The following is a guest post by Myrmecologist Brendon Boudinot.

The objective of this guest post is to raise awareness of and demystify, in part, the doubled secret of every worker and queen ant’s genome: male ants. It is well known that male ants are produced by arrhenotokous parthenogenesis, i.e. from unfertilized eggs. What is vastly less known is the male ant itself. Male ants are the dark side of the moon for myrmecology. We know full well that they exist, but we hardly know their diversity, ecology, and behavior, and we often willfully ignore males. When I had the pleasure of meeting E.O. Wilson, he said to me that it’s a good thing I work on male ants as, for example, when male ants come to one’s porch light, one’s first reaction is “not to collect them, but to turn the light off.”

Figure 1. Representatives of the adult castes of ants (Camponotus discolor, Formicinae). Alate queen right, worker center, male left.

Now, in terms of what I can and cannot demystify, I can demystify morphology, but I can hardly change the way we think about male behavior or ecology. With respect to the latter, Jon Shik and his team found that, contrary to our expectations, male ants may live for up to an entire month outside of their natal colonies (Shik et al. 2012). What are these males actually doing outside of the nest? We don’t know. Why do these long-lived males survive outside of the nest? We don’t know. What is clear, however, is that males are more than just sperm missiles (or “sperm vessels” as Shik et al. so politically euphemized in their publication). Moreover, morphology suggests that perhaps male ants of some genera or lineages may contribute to work inside the nest. The males of most basicerotine genera, for example, have fully-formed worker-like mandibles, including the nasty fangs of Rhopalothrix (see the dacetine Phalacromyrmex, for example). It is thus apparent that there are open questions about and work to do on male ant behavior and ecology, especially flight phenology and mating systems.

Perhaps surprisingly, I have found that to identify male ants to subfamily, or even genus and species, it is not absolutely necessary to examine genitalia. The unfamiliarity of male morphology should not deter us from pursuing questions about male biodiversity. Male ants have confounded taxonomists for centuries, dating back to Linnaeus (1764), who described the first male ant as a wasp: Vespa helvola (= Dorylus helvola, Dorylinae). Male ants have also been subjected to a pair of misconceptions which has possibly stunted the study of males. First, that male ants are too stable (Wheeler 1910), and second that male ants are too variable. As has been noted by Brown & Nutting (1949) those variable males belong to genera for which workers are also confoundingly variable. In a positive sense this is not always the case. The notorious invasive Rasberry Crazy Ant, Nylanderia fulva, remained for many years without a scientific identity as workers of the Nylanderia species complex to which N. fulva belongs are not discretely distinguishable; males of N. fulva, however, are comparatively easy to separate from those of N. pubens by male genitalic characters (fig. 2; Gotzek et al. 2012). Moreover, males have been found to be important for separating species in other subfamilies (Odontomachus, Ponerinae: Deyrup & Cover 2004) and for identifying generic boundaries (Prenolepidini, Formicinae: Lapolla 2012) and even new genera (Yoshimura & Fisher 2009; Boudinot in prep.).

Figure 4

Figure 2. Terminalia of Nylanderia fulva left and N. pubens right, displaying conspicuous differences between the telomeres. Images modified from Gotzek et al. (2012).

 Honing in on particular morphological characters of males, I will first provide a minor overview of male characteristics. Like queens, male ants are usually winged, with the associated characteristics of flying Hymenoptera, including the muscular mesosoma, large eyes, and of course wings. A few salient characteristics of the male mesosoma (fig. 3) are the anapleural sulcus dividing the mesokatepisternum from mesanepisternum, mesepimeron and epimeral lobe, notauli, mesoscutum and mesoscutellum, and finally the notum. These characters, as well as characters of the head and other body parts, vary informatively at the species and genus level, as indicated by Yoshimura & Fisher (2007, 2012).

Fig 3_Leptogenys

Figure 3. Profile and dorsal views of a male Leptogenys angustata (Ponerinae). AplSc = anapleural sulcus; EpmL = epimeral lobe; MsAst = mesoanepisternum; MsEpm = mesepimeron; MsKst = mesokatepisternum; MsScl = mesoscutellum; MsSct = mesoscutum; MtAst = metanepisternum; MtKst = metakatepisternum; Mtn = metanotum; Not = notaulus; Prnt = pronotum; Prpd = propodeum; Teg = tegulum. Modified from images captured by D. Raharinjanahary, copyright AntWeb 2002–2013, Creative Commons Attribution License.

