Hypognathus condition in insects (left image from Wikimedia commons; right drawing modified after Snodgrass 1935)

In most insects, and certainly in all bees and most wasps, the mouthparts hang at the bottom of the head and, since each set of mouth pieces derives from a particular segment along the main axis of the body, they are positioned one after the other in a sequence from front to back: labrum¹; mandibles, maxillae, and labium. This head arrangement is known as the hypognathous condition, and can be considered the groundplan for insects.

In hypognathous insects the very first pair of appendages at the front of the head are the antennae, quite important since they are the primary tactile and smelling organs, so this makes sense (no pun intended).

Prognathus condition in insects (left image modified from ©Alex Wild; right drawing modified after Snodgrass 1935)

In ants, however, the very first thing at the front of the head are the mounthparts. Usually the large mandibles of these insects are at the forefront. But the term prognathy here (that is, “projecting jaws”) is really describing a functional condition that results from a significant structural rearrangement of the ant head: the entire head capsule is tilted almost 90 degrees forward, so what used to be the anterior region in a hypognathous insect is now the upper part of the head, and what used to be the bottom (the mouth) is now the front-most region.

In prognathous insects the antennae are no longer anterior in the head but are attached dorsally, and the different mouth pieces no longer run from front to back but are arranged from up to bottom (in a dorso-ventral axis). In fact, in relation to the rest of the elements in the head the mouthparts have not changed position. There is one important exception to this– the place where the head attaches to the neck and which has the hole by which the digestive tube, neural cord and the rest of the entrails go through has shifted from its ancestral place opposite to the antennal sockets to the upper back of the head, opposite to the mouth.

One way to envision this major structural rearrangement with more familiar examples is to compare the head of your cat or dog with your own head. Look at the head of your pet (even your goldfish will do). If you trace an imaginary line that passes right between the eyes (imaginary is the keyword here), that line will exit at the back of the head right through the hole that connects the head with the neck, the hole through which the neural cord coming from the brain passes (the foramen magnum in anatomical speech). Assuming your pet is standing straight in four legs, this imaginary line will continue parallel to the vertebral column all the way to the end and exit at the rear (the anatomical name of which I will spare for you). Now perform the same for your own head. In your case the imaginary line that went in-between your eyes will find a dead end at the back of your skull, right above the nape. In us, the “back” hole of the skull is located at the floor of the head. What happened is that as humans evolved up-rightness, the foramen magnum shifted position from back to bottom to balance our big heads and keep our faces looking to the front. This is also why if we lay chest down we look utterly ridiculous with our faces kissing the floor (or risk torticolis), as opposed to our cat or dog which will be graciously resting in front of the fireplace face-straight. Well, from wasps-like ancestors to ants the insect foramen magnum shifted exactly in the opposite way.

Now, in us jawed vertebrates (you and your pets) none of these conditions are called prognathous. This term has a very different meaning and refers to cases where either the upper jaw projects beyond the lower jaw or vice versa, something that can be appreciated in certain dog breeds like the Pug and in people that have subject themselves to large quantities of anabolic steroids, like certain current Governor of California.

Rhytidoponera metallica (April Nobile http://www.antweb.org/)

Back to insects, I have heard entomologists deny that prognathy is a diagnostic feature of ants, a synapomorphy. It is true that in some ants their mandibles seem to point downward, but this is just because having the neck attachment way in the upper back does provides the head articulation with a wider range of play. Again, the important point is not in which direction do the mouthparts project, but where is the location of the foramen magnum within the insect head.

Detach head of a Figitidae wasp (Via Mattias Forshage http://www.morphbank.net/)

Case in point. If you want to take a SEM of the base of the mouthparts in a regular wasps, the first thing you are forced to do is to detach the head from the body and place it face-down into the mounting stub. Your SEM will nicely show both the mouthparts and the foramen magnum.

Underside of head of a worker of Cerapachys nitidulus (Scanning Electron Micrograph, Roberto Keller/AMNH)

I have taken hundreds of SEMs of ant mouthparts and I never had to detach the head. The only thing you need to do is flip the ant, legs up, and you will have a unobstructed view of the base of the mouthparts. You won’t be able to see the foramen magnum in the same image though!

Notes and references

Starting next year I will be working as a postdoc in the laboratory of Patrícia Beldade at the Instituto Gulbenkian de Ciência in Portugal. This is an evolutionary developmental biology lab, an area of research fondly know as EvoDevo.

EvoDevo ask questions that are of a different nature than the classical Neo-Darwinian ones. For example, in the latter you always presuppose that variation exists in populations and that there is a link between what you see at the level of an organism’s morphology (its phenotype) and the underlying genetics (its genotype), and you study how natural selection then goes to mess things around. In EvoDevo you don’t give these things for granted. Rather, you ask how do new features (novelties and innovations) arise in the first place and exactly how does the link between genotype and phenotype comes about through the developmental process. From there, what you seek is to understand evolution as a process of modification of development.

