Seeing Vatesus beetles passing by when following an army ant emigration has something magical. With their beautiful reddish-shinning appearance and their teardrop-shaped body they look like running diamonds. In fact, they are among the most conspicious army ant guests and every observer - if experienced or not - quickly realizes that something else than an ant is joing the ants' emigration. A local guide at La Selva asked me once about the reddish critters in ant trails - he apparently saw them reguarly by chance during night walks. Spotting other ant guests in emigrations requires more experience, so new students primarily come up with collection vials full of Vatesus and little else. There are a few studies about Vatesus that I will introduce below, but many aspects of their biology still remain unknown - as it is the case for most army ant-associated symbionts.
Vatesus behavior - The studies about the behavior and life history of army ant symbionts by Carl Rettenmeyer, Roger Akre and Richard Torgerson in the 60s and 70s of the 20th century acompanied and inspired my own studies. Previous to the work of these researchers, little else than host records, deriving from pure taxonomic studies, were known about army ant symbionts. In his dissertation, Carl Rettenmeyer set out to provide the first detailed information about the biology of these fascinating arthropods. He described that Vatesus runs "in the central parts of the emigration while the brood was being transported". He also discovered that individuals lived inside the ants' bivouac - the temporary nesting site of army ants - close to where the ants' brood was stored. Occasional observation in ant refuse sites - the places where army ants dump their partly consumed prey - together with observations in laboratory nests showed that adult Vatesus fed on ant booty - whether they feed on ants themselves is as yet unknown. It was also Carl Rettenmeyer who discovered the first larval stage of any army ant symbiont - larvae of Vatesus.
© Daniel Kronauer
Army ants are migratory, i.e. colonies regularly move to new bivouac sites. Many myrmecophiles are able to participate in the emigrations, either by following the ants' trail pheromone or by passive transport using ants as vehicles (see other symbionts). Left: Slow-motion video showing an emigration of E. hamatum and several myrmecophiles following the ants' emigration: phorid fly, Vatesus larva, Tetradonia beetle. Vatesus larvae generally appear when the ant emigrations comes to an end. Right: End of E. hamatum emigration with many Vatesus larvae following the host colony.
© Jay Ireland
Vatesus life history - Carl Rettenmeyer collected some beetle larvae following the ants' emigration column, reared one individual to the pupal stage and concluded correctly, that the larvae are indeed Vatesus larvae. Following Rettenmeyer's example, we also reared several Vatesus larvae to adulthood, which gave us further information about the beetles' dispersal abilities and chemical integration strategies. We bred seven Vatesus specimens to adulthood and interestingly all specimens had intact wings. This seems logical, but once you know that beetles collected from host colonies have mainly broken wings (129 out of 133 inspected specimens), this fact is getting more interesting. For me the most likely explanation is that Vatesus adults have to find new host colonies each generation, and once they found a suitable host colony loose their wings. Whether this is a physiological process - a "wing shedding" initiated by the beetles themselves- or whether ants rip off wings is unknown (see photos on the right and discussion and supplement here). Below you find some more information about Vatesus life history adaptations.
The first study during my postdoctoral investigations in New York at the Kronauer Lab was about the diversity and life history of Vatesus beetles. Colleagues gave me a baby bodysuit as present for my newborn daughther - prominently decorated with a beautiful Vatesus specimen - what a great gift for a coleopterologist. Still have it - thanks friends. The studies on Vatesus at La Selva Biological Station, Costa Rica (see article here) uncovered some interestings aspects of the beetles' biology. Intensive community sampling, coupled with molecular and morphological species delineation, allowed me to detect cryptic species and to unveil a high degree of host specificity with strict host partitioning among sympatric Vatesus species . Further, matching of adults and larvae via DNA barcodes, plus surveys of female germline reproductive status, revealed that beyond the anatomical adaptations of adults, Eciton-associated Vatesus beetles have evolved sophisticated life history adaptations to synchronize with the cyclical phenology of host army ant colonies. Remarkably, I found that Vatesus reproduction and larval development are regulated such that eggs are laid, and early larval development is completed during the stationary phase of the host colony; larvae then disperse with nomadic host colonies by walking in emigration columns before pupating in soil. On eclosing, the new adults fly to locate new nests to parasitize.
left image: P. Hönle
Host records and cryptic diversity - A: Network depicting published host records of Vatesus species. Coloured boxes depict host ant species and circles Vatesus species. The turquoise-coloured circle depicts the V. clypeatus species complex and filled black circles V. gemellus and V. rufus - the only two species described to be associated with host species of different genera. Note that host associations have not been studied systematically and are based on scattered collections. B: Neighbour-joining trees for mitochondrial (COI; left) and nuclear DNA (concatenated wg and CAD, right) revealed three genetic clusters in Eciton-associated Vatesus beetles at La Selva, Costa Rica. Two of the three candidate species keyed out as Vatesus clypeatus and were denoted as V. cf. clypeatus sp. 1 and V. cf. clypeatus sp. 2. Male genitalia dissection confirmed that V. clypeatus from La Selva are in fact two distinct species. Host records are given below species names.
