A blog post highlighting the article by S. Pérez-Espona, W.P. Goodall Copestake, S. M. Berghoff, K. J. Edwards, N.R. Franks in Insectes Sociaux

By Sílvia Pérez-Espona

Neotropical army ants of the genus Eciton represent one of the many fascinating examples of interaction between species, with hundreds of (vertebrate and invertebrate) species reported associated with Eciton burchellii, and many more yet to be described (Rettenmeyer et al., 2011). Among the plethora of species found with this army ant, are the staphylinid beetles belonging to the genera Ecitophya and Ecitomorpha. These beetles have evolved to mimic the appearance and colouration of the most abundant worker cast (medias) of different Eciton species. These army ‘imposters’ are considered hunting guests, as they are found in the conspicuous raiding (and emigrating) columns of Eciton colonies ants where they feed on dropped prey or at booty caches. The mimicry of these two genera of myrmecophiles can be explained as a combined strategy to avoid predators (Bayesian mimicry) and to integrate into colony life (Wasmannian mimicry).

This intriguing example of mimicry and adaptation of Ecitophya and Ecitomorpha with their Eciton host was first described by Erich Wassmann in the late 19th century. Since then, studies of these two myrmecophile genera have mainly focused on resolving their challenging taxonomy as well studies of their behaviour in the field (e.g Akre and Rettenmeyer, 1966; Kistner and Jacobson, 1990; Reichensperger, 1935, 1933). We took a genetic approach to assess the evolutionary relationships between Ecitophya and Ecitomorpha with their Eciton hosts, with a special emphasis on the association of these myrmecophiles with E. burchellii, the only Eciton species known to harbour both beetle genera. To this end, we sequenced the same mitochondrial marker, cytochrome oxidase subunit I (COI, cox1), for ants and beetles collected from colonies located in west (Bosque Protector de Palo Seco, Reserva Forestal Fortuna) and central Panama (Área Protegida de San Lorenzo National Park and its buffer zone). COI is a maternally-inherited genetic marker widely used for studies assessing phylogenetic relationships between closely related taxa, as well as phylogeographic and population-level studies such as the ones we conducted in our study. Phylogenetic, molecular clock and population genetics analyses were conducted in order to determine the degree of specialization of species of Ecitophya and Ecitomorpha to their Eciton host. If there was a high specialization of the myrmecophiles with one particular host, molecular signatures would support earlier taxonomical classifications of Ecitophya and Ecitomorpha by Reichensperger (1933, 1935), based on the assumption that each myrmecophile species evolved to adapt to colony life of a particular Eciton species.

Indeed, our analyses revealed that Ecitophya and Ecitomorpha are truly host-specific and thus support the earlier taxonomic classifications by Reichensperger. Therefore, current taxonomic classifications that considered a lack of consistent morphological characters to support Reichensperger’s views need to be revised. Phylogenetic relationships between species of Ecitophya (found with different species of Eciton, in contrast to Ecitomorpha which is only found with E. burchellii), however, did not mirror those of their host; indicating that at this more specific level, the evolutionary path of this myrmecophile differed from that of its Eciton hosts. These analyses also provided further insights into the taxonomy of Eciton burchellii, indicating that the genetic divergence between the subspecies E. b. foreli and E. b. parvispinum was higher than between other recognised Eciton species, and that therefore E. burchellii ‘s taxonomy also warrants further taxonomical revision. Our molecular clock analyses indicated that the diversification of Eciton is likely to pre-date the diversification of the myrmecophiles and that Ecitophya’s species diversification (and therefore potential association with Eciton) might be older than that of Ecitomorpha. This possible earlier association of Ecitophya with Eciton, and therefore longer time-frame to adapt with the host, could explain why beetles from this genus are found with a larger number of Eciton species.

Population-level analyses of the Ecitophya and Ecitomorpha associates of Eciton burchellii showed strong patterns of population structure between colonies at broad geographical scales (west versus central Panama). In contrast, higher gene flow was observed at small geographical scales, with Ecitophya and Ecitomorpha lineages not being Eciton lineage- or colony-specific. Gene flow within each species of myrmecophile was also detected across the Chagres River, a landscape feature that acts as dispersal barrier for E. burchellii females (Pérez-Espona et al., 2012). This, therefore, confirms a higher dispersal ability of female Ecitophya and Ecitomorpha than their Eciton hosts. Morphological studies have described fully developed wings in both myrmecophiles (Kistner and Jacobson, 1990); however, flight ability in these beetles has only been reported anecdotally as observations of hovering during disturbance of colonies (Mann, 1921; Pérez-Espona pers.obs.). Considering the strong specialization to their host, and the likely dependence of these myrmecophiles to colony life, it is possible that the main dispersal events between colonies might take place by the beetles riding on alate Eciton males when they leave their natal colonies in search of a mate.

Ecological and evolutionary studies of Ecitophya and Ecitomorpha with Eciton army ant colonies are still in their infancy. This study demonstrates the usefulness of genetic approaches to provide insights into the biology and evolutionary history of these myrmecophiles with their Eciton hosts, as well as to help resolve the taxonomic challenges they present. We hope that our study will serve as a platform for the many further investigations that are still needed to fully understand this captivating manifestation of Darwin’s ‘entangled bank’.

References

Akre, R.D., Rettenmeyer, C.W., 1966. Behavior of Staphylinidae associated with army ants (Formicidae: Ecitonini). J. Kansas Entomol. Soc. 39(4), 745–782.

