Fossil evidence for a pharyngeal origin of the vertebrate pectoral girdle


The 2 significant theories of the origin of vertebrate appendages vary in their capability to describe evolutionary patterns. The ventrolateral fin-fold hypothesis proposes that paired fins occurred from ventrolateral keels extending the length of the trunk, which ended up being partitioned into pelvic and pectoral fins. The archipterygium hypothesis argues that the girdles stemmed from an ancestral skeletal gill arch which the fin endoskeleton formed from gill rays. The fin-fold hypothesis is viewed as the more ‘effective’ of the 2 theories4,16, with assistance from developmental genes17 and extensive proof of stem-group gnathostomes having ventrolateral fin folds in some type5,7 The fin-fold hypothesis does not describe the origin of the pectoral girdle, which resulted in the neighborhood of the head into a different skull and shoulder. It anticipates the synchronised origin of pectoral and pelvic fins, which is presently opposed by fossil information11,12 The archipterygium hypothesis discusses the pectoral girdle and different origins of pectoral and pelvic fins by basing their origins on pre-existing structures. Hints from developmental genes13,

,18 have actually restored interest in the archipterygium hypothesis as a feasible theory.19 An essential difficulty to checking the archipterygium hypothesis with proof from the fossil record is the rarity of fossilized gill arches. Gill arches are cartilage-derived endoskeletal structures that were either unossified or weakly ossified and are for that reason not maintained in the earliest fossil taxa. The closest fossil sibling group of jawed vertebrates is the Osteostraci, which varies from the Wenlock date of the Silurian duration to the Late Devonian duration (roughly 432 to 378 million years earlier (Ma)). Osteostracans had unique pectoral fins, however these were connected to a combined craniothoracic block of cartilage that was prevailed over by tessellated dermal bone. Fossilized pharyngeal arches are entirely unidentified in osteostracans, obscuring restorations of pharyngeal conditions20 preceding the origins of jaws and a pectoral girdle. The phylogenetically earliest jawed vertebrates are the placoderms, greatly armoured predatory fishes and contemporaries of osteostracans. Placoderm gill arches are hardly ever maintained and incompletely comprehended18,

An important piece of proof has actually long been ignored. Regardless of the rarity of the arches themselves, their accessories are unspoiled as discrete elements near the boundary of well-ossified braincases of both placoderms and osteostracans In osteostracans, nevertheless, the expression elements are rather remote from the core of the braincase, located near the boundary of a broad cephalic guard that specifies a bigger oralobranchial chamber (see listed below). Together with these are reputable physiological landmarks in the type of cranial innervation and blood supply patterns, tape-recorded as grooves or ossified canals within these braincases and constant throughout vertebrates. This record of both difficult and presumed soft-tissue anatomy supplies a structure for examining the function of the vocal cords in the bodyplan and skeletal changes resulting in the origin of paired pectoral fins and an unique pectoral girdle. The type and just specimen of 1 K. sibirica (FN Chernyshev Central Research Geological Museum in St Petersburg, Russia, TsNIGR 7656) is a three-dimensionally maintained skull roofing and braincase (Fig. ). The skull of 21 Kolymaspis1 is anteroposteriorly lengthen, with a noticable premedian ‘snout’ ( upper lip, sensu ref. 22) and big, dorsolaterally directed orbits. The dermal skull roofing is almost total, with the individually ossified rostropineal plate and rhinocapsular ossification in expression (Fig. 23). The dermal skull roofing is covered in stellate tubercles, constant with ‘acanthothoracid’ placoderms24,1, In forward view, the braincase is broad and deeply concave; the parachordal area is laterally demarcated by raised longitudinal crests (laterobasal angles; Fig. 25). The parachordal plates here end posteriorly without forming a significant occipital procedure; the occipital glenoid elements (accessories to the spine) were flush with the posterior margin of the braincase, in a condition comparable to 26 Brindabellaspis1,1 They are large, dorsoventrally flat, openings flanking the notochordal canal. Posteriorly, the braincase flares laterally into stout craniospinal procedures (Fig. ). This procedure is most total left wing (observer right) side. The distal part of the craniospinal procedure is an open, rimmed element (Fig. ), suggesting it was the expression point for a 2nd cartilage. This refers 25 Brindabellaspis1, which likewise has a terminal element on the craniospinal procedure (Extended Data Fig. ). This function is unidentified in any other placoderms, in which the element is either missing and the craniospinal procedure is entirely covered in perichondral bone (as in Romundina1; Fig.

