Mimicry of ants by social parasites

To date, detailed studies of the adaptations allowing non – ant parasites (parasitic myrmecophiles) to infiltrate and live in ant societies were largely restricted to a few Coleoptera and Diptera, whilst detailed population interactions between a social parasite and its ant host have been studied only in Maculinea (Large Blue) butterflies.

Our aim is to understand why social parasites are generally rare when the ants whose social systems they penetrate are often widespread and abundant species. A need for another resource to coexist with ants, such as the initial food plant eaten by young Maculinea larvae, is only a partial explanation: many host ant species colonies kill the Maculinea larvae they adopt, and most other social parasites have no secondary resource and yet are no less rare.

We hypothesise that local selection pressures operating on social parasites may lead to a trade-off between ever increasing specificity to hosts at the regional, population and even super-colony level and a cost of being restricted to ever smaller parts of their host species ranges. There is strong indirect, and some direct, evidence that this is achieved through chemical mimicry, while recent research also finds a role for acoustic mimicry of ant stridulations.

Many substances used in chemical mimicry are common and widely distributed in insects, but specificity is possible because insects can detect very subtle differences in complex blends of substances. The incorporation of a novel compound into their blend, which is not shared by a sympatric species, is enough to achieve greater specificity. Even a subtle alteration in proportions between compounds may be sufficient to distinguish between colonies. If specificity of chemical mimicry at the level of individual ant populations proves to be widespread in myrmecophiles, it would explain why ant colonies vary so greatly in their suitability as hosts. Specificity may lead to speciation, which is likely to be cryptic if the main type of mimicry is to copy the chemistry of the host. This may have implications for conservation. Recent genetic analysis supports our deduction that Maculinea alcon exists as three sub-species or cryptic species in different regions of Europe.

In 2002 we showed that a myrmecophilous syrphid hoverfly known as Microdon mutabilis lives in one part of its range with Formica lemani as host ants and in other parts with another host ant, Myrmica scabrinodis. While both ant species have widely overlapping ranges the hoverflies are very specific to one or the other. In fact, we established distinguishing characters on the pupae of both types that justified the introduction of M. scabrinodis associated Microdon hoverflies as a new species, Microdon myrmicae(Schönrogge et al., 2002), separate from M. mutabilis, which uses F. lemani. Most syrphid species have been described from the adults, which are quite cryptic between M. mutabilis and M. myrmicae. Very little was known about the larvae and pupae, which as the stages that interact with the ants are likely to be subject to much stronger selection.

Within M. mutabilis there are also indications of extreme host specificity not only to a host ant species, but also to particular populations or even colonies (Schönrogge et al., 2006). We are determining how Maculinea and Microdon penetrate and survive in ant societies, and how their populations interact with those of their host ants by identifying and characterising the compounds relevant to this interaction (Akino et al., 1999; Gardner et al., 2007; Schönrogge et al., 2008; Schönrogge et al., 2004). While in Maculinea the role of chemical mimicry in interactions with ants and their geographical variation is well supported (see also Nash et al., 2008, Science), we identified a range of compounds on Microdon immature stages, yet their role is as yet unknown. We hypothesise that they are mimetic and predict that Microdon mutabilis and the cuckoo-feeding species of Maculinea are more dependent on chemical mimicry than the predacious Maculinea, which will rely more on evasion, chemical camouflage (ie the adsorption of ant chemicals), aggression or armour (Thomas et al., 2005). Having identified the chemicals used to mimic ant recognition signals in each species - and having determined whether they are closest to those of a particular ant caste or stage within the colony - we aim to use synthetic compounds to mimic the chemicals identified and test specificity on various hosts.

We could show in a recent study that some signals, here stridulations by ants, are characteristic to caste so that workers show a different behaviour towards sound made by queens than those from other workers. Maculinea caterpillars and pupae were known to make sounds. In behavioural experiments ant workers treated sound from both Maculinea stages like those from queens rather than workers. This is even more astonishing considering that they use different instruments or stridulation organs to produce the sounds suggesting that selection on making the correct sound is strong. Little is known about how characteristic sounds are among ant or Maculinea species; however, at this time the study provides at least part of a mechanism to explain how the parasite inserts itself into the hierarchy of an ant society at a high rank. Future studies will aim to characterise the aspects of sound recognised by the ants and study within and between species variation. We would also predict that other species of myrmecophiles could use acoustic mimicry. This should be most likely to occur where the host ants themselves use sophisticated acoustic communication and with social parasites that have non-parasitic sound producing relatives. Such species would be likely to have pre-adaptions to acoustic mimicry when their parasitic life-style evolved. (Karsten Schönrogge)

Collaborations

Many people have contributed to our studies in various ways. Collaborations are ongoing with partners in a past EU FP V project MacMan. We also continue to work with Dr Mike Gardner who used to be based at CEH and moved back to Melbourne; and with the Chemical Ecology Group and Prof. John Pickett at Rothamsted Research. Finally, not so much a collaboration, since Prof Thomas is still very much part of the group as a Professorial Fellow of CEH, but he has moved some of his activities to the Zoology department at the University of Oxford:

Recent publications

Barbero, F., Thomas, J.A., Bonelli, S., Balletto, E., Schönrogge, K. (2008) Queen ants Make distinctive sounds that are mimicked by a butterfly social parasite. Science, 323, 782 - 785.

Schönrogge, K., Napper, E.K.V., Birkett, M.A., Woodcock, C.M., Pickett, J.A., Wadhams, L.J., & Thomas, J.A. (2008) Host recognition by the specialist hoverfly Microdon mutabilis, a social parasite of the ant Formica lemani. Journal of Chemical Ecology, 34, 168-178.

Gardner, M.G., Schönrogge, K., Elmes, G.W., & Thomas, J.A. (2007) Increased genetic diversity as a defence against parasites is undermined by social parasites: Microdon mutabilis hoverflies infesting Formica lemani ant colonies. Proceedings of the Royal Society B-Biological Sciences, 274, 103-110.

Schönrogge, K., Gardner, M.G., Elmes, G.W., Napper, E.K.V., Simcox, D.J., Wardlaw, J.C., Breen, J., Barr, B., Knapp, J.J., Pickett, J.A., & Thomas, J.A. (2006) Host propagation permits extreme local adaptation in a social parasite of ants. Ecology Letters, 9, 1032-1040.

Thomas, J.A., Schönrogge, K., & Elmes, G.W. (2005). Specializations and host associations of social parasites of ants. In Insect Evolutionary Ecology (ed. by M.D.E. Fellowes, G.J. Holloway & J. Rolff), pp. 479 - 518. CABI Publishing, Wallingford, UK.

Schönrogge, K., Wardlaw, J.C., Peters, A.J., Everett, S., Thomas, J.A., & Elmes, G.W. (2004) Changes in chemical signature and host specificity from larval retrieval to full social integration in the myrmecophilous butterfly Maculinea rebeli. Journal of Chemical Ecology, 30, 91-107.

Schönrogge, K., Barr, B., Wardlaw, J.C., Napper, E., Gardner, M.G., Breen, J., Elmes, G.W., & Thomas, J.A. (2002) When rare species become endangered: cryptic speciation in myrmecophilous hoverflies. Biological Journal of the Linnean Society, 75, 291-300.

Akino, T., Knapp, J.J., Thomas, J.A., & Elmes, G.W. (1999) Chemical mimicry and host specificity in the butterfly Maculinea rebeli, a social parasite of Myrmica ant colonies. Proceedings of the Royal Society of London Series B-Biological Sciences, 266, 1419-1426.

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