Synchronization to host colony cycle - It was the article of Akre & Torgerson (1969) on the behavior of Vatesus beetles that greatly influenced my studies about life history adaptations. They provided many valuable information about Vatesus biology: the feeding habit, the broken wings in adults, host specificity (although constrained by valid species identifications), and life history adaptations. The latter aspect fascinated me most. Here is a quote from their paper:
"Our collections indicate Vatesus lays eggs and the larvae develop during the host’s statary phase."
Furthermore they recognized that:
"We have only one record of a colony from which we collected larvae still following the emigration on the fourth nomadic day. In this instance only 7 larvae were collected. It appears that the Vatesus larvae probably follow the ants with a few larvae dropping out of the column and pupating each day."
I wanted to figure out whether this hypothesis based on a few observations was indeed true. A synchronization of Vatesus life cycle with the cyclical phenology of host army ant colonies would be an extremely cool story - showing that these social insect guests even evolved life history adaptations to their symbiotic way of life. So I set out to systematically study this aspect. For this, I first matched adults and larvae via DNA barcodes to disentangle species affiliations, and then I surveyed female germline reproductive status. Indeed, this revealed that beyond the anatomical adaptations of adults, Eciton-associated Vatesus beetles have evolved sophisticated life history adaptations to synchronize with host cycles of army ant colonies. Remarkably, I found that Vatesus reproduction and larval development are regulated such that eggs maturate during the nomadic phase, are laid during the early statary phase, so that early larval development is completed during the stationary phase of the host colony; larvae then disperse with nomadic host colonies by walking in emigration columns before pupating (probably in the soil, but this is unknown). On eclosing, the new adults fly to locate new nests to parasitize.
The Vatesus life cycle is synchronized to the stereotypical colony cycles of army ant hosts. Eciton colonies alternate between statary (approx. 3 weeks) and nomadic phases (approx. 2 weeks), which are synchronized to brood development of the ants (see article by Yuko Ulrich). Depicted is a schematic host colony cycle, highlighting the consecutive development of Vatesus from eggs via three different larval instars to pupae. Coloured Vatesus images depict direct observations in the field. Grey Vatesus images depict stages of the life cycle that have been inferred from laboratory observations and population genetic data (for details see our article).
Chemical mimicry - I am currently working on a manuscript detailing a community study of army ant myrmecophiles. It reveals that adult Vatesus beetles mimic the chemical nest-mate recognition cues of their host colony, thus avoiding recognition by their aggressive ant host. Chemical mimicry is a ubiquitous strategy of social insect guests to avoid host aggression. Still, adult beetles were sometimes attacked, but their teardrop-shaped, slippery body protected them from being caught by ant workers. In stark contrast, larvae do not express any chemical recognition cues at all on their cuticle, i.e. they chemically hide. Vatesus larvae were rarely attacked by host workers in laboratory nests (see section below). We do not know why ants did not attack larvae, alone the movement of larval individuals should be a cue that allows ants to recognize and attack them. I think their many long setae (hairs) might protect them from ant attacks and defensive chemical compounds might play an additional role, but this is pure speculation at this point. Interestingly, freshly eclosed adults did not carry any cuticular hydrocarbons (CHC), indicating that they must acquire these compounds during physical contact with host ants. Further support for acquired mimicry comes from the fact that adult specimens mimicked the CHC profile of the colony we collected them from. That means the same species of Vatesus show different CHC profiles depending on the host species we collected it from. By expressing radical modifications in external anatomy, chemistry, behavior and life history to their socially parasitic lifestyle, Vatesus beetles are certainly striking examples of obligate social insect symbionts.
Shown are representative gas chromatograms of adult host ants (black lines) and adult Vatesus beetles (red lines; data unpublished). Each peak represents one cuticular hydrocarbon (sometimes a mix of few similar compounds). Adult Vatesus have the exact same CHC compounds in the same relative ratio compered to adult ants of their host colony. Interestingly, the same Vatesus species can express different chemical profiles, depending on the host species the specimens were collected from, providing evidence that they acquire the CHC compounds from their host ants via physical contact. Alternatively, they might be able to biosynthesize CHCs differently depending on host association, which seems less likely to me.
Host aggression against Vatesus - Left: Boxplot showing the aggression of host workers against focal adult and larval specimens in three minute behavioral assays (unpublished data). Right: Adult and larva of Vatesus cf. clypeatus side by side in a laboratory nest setup containing Eciton hamatum host ants. Prior to extraction of CHCs we made behavioral studies to quantify the level of host aggression against focal Vatesus specimens. Interestingly, adults were attacked occasionally, but we seldom saw aggression against Vatesus larvae. Photo credit: P. Hönle