T. F. Hlavac.
The Prothorax of Coleoptera: Origin, Major Features of Variation.
Psyche 79:123-149, 1972.

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PSYCHE
Vol. 79 September, I 972 No. 3
THE PROTHORAX OF COLEOPTERA:
ORIGIN, MAJOR FEATURES OF VARIATION1
BY T. F. HLAVAC~
Biological Laboratories, Harvard University, Cambridge, Massachusetts
The unique evolutionary success of the order Coleoptera is a. re- sult of great size combined with enormous biological diversity. The huge number of species (ca. 280,000) is arrayed across a broader ecological spectrum than that of any other group of terrestrial ar- thropods. Four adaptive zones have been extensively occupied: sur- face. substrate, aquatic, aerial. Higher categories of beetles are, with exceptions, very broad, overlapping adaptive radiations. This evolutionary conlplexity is associated with great structural variation and a small number of basic adaptations, particularly in the Iocomo- tory system.
Because the Coleoptera are a series of replicated experiments in ecological differentiation, the group may be used for studying a suite of problems in the evolution of adaptation. And, because beetles are such a large, diverse and ubiquitous group of insects, they should have a place as subjects for developing and refining modern syste- matic methodologies. Work at these two superficially different levels has been hindered or made unfeasible (q. v. Brundin 1972: 72) by the lack of a firm foundation of comparative morphology. "Most work on comparative structure of beetles suffers from one 'A preliminary version of this work was submitted as part of a Ph.D. thesis to the Biology Department, Harvard University. 'I thank Drs. R. A. Crowson, H. E. Evans, J. F. Lawrence, E. Mayr, and E. 0. Wilson for many useful comments on the manuscript. Work on
thoracic morphology has been supported by NSF grants GB 19922 (Reed C. Rollins, Harvard University, Principal Investigator), GB 12346 (P. J. Darlingtun, Jr., Harvard University, Principal Investigator), and GB 31173 (F. M. Carpenter, Harvard University, Principal Investigator). Manuscript received by the editor October 1,1972



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124 Psyche [September
or more of the following limitations: small and/or poorly chosen sample; superficial analysis of raw data, or none at all; impoverished treatment of adaptive phenomena. There are few even moderately comprehensive studies of structural variation; see Arnett ( 1967) for list and brief descriptions. And, many glaring problems have not been dealt with. For example, prothoracic characters have long been used in subordinal diagnoses, yet detailed comparisons of representatives of each taxon have not been made.
Since ecological differentiation and thoracic adaptation are so in- timately related, understanding the locomotory system is particularly important for the future development of beetle systematics. Due to
size and diversity of the group, work on this functional complex is neither easy nor quickly accomplished. The only feasible compromise is to select a natural subunit of this system for detailed study. The prothorax is the obvious, initial choice. Prothoracic structure and mechanics are simple as compared to those of the two pterothoracic segments where both ambulatory and flight functions are combined. Differences in size, structure and f~inc- tion in the prothorax are readily perceived and correlated with phys- ical demands of various environments. Furthermore, details of pro- thoracic mechanisms are commonly diagnostic of higher categories. The interplay between adaptive phenomena and historical clevelop- ment in the prothorax is considered below at 2 levels: origin of the coleopterous prothorax and variation within the two biologically diverse suborders.
The generalizations and evolutionary hypotheses presented here are based on dissection of over 600 selected genera, and external ex- amination of many others. Raw data, primarily drawings, group diagnoses, and discussions of variation within major taxa, will be presented elsewhere as will results of a current study of pterothoracic structure.
The walls of the rigid, cylinder-like prothorax of Coleoptera are always formed by the notum dorsally, by the sternum ventrally, and, in some forms, the pleuron forms distinct lateral walls (figs. 1-9). The trochantin, a small, sometimes movable sclerite, is attached to the sternum and pleuron and along with the latter articulates with the coxa, the basal leg segment (figs. 2, 7 Tn). The coxa also
rests on and sometimes mechanically articulates with the posterior section of the sternum - the cryptosternum (fig. 7 CrS) .