Now, one cool thing about the Variation: Development and Selection lab of Patrícia Beldade is that her research focuses right at the area of confluence between the two views just described. She seeks to understand the mechanism by which development generates phenotypic variation of the sort that is important for natural selection to act upon.

We will be working with ants, of course, looking at the evolution of the caste system in the group. Most studies into caste evolution take the Neo-Darwinian approach to the problem. The classical work on the subject is Oster and Wilson 1978 book Caste and Ecology in the Social Insects¹, where the authors specifically set to focus “attention on the ecological and evolutionary aspects of caste, as distinct from developmental and physiological processes”². For example, there is a lot of work in this area on optimal caste ratios, looking at the proportion of the different castes within a colony in terms of how costly they are to produce. In contrast, we will look at the problem in terms of the potential that the developmental system has to produce a variety of alternative caste morphologies as dramatic as fully winged queens versus completely wingless workers.

Worker ants are, ecologically, the most conspicuous adult forms, so we often take this caste for granted. But from a comparative perspective workers are the odd ones: the flightless form arose in the common ancestor of the group as a modified version of a winged female. Once this ability originated, once this extreme plasticity in development was gained, it evolved as ants speciated giving rise to the extraordinary diversity of castes and forms we see today. But, for the most part, queens remain fully winged individuals, so in understanding ant evolution it is important to keep in mind that we are dealing with a caste-producing developmental system– just concentrating on workers wont do.

The project was written in collaboration with Christian Peeters from the Université Pierre et Marie Curie in Paris. As I have mentioned before, he specializes in all those ant species where the queen is not a winged individual, but rather a wingless form intermediate between the typical queen and the worker. This component is also important for our project, not only because such peculiar type of queens gives us more insight in this plastic developmental system, but also because queen morphology has a direct impact in the reproductive strategy of colonies. So this is a way to tie morphology and development with behavioral ecology and thus ask questions on selection and adaptation.

Does this means I am turning away from systematics? Not at all (again, for the joy of some and fear of others). My research centers on understanding the evolution of form, and while comparative anatomy and systematics serve to establish evolutionary patterns, it is development that provides the process side of the explanation. In fact, the first part of the project is pattern oriented, our goal been to identify and characterize relevant anatomical modifications. Besides, I still have a backlog of systematic manuscripts from my PhD research that I am preparing for publication.

Expect to see more on this topic in the coming months.

Notes and references

Gigantiops destructor (via Michael Branstetter - www.antweb.org)

The lateral eyes of adult insects (and most Arthropods) known as compound eyes, are like no other visual organs found in animals. You can think of our vertebrate eye as a simplified, one-lens photographic camera with a sensor composed of millions of light sensitive cells (and a blind spot, mind you). Well, that’s nothing. Each insects eye is composed of several small photographic cameras, each with its own lens and light sensitive cells (albeit, commonly only six of these). These units are called ommatidia (sing. ommatidium), and the image if formed by the combined information from all of them.¹

An interesting property of this peculiar anatomical arrangement is that compound eyes exhibit modularity– each ommatidium acts as an independent, yet fully functional building block that can be repeated multiple times to form a whole eye in different configurations. In layman’s terms, the eyes of insects are built out of sets of identical Lego pieces.

Compound eyes of a queen (a) and a worker (b) of the citronella ant Lasius (=Acanthomyops) occidentalis. The images are shown at the same scale (Scanning Electron Micrograph, Roberto Keller/AMNH)

Ommatidia do vary in size from species to species, but the diversity in size and shape of the compound eye as a whole comes primarily from the number and position of these elements. This can be easily appreciated by comparing the different castes in ants, since queens of a given species have large, well-developed eyes while in workers the eyes are smaller due to the fewer number of elements, even though the ommatidia in both castes are equal in size (see image above).

Blind as an ant. The eye-less worker of the Old World army ant Aenictus binghami (Scanning Electron Micrograph, Roberto Keller/AMNH)

Compared to their flying counterparts, both within the family as well as among bees and wasps, worker ants have in general poor vision. It is not uncommon for this caste to have no compound eyes at all, a characteristic that has evolved multiple times independently across the ant family tree.

As always in biology, they are notable exceptions. Genera like Myrmecia, Harpegnathos and Gigantiops (Greek for “mighty eyes”; see image opening this post) have huge eyes and excellent vision. I don’t have field experience with ants in the first two genera, but I once encountered Gigantiops ants in the Venezuelan Amazon. Let me tell you, if you are used to staring at live ants from a few centimeters away unnoticed, approaching a large ant that suddenly stops what she is doing to turn and stare at you in return is quite frightening.

