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Logo of nihpaAbout Author manuscriptsSubmit a manuscriptNIH Public Access; Author Manuscript; Accepted for publication in peer reviewed journal;
Ann N Y Acad Sci. Author manuscript; available in PMC Jul 1, 2010.
Published in final edited form as:
PMCID: PMC2801554
NIHMSID: NIHMS160080

Dimorphic Olfactory Lobes in the Arthropoda

Abstract

Specialized olfactory lobe glomeruli relating to sexual or caste differences have been observed in at least five orders of insects, suggesting an early appearance of this trait in insect evolution. Dimorphism is not limited to nocturnal species, but occurs even in insects that are known to use vision for courtship. Other than a single description there is no evidence for similar structures occuring in the Crustacea, suggesting that the evolution of dimorphic olfactory systems may typify terrestrial arthropods.

Although sex specific behaviors may be ubiquitous across phyla, obvious neural correlates are not easily recognized. Exceptions are centers that support sex-specific acoustic perception and song-released behaviors in birds1,2 and quite different but no less remarkable sensory dimorphism in orthopteran and dipterous insects3,4; male-specific visual neuropils in flies that mediate target pursuit5-7; and, in insects, sex-specific olfactory organs and the neuropils that they serve8-12. It is, however, insects, particularly those lepidopterans that we know as “moths”, that have provided such a wealth of experimental data demonstrating how complex blends that make up species-specific pheromones are processed by uniquely identifiable neurons and how these provide early information for odortactic flight13-16. Yet, while almost every moth investigated has been shown to possess sexually dimorphic antennae and sexually dimorphic olfactory lobes what is less secure is whether few or many other insect species, or even other land arthropods, are similarly endowed.

The olfactory (aka “antennal”) lobes of insects comprise discrete islets of neuropil, called glomeruli. In the moth Manduca sexta, which is often taken as a representative nocturnal lepidopteran, males and females possess in common a characteristic complement of glomeruli that have comparable topographic relationships with each other17. Indeed, it is typical for all insects examined that for any species there is a fixed number of antennal lobe glomeruli common to both sexes18-20. These “ordinary glomeruli” serve specific populations of odorant receptors on the antennae that are selectively tuned to a range of odors that attract or repel both males and females of the species15. In males, however, a system of sex-specific glomeruli make up what has been termed the macroglomerular complex. Each male-specific glomerulus receives the terminals of a set of odorant receptor neurons specifically tuned to one of the components of the pheromone blend emitted by the female11,21. Counterparts of these male-specific glomeruli also exist in females. They are much smaller, but are tuned to odors that are particularly relevant to female behavior8,22.

Antennal lobe dimorphism, in which males have large and distinct glomeruli (Fig. 1), is not simply restricted to males versus females. Studies of social hymenopterans, for example honey bees, have shown that the antennal lobes of workers have a different number of glomeruli compared to those of drones23. Likewise, there is evidence that in some species of ants the numbers of glomeruli vary according to caste24-26. Even from these few examples the observer is persuaded that within a species, in which there are clear sex- or task related differences of odorant-induced behaviors, there will likely be differences in the number and organization of glomeruli. Two other examples come to mind. Male and female Anopheles gambiae mosquitoes have quite different food preferences and have sexually dimorphic antennae and glomeruli27. These are not specializations of males to detect females. Rather, the male olfactory system detects floral odors so that the male can obtain nectar and hence the energy to acoustically locate and fly to females; the female olfactory system is tuned to human odors enabling her to obtain proteins for her eggs. In general, olfactory behaviors that are specific to each sex are driven by molecular features of odorants that are detected by specifically tuned odorant receptor cells on the antennae, the axons of which target specific glomeruli in the male and different but no less specific glomeruli in the female8. Another example comes from the Mutillidae. These are parasitic wasps, the females of which once fertilized loose their wings and spend weeks or even months searching out the burrows of solitary bees. The larvae of the bees, when large enough for the purpose (and, presumably smelling just right), receive a mutilid egg. Both male and female mutilids possess enormous antennal lobes, which like those of most other hymenopterans consist of scores of small ball-like glomeruli. However, the antennal lobe of a mutilid male looks quite different from that of the female: while males do not possess a small group of male-specific glomeruli as do moths, the two sexes have substantially different numbers of glomeruli arranged in sex-specific constellations28.