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19721 {Hlavac - Prothorax of Coleoptera 1 25 Almost without exception, the pleuron is divided into an external section and an internal, invaginated region, the endopleuron, that is concealed by the notum (figs. 2, 7, 9, PI, EndPl). The rim of the external portion may be completely folded over, broadly so anteriorly and posteriorly to form flanges, parts of paired articulation-collars and quite narrowly so ventrally forming half of membranous sternal and trochantinal attachments and part of the coxal articulation (figs. 2, 4, g ANFL, APLFL, PNFL, PPLFL, RFM, AF, VF, PF). These anterior notal, sternal, and sometimes pleural flanges pro- duce a complete articulation-collar or socket which encloses the pos- tenor aspect of the head, cervical membrane, and, if present, cervical sclerites. Likewise, the posterior notal flange, and sometimes a pleural Figs. 1-5. Prothoraces of Archostemata and Myxophaga. Figs. 1, 2. Lateral external and internal views of Priacma serrata (Ar-
chostemata, Cupedidae).
Figs. 3, 4. Same of Pryopteryx britskil (Myxophaga, Torridinicolidae). Fig. 5. Lateral view of Hydroscapha natans (Myxophaga, Hydrosca- phidae).
Margins of enclosed structures indicated by dashed lines.



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126 Psyche [September
flange as well, form an incomplete collar enclosing part of the meso- thoracic rim and some intersegmental membrane (fig. 8). The fold forming the anterior sternal flange may continue dorsally to join with a pleural or notal rim fold and then extend ventrally to form a membrane enclosing joint with the trochantin. Below the trochantin, the sternum generally bears a shelf-like, poorly pigmented, concave region, the cryptosternum, which supports and is concealed by the coxa (figs. 7, g CrS). The cryptosternum also bears a pair of invaginations or apophyses close to the posterior margin. Frequently, the sternum is evaginated medially, forming a projection which may extend between, behind, and sometimes above the coxa. Sometimes a second, smaller sternallar projection is present as well (fig. 7 Spj, SLpj). A complete posterior collar is commonly formed from union of either of these projections with notal or pleural projections (figs. 333 43,467 48,k 64).
SUBORDINAL DIFFERENCES AND THE HYPOTHETICAL STEM CONFIGURATION
There are major differences in pleural size, structure, motility and in its trochantinal attachment among the four suborders of Coleop- ten. Subordinal configurations can be diagnosed as follows. ARCHOSTEMATA. Pleuron large, rigid, forming lateral wall of segment. Trochantin motile, external. Anterior pleural flange exter- nal, small and enclosed, or absent with internal anterior fold. Ster- nal joint membranous to solidly fused (figs. I, 2, I I, 12, 14). MYXOPHAGA. Pleuron variable in size (figs. 3-5), rigid, fused to trochantin. Anterior pleural flange external or enclosed (figs. 3-5). Sternal joint membranous.
ADEPHAGA.
Pleuron, a prominent part of body wall, rigid. Tro- chantin, small, motile, enclosed along with coxal articular region by pleural and sternal cowlings. Anterior pleural flange absent, ante- rior fold internalized by union of noltal (and sternal flanges (figs. 8, 9. I 3, 61-65). Sternal joint fused.
POLYPHAGA. Pleuron greatly reduced in size and fused to tro- chantin; this highly variable compound structure may be motile and contribute to coxal movement, and may be completely enclosed. No- tun1 and sternum attached anterior to pleuron to form body wall. Anterior pleural fold and zone of fusion between pleuron and tro- chantin present in a few primitive groups. Sternal joint membranous to solidly fused (figs. 6, 7, I 5-1 7, 23-55).



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19721 ~Hlavac - Pro thorax of Coleoptera 127 In addition, rim-fold joints between body wall sclerites and mov- ing parts are very widely distributed within the Coleoptera. Prothoracic configurations of extant forms can be derived from a single hypothetical stem form diagnosed as follows. HYPOTHETICAL STEM CONFIGURATION: Pleuron large, rigid, forming distinct part of body wall, with broad anterior and posterior flanges; attached by rim-fold joints to notum and sternum. Endo- pleuron present. Trochantin external, motile. A complete anterior collar and partial posterior collar enclose most of the intersegmental Figs. 6-9. Prothoraces of Polyphaga and Adephaga. Figs. 6, 7. Lateral external and internal views of Omalium marginaturn (Polyphaga, Staphylinidae). [See text and captions of Figs. 25-55 for ex- planation of Fig, 6A, B].
Figs. 8, 9. Same of Amphiwa insolens (Adephaga, Amphizoidae).



