Chemical and behavioral integration of army ant-associated rove beetles – a comparison between specialists and generalists

Abstract

Host-symbiont interactions are embedded in ecological communities and range from unspecific to highly specific relationships. Army ants and their arthropod guests represent a fascinating example of species-rich host-symbiont associations where host specificity ranges across the entire generalist - specialist continuum. In the present study, we compared the behavioral and chemical integration mechanisms of two extremes of the generalist - specialist continuum: generalist ant-predators in the genus Tetradonia (Staphylinidae: Aleocharinae: Athetini), and specialist ant-mimics in the genera Ecitomorpha and Ecitophya (Staphylinidae: Aleocharinae: Ecitocharini). Similar to a previous study of Tetradonia beetles, we combined DNA barcoding with morphological studies to define species boundaries in ant-mimicking beetles. This approach found four ant-mimicking species at our study site at La Selva Biological Station in Costa Rica. Community sampling of Eciton army ant parasites revealed that ant-mimicking beetles were perfect host specialists, each beetle species being associated with a single Eciton species. These specialists were seamlessly integrated into the host colony, while generalists avoided physical contact to host ants in behavioral assays. Analysis of the ants’ nestmate recognition cues, i.e. cuticular hydrocarbons (CHCs), showed close similarity in CHC composition and CHC concentration between specialists and Eciton burchellii foreli host ants. On the contrary, the chemical profiles of generalists matched host profiles less well, indicating that high accuracy in chemical host resemblance is only accomplished by socially integrated species. Considering the interplay between behavior, morphology, and cuticular chemistry, specialists but not generalists have cracked the ants’ social code with respect to various sensory modalities. Our results support the long-standing idea that the evolution of host-specialization in parasites is a trade-off between the range of potential host species and the level of specialization on any particular host.Electronic supplementary materialThe online version of this article (10.1186/s12983-018-0249-x) contains supplementary material, which is available to authorized users.

Strategies of the beetle Oochrotus unicolor (Tenebrionidae) thriving in the waste dumps of seed‐harvesting Messor ants (Formicidae)

“…The lack of colony‐specific similarity was reflected in similar behaviour of the ants towards associated beetles and those found in an alien M. barbarus colony. It has been hypothesised that a certain overlap in cues may already lower host aggression (Witte et al ., ; Pérez‐Lachaud et al ., ; von Beeren et al ., ). In addition, the absence of certain key recognition cues could also be under selection (chemical transparency) (Martin et al ., ).…”

“…Although speculative, the reasonable convergence in chemical odour could be the result of natural selection to smell more like the host, a process that has been perfected in very specialised myrmecophiles (Nash et al ., ). Nevertheless, the chemical mimicry in the beetle is imperfect (cf.Witte et al ., ; Pérez‐Lachaud et al ., ; von Beeren et al ., ) and the beetles do provoke a mild form of aggression. The hydrocarbon profiles of Messor ants were colony‐specific, but those of the beetle did not cluster with their host.…”

Low Host Specialization in the Cuckoo Wasp, Parnopes grandior, Weakens Chemical Mimicry but Does Not Lead to Local Adaption

“…We found support for the first hypothesis: the low specialization in host use of P. grandior lead to a low-level, albeit appreciable chemical mimicry allowing it to successfully attack any of its available host species. A large comparative study is needed to finally test the hypothesis that host range in cuckoo wasps effectively correlates with the precision of chemical mimicry, as previously found in other insect brood parasites of Hymenoptera [69].…”

Fine-tuned intruder discrimination favors ant parasitoidism

“…Furthermore, differential aggressive behavior against myrmecophiles that differ in their degree of integration into the colony has been reported for some ant species such as Eciton burchellii foreli Mayr, Leptogenys processionalis distinguenda (Emery), L . borneensis Wheeler, or Formica rufa L. [23,78,79].…”

“…Nestmate recognition and communication in social insects is based extensively on chemical signals, i.e., cuticular hydrocarbons (CHCs) [19–21], although acoustics also play an important role [22]. Myrmecophiles range from highly integrated guests that rely on physiological, morphological and behavioral adaptations that allow them to be treated as nestmates, to poorly integrated species that elude the hosts as much as possible [23]. Studies on myrmecophiles that exploit ant communication signals to successfully integrate the society are numerous [24,25].…”