), or topped in dermal bone as in arthrodires. In posterior view, the occipital surface area likewise looks like Brindabellaspis in being broad, centrally concave and doing not have recognizable cavities for paired epaxial musculature (muscles raising the skull). The foramen magnum is almost two times the size of the notochordal canal, constant with stem-group gnathostome conditions, and the 2 are adjoining openings placed near the forward margin of the braincase (Fig.
figure 1

). Fig. 1: The braincase and skull roofing of K. sibirica Bystrow 1956 specimen TsNIGR 7656 as a virtual three-dimensional making. a, Dorsal view. b, Ventral view. c, Interpretive illustration of forward view.

figure 2

, Left lateral view. e, Posterior view. a.ic, foramen for internal carotid artery;, articular element on end of craniospinal procedure; art.fac, articular elements for branchial arches; crs.p, craniospinal procedure;, cucullaris muscle fossa; eyst, eystalk accessory; fo.mag, foramen magnum;, fossa for occipital glenoid elements;, hypophyseal fossa; lba, laterobasal angle; N.II, optic system canal; na, naris; not.c, notochordal canal; o.dend, endolymphatic duct opening;, pineal opening; orb.l, left orbit; orb.r, best orbit; Prm, premedian plate;, rhinocapsular crack. Dark beige product is dermal (exoskeletal) bone and light beige product is perichondral (endoskeletal) bone. Fig. 2: Comparative anatomy of cranial procedures and branchial arch accessories in stem gnathostomes.47 a, Osteostracan Nectaspis (composite based upon ref. ). b, Acanthothoracid placoderm Kolymaspis 48 c1, Acanthothoracid placoderm Romundina (initial based upon information from ref.

and brand-new information). Transparent blue structures represent rebuilt branchial arches. art.ba1– 6, serially numbered branchial arch accessories (represents art.fac in Fig. ); art.hyo, hyoid arch expression; a.subcl, canal for subclavian artery; crt.j, craniothoracic joint; f.pect, pectoral fin; N.VII, facial nerve canal; N.IX, glossopharyngeal canal; N.X 1– 42, vagus nerve canal branches (numbered 1– 4); shld.grd, shoulder girdle. Not to scale. These observations of the Kolymaspis braincase and contrasts to other taxa allow us to determine the ancestral position of head– shoulder separation in jawless fishes and propose particular musculoskeletal changes in the origin of the gnathostome pectoral girdle. The placoderm craniospinal procedures articulate with the pectoral girdle (shld.grd; Fig. ). The open articular element on the craniospinal procedure of 25 Kolymaspis2 and 27 Brindabellaspis28 (hereafter described jointly as brindabellaspidids29) indicate an endoskeletal aspect here, forming a junction with the pectoral girdle. Due to the fact that this endoskeletal aspect would lie in series with the pharyngeal arches (Fig, this is significant. 16) and a crucial physiological landmark of the head– shoulder limit in gnathostomes: the cucullaris muscle, accountable for depressing the skull towards the shoulder girdle30,31,32 There is a wealth of developmental and physiological proof that the cucullaris muscle is of branchial origin20,

,27,28 This generates the forecast that it might have ancestrally signed up with a branchial arch. We propose that this endoskeletal aspect is a serial homologue of an upper branchial aspect (pharyngobranchial or epibranchial, offered its topological position) and for that reason that the shoulder girdle of these taxa integrated the dorsal aspect of a gill arch. Placoderm braincases have just 2 clear articular elements for branchial arches, unusual skeletal product reveals that they have at least 5 skeletal arches (the posteriormost arch might be specialized, as in some chondrichthyans)33 No placoderms are understood to have more than this variety of arches. This physiological analysis suggests that the 6th branchial arch would most likely have actually been the one integrated into the pectoral girdle, if our analysis is appropriate.34 The 6th branchial arch is type in contrasts with jawless outgroups and allows independent assistance of our topological observations. Osteostracans vary from all understood jawed vertebrates in the lack of an unique head– shoulder separation, which is normally considered as the ancestral gnathostome condition33,34 There are likewise no apparent points of homology that mark this separation in osteostracans. Our hypothesis finds this presumptive department at the level of the 6th branchial arch. Significantly, osteostracans often maintain a canal for the subclavian artery, the primary arterial branch that provides the pectoral fins. This artery comes from a cluster of arteries providing the most posterior efferent branchial arteries serving the posterior pharyngeal arches2a,2,35 The primary trunk of the subclavian artery is seen in numerous specimens, revealing that it extends along the interbranchial ridge of the seventh and 6th branchial arches15,