So, how few ommatidia does the eyes of worker ants can have? Let’s see:

A worker of the small ponerine Cryptopone gilva (Scanning Electron Micrograph, Roberto Keller/AMNH)

Above is a worker of the leaf-litter inhabitant Cryptopone gilva with four ommatidia.

A worker of the tiny formicine Acropyga sp (Scanning Electron Micrograph, Roberto Keller/AMNH)

Workers of the tiny formicine ants in the genus Acropyga can have three ommatidia.

A worker of the elusive Concoctio concenta, from Gabon (Scanning Electron Micrograph, Roberto Keller/AMNH)

Workers of Concoctio concenta from west central Africa have compound eyes with just two ommatidia (this image is from the holotype, by the way). But, how about eyes with just one ommatidium?

Eciton burchelli (via Myrmecos Blog. © Alex Wild)

At first glance workers in the army ant genus Eciton seem to fit the bill: each eye has just a huge single lens. But external close inspection already reveals that this is not one enlarged ommatidium. Rather, the single dome-shaped lens is formed by the fusion of several ommatidia²:

The domed compound eye of an Eciton worker (Scanning Electron Micrograph, Roberto Keller/AMNH)

A detailed histological study of these modified eyes done by Werringloer in 1932³ revealed that it is not only the external facets that are fused. Internally the photoreceptor cells from the vestigial ommatidia are also united into a single light sensor, pretty much like the retina in the eyes of vertebrates and cephalopods.

In 1974 Bill Brown described some worker ants in a species he named Proceratium avium that also have huge single-faceted eyes⁴. I have yet to look at these ants in detail, but given what we know from the eyes of Eciton my guess is that the eyes in P. avium are also a fused set of several ommatidia.

Whether these vestigial eyes in workers are the result of re-evolution of eyes from blind ancestors will have to be the subject of a future post.

Notes and references

The unusual hook-shaped mandible closer apodeme (left one in the pair) of species in the Odontomachini genus group (Anochetus emarginatus pictured here). Piece dissected out and cleared from all muscles (Scanning Electron Micrograph, Roberto Keller/AMNH)

Last August, before taking a break from blogging, I posted an impossible-to-answer trivia. It consisted of the image above depicting an unidentified mysterious skeletal piece (sclerite) in the shape of a hook, together with two key pieces of information: a) it is entirely internal; b) it comes in pairs.

A regular visitor to this blog, Marc “Teleutotje” Van der Stappen quickly asked if it was part of the sting apparatus. This was a perfectly good guess, since it satisfies both a) and b), but the mysterious sclerite occurs on the opposite end of the ant. A subsequent comment by C.M. Wilson guessed the tentorium. It was also a good guess. We are now correctly assuming it is something inside the head, but I will argue that, since the tentorial arms are invaginations of the outer cuticle, strictly speaking they are not entirely internal.

The sclerite in question is nothing but the structure that serves as a link between the insect mandible and some of the muscles moving it. It is a specific type of apodeme: a term used to describe any internal piece of the arthropod skeleton that gives support to muscles¹. The tricky part of the trivia was that, while these apodemes exist in all ants (in all insects with mandibles in fact), they are extremely modified into strong hooks only in a small clade consisting of the ponerine trap-jaw genera Anochetus and Odontomachus (a group sometimes referred as the subtribe Odontomachini, but not currently recognized).

Ants have the basic type of mandible articulation found in most insects and known as dicondylic: each mandible interacts with the head capsule through a couple of hinges (called condyles in 1337 anatomical speak), and has two sets of muscles connected to it that pull on opposite sides– one for opening the mandible (abductor) and one for closing it (adductor). Now, the muscles don’t attach directly to the mandible but do so by way of a membranous ligament that, in the case of the mandible closer, connects in turn to an apodeme that receives all the muscle packs, hence the name mandible closer apodeme (in German, of course, all of the above information is summarized into a single, long word).

The left column shows the shape and location of the mandible closer apodemes (solid black) inside the head in Myrmecia sp. and Odontomachus chelifer. Right column: mandible closer apodemes painted (in orange) as they would appear internally on the head of an Odontomachus bauri worker ant. b, apodeme base; c, apodeme collateral branches; l, ligament; SOG, suboesophageal ganglion (Drawings from Paul and Gronenberg, 1999; SEM image by Roberto Keller/American Museum of Natural History)

In most ants the mandible closer apodemes consist of a highly sclerotized (that is, hardened) basal body (b) that branches into three long extensions (c) running towards the back of the head, as exemplified with Myrmecia sp. in the illustration above². Numerous muscle packages run from the inside of the head capsule to these collateral branches, so when the muscles contract all the force generated concentrates on the massive sclerotized base that pulls the mandible shut via the flexible ligament (l).

