Arthropod head problem
The arthropod head problem is a long-standing zoological dispute concerning the segmental composition of the heads of the various arthropod groups, and how they are evolutionarily related to each other. While the dispute has historically centered on the exact make-up of the insect head, it has been widened to include other living arthropods, such as chelicerates, myriapods, and crustaceans, as well as fossil forms, such as the many arthropods known from exceptionally preserved Cambrian faunas. While the topic has classically been based on insect embryology, in recent years a great deal of developmental molecular data has become available. Dozens of more or less distinct solutions to the problem, dating back to at least 1897, have been published, including several in the 2000s.
The arthropod head problem is popularly known as the endless dispute, the title of a famous paper on the subject by Jacob G. Rempel in 1975, referring to its seemingly intractable nature. Although some progress has been made since that time, the precise nature of especially the labrum and the pre-oral region of arthropods remain highly controversial.
Background
Some key events in the evolution of the arthropod body resulted from changes in certain Hox genes' DNA sequences. The trunks of arthropods comprise repeated segments, which are typically associated with various structures such as a pair of appendages, apodemes for muscle attachment, ganglia and coelomic cavities. While many arthropod segments are modified to a greater or lesser extent, arthropodists widely assume that all of the segments were nearly identical in the ancestral state. However, while one can usually readily see the segmental organisation of the trunks of adult arthropods, that of the head is much less obvious. Arthropod heads are typically fused capsules that bear a variety of complex structures such as the eyes, antennae and mouth parts.The challenge that the arthropod head problem has to address is to what extent the various structures of the arthropod head can be resolved into a set of hypothetical ancestral segments. Given the high compaction and complexity of adult arthropod heads, much attention has been directed towards understanding the developmental processes that give rise to them, in the hope that they will reveal their segmental organisation more clearly.
Head components
A typical insect head possesses a pair of antennae; eyes; mandibles, labrum, maxillae and labium. Lying above the oesophagus is the brain or supraesophageal ganglion, divided into three pairs of ganglia: the protocerebrum, deutocerebrum and tritocerebrum from front to back. Nerves from the protocerebrum lead to the large compound eyes; from the deutocerebrum to the antennae; and from the tritocerebrum to the labrum and stomatogastric nervous system. Circum-oesophageal connectives lead from the tritocerebrum around the gut to connect the brain to the ventral ganglionated nerve cord: nerves from the first three pairs of ganglia lead to the mandibles, maxillae and labium, respectively. The position of the mouth and the circum-oesophageal connectives allows a distinction to be made between pre- and post-oral structures; although it should be borne in mind that because structures can move around during development, a pre-oral position of a structure in the adult does not necessarily prove that its developmental origin is from there. The myriapod head is very similar to that of the insects.The crustacean head is broadly similar to that of the insects, but possesses, in addition, a second pair of antennae that are innervated from the tritocerebrum. In place of the labium, crustaceans possess a second pair of maxillae.
Chelicerate head structures differ considerably from those of mandibulates ; they possess eyes and a single pair of grasping appendages innervated from the brain, plus a labrum-like structure. Behind the mouth lies another pair of mouthparts, the pedipalps, and behind them lie the series of walking limbs. In chelicerates, the leg-bearing segments are fused with the anterior segments to form a prosoma, so that in living arthropods a distinct head only exists in mandibulates.
The acron concept
The arthropod head problem has until recently been predicated on the Articulata theory, i.e. that the arthropods and annelids are close relatives. Although arthropods are essentially direct developers that do not possess a trochophore-like larva, the annelids do. During annelid metamorphosis, segments are added close to the posterior of the body, behind the mouth; whereas the brain is derived from the episphere or region in front of the mouth. Recognition of this led to the concept of a primary, non-segmental component of the body in annelids known as the acron being developed, from which the brain is ultimately derived. Because the arthropod and annelid heads, in the light of the Articulata theory, were assumed to be structurally homologous in some way, the arthropod head was also often considered to incorporate a non-segmental acronal component. Taking the homology between annelid and arthropod heads at face value, Swedish workers such as Hanström and Holmgren assumed that a large part of the arthropod head must correspond to the acron, a view followed later by several prominent American insect workers such as Butt and Snodgrass. They proposed that all pre-oral structures in insects were non-segmental, although such a view is at odds with the preoral position of apparently bona fide appendages such as the antennae. A less extreme set of theories propose that only the protocerebrum and associated structures should be considered to be acronal.The view that the arthropod head must contain an acronal remnant has been shaken by the relatively recent revision of protostome phylogeny, which has dismantled the Articulata and placed the arthropods together with a group of unsegmented worms often referred to as the Cycloneuralia within Ecdysozoa. All members of Ecdysozoa are direct developers without a trochophore, and the cycloneuralians have terminal mouths. As a result, the idea of the arthropods having inherited a preoral acron from their ancestors seems less likely.
