Processes in the Evolution of Communication Signals

Improving our understanding of the evolution of communication in ant–plant symbioses will require determining what may constrain the signal. Plant biosyn- thetic pathways for volatile production are considered to be highly constrained by phylogeny. They have even been proposed as characters for phylogenetic recon- struction (Barkman2001). However, hierarchical clustering of blends of volatiles proved to be mostly incongruent with DNA-based phylogeny (Levin et al.2003). Production of secondary metabolites by plants is indeed known to depend not only on taxonomy but also on evolutionary interactions with herbivores or pollinators (J€urgens2004; Agrawal et al.2009). The nature of plant–invertebrate communica- tion signals thus seems to result from both phylogenetic (sensus McKitrick1993) and ecological constraints.

What are the respective roles of these constraints in the evolution of ant–plant communication? No study has addressed this question yet, but ant and plant traits suggest some hypotheses for future investigations.

The fact that very few biosynthetic pathways are involved in the numerous cases of emission of herbivore-induced plant volatiles attractive to natural enemies (Turlings and W€ackers2004) suggests that the biosynthetic pathways may consti- tute the most important phylogenetic constraint on the nature of the communication signal between plants and ants. Insect olfactory receptor neurons exhibit high selectivity and respond to specific compounds, but the identity of these compounds can be very different across related insect species (Todd and Baker1999). Thus, antennal receptors appear to impose little phylogenetic constraint on the evolution of signals. Plants are known to produce more than 1,000 volatile compounds (Pichersky et al.2006), and more than 1,500 compounds with a pheromonal action have been identified in social insects (Passera and Aron2005). Moreover, we saw that there is structural overlap between ant pheromones and plant volatiles. Thus, the few phylogenetic constraints, i.e. mostly those affecting plant biosynthetic pathways, allow for a wide range of compounds to become potential signals.

The ecological selective pressures exerted on the signal depend on the type of interaction between the two partners. We have identified five settings where communication is expected to have evolved in ant–plant symbioses: the selection of ant-garden seeds to sow the garden, the discrimination of the host plant by pruning plant–ants, the detection of the host myrmecophyte by founding queens, the selective continuous patrolling on young shoots of myrmecophytes, and the damage-induced ant-mediated protection of myrmecophytes. The specificity of the signal is expected to be high in the first two settings because competition with non- symbiotic plants is expected. Therefore, cues reducing ant choice errors should be favoured by selection. The third setting may select for a high specificity for the same reason, except when the density of founding queens is constantly higher than that of the available host plants. In this last case, competition between plants for occupants is relaxed because myrmecophytes have a high probability of being colonised under high ant density. In these three settings, i.e. dispersal of ant-garden

seeds, pruning of non-host-plants and host-plant recognition by founding queens, ecological constraints may be expected to shape a more or less specific signal. However, in the last two settings, i.e. patrolling of young shoots and damage- induced protection, the ants are permanently in close proximity to the plant and the signal does not need to be so specific. Constraints are thus very low, and we may expect any compound with the appropriate physical properties to be used as signal. Nevertheless, efficiency of the communication process should be favoured. The selection of one particular signal and further coevolution of the production by the plant and perception/integration by the ants would result in increased efficiency. Reciprocal adaptation would lead, over evolutionary time, to a higher production of the signal by the plant and a stronger ant behavioural response to it. Since the nature of the signal is not expected to be particularly constrained, the compounds which evolve as signals may be the outcome of a random or unpredictable chain of events, each step contingent on the history of previous steps. Historical contingency has been demonstrated in experimental evolution with bacteria (Blount et al. 2008). Such demonstrations are of course impossible in biological systems such as ant–plant symbioses, but a detailed analysis of communication signals in symbioses in which both partner species have undergone evolutionary radiation could give some clues about the processes underlying the evolution of communication signals. Under contingent evolution, many different signals are expected to have been selected across species, with low repeatability. Under phylogenetic constraints, the pattern of signal variation should be congruent with phylogeny either of the plants or the ants, respectively, depending on whether emission or reception is constrained. Under ecological constraints, a predictable and reduced set of signals should occur, irrespective of phylogeny. Signal evolution probably results from interactions between those constraints. Ant–plant associations that show radiation in both lineages may thus constitute good models for understanding the respective roles of the two kinds of constraints in the evolution of communication signals in these and other plant–insect mutualisms.

5

Conclusions

The emission of communication signals by plants addressed to arthropods is largely documented. However, there is a huge gap in the investigation of communication signals from arthropods to plants. Despite the many examples of signals emitted by plants for reception by ants, there is hardly any work on signals emitted by ants to which plants respond. An indication that such signals exist is found in myrmeco- phytic Piper, where food body production is induced by the presence of the ant symbiont (Risch and Rickson1981; Letourneau1983). The plant probably uses ant cues to match the production of myrmecophytic traits with ant presence, and thus avoids wasting resources when ants are absent. Ant–plant symbioses involve partners that live together during most of their respective life-spans. This means that there is a great potential for mutual exchange of information. Communication

signals in both directions are more likely to have evolved in ant–plant symbioses than in any other plant–insect relationship. The search for communication from ants to plants may constitute a promising field for future research.

Communication in ant–plant symbioses remains understudied and poorly under- stood. This chapter provides research directions, which we hope will stimulate further investigations. The discovery a few decades ago that plants attract natural enemies of herbivores led to a better understanding of plant–arthropod communi- cation and opened the door to a new research area. This area highlighted the complexity of inter-specific interactions and led to the view that communication between organisms as different as plants and arthropods has tremendous implica- tions for the structure and functioning of ecological communities. Ant–plant sym- bioses set various contexts for inter-specific communication to evolve. Because of their particular life history, myrmecophytes provide interesting comparisons with other plants that “cry for help”. Comparing the various settings of plant-arthropod communication constitute an interesting framework for a better understanding of evolutionary community ecology.

Acknowledgments We thank Doyle McKey for discussions and proof-reading the manuscript, and Finn Kjellberg for stimulating discussions. Studies of ant–plant interactions were funded by two grants from the French Agence Nationale de la Recherche to R.B. (“Young scientists” programme, research agreement no. ANR-06-JCJC-0127, and “Biodiversity” programme, IFORA project).

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