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19721 li/avac - Prothorax of Coleoptera 129 membrane. Peri-coxal .and trochantinal membrance enclosed by cowl- ings on pleuron, sternum and trochantin (fig. 24). Evidence for the primitiveness of individual characters is obtained from both extant and fossil forms.
The tripartite body wall and anterior collar is a major feature of the archtypical coleopterous prothorax. This arrangement is geo- metrically the simplest way of producing a sclerotized cylinder bear- ing paired sockets, i.e., through anterior development and folding of dorsal, lateral and ventral elements without shift in relative position. Pleural size and structure of three suborders (Archostemata, Ade- phaga, Myxophaga) is similar to that of the stem configuration but differ from it in having a reduced or internalized anterior flange. A relatively small, external, anterior pleural flange is present only in some extant members of the Archostemata and Myxophaga. In other members of both groups, the flange is even further reduced and enclosed by overlap of notal and sternal elements (figs. 1-5, I I, 12). In one group of Archostemata (Cupdidae, Ommadinae) and in all Adephaga, the anterior flange is absent, and a small anterior pleural fold is internalized, frequently by membranous connection of a lobe- like expansion of the sternal flange with the notal flange (figs. 8, 9, 13, 14). In some Adephaga and Myxophaga notal and sternal flange rims may overlap but are not connected
(figs. 3, 8). The Myxo-
phaga and Adephaga then overlap the Archostemata at opposite ends, of this morphocline.
In many Mesozoic Coleoptera of dubious subordinal position, the notum and sternum are widely separated by the pleuron (e.g., Pono- marenko 1969; figs. 74, 102). No internal evidence is available. However, since the posterior rim of the head is clearly enclosed by Figs. 10-19. Morphology of anterior section of the pleuron and surround- in,g structures ; sclerites slightly disarticulated. Figs. 10-15. Internal views.
Fig. 10. Hypothetical stem configuration. Fig. 10A. Section through pleuro- sternal joint.
Fig. 11.
Priacma serrata (Archostemata, Cupedidae, Cupedinae) , Fig. 12. Cupes concolor (Cupedidae, Cupedinae) . Fig. 13.
Amphisou insolens (Adephaga, Amphizoidae) . Fig. 14. Tetraphalerus wagneri (Cupedidae, Ommadinae). Fig. 15. Generalized Polyphagon.
Figs. 16-18.
External views of Polyphaga.
Fig. 16. Peltastica turberculata (Derodontidae) . Fig. 17. Sarabandus robustus (Helodidae) . Fig. 18. Megarthrus robustus (Staphylinidae). Fig. 19. External view of Pr'iucma; sections included above, heavily stippled.




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1 30 Psyche [September
the prothorax in these forms, it is reasonable to infer the existence of a tripartite anterior collar. In other fossil beetles, the notum and sternum extend in front of the ~leuron. This could represent either a stage of anterior ~leural reduction as in figs, 3, 4, 12, or a distinct noto-sternal joint. The evidence is ambiguous. Based on the geometry of major sclerites, and structural variation in extant and fossil forms, a three element body wall and anterior collar is taken to be primitive for Coleoptera. The distribution of extant forms evolved though variable, possibly, parallel reduction of the anterior flange.
A separate, motile trochantin occurs in the Archostemata, Ade- phaga and in other holometabolous orders. The trochantin and pleu- ron are fused in the Myxophaga and Polyphaga. A separate tro- chantin is doubtless a primitive trait in Coleoptera. The almost universal presence of membrane enclosing rim-fold joints between major sclerites, and moving parts within both extant and fossil forms is evidence for the primitiveness of these articula- tions within the Coleoptera. A rigid rim-fold joint is produced by medially bending the edges of two sclerites to form a pair of flat- tened, normally horizontal articulation surfaces which may bear tongue-groove devices (fig. IoA). Attachment membrane extends between the margins of the two sclerites and is enclosed. In all ex- tant forms, the body wall elements are connected with mebranous rim-fold joints (frequently in primitive members of higher taxa) or are solidly fused together, sometimes with a distinct internal carina and often without the slightest vestige of a suture (figs. 9, 59, 50). Rigid rim-fold joints seem to be universally present in fossil Coleop- tera, as well.
Except in extreme surface grade polyphagans, membrane around the coxa and trochantin is enclosed by loose rim-fold joints or both structures may be entirely enclosed by cowlings, see below. There is no obvious membranous band between moving parts in the fossil Coleoptera depicted by Ponomarenko ( 1969). It is assumed, then, that rigid and loose rim-fold joints are primitive characters in the Coleoptera.
Except for the Polyphaga, Recent suborders and early fossil Cole- optera are similar to the stem configuration in basic organization. The major differences between the Adephaga, Archostemata, and Myxophaga are either simple modifications of structural details (re- duction of anterior pleural flange, trochantinal fusion) or adaptations for improving structural integrity (enclosure of coxal articular re- gion and trochantin in the Adephaga). The grea,t differences between