Figure 1
Laser-scanning confocal microscopic images of output neurons in the antennal lobe of male M. sexta with arborizations confined to one of the male-specific glomerulus (leftmost neuron) and a sexually isomorphic glomerulus (rightmost).

How general are sex-specific olfactory systems across the Insecta? Unfortunately, too few comparative studies have been done to answer this with anything approaching precision. Nevertheless, some assumptions can be made. One is that because sex-specific glomeruli occur in basal as well as crown groups, it is likely that a sex-specific organization of the antennal lobe may have evolved early in the evolution of the Insecta and may be a synapomorphy of at least the Neoptera. Thus far, sexually dimorphic antennal lobes have been documented in the Dictyoptera, Lepidoptera, Hymenoptera, Coleoptera, and Diptera. Nocturnal Lepidoptera, such as sphingid, heliothine, and noctuid moths are renown for their sexually dimorphic antennae and antennal lobes17,20,29-30. However, even diurnal species, such as the humming bird hawk moth Macroglossum stellatarum and the burnet moth Zygaena filipendulae possess antennal lobes that in males are equipped with three to five male-specific glomeruli (Fig. 2). Interestingly, unlike their nocturnal cousins, the antennae of these species show no obvious sexual dimorphism so one must assume that sensilla on the male antennae housing receptors tuned to components of the female pheromone are discrete, appearing little different from sensilla decorating the females' antennae.

Figure 2
Macroglomerular complexes (boxed) of two diurnal Lepidoptera, the sphingid moth Macroglossum stellatarum (A, C) and the six-spot burnet moth Zygaena filipendulae stephensi (B, D). Ordinary glomeruli are indicated at one glomerulus (OG).

It is sometimes suggested that sex pheromones confer a particular advantage for species that are nocturnal; or species that are sympatric yet are required to mate with the genetically appropriate partner; or species that need to attract conspecifics over long distances. Particularly beneath or within the canopy, acoustic communication or communication by odor are more effective over distance than visual communication. So it comes as something of a surprise that brightly colored diurnal moths equipped with color and form perception are also equipped with sexually dimorphic antennal lobes.

More surprising is that butterflies also have dimorphic antennal lobes, males being equipped with prominent male-specific glomeruli located at the same position in the lobes as those found in moths. So much, then, for the idea that visual sexual signals are most effective in daylight and odor-mediated ones are most effective at night. And, in this context, it is worth noting that studies on nocturnal Hymenoptera demonstrate that insects probably possess the most acute nocturnal vision of any group of animal31.

If antennal lobes are sexually dimorphic, then what about higher brain centers of the protocerebrum to which they send relay neurons? Insects can be categorized into three somewhat artificial groups: those that are equipped with antennal lobes and mushroom bodies, those that lack antennal lobes, and those that lack mushroom bodies. Absence of antennal lobes, as occurs in many aquatic genera, does not preclude a lack of mushroom bodies. Indeed, as far as is known all dicondylic insects have them32. However, those that do have antennal lobes supply two protocerebral areas: the mushroom body calyces and a volume of the rostrolateral protocerebrum called the lateral horn33,34. In coleopterans, the males of which are equipped with at least two macroglomeruli (Fig. 3), the antennal lobes supply just one ascending pathways that extends to the lateral horn. En route, its projection neuron axons provide a massive collateral input to the mushroom body calyces. This, then, represents the simplest relationship between first order olfactory neuropil of the deutocerebrum (the second brain segment) and areas of the protocerebrum (the first brain segment). In contrast, the antennal lobes of flies provide at least five ascending pathways, although some comprise only a few axons35. In honey bees there are also five such pathways and in both genera a subset of antennal lobe projection neurons in one of the ascending tracts supplies first the lateral horn and then sends prolongations into the calyx whereas another ascending tract first supplies collaterals to the calyces before terminating in the lateral horn36. Studies on Drosophila melanogaster have shown that the calyx is parsed into three discrete zones, each of which is supplied by projection neurons arising from one of three characteristic ensembles of antennal lobe glomeruli. Similarly, the lateral horn neuropil is parsed into three discrete layer-like domains, each domain also representing one of the same three ensembles of glomeruli35. A comparable representation has been described for ants and honey bees. Specific ensembles of antennal lobe glomeruli are differently represented in concentric domains of the lip region of the calyces36-37.