The mandible closer apodeme in members of the ponerine trap-jaw ant clade also has a stout base and three collateral branches. Here, however, the lateral branch is modified into a massive (really massive) and highly sclerotized hook. This is what you see in the image opening this post and in the illustration immediately above. Also above, to the right is an SEM of the head of a Odontomachus species where I painted in orange how these apodemes would look internally in place, so you can appreciate the size of these structures. They are also highly pigmented due to sclerotization: when you prepare workers of these ants for regular skeletal observation by clearing the muscles and other soft tissues with a strong base (KOH), you can see the couple of large pigmented spirals through the semitransparent cuticle of the head.

The hook-shaped branches provide extra attachment surface and support to the powerful adductor muscles, that in the case of these ants fill about two thirds of the entire head volume³. The apodeme in ants of this group also differs from the basic type in that it has a ventral projection that receives a specialized muscle called “trigger muscle”⁴. This muscle, one on each side of the head, is responsible for causing the subtle deformation of the frontal part of the ant’s head that releases the mandibles that were locked in the catapult mechanism to either strike prey or propel the ant into the air.

You can read all the details of this mechanism in the papers cited below.

Notes and references

The anterior tentorial pits (arrows) in a Tetraponera aethiops worker (Scanning Electron Micrograph, Roberto Keller/AMNH)

The head of an ant in frontal view has a couple of holes usually located in the area between the mouth and the place where the antennae are inserted. These holes look intriguing from the outside– Are they part of a sensing organ? Do they secrete a special chemical signal or defense substance through them? Are they use for breeding? The answer is more mundane than that. As I mentioned in an earlier post, most of what one sees in the outer surface of the arthropod’s exoskeleton does not have an external function, but is rather a symptom of the inside working in these wonderful machines. These particular holes mark the places where the cuticle invaginates to form the internal skeleton of the insect cranium known as the tentorium. The external holes produced by these invaginations are thus termed the tentorial pits.

The tentorium is the H-like structure of the internal skeleton of the head, marked in red as it looks in the inside. Tetraponera attenuata worker, left antenna removed (Scanning Electron Micrograph, Roberto Keller/AMNH)

In ants, the tentorium consists of two elongated arms or apophyses that start on the front of the head, right at the anterior pits, and extend towards the back to where the head attaches to the neck. The arms fuse with each other half-way through before parting again, forming an H-like pattern. In the image above, I painted in red how does the tentorium normally looks like internally. The tentorium is the place of attachment for some of the muscles that move the mouthparts and dilate the first section of the digestive tube. It also plays an important role as a support antagonist to the powerful muscles that close the mandibles in ants: these huge muscles originate back at the inside of the nape and connect forward to the base of the mandibles via strong tendons. Without the tentorium the head would probably collapse under the bite’s pressure¹.

Acropyga ant workers are minute individuals displaying a very reduced external morphology. Arrows point to the anterior tentorial pits (Scanning Electron Micrograph, Roberto Keller/AMNH)

The couple of anterior tentorial pits are always located right at the posterior margin the clypeus and, maybe due to a functional constrain, are very conserved in terms of their absolute position in the head. Knowing this is handy when you are doing comparative morphology, because these pits are always present regardless of how reduced other features of the head can become, so they are wonderful landmarks when it comes to understanding what went on with head morphology during the evolution of the group. In the minute Acropyga pictured above, for example, the clypeus is completely fused to the rest of the head. However we can not only know that the clypeus is still there, but also that it remains quite large due to where the tentorial pits are located.

The antennal sockets in Leptanilloides biconstricta lay very close to the anterior margin of the head. Arrows point to the anterior tentorial pits (Scanning Electron Micrograph, Roberto Keller/AMNH)

Also in the minute Leptanilliodes, the position of the tentorial pits tells us that the antennal insertions are very close to the front of the head not only due to extreme reduction of the clypeus but also because the antennal sockets have further migrated forward, passing the imaginary line that can be drawn between the pits (dotted line).

The antennae of Discothyrea ants sit on a shelf-like projection of the front of the head. Note the forward position of the antennal socket in relation to the large tentorial pit (arrow; left antenna removed. Scanning Electron Micrograph, Roberto Keller/AMNH)

The example I like best, however, is the location of the tentorail pits in Discothyrea and Probolomyrmex. In these genera the antennae are inserted in a shelf-like projection of the anterior part of the head that is otherwise completely fused and devoid of any line or suture. Looking at the position of the large tentorial pits one can appreciate just how much this peculiar modification protrudes forward, as the full antennal apparatus sits well beyond the tentorial pits.

Notes

The Alhambra in Granada, Spain.

I recently traveled to Andalusia, in the southern part of the Iberian Peninsula, to meet fellow myrmecologists Christian Peeters, from the Université Pierre et Marie Curie, and Alberto Tinaut, from Universidad de Granada. The reason for my trip was that I am fortunately enough to have been invited to collaborate in one of their ongoing projects studying the native ant species Monomorium algiricum. We set out to collect some colonies of this species as well as some others in the genus.