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19721 Hlovac - Prothorax of Coleoptera I3 1 Polyphaga and other Coleoptera are integral parts of a unique pleuro- coxal mechanism.
In all Polyphaga, the trochantin and pleuron are fused together; in a few members of apparently primitive groups (Staphylinoidea, Eucinetoidea) the structure of a distinct internal zone of fusion be- tween the two sclerites indicates union of a pair of rim folds (figs. 7, 24). This compound structure is frequently movable and can contribute to coxal rotation and/or flexation. Since the pleuron is a moving part, it can not contribute to the rigidity of the segmental wall, and is greatly reduced in length and width. In most cases, pleural height is so reduced that the coxal apex is concealed by the notal rim-fold. A rigid segment is obtained by anterior attachment of notum and sternum. Evidence that this specialized mechanism has evolved from a configuration with a tripartite body wall is found in what are probably vestiges of the anterior pleural fold between the notum and sternum in members of these presumed primitive groups of Polyphaga (Eucinetoidea, Staphylinoidea, Derodontidae) (figs. 16-18). The major muscle powering pleural motility in the Poly- plhaga is also found in other suborders, but its function, in these groups, given rigid external pleural walls, is problematical (figs. 2, g MI^) . The Polyphaga can therefore be derived from the hypo- thetical configuration through modification of the pleuro-coxal mech- anism resulting in the acquisition of pleural motility. It is generally concluded that the Holometabola is a strictly mono- phyletic taxon, but see Matsuda ( 1970: 215). The Coleoptera and the other major orders are believed to have evolved from a general- ized stock of lower Holometabola, closest to Neuroptera and Mecop- tera (Crowson 1956: I, 1960: 111).
There are enormous differences in prothoracic structure between the Coleoptera and other Holometabola; and there is only moderate variation within the Lower Holometabola. Based on study of mem- bers of all major groups, it is possible to diagnose a presumed prim- itive configuration as follows:
GENERALIZED HOLOMETABOLUS PROTHORAX: Noto-pleural joint, loose, membranous. Dorsal prtion of pleuron enclosed by notum but the pleural rim only narrowly folded over; there is no deep, hori- zontal, endopleural imagination as in Coleoptera. The pleuron does bear a vetrical invagination, or apophysis, which divides it into an episternum, anteriorly and an epimeron, posteriorly. Pleural apophy- sis fused internally to sternal apophysis. Trochantin motile, closely



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132 Psyche [September
attached to pleuron and as heavily sclerotized as the other structures. Sternum joined only internally to pleuron, does not extend in front of the coxa. Anterior and posterior collars absent, coxal a.rticulation external so that considerable cervical, intersegmental, and pericoxal membrane is exposed (fig. 23).
This configuration is most similar to the extant Australian genus Ithone (Neuroptera) (fig. 20) but with a large, articulatory tro- chantin, as in the Trichoptera (fig. 22). Reducing the trochantin while maintaining associated musculature may be a modification for increasing the angle of coxal flexation. Division of the pleuron into Figs. 20-22. Prothoracic structure of the Lower Holometabola. Fig. 20. External lateral view of Ithone sp. (Neuroptera). Fig. 21. Internal lateral view of Panorpa virginica (Mecoptera). Fig. 22. External lateral view of coxal articulation of Ptilostomis ocel- lifera (Trichoptera) .




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19721
'Hiavac - Prothorax of Coleoptera
Fig. 23. Generalized Prothorax of the Lower Holometabola; Fig. 24, Hypothetical stem prothorax of Coleoptera. Membranous regions stippled. two parts by an apophysis, or pleural suture is a common feature of pterothoracic segments. Among Holometabola this arrangement is preserved in the prothorax only in Ithone and a few related forms (fig. 20, Eps, Epm, Invg). In the Trichoptera, a detached epimeron is present (fig. 22). In all other Holometabola the posterior rim of the apophysis is membranous. Ventral enlargement, and fusion of sternum, pleuron and even the cervical sclerites of the Corydalidae and Raphidioidea are doubtless specialized features readily derived from a generalized configuration
(Kelsey 1954, figs. I, 7 ; Ferris
and Fennebaker I 939, fig. 61 ) .
Comparison of the generalized holometabolous prothorax (GH) with that of the hypothetical stem coleopteran (SC) yields differ- ences in five major categories (figs. 23, 24). The abbreviations (GH and SC) are employed below for simplicity and to emphasize the fact that two abstract assemblages are being considered rather than elements of actual organisms.
A). Head-Prothoracic Joint. - In SC an anterior articulation- collar composed of notal, pleural and sternal flanges encloses part of the head and all cervical membrane as well as the cervical sclerites. The sternum is developed anteriorly and joined to the pleuron. An articulation-collar is absent in GH, the head may be slightly en-



