Army imposters: the art of blending in

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).

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Ecitophya simulans next to an Eciton burchellii foreli media worker. Photo: Taku Shimada.

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.

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Raiding column of Eciton burchellii foreli. Photo: Silvia Perez-Espona

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

PerezEspona_image_3(1)

Dr Sílvia Pérez-Espona during collection of specimens in a forest fragmented area in the Área protegida de San Lorenzo’s buffer zone.

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