This was quite a pleasant trip. Collecting was a success, our host treated us well, and the scenery was great. The historic center of Granada is remarkable beautiful and, to my surprise, the locals speak a language very much like Spanish, for which I am accidentally fluent.

Sierra Nevada, southern face. The collecting site for M. algiricum is at the center of the picture on the mountain slope far back.

The species we are studying is also quite charming. Monomorium algiricum was originally described in the 1950s from a population in northern Africa, but the species happens also to be well established on the European side of the Mediterranean sea at mid-elevation in the Sierra Nevada, near Granada. Peculiar about this species is that the queens never develop wings, having a rather reduced thorax that very much resembles the worker’s. In general, such reproductive individuals are termed ergatoid queens, that is, worker-like queens (for ergatos = gk. worker).

The wingless thorax in the ergatoid queen of Monomorium algiricum.

Flightless queens pose a tremendous change in strategy when it comes to how the colony reproduces. The textbook version of an ant colony’s life cycle entails a newly emerged winged queen leaving the maternal nest and flying away by herself to find a suitable bachelor (or a suitable party of them). After mating, the queen sheds her wings and burrows into the ground to start a new colony by raising the first generation of workers, also by herself, without ever leaving the nest. The queen is able to perform this “claustral” colony founding by burning up her fat bodies together with the huge wing muscles to produce the energy necessary to lay eggs and feed the growing larvae. Most species of the  ~400 known in the genus Monomorium more or less display this mode of colony reproduction. By contrast, reproduction in species with ergatoid queens entails a process of colony budding: the newly mated flightless queen goes out of the maternal nest for a casual walk with some of the workers and never comes back, settling nerby to start a new independent colony. Together with the loss of wings, ergatoid queens lack the flight musculature normally used as body reserves, so they depend on the help provided by the accompanying workers to procure food and raise further generations of workers.

Collecting Monomorium subopacum in the Mediterreanan coast. Christian Peeters (standing) and Alberto Tinaut.

Christian Peeters has devoted more than two decades studying the various aspects of these “alternative” modes of colony reproduction that correlate with different queen morphologies, for which ergatoid queens are just one type among many. A major result of his extensive work is that the textbook caricature of colony life cycle I just described¹ is anything but the norm. Moreover, during their evolutionary diversification ants have deviated from the “normal” mode of reproduction multiple times independently in an astonishing high degree. Within Monomorium alone, the evolutionary switch from winged queens to ergatoid ones has probably occurred multiple times. The biology of ergatoid queens in Monomorium is better known for the North American species after the pioneering work done by William Morton Wheeler in the early 1900s, therefore the interest in the Mediterranean M. algiricum.

Collecting complete live colonies of Monomorium (Note: the hole was NOT done with the aspirator).

But, what’s in all these for me, a person more interested in the homology of obscure body structures than in colony reproduction dynamics and adaptation scenarios (hell, adaptation is not even in my vocabulary)? Well, it is exactly the fact that changes in colony reproduction strategy in ants is intimately linked to changed in the morphology of the reproductive individuals. As in the case of ergatoid queens, these morphological changes can be dramatic. These adult forms are not like workers, nor like the usual winged queens. These forms correspond to completely different castes and come with their unique anatomical specializations.

Colonies will normally have multiple queens. We want to know exactly how many there are per nest.

Just within Monomorium, the morphology of ergatoid queens is quite variable. For example, in the the North American wingless forms it is possible to homologise most thoracic plates with the ones in the thorax of a flying individual, even though the plates are fused together. But in M. algiricum the sutures between the much reduced skeletal parts are completely gone, and one has to guess what corresponds to what by careful examination of the faint depressions on the cuticle and the internal attachment of some of the muscles left.

Tinaut's lab in Granada's University. Peeters performs dissections to check how many queens have been inseminated and if their ovaries are active.

What we hope to do is to assemble a detailed picture of the life history of M. algiricum from many different angles and so understand how does this species fits into the larger pattern of the evolution of ergatoids in the genus.