Molecular development and the arthropod head problem
The study of how developmental genes are expressed during embryogenesis has become an important new tool in the last twenty years for understanding the structure and evolution of morphology. The arthropod head problem has been tackled in three main ways in this regard, first by using genetic segmental markers to probe the obscure region in front of the mouth, especially in insects; second by looking at Hox gene expression patterns to detect patterns of homology among different arthropods; and third, by studying gene expression in particular features to determine its appendiculate or other status. Because all arthropods have the same complement of nine Hox loci, the morphological diversification observed is caused by heterochrony, meaning that the genes are expressed at different times.Areas of agreement
It is widely agreed that the insect, myriapod and crustacean heads are very similar. The apparent lack of a second antenna in insects and myriapods is explained by the idea that this appendage has been lost, leaving an appendage-less segment known as the intercalary segment. Modern phylogenies do not in general support an insect-myriapod relationship, suggesting that the second antenna has been lost independently in each group, perhaps as a result of a convergent adaptation to life on land. Furthermore, there is general agreement that the mandibles, first maxillae and labium/second maxillae each represent a post-oral segment; and that the first antenna represents a preoral segment.Areas of disagreement
Areas of disagreement can be grouped into three categories: the nature of the pre-antennal region in mandibulates; the nature of the labrum; and the relationship between the chelicerate and mandibulate anterior segments.Nature of the preoral region
The degree to which the area in front of the mouth is segmented remains one of the major controversies in the arthropod head problem. As already mentioned, earlier workers often considered the entire pre-oral region to be "acronal" and thus nonsegmental. Modern workers universally accept that at least the deuterocerebrum is segmental. However, the nature of the region in front of this is much less certain. Some molecular development studies have given limited support to the idea of an "ocular" segment corresponding to the protocerebrum; but these data are not unequivocal. The idea of the protocerebrum actually comprising two components has also received support from both molecular and embryological data.On this view, the protocerebrum comprises a typical 'segment', the prosocerebrum, marked by the expression of engrailed at its caudal margin and a pair of appendages, and a pre-segmental region, the archicerebrum, which bore a pair of appendages that are not serial homologues of the trunk appendages; these are represented by the onychophoran antennae and the 'great appendages' of certain stem euarthropods. The archicerebrum is in some ways equivalent to the 'acron', and may be equivalent with the annelid prototroch; it can be recognized by the expression of the genes optix and six3 during development, whereas the prosocerebrum is associated with orthodenticle and its homologs.
The labrum
The labrum is a flap-like structure that lies immediately in front of the mouth in almost all extant euarthropods, the general exception being provided by the probable chelicerate-relatives the pycnogonids. It has proved to be by far the most controversial of all arthropod head structures. It is innervated in crustaceans and insects from the tritocerebrum, i.e. the back of the brain. However, in development it often appears at the anterior of the head, and migrates backwards towards its adult position. Furthermore, it often appears as a bilobed structure, with a set of muscles, nerves and gene expression in many ways similar to that of a trunk appendage. This evidence has been used to suggest that the labrum is in fact a highly reduced appendage.Its innervation from the rear of the brain has suggested to some workers that, if an appendage, it is the appendage of the tritocerebral segment; a point disputed by others who argue that the presence of a well-developed appendage in at least crustaceans in this segment rules this out. If the labrum is an appendage then, it seems possible that its origin is indicated by its developmentally anterior position, i.e., that it is the appendage of a segment anterior to the first antenna. The most obvious choice for this is the segment whose ganglion is the protocerebrum, which in extant euarthropods bears no appendage. Strausfeld finds support for this hypothesis in the presence of a median nerve bundle connecting the labrum to the anterior of the protocerebrum, and the expression of the gene six3 in the labrum has been taken as evidence for its homology with onychophoran antennae.
If the labrum is really an anterior appendage that has migrated to the posterior, then it may be homologous to the "antennae" of onychophorans, which, as discussed below, seem to be innervated from a very anterior part of the brain, i.e. in front of the eyes. It has even been suggested that the labrum belongs to an even more obscure segment that lies in front of the ocular one. Nevertheless, many workers continue to be highly skeptical about the appendiculate nature of the labrum, preferring to see it as it appears, i.e., as an outgrowth of the body wall just in front of the mouth.
Particularly in some fossil groups, such as certain trilobites, the labrum is often covered with a sclerotised plate, the hypostome. Confusion can arise where the two structures are conflated or mistaken for one another.