With respect to wings, I am a proponent of the Brown & Nutting (1949) system of abscissa-oriented nomenclature, with specific names provided to each vein segment given that segment’s homology with basal Hymenoptera. The Brown & Nutting system is eminently useful for concisely conveying information about hymenopteran wing venation, and is only intimidating until one has gained experience thinking about the wings of several taxa, which is no different from the intimidation first engendered by the dreaded Comstock-Needham system in general entomology. The ancestral hymenopteran wing underwent two major fusion events: Fusion of the Radius with Radial Sector (forming R+Rs) and Media with the Cubitus Anterior (forming M+CuA). Subsequently, the Subcosta fused with the Radius and Radial sector (forming Sc+R+Rs). With this in mind, Brown & Nutting named the unfused, or free abscissae sequentially, thus giving us Rsf1 (f = free), Rsf2+3, and Mf1 etc. (fig. 4). There is more to the story here, but I’ll let the figures do the talking.

Fig 4_Wing venation

Figure 4. Brown & Nutting system, modified by the author, applied to the forewings of Macroxyela (Xyelidae, top) and Myrmecia (Myrmeciinae, bottom). Longitudinal veins capitalized (C = Costa, Sc = Subcosta, R = Radius, 1Rs = 1st Radial sector, 2Rs = 2nd Radial sector, M = Media, CuA = Cubitus anterior, CuP = Cubitus posterior, 1A = 1st Anal, 2A = 2nd Anal); crossveins lowercase and indicating anterior longitudinal vein followed by posterior longitudinal vein (e.g. 1r-rs = 1st radial-radial sector crossvein); Ptstg = pterostigma, Clvfw = claval furrow; note that Rsx is an aberrant abscissa without homology outside of ants. Macroxyela figure modified from Comstock & Needham (1898); Myrmecia figure modified from Brown & Nutting (1949).

This leaves us with the final male-based enigma: Male genitalia (see Boudinot 2013). Male ant genitalia may be thought of as copulatory multitools, with each element adapted for the particular behavioral or mechanical aspect of gamete transfer for the lineage in question. The ninth abdominal sternum is usually included in discussions of male genitalia, as this sternum has muscles which control the anteroposterior movement of the genital capsule. The genital capsule itself is composed of a muscular, ring-shaped cupula, and three paired valves termed, from lateral to medial, the parameres, volsellae, and penisvalvae. The parameres generally grasp the apex of the female’s abdomen in copulo, and are composed of a basal basimere and distal telomere. Moving inward, the volsellae are composed of the basivolsella (at the base, of course), the apicolateral cuspis, and the apicomedial digitus. The volsella displays some of the most remarkable variation observed in male ants, and is possibly one of the most spectacular, albeit inconspicuous, mechanical wonders of the entomological world. In general, the cuspis is lobe-shaped, while the digitus is either club- or hook-shaped. Finally, we have the penisvalvae. Note ahead of time, for those still reeling all these years after Ento 101, the aedeagus is technically both the membranous and sclerotic elements of the intromittent organ. The sclerites (penisvalvae) have a basal (or anterior) apodeme called the valvura, to which most of the penisvalvar muscles are attached, and which acts as the penisvavlar lever or joy-stick (do ants know joy?). The blade-like element of the pensivalva is called the valviceps, is usually ventrally serrate, and acts to our knowledge as an anchor during copulation. Much variation can be observed in the components of male ant genitalia—variation which it is hoped will resolve taxonomic problems. Will male ant genitalic characters be revealed to be synapomorphic of as-yet morphologically undiagnosed clades, such as the formicoid clade? We cannot know if we do not attempt to understand them.

Fig 5_Genitalia

Figure 5. Genitalia of Ectomomyrmex (= Pachycondyla) javanus. A) Genital capsule, dorsal view; B) genital capsule, ventral view; C) paramere and volsella, mesal view; D) genital capsule lateral view; E) abdominal sternum IX, ectal view, F) penisvalva, ectal view. A, B, and E are oriented such up is anterior and down is posterior; C, D, and F are oriented such that left is anterior and right is posterior. AsIX = abdominal sternum IX; Bm = basimere; Bv = basivolsella; Cs = cuspis; Cu = cupula; Di = digitus; Pm = paramere; Pv = penisvalva; Sp = spiculum; Tm = telomere; Vc = valviceps; Vu = valvura. Figures modified from Ogata (1987).