Notes

An isolated second abdominal segment constitutes the characteristic petiole (blue) in ants. Pachycondyla stigma worker (Scanning Electron Micrograph, Roberto Keller/AMNH)

The easiest way to know you are looking at an ant is to pay attention to its waist: if it consists of one or two nicely isolated segments you can be sure you made a positive identification. The basal condition for the family, common to all ants, is to have the second abdominal segment in the shape of a node or scale and distinctly isolated from the rest of the abdomen to form a petiole (remember that the first abdominal segment is coupled to the thorax as the propodeum). The functional advantage of such novel architecture seems to be an enhanced articulation between body segments, and thus greater mobility for a posterior part of the body that bears the ant’s weapons in the form of a sting or other specialized chemical producing  organs like the acidopore.¹

Petiole (blue) in a Metapolybia cingulata vespid (Scanning Electron Micrograph, Roberto Keller/AMNH)

Adetomyrma sp. worker showing the broad posterior attachment of the petiole (in blue; Scanning Electron Micrograph, Roberto Keller/AMNH)

In reality, the presence of a petiole is not as clear cut as we would like from a systematic point of view. Wasps in other families may have a petiole as isolated as many ants (see the vespid Metapolybia above), and the petiole in some ants can have such a broad posterior attachment as to be quite similar to the usual condition found in the rest of the stinging wasps and bees (see Adetomyrma above). Still, our current understanding of phylogeny, both in terms of the position of Formicidae within Aculeata as well as the internal relationships within ants, suggests that the the petiole originated anew in the common ancestor of the group. In the case of Adetomyrma, even though its parent clade Amblyoponinae is believed to be close to the root of the ant tree, the genus is well nested within the subfamily and so the “unpetiolated” condition must be explained as a secondary derivation from a petiolated condition, as Phil Ward discussed when he first described this taxon ².

Petiole (blue) and postpetiole (purple) in a Manica rubida worker (Scanning Electron Micrograph, Roberto Keller/AMNH)

Petiole (blue) and postpetiole (purple) in a Aenictus binghami worker (Scanning Electron Micrograph, Roberto Keller/AMNH)

More interesting among ants is the subsequent modification of the third abdominal segment into a similar constricted node to form the postpetiole, thus resulting in ants with two segmented waists. This appears to have occurred at least seven times in parallel, in the subfamilies Aenictinae, Agroecomyrmecinae, Ecitoninae, Leptanillinae, Leptanilloidinae, Myrmicinae, and Pseudomyrmecinae (see phylogeny below). Moreover, some ants have a condition that seems intermediate between an undifferentiated segment and a true postpetiole (e.g., Cerapachyinae, Myrmeciinae). The similarity of this feature across the different unrelated groups is striking. It was once thought, for example, that the two segmented waist in myrmicines and pseudomyrmecines was a case of homology rather than independently derivation. Again, the functional advantage of having an extra “hinge” is greater flexibility of the metasoma. A weak, yet curious correlation is that ants that have evolved a two segmented waist retain, for the most part, a powerful sting, whereas in derived ants with single segmented waists the sting is either vestigial (e.g., Dorylinae) or is completely absent and has been replaced by chemical spraying glands (e.g., Dolichoderinae and Formicidae).

The origin of the petiole in ants can be traced back to the common ancestor of the group. Modification of the the third abdominal segment into a postpetiole have ocurred in parallel in the clades marked in purple. Subfamily names in yellow contains species with further tubulation of the abdominal segments IV to VI (ant phylogeny simplified from Brady et al. 2006, Moreau et al. 2006, and Rabeling et al. 2008)

Some structural details are of interest here. The metasomal segments are arranged like the cylindrical sections of a hand telescope, with each segment entering the previous one in a series. Abdominal sclerites (the skeletal plates that form each segment) have a well-marked anterior section corresponding to the part that articulates inside the preceding piece, which can be recognized by its smooth and shiny surface lacking hairs (colored in yellow in the images below). Barry Bolton³ introduced the terms presclerite for this anterior section and postsclerite for the remaining posterior one. All the metasomal segments are divided into these two sections but, as Robert Taylor⁴ pointed out, sometimes the segments bear a strong constriction right at the boundary between the presclerite and the postsclerite sections. He termed this “tubulation”, and noted that the transformation of a segment from an undifferentiated structure into a petiole or/and postpetiole entailed nothing but an extreme case of tubulation.

Presclerites (in yellow) along the segments of the metasoma in a Leptogenys sp worker. Note how the IVth abdominal segment is "tubulated" but there is no true postpetiole (Scanning Electron Micrograph, Roberto Keller/AMNH)

The concept of tubulation has been important in discussing the different degrees of constriction found in the third abdominal segment across the ants, from untubulated ones to full postpetiole, mainly from the point of view of phylogenetics and classification. But one overlooked but nevertheless highly interesting aspect of tubulation is its occurrence beyond the second and third segments of the abdomen and what does this pattern suggests about the underlying developmental process of segment modification.

Metasomal segments showing serial tubulation of segments in a Dorylus helvolus worker. Presclerites in yellow (Scanning Electron Micrograph, Roberto Keller/AMNH)

The evidence from comparative anatomy points towards tubulation as a case of morphological diversification through homeosis: once a genetic mechanism was established for the constriction of the second abdominal segment in the common ancestor of ants, this mechanism seems to have been coadapted, independently, for the formation of the postpetiole in the third segment, explaining not only its recurrence in phylogeny but also the almost identical nature of this structure in various adult workers of distantly related clades. Tubulation further occurs in the fourth, fifth and sixth abdominal segments in the genera Dorylus, Leptanilloides and Sphinctomyrmex (also independently as far as we know) forming a pattern of serially homologous constrictions of abdominal segments along the body axis.

