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

The meeting is organized by young researches, and this year will be specially interesting because there will be a discussion about creating a national society of evolutionary biologists.

I will be talking about the evolution of mouthparts within ants, covering some fascinating new discoveries that I haven’t share here yet but will blog about some time in the near future. In the mean time, here are a couple of my slides.

Media sources: antweb.org; Roberto Keller/AMNH.

Media sources: Wiki Commons; Alex Wild (http://www.alexanderwild.com/); R.E. Snodgrass 1935.

Here is a hidden treasure in the web.

Robert E. Snodgrass was an American entomologist who published extensively on arthropod anatomy and evolution during the first half of the twentieth century. He was as knowledgeable about arthropod morphology as he was a superb artist– you can see some of his illustrations decorating the banner of this blog. His name is synonymous with insect morphology: his 1935 textbook on the subject (reedited by Cornell University Press in 1993) is still the main reference for any modern course in entomology.

Snodgrass was a lecturer in the University of Maryland for most of his academic life. In 1960, two years before his death, he gave a series of three lectures that were recorded in audio tape. Fortunately for us Jeffrey W. Shultz, professor of entomology at Maryland, has digitized and made these lectures available through a nicely designed page called The Snodgrass Tapes.

Adding to the audio files, Shultz provides well annotated transcripts and, even more impressively, has taken the time to got through Snodgrass’ extensive body of anatomical illustrations to incorporate those suitable for each passage. You have the option of following the lectures in your web-browser with sound, text and illustrations, download the transcripts as pdf files, or just the audio as mp3 files and put them into your iPod¹.

The audio itself is a real treat. Adding sweet to the lectures is the constant sound of chalk against the blackboard as Snodgrass masterly drew his illustrations for the audience. But these are not dry lectures. As he deals with the particularities of arthropod anatomy he constantly pauses to introduce the listener to general terms and concepts of evolutionary theory, all done with parsimonious grace and elegance. For example, when laying out the difference between the often confused pair of terms rudiment and vestige (the former referring to ontogeny while the later to phylogeny), he states:

[...]the rudiment is something that has a future, and a vestige is something that has a past.

The page also provides links to pdf versions of Snodgrass biography and list of publications compiled and published by Ernestine B. Thurman in 1959.

Note

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

Now Gregory M. Erickson and co-workers published a paper in which they did just that to a specimen of one of the most famous fossil forms around: Archaeopterix. Watch Mark Norell, paleontologist from the American Museum of Natural History and co-author of the paper, explain the results:

George Campbell Eickwort (1949–1994)

The Department of Entomology at Cornell University saw a time of great research and teaching in insect morphology at the end of the Twentieth Century, most of which came from the efforts by two extraordinary systematists: William L. Brown Jr. and George Campbell Eickwort.

Brown was the premier ant systematist of his time. His publications on ant taxonomy exude his masterly grasp on morphology, and he supervised a multitude of students doing dissertations on basic comparative anatomy for the group. Two excellent examples are Thomas Eisner’s 1957 work on the proventriculus¹ and Gotwald’s 1967 detailed work on mouthparts². Eickwort main research focused on sweat bees, but as a teacher he was responsible for the course on insect morphology that covered all insects groups plus relevant outgroups. Sadly, by the end of the 1990′s both men had died.

Eickwort course was legendary. I know of students pursuing PhDs on other prominent universities, like Harvard, that spend one semester at Cornell just to take this course. The main part of it consisted on laboratory practices that gave students direct experience with morphology while at the same time it introduced basic techniques on dissection, microscopy and drawing. The last of these is essential for understanding morphology: drawing forces you to truly look at the details of the structure under analysis.

Eickwort’s laboratory manual was compiled and it is available on the web as a series on pdf’s. This is the version of the course I took during my graduate student years at Cornell. It is a great teaching resource. Oh, and the drawing in the cover is by yours truly.

Notes

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

Grant proposals have been dealt with (more or less), and next week I will be in Turin, Italy, for the congress of the European Society for Evolutionary Biology. I just don’t want to won’t have time to blog during the congress, unfortunately.

But do not fear, for I leave you with a very tough quiz. Let see if someone knows what’s depicted below. A couple of tips:

- It is one of the few sclerites (skeletal pieces) in adult workers that is completely internal.

- It comes in pairs (left one pictured).

The answer will be revealed upon my return.

The mysterious sclerite X (Scanning Electron Micrograph, Roberto Keller/AMNH)

I can only access the abstract of the original publication unfortunately, but it does seems to be a well done and thorough study. The problem is the way the report gets increasingly hyped by the news media. I first got this: Evolution of the appendix: A biological ‘remnant’ no more. OK, that’s not bad. I then got this: Appendix redux. Yeah, sure, succinct and clever. But today I got this: Darwin wrongly called the appendix a biological ‘remnant’, say researchers:

Charles Darwin was wrong when he theorized that the appendix in humans and other primates was the evolutionary remains of a larger structure, called a cecum, which was used by now-extinct ancestors for digesting food, according to research collaborators from three U.S. institutions.

Here we go again. There is nothing better to sell a story than to bash a long dead historical figure in the very year devoted to celebrate his legacy.

Some precious quotes:

“Darwin simply didn’t have access to the information we have. If Darwin had been aware of the species that have an appendix attached to a large cecum, and if he had known about the widespread nature of the appendix, he probably would not have thought of the appendix as a vestige of evolution,” said Parker.

and

The study report further states that Darwin was not aware of the fact that appendicitis [...] is not due to a faulty appendix, but rather due to cultural changes associated with industrialized society and improved sanitation. [...] The researcher added that that notion wasn’t proposed until the early 1900’s, and “we didn’t really have a good understanding of that principle until the mid 1980’s.”

This last quote completely destroys my admiration for Darwin. I mean, was it all that difficult for him to anticipate scientific findings 100 years into the future? And, why didn’t he embark into time travel instead of wasting his time traveling to the Galapagos islands?

Darwin on rudiments

In the Origin of Species¹. Darwin devotes an entire section in Chapter XIII (the best chapter mind you) entitled Rudimentary, atrophied, or aborted organs in which he discusses how an evolutionary perspective provides the best explanation for the common occurrence of organs that seem not have any apparent function, organs that shouldn’t be there if organisms were independently designed for a specific purpose. They are simply anatomical leftovers from a more glorious past. Darwin even draws an analogy with spelling and pronunciation in comparative linguistics: words may retain letters that are no longer useful in pronunciation. For example, the word for ant in Latin is formica, from which we got formiga in Portuguese and hormiga in Spanish. The latter retained a vestigial h even thought it is mute, and so it has no function in pronunciation.

Now, Darwin does discuss that rudimentary does not necessary means functionless:

An organ serving for two purposes, may become rudimentary or utterly aborted for one, even the more important purpose; and remain perfectly efficient for the other. [pag. 451]

and,

[A]n organ may become rudimentary for its proper purpose, and be used for a distinct object. [pag. 452]

Some of Darwin’s examples for particular evolutionary processes will surely turn out to mistakes, but his clear insight into how evolutionary theory explains the facts of comparative anatomy will always be impeccable. By the way, the new study on the appendix shows that once morphology is done properly, everything falls neatly into place.

Oh, and while we are at historical figure bashing, let me point out that Aristotle did not know that that DNA is the main hereditary material of living systems. What an idiot.

References