With these facts about male morphology in mind, it is my hope and vision that male-based keys to the world fauna of ants may be composed. Male ants will play a pivotal role in our molecular era, being the golden key for genomics due to their haploidy, while simultaneously providing meaningful morphological characters which are not only understood in their variation, but in their function. It has been a delight to experience a shift in my collecting priorities (and obsessions), from first collecting a good series of workers, to collecting queens, and now to collecting males—associated or not. Every male collected now may be linked to workers given DNA barcoding technology and sufficient sample size, and every nest collection which contains males is a valuable contribution. As an eminent arachnologist once told me “males have all the characters! Male ants aren’t just the dark side of the moon; they’re the other side of the rainbow!” Our journey over the rainbow has begun in earnest. Over the past year I have been working on keys to all of the subfamilies and genera of the New World based on males and soon I hope to see an uptick in the number of male-based publications. Trust me, I’m counting them.

Literature cited

Boudinot, B. E. (2013) The male genitalia of ants: musculature, homology, and functional morphology (Hymenoptera, Aculeata, Formicidae). Journal of Hymenoptera Research, 30: 29–49.

Boudinot, B.E. (in prep.) Male ants of the New World (Hymenoptera: Formicidae): Keys to and diagnoses of the subfamilies and genera.          

Brown, W. L., Jr. & Nutting, W. L. (1949) Wing venation and the phylogeny of the Formicidae. Transactions of the American Entomological Society, 75: 113–132.

Comstock, J.H. & Needham, J.G. (1898) The wings of insects. American Naturalist, 32: 43–48, 81–89, 231–257, 335–340, 413–424, 561–565, 768–777, 903–911.

Deyrup, M. & Cover, S. (2004) A new species of Odontomachus ant (Hymenoptera: Formicidae) from inland ridges of Florida, with a key to Odontomachus of the United States. Florida Entomologist, 87: 136–144.

Gotzek, D., Brady, S.G., Kallal, R.J. & LaPolla, J.S. (2012) The Importance of Using Multiple Approaches for Identifying Emerging Invasive Species: The Case of the Rasberry Crazy Ant in the United States. PLoS ONE, 7: e45314. doi:10.1371/journal.pone.0045314

Lapolla, J.S., Kallal, R.J. & Brady, S.G. (2012) A new ant genus from the Greater Antilles and Central America, Zatania (Hymenoptera: Formicidae), exemplifies the utility of male and molecular character systems. Systematic Entomology, 37: 200–214.

Linnaeus, C. (1764) Museum S:ae R:ae M:tis Ludovicae Ulricae Reginae Svecorum, Gothorum, Vandalorumque, &c. In quo animalia rariora, exotica, imprimis. Insecta & Conchilia describuntur & determinantur. Prodromi instar. Holmiae [= Stockholm]: Salvius, 8 + 720 pp.

Ogata, K. (1987) A generic synopsis of the poneroid complex of the family Formicidae in Japan (Hymenoptera). Part I. Subfamilies Ponerinae and Cerapachyinae. Esakia, 25: 97–132.

Shik, J.Z., Flatt, D., Kay, A. & Kaspari, M. (2012) A life history continuum in the males of a Neotropical ant assemblage: refuting the sperm vessel hypothesis. Naturwissenschaften, DOI 10.1007/s00114-012-0884-6.

Wheeler, W. M. (1910) Ants: their structure, development and behavior. New York: Columbia University Press, xxv + 663 pp.

Yoshimura, M. & Fisher, B.L. (2007) A revision of male ants of the Malagasy region (Hymenoptera: Formicidae): Key to subfamilies and treatment of the genera of Ponerinae. Zootaxa, 1654: 21–40.

Yoshimura, M. & Fisher, B.L. (2009) A revision of male ants of the Malagasy region (Hymenoptera: Formicidae): Key to genera of the subfamily Proceratiinae. Zootaxa, 2216: 1–21.

Yoshimura, M. & Fisher, B.L. (2012) A revision of the Malagasy endemic genus Adetomyrma (Hymenoptera: Formicidae: Amblyoponinae). Zootaxa, 3341: 1–31.