Leptanilloides biconstricta worker. Note the elongated body and the serial tubulation of the metasoma (Scanning Electron Micrograph, Roberto Keller/AMNH)

Since tubulation is prominent among the minute, subterranean groups of ants (e. g., Leptanillinae and Leptanilloidinae), and since this seems to be the final frontier in the discovery of new ant forms, I predict that it won’t be long until an ant with a three segmented waist shows up in our winklers sacks.

Update June 9th, 2009: Added figure with phylogenetic tree.

Notes and references

Tetraponera aethiops worker showing the location of the clypeus in green (Scanning Electron Micrograph, Roberto Keller/AMNH)

When looking at an arthropod from our vertebrate perspective it is easy to forget that we are looking right at the animal’s skeleton. While our own vertebrate skeleton consists of a series of internal compact pieces with sponge-like cores that support an external layer of muscles and entrails (all nicely wrapped in skin), the reverse is true for arthropods. The arthropod skeleton consists of a series of external plates and hollow tubes that form enclosed spaces within which the internal musculature system attaches¹. One consequence of this peculiar body architecture is that most of what we see on the outer surface of this exoskeleton is but a reflection of what is going on on the inside– minute external pits correspond to places where the cuticle folds in to form internal pillars, and innocent looking shallow furrows on the surface are large internal walls where powerful muscles originate. A simple examination of the exoskeleton, therefore, can tell us a lot about particular functions and consequently about an insect’s behavior.

The clypeus (in green) on the turtle ant Procryptocerus, with a characteristic brush on its anterior border (Scanning Electron Micrograph, Roberto Keller/AMNH).

A good example of this is provided by the clypeus in ants and its wide diversity of forms across the different species in the family. The clypeus corresponds to an unpaired skeletal plate lying right at the center of an insect face. It is normally located lower in the head just in front to where the antennae are inserted, but in many ant groups it quite commonly extends in between the antennal sockets. The anterior border of the clypeus is involved in two important articulations relating to the movement of the mouthparts. The central part forms a wide hinge with the mouth’s “lid” or labrum, allowing the latter to move forward and backwards to open and close the preoral cavity where the intricate ant tongue is stored when retracted (the actual opening of the mouth lies internally at the back-end of this preoral cavity). The sides of the clypeal border, on the other hand, form deep cavities where the anterior condyle of each mandible articulate.

Those articulations occur externally. But what is going on the inside of the clypeus? The inner surface on the clypeus provides attachment to a set of muscles that originate right at the anterodorsal section of a special elastic chamber located just before the mouth known as cibarium. When these muscles contract the cibarium expands producing a suction action. It is basically the sucking pump of the insect, and the bigger the clypeus the bigger the pump muscles and the larger the sucking force. You may have probably noticed the big goofy snout in cicadas; well it is nothing but the hypertrophied clypeus attesting to the large sucking pump of these dedicated suckers. Ants never reach such extremes, but the clypeus can be quite large in some groups.

Clypeus (in green) on a Onychomyrmex doddi worker. Species in this genus display a convergent army ant like behavior (Scanning Electron Micrograph, Roberto Keller/AMNH)

In clades of chiefly predatory ants, like amblyoponines, the clypeus is never large and has become rather reduced in the more specialized genera like Apomyrma and Onychomyrmex. The same pattern occurs more or less among ponerines.

The large clypeus (in green) on a Formica fusca worker (left antenna removed. Scanning Electron Micrograph, Roberto Keller/AMNH).

Oh, but formicines and dolichoderines, those ants are such big suckers. Those are the ants you will most commonly see wandering between flowers looking for nectar and tending aphids for honeydew (that is, they suck ass big time²). Myrmecines ants have large clypeus in general, and it is not surprising to see a correlation between tending other insects and having a well developed clypeus in genera like Crematogaster.

The clypeus (in green, maybe) in a Neotropical army ant Labidus coecus worker (the clypeus is there, I swear. Left antenna removed. Scanning Electron Micrograph, Roberto Keller/AMNH)

Now army ants, the ultimate specialized predators of the insect world, they are not suckers at all. All clades can be easily characterized by having almost no clypeus, so that the antennal sockets seem to fall off their heads forward.

The swollen clypeus (in green) on an Acanthoponera minor worker (left antenna removed. Scanning Electron Micrograph, Roberto Keller/AMNH)

One genus that intriges me is Acanthoponera. Species in this genus have a very large and swollen clypeus for what you will expect given the group’s phylogenetic position in between other major clades of ants. I don’t think much is known about the biology of this genus other than it is a nocturnal ant. But I bet you this ant is sucking around something.