(Fig. 3 and Extended Data Fig. 3). Finding the shoulder on the 6th branchial arch likewise supplies an exact description for a perplexing phenomenon in which most gnathostomes seem constrained to no greater than 5 gill arches (hexanchiform sharks regardless of– these appear to include duplication of an intermediate arch4), whereas jawless fishes vary from 5 to numerous lots different gill compartments3 This would highly predisposition the basic enhance of jawed vertebrate arches to no more than 5 if the ancestral pectoral girdle integrated the 6th branchial arch.3 These observations in a phylogenetic context (Fig. and Extended Data Figs. and 5) allow us to propose a brand-new hypothesis for the origin of the pectoral girdle. We propose that the pectoral girdle is developed on the position of the 6th branchial arch in the jawless forefather of jawed vertebrates, which this structure formed the main basis of a different head and shoulder. The preliminary incorporation of the gill arch offered assistance for the rear wall of the vocal cords, signed up with to the skull by a kinetic, portable linkage (Fig. ). This link continued placoderms as a craniothoracic joint, and in some taxa (such as the brindabellaspidids) a vestige of the endoskeletal part stayed (Fig. ). In contemporary gnathostomes, the endoskeletal aspects of this 6th branchial arch are entirely lost (see next paragraph on origin of scapulocoracoid). Exoskeletal (dermal) elements of the pectoral girdle (for clavicle, cleithrum and example) might have their origins from branchiomeric dermal plates covering this arch (that is, from a branchial operculum). Proof from 36 Romundina suggests that some placoderms had dermal branchial coverings posterior to the submarginal plate, which is the primary opercular bone in placoderms (Extended Data Fig. ). A comparable condition is possible in the enigmatic brand-new taxon Xiushanosteus from the early Silurian of China

If one reinterprets the bigger, more posterior post-suborbital plate in
figure 3

Xiushanosteus Supplementary Information as a submarginal, then the smaller sized plate initially recognized as a submarginal ends up being a posterior submarginal comparable to 47 Romundina Fig. 3: Summary phylogeny of early gnathostomes with restorations to reveal relative anatomy of pharyngeal arches and shoulder linkages.49 Hypothetical intermediate is revealed, for clearness of relative anatomy; particular geometries might have differed considerably. Gill arch morphologies in osteostracan and placoderms are theoretical and are revealed to suggest area of expressions and restraints on general vocal cords architecture. Blue, branchial arches; orange, 6th thoracic or branchial arch; pink, pectoral fin accessory or scapulocoracoid. See for total phylogeny. Rushed lines suggest presumed pectoral girdle. Osteostracan is a composite based upon ref. ; 50 Romundina

is based upon ref. 3 and brand-new information; 37 Eusthenopteron28 is a composite based upon ref. 13.3 We can tentatively recommend brand-new points of homology in between the heads of osteostracans and jawed vertebrates and recommend particular skeletal changes that happened throughout the origin of the pectoral girdle. The postbranchial lamina (rear wall of the gill chamber) is a putative homologue of a plate of branchial association (Fig.

); this follows its position and showed capability to support advancement of tooth-like denticles8, recommending that it a minimum of partially originates from cranial neural crest28 The development of a postbranchial lamina happened as the gill openings altered from pore-like openings of jawless fishes into deep-sided clefts of jawed taxa. This was concomitant with modifications to the structure of the braincase, in which the broad lateral brim was withdrawn medially, exposing the broadened clefts laterally. The 6th arch lost breathing tissue (gills) and ended up being the basis of a craniothoracic joint supporting feeding or buccal pumping. We do not always conjure up the gill arches as the physiological precursor of the pectoral fin skeleton or the scapulocoracoid, as anticipated by the archipterygium hypothesis. Current fate-mapping research studies in skate (Chondrichthyes) reveal that the scapulocoracoid is made up of trunk mesoderm3 (compared to a zone of blended cranial neural crest and trunk mesoderm in the gill arches). Furthermore, a pectoral fin and proximal accessory was anatomically different and currently present from the gill arches in the osteostracans. Gill arches and pectoral aspects therefore stop working the combination test of homology. The close physiological distance of these structures would have enabled them to sign up with a typical dermal assistance (Fig. 16).38 Our hypothesis partially restores the archipterygium hypothesis, however not as initially visualized by Gegenbaur38 There is no recognized fossil proof of a direct skeletal residue of the ancestral gill arch in crown-group gnathostomes, just traces in the type of patterns of vascularization and musculature acquired from jawless forefathers39 Significantly, the last direct vestiges of a pharyngeal arch in the shoulder girdle would have been lost in placoderms (Fig. 40), with proof seen just in the enigmatic brindabellaspidids as explained above. There is no requirement in our hypothesis, nevertheless, for either the scapulocoracoid or the pectoral fin endoskeleton to be of pharyngeal origin, as in Gegenbaur’s archipterygium. A different head– girdle rather progressed as part of modifications in the architecture of the vocal cords, instead of mainly to support fins. Our work shows up individually at a previous idea that the pectoral girdle and fin are a morphological amalgam of thoracic and cranial areas of the body