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1 34 Psyche [September
closed by the notum, cervical membrane, and sclerites are exposed, and the sternum is not externally joined to the pleuron. B). Pro-Mesothoracic Joint. - In SC a partial posterior articu- lation-collar is formed from notal and pleural flanges, which rest on the mesothorax and enclose dorsal and lateral intersegmental mem- brane. Such flanges are absent and intersegrnental is exposed in GH. C). Notlo-Pleural and Pleuro-Sternal Joints. - In SC these con- nections are of the rim-fold type and result in a rigid frame pro- thorax. The horizontal invagination that forms the endopleuron is located close to the notal rim. In GH, the noto-pleural joint is loose and there is neither an external ~leuro-sternal connection nor D) . Trochantinal and Coxal Articulations. - In SC the coxa and trochantin are connected to one another and to the sternum and pleuron via loose rim-fold joints, which enclose peritrochantinal and pericoxal membrane (fig. 56). Loose rim-fold joints are absent in GH and these membranous regions are exposed. E.)
Attachment of Sternal and Pleural Imaginations (or 40- physes). -There is no vertical pleural apo~hyseal invagination in any extant coleopteron; the sternal apolphyses are always present. In all other Holometabola, both sternal and pleural apophyses are pres- ent, and these invaginations are solidly fused together (fig. 2 I ) . These differences are of two major types, those that result in the enclosure of membrane between moving parts (A, B, D) and one that results in a rigid frame prothorax (C). Major features of the hypothetical stem prothorax of beetles re- sult in great improvements in structural integrity over the ancestral condition due to development of rigidly attached segmental walls, and widespread enclosure of membrane. Two differences seem to be side effects of an increase in structural stability. An anterior, exter- nal sternal attachment provides potentially rigid attachment for this sclerite to the pleuron or notum, and permits the sternum to form the ventral body wall, and part of the anterior collar. An internal attachment can give only rigidity.
To have both is redundant. Loss
of both the internal sterno-pleural attachment and the pleural apo- physis itself may be a structural simplification occurring after devel- opment of a multi-purpose anterior sternal attachment. Parenthet-
ically, the line of fusion between the posterior rim fold and the body



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19721 Hlavac - Prothorax of Coleoptera I35 wall, is sometimes incorrectly called a pleural suture (= apophysis) in the taxonomic literature especially in the Adephaga. The endopleuron ~rovides increased surface area for muscle at- tachment. It is argued below that the key event leading to the unique coleopterous locomotory system was entrance into a substrate adaptive zone. Strength and power are both important in substrate locomotion. The features described above provide increased strength. The endopleuron is part of a mechanism for improving power gen- eration.
All features of the stem prothorax are either direct improvements in structural integrity or ancillary modifications. The unique structure of the pterot'horax and abdomen of Coleop- tera also represents a great increase in structural integrity over the ancestral condition.
In Lower holometabolous groups, the pterothoracic segments and wings are quite similar. The two pairs of wings are membranous. There are generally considerable patches of exposed membrane be- tween abdominal segments. In beetles the pterothoracic segments and wings are highly differentiated in structure and function. The mesothoracic wings of beetles are modified into rigid, heavily sdero- tized elytra whose rims can be fitted together, via a tongue-groove device, and which also lie on the pleural margins olf the pterothoracic and abdominal segments, thereby forming a structurally stable unit protecting abdominal tergites and folded wings. The abdomen is reduced in relative length, does not often extend behind the elytra, and the sternites are connected by rim-fold joints or are solidly fused together.
The membranous metathoracic flight wings are folded lengthwise, as well as widthwise, and are generally completely enclosed at rest, within the cavity formed by union of the body and elytra. The pterothoracic segments themselves are also highly differentiated. The metathorax, which houses all flight muscles, is much larger and high- ly modified as compared to the mesothorax. The characters discussed above as improvements in structural in- tegrity or side effects thereof encompass all major adult diagnostic features of the order Coleoptera.
Improvements in structural integrity can be responses to two po- tentially quite different but blendable selection pressures involving locomotion or defense. In a surface zone (i.e., crawling on a leaf) where environmental geometry does not oppose forward motion, high structural integrity can be the mechanical portion of an anti-predator system. For example, many arthropod predators, even relatively large