Figure 3
Macroglomeruli in the antennal lobe of the social beetle Odontotaenius disjunctus (inset to Panel B). Most of the antennal lobe consists of isomorphic ordinary glomeruli (OG) that are similar in appearance (Panel A). However, dorsally in the female antennal ...

If subsets of ordinary glomeruli are represented as discrete domains centrally then it should also be expected that projection neurons from sex-specific glomeruli would be differently represented in the calyces and lateral horn. This is confirmed from observations of dye-filled projection neurons from both types of glomeruli in Manduca sexta: there are two different terminal morphologies in the calyces and, in males, macroglomerular projection neurons terminate in a region situated directly beneath the lateral horn neuropils receiving terminals from ordinary glomeruli34. The same type of spatial segregation has also been shown for the cockroach Periplaneta americana: male projection neurons end in a zone of the protocerebrum that is inferior to the lateral horn, which receives the layered terminals of projections neurons from ordinary glomeruli (Fig. 4). In Drosophila melanogaster projection neurons with arborizations in a uniquely identifiable glomerulus that in both sexes detects male pheromone terminate in different sex-specific domains in the lateral protocerebrum38. While there as yet is too little data to generalize this sex-specific arrangement across taxa, the segregation documented for the four species above at least serves as a search image for further studies.

Figure 4
Sex-specific termination areas of antennal lobe projection neurons, exemplified here by Periplaneta americana. Male-specific neurons from the macroglomerulus (MG) ascend in front of the mushroom body's medial lobe (M) to beneath the calyces (ca) where ...

What about the third category of insects: those lacking mushroom bodies? These are the Machilidae, which comprise four families of monocondylic flightless insects, commonly known as bristletails, that were probably amongst the first hexapods to colonize land in the mid-Devonian39. The brains of machilids are equipped with glomerular antennal lobes. Although it is not yet known if these are sexually dimorphic, these shrimp-like insects typically live as groups and are often found nestling together under moss or in rock crevices. They have splendidly long antennae and, like all insects, male machilids are required to locate females. The presence of sex-specific glomeruli in these primitive insects would be an interesting finding because machilid antennal lobes provide projection neurons to a substantial and clearly partitioned volume of the lateral protocerebrum. Indeed, this part of the brain is comparatively much larger than the lateral horn of a fruitfly or cockroach. As machilids lack mushroom bodies but have large target neuropils for their projection neurons, in this aspect their brains are more similar to those of malacostracan crustaceans than they are to the Dicondylia. In the Malacostraca, projection neurons from the antennular lobe send bilateral axons to two or three (depending on the species) discrete neuropils in the lateral protocerebrum. These are called the terminal medulla and the hemiellipsoid bodies40. None of them are comparable to mushroom bodies but they are comparable to the lateral protocerebrum of machilids and the highly attenuated homologue in dicondylic insects, the lateral horn.

This brings us to the next question. If the malacostracan lateral protocerebrum is homologous to an equivalent region in insects, is there evidence for sexual dimorphism of the malacostracan antennular lobes? Thus far, there has been only one report of a putative sexual dimorphism in a mysid shrimp41. Although in many malacostracans the antennular lobes appear to be subdivided into two or more bulging ensembles of glomeruli, these have never been ascribed to sexual differences. However, with one glaring exception, these glomeruli are very different from those of the Insecta, a feature that alone suggests caution before claiming that crustacean antennular lobes are homologous to the olfactory lobes of insects42. And here it should be noted that we have avoided the term “antennal lobes” because even though insects only have one pair of cerebral appendages to the crustaceans' two, the single pair are the first antennae. This means that they are antennules, sensu stricto, and should be not confused with what crustacean biologists term “the antennae”43. The latter comprise the second antenna pair, which does not exist in hexapods.

