficacy of other traits in the adaptive portfolios of hosts and parasites [3,5].…”

“…This could result in complex defence portfolios, deployed in hierarchical sequence [3,4]. Consequently, in host-parasite systems, the evolution of host defences may not only depend on attributes of parasites, such as parasite pressure and their degree of specialization, but also on the efficacy of other traits in the adaptive portfolios of hosts and parasites [3,5]. Recent modelling approaches conclude that victims have unique evolutionary advantages when coevolution involves multiple traits in hosts and parasites [6].…”

“…Although the evolutionary principles governing adaptive portfolios are generally applicable to exploiter -victim systems [2], the concept has almost exclusively received attention in avian brood parasites and their hosts [3,5,7]. Nonetheless, hosts of insect social parasites and avian brood parasites show striking similarities in the trajectories and outcomes of their coevolutionary arms races [3].…”

“…Nonetheless, hosts of insect social parasites and avian brood parasites show striking similarities in the trajectories and outcomes of their coevolutionary arms races [3]. Like avian hosts, social insects exhibit a range of morphological, behavioural and physiological adaptations to social parasites, which often co-occur in a single host species [9][10][11][12][13].…”