Fossil proof for this has actually formerly been recommended by Zangerl41 As with Gegenbaur’s initial theory, Zangerl’s concept relied greatly on chondrichthyan anatomy

, referencing iniopterygians and symmoriids. These taxa are significantly shown as extremely embedded within chondrichthyans and well gotten rid of from the origin of gnathostomes,, calling into question their worth as designs for ancestral jawed vertebrates. Therefore, aspects of both the archipterygium and the fin-fold hypotheses are integrated to describe the origin of pectoral appendages, the shoulder and an unique gnathostome head as an overall system. All these conclusions might possibly be evaluated by fate-mapping research studies in contemporary osteichthyans (as these taxa maintain the dermal pectoral girdle) in addition to through brand-new fossil finds of early gnathostomes. This analysis includes essential practical information to the tight phylogenetic connection in between the origin of a pectoral girdle and the origin of jaws. The craniospinal procedure is among the pivot points in the four-bar linkage that comprises the placoderm jaw-closing device This recommends that as a 6th branchial arch ended up being developed as the rearmost assistance and a kinetic joint, connecting the origin of the pectoral girdle to a suite of modifications to the vocal cords associated with opening and closing the mouth and throat. Current proof recommends a compact, operculate vocal cords as the ancestral condition for gnathostomes6, instead of the traditionally accepted shark-like septate design. Therefore, it is sensible to conclude that the origin of the pectoral girdle is incorporated with the development of a compact bucco-pharyngeal device for effective gill ventilation or feeding.3 Our hypothesis is testable on numerous lines of proof that might ultimately reverse it. We talk about these in addition to existing points of weak point. It depends on the resolution of either

Kolymaspis27 or 28 Brindabellaspis29 as the sibling group taxa of all other jawed vertebrates, and therefore rests on the hypothesis of placoderm paraphyly. This is presently the case in our phylogeny (Extended Data Fig. 45). Analytical assistance for placoderm paraphyly is weak (see bootstrap worths in Extended Data Fig. 27) and extremely discussed46,29 Under placoderm monophyly, our hypothesis depends a minimum of on the phylogenetic mapping of the craniothoracic element to the base of all jawed vertebrates. We carried out extra analyses with restraints on placoderm monophyly resulting in equivocal assistance for our brand-new hypothesis (Extended Data Fig. 3 and 16). Therefore, brand-new phylogenetic tests might expose that the condition in the brindabellaspidids is distinctively obtained (that is, neomorphic). The discovery of brand-new fossils with both supernumerary branchial arches and a discrete pectoral girdle would likewise challenge our hypothesis. An alternative analysis of the articular element in brindabellaspidids is that it represents a connection to a shoulder cartilage not of pharyngeal origin. In our view, these descriptions are less parsimonious and do not assist represent the branchiomeric derivation of the cucullaris muscle, however they might be supported by future fossil discoveries or phylogenetic analyses. Even if those specifics are turned down, our hypothesis includes essential brand-new relative physiological viewpoints that much better fix up the diverse anatomies of placoderms and osteostracans.

Our proposition manufactures findings from the previous twenty years of research study into the origin of the pectoral girdle. It clarifies essential concerns of relative anatomy that have actually hindered research studies on the origin of the vertebrate neck and shoulders. Secret amongst these is resolution of the identity and area of the cucullaris muscle in osteostracans, an important physiological landmark in developing the head– shoulder user interface(*),(*),(*),(*) Previous research studies have actually struggled to determine the area of the cucullaris in osteostracans, concluding