Notes

Red Hot Chilli Peppers? No, dentiform setae in the labrum of an Onychomyrmex doddi worker (Scanning Electron Micrograph, Roberto Keller/AMNH)

Just as the anterior margin of an ant’s cranium can sometimes be armed with rows of dentiform clypeal setae (that is, especially modified hairs), the lid that closes the insect’s mouth called labrum can bear identical structures. The image above shows two of these specialized teeth-like pieces (in red) flanking an empty broad socket where a third piece used to be inserted.

The labrum and part of the clypeus of an Onychomyrmex doddi worker. A row of dentiform setae adorn the labrum (in red) and the clypeus (in yellow; Scanning Electron Micrograph, Roberto Keller/AMNH)

Although these dentiform setae vary in size and shape quite considerably from species to species, when they are present in different parts of the body within an individual they show the same morphology, suggesting that they are the result of a similar developmental program that switches on at the different positions.

Head of the African subterranean ant Apomyrma stygia showing the hypertrophied dentiform setae in the labrum (in red; Scanning Electron Micrograph, Roberto Keller/AMNH)

Moreover, there is a interesting similarity between dentiform setae that have developed in similar but apparently independent (non-homologous) conditions. The hugely grown dentiform setae restricted to the labrum in Apomyrma stygia are identical to the similarly hypertrophied ones found in Amblyopone pluto but that occur exclusively in the clypeus (see last image on this post). Though not sisters, these two taxa belong to the same Amblyoponinae clade.

Lastly, a couple of comments regarding a recent paper describing the ant fossil Gerontoformica, which has similar detiform setae in both the clypeus and labrum. Nel and coworkers¹ mention that dentiform setae in extant ants are found either in the clypeus or in the labrum but never in combination. This is not the case as can be seen in the example of Onychomyrmex pictured above. There is also the suggestion that Probolomyrmex, a non-amblyoponine genus, has dentiform setae on the labrum. However, close inspection revels that this is also not the case. Rather, most setae covering the body in this genus, including the few stout ones on the labrum surface, are short and scale-like and can easily be confused with pegs at low magnification.

So far, in extant taxa these peculiar dentiform setae arming the clypeus and/or labrum are only known to occur within the subfamily Amblyoponinae.

References

Frontal part of the head in an Anochetus emarginatus worker, profile view (Scanning Electron Micrograph, Roberto Keller/AMNH)

This image shows the mouthparts of a trap-jaw ant in resting position. The only structures really visible are the prominent elongated mandibles (in yellow) that project forward. The rest of the pieces, laying immediately below, are retracted inside the preoral cavity.

Fully extended mouthparts in an Anochetus emarginatus worker, profile view (Scanning Electron Micrograph, Roberto Keller/AMNH)

And this is how the mouthparts look fully extended, when the ant is sticking its tongue out. There are four different sets of structures here: the labrum (in green); the mandibles (in yellow); the maxillae (in orange); and the labium (in red). Each set corresponds originally, both phylogenetically and ontogenetically, to a pair of structures, although only the last three are modified limbs properly (each correspond to a pair of head appendages).

These are very complex structures, each part deserving its own separate discussion. But I wanted to thrown these images here now to serve as reference for future posts, and mention a few important generalities.

Ants display the unmodified general architecture of a biting insect. The mouthparts of adult ants are typical for what is found when comparing different insect groups, and one can readily homologize each part with a corresponding structure in a grasshopper or a beetle for example. Even the most derived mouthpart morphologies found within ants, like that of the trap-jaw ant pictured here, preserve this general pattern.

However, ants do have some uniquely derived features. They are truly prognathous insects, something uncommon within Hymenoptera (but not exclusive). While in bees and in most parasitic and stinging wasps the mouthparts hang down below the head pointing to the ground, in ants they are directed forward, always pointing to the front.

Ant prognathy, however, is not only a function of the fact that the whole head is tilted forward. Examine the image above and you will notice that the labrum, maxillae and labium are fully extended while the mandibles remain closed. That is, unlike other Hymenoptera, prognathous or not, in ants the mandibles do not fold right on top of the rest of the mouthparts at rest. Instead the main body of the mandible “steps-up” immediately after the mandible’s articulation (the rounded yellow piece at the far right), thus laying out of the way from the remaining structures.

The much derived Anochetus pictured here provides an extreme example illustrating this, but the exceptional modification is universally shared within the family. It is another unique ant synapomorphy. Obvious as it may seem once explained, I have to confess it took me a while (a few years actually) to figure out what was happening structurally in ants that was different from the non-formicid outgroups. But since then, after the explanation clicked, I cannot look at an ant without seeing it.