Antennular lobes are usually subdivided into column or wedge-shaped subunits that hare termed glomeruli, though is somewhat misleading. Each subunit is clearly stratified, and in one representative taxon, the spiny lobster Panulirus argus, axons of olfactory receptor neurons can supply more than one subunit, something not observed in an insect olfactory lobe44. Moreover, whereas insects have mainly uniglomerular projections neurons - that is, relay neurons whose dendrites are constrained to a single glomerulus (Fig. 1) - the malacostracan antennular lobe is populated by wide-field multiglomerular projection neurons45. Thus far, no uniglomerular projection neuron has been described in a crustacean. If in some malacostracans it turns out that there is indeed sexual dimorphism of the olfactory system then it is likely that sex-specific morphologies would relate not to a few large glomeruli but to ensembles of many glomeruli that share the dendrites of a set of wide filed projection neurons. Possible exceptions may be the Stomatopoda, commonly known as mantis shrimps. These have antennular lobes that are remarkably insect-like in that they are partitioned into discrete islet-like units (Fig. 5).

Figure 5
Comparisons of crustacean and insect olfactory lobe glomeruli. A. Islet-like glomeruli of the stomatopod Pseudosquilla ciliata. B. Wedge-shaped “glomeruli” of the ghost shrimp Callianassa californiensis. C. An “antennal” ...

In summary, apart from the single description of a putative sex-specific glomerulus in a mysid shrimp, the occurrence of sex-specific glomeruli within the Tetraconata (Insecta+Crustacea) may be constrained to insects with terrestrial imagines. Within the Insecta, it is likely that sexual dimorphism of the antennal lobes occurs in many genera and even where obvious glomerular dimorphism is absent sex-specific differences can still be manifested by sex-specific projections into the protocerebrum, as described from Drosophila melanogaster38. In insects where there are neither sex-specific glomeruli nor sex-specific projection neurons, this absence may indicate secondary loss or may suggest multiple evolution of sex-specific glomeruli in distantly related taxa. One key to our understanding of the evolution of sex-specific glomeruli will come from further studies on the primitive machilids. However, even if dimorphism is found in this group, it cannot resolve the question as to whether or not the trait has evolved independently in different insect lineages (Fig. 6).

Figure 6
Occurrence of glomeruli and sexual/caste dimorphism. Within the Eucrustacea, only malacostracan taxa are reported to be equipped with antennular lobes (character 1). These appear to comprise isomorphic subunits (see Fig. 4A, B). Uniquely identifiable ...

The possibility that sexual dimorphic olfactory systems are typical of terrestrial arthropods needs still to be resolved. Studies on the Chelicerata have identified pheromones from three groups: the Acari (ticks), Araneae (spiders), and Scorpionida46-48. Preliminary studies on amblypygids (whip spiders) and solfugids (sun spiders), which are arid land chelicerates that have antenna-like appendages (the first leg pair and pedipalps, respectively), suggest that in these taxa their primary olfactory centers comprise two kinds of glomerular arrangements: small densely packed glomeruli reminiscent of those of Hymenoptera accompanying a very few large glomeruli, reminiscent of lepidopteran or dictyopteran macroglomeruli, or many small glomeruli alone. Such differences between individuals of the same species suggests that there is indeed dimorphism in these chelicerate olfactory systems (Fig. 7). If confirmed, this would be an intriguing example of parallel evolution of macroglomerular complexes in two groups of arthropods, insects and chelicerates, whose last common ancestor probably existed about 540 million years ago.

Figure 7
Primary olfactory neuropils of chelicerates show dimorphism. A. Solfugids are equipped with olfactory receptors on their pedipalps (black), which provide several dozen glomeruli in the brain that have connections to the paired mushroom bodies (B: central ...

Acknowledgments

Research for this article derives from support from the National Institutes of Health Grant R01-DC-02751 and from the John D. and Catharine T. MacArthur Foundation (NJS).

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