Kistner, D.H., Jacobson, H.R., 1990. Cladistic analysis and taxonomic revision of the ecitophilous tribe Ecitocharini with studies of their behavior and evolution (Coleoptera, Staphylinidae, Aleocharinae). Sociobiology 17, 333–480.

Mann, W.M., 1921. Three new myrmecophilous beetles. Proc. United States Natl. Museum 59, 547–552.

Pérez-Espona, S., McLeod, J.E., Franks, N.R., 2012. Landscape genetics of a top neotropical predator. Mol. Ecol. 21, 5969–5985. doi:10.1111/mec.12088

Reichensperger, A., 1935. Beitrag zur Kenntnis der Myrmecophilenfauna Brasiliens und Costa Ricas III. (Col. Staphyl. Hist.). Arb. iiber Morphol. Taxon. Entomol. aus Berlin-Dahlem 2, 188–218.

Reichensperger, A., 1933. Ecitophilen aus Costa Rica (II), Brasilien und Peru (Staph. Hist. Clavig.). Rev. Entomol. 3, 179–194.

Rettenmeyer, C.W., Rettenmeyer, M.E., Joseph, J., Berghoff, S.M., 2011. The largest animal association centered on one species: The army ant Eciton burchellii and its more than 300 associates. Insectes Soc. 58, 281–292. doi:10.1007/s00040-010-0128-8

A blog post highlighting the article by S. Popp, P. Buckham-Bonnett, S.E.F. Evison, E.J.H. Robinson and T.J. Czaczkes in Insectes Sociaux

Written by Tomer Czaczkes and Sophie Evison

Anyone who has spent a few minutes watching ants running along a trail will have noticed that when two ants meet, they often interact for a second or two. It seems obvious to anyone watching that some sort of information transfer is occurring. But what could they be communicating? One of the most tempting hypotheses is that the returning ant is telling the outgoing ant where to go: “take the next left to a great patch of aphids!” in the way that the honey bee waggle dance conveys information about the location of food patches to other workers. However, as inviting as this hypothesis is, multiple investigations over the centuries have found no evidence to support an antennal language in ants. The widely accepted view is summed up by Hölldobler and Wilson in their bible of myrmecology (1990): “‘ants antennate nestmates in order to smell them, not to inform them’’.

However, from the mid 1990s, a Russian scientist named Zhanna Reznikova has been researching the communication skills and numerical competency of wood ants (family: Formicidae). Reznikova and colleagues report finding astounding physical communication abilities: not only could ants communicate a complex series of turns to nestmates by physical contact, they could also encode numbers (i.e. take the 27^th turn to the food”) (Reznikova and Ryabko 1994). Sophie Evison first heard about this during her doctoral studies from Reznikova herself, at a Central European Workshop on Myrmecology. Of course, she had to try this herself, so using the ants Evison had available at the time – Lasius niger – she carried out a (fairly rudimentary) replication of Reznikova’s experiment. Evison’s experiment simply tested whether returning L. niger foragers could tell outgoing foragers the correct direction to go at an upcoming T-maze. Amazingly, initial experiments appeared to show that these ants were communicating a form of directional information about a T shaped maze simply via antennation, with no other cues. However, to be candid, these results had similar impact to those of Reznikova’s, and the findings only ever appeared in Evison’s doctoral thesis.

Reznikova’s discoveries are incredible. Why were they not picked up? Simply put, no one believed them. However, incredulity is not a basis for scientific discourse. Many incredible scientific findings – in both the current and original meaning of the word – have gone on to be proven right, and changed the face of science forever. It seems incredible that we live on a spherical ball of rock, but it is true. Although before it was widely accepted, this fact had to be independently verified by repeated observations. The appropriate response from a modern but incredulous scientific community should be replication, not dismissal.

Why then did no one try to replicate these results? Why didn’t we, in our recent Insectes Sociaux study, try to replicate it exactly? The answer is simple: No incentives. Replication – the backbone of the scientific method – has no career rewards – especially for low traction ideas. We all remember the STAP cell fiasco, but do you remember who tried to replicate it and failed? Indeed, when we take into account the time lost performing such replications, they can reasonably be considered harmful to a career. This is especially true in the specific Reznikova case, as their method requires weeks of patient observation to define stable working ‘teams’ before tests can even begin.

Our recent study in Insectes Sociaux has convinced us that, at least in two Lasius species, on-trail physical interactions do not communicate direction, but these are only two species. This increases the burden of proof for such physical communication, but does not rule it out. Of course, even though we set out to find evidence for such communication, we also find the results of Reznikova incredible. And while incredulity alone is not a basis for scientific discourse, it is far from meaningless. The collective intuition of our research community should not be ignored. Perhaps we should be taking a Bayesian approach, adjusting our demands for evidence by our level of incredulity. There an important part of this story that helped to keep our collective investigation going all these years: during a Royal Society event, the artificial intelligence expert Donald Michie mentioned to Elva Robinson that he had spent some time with Reznikova, and was very interested by her results. He had planned to investigate the claims further, but tragically lost his life in a car accident. Donald’s perspective on the work of Reznikova was important; it provided an externally driven impetus to resolve our contrasting findings.

So what would it take to convince us of the Reznikova findings? We propose replication by an unaffiliated research team, with meticulous video documentation. But let’s face it – for the reasons stated above, we don’t think this is going to happen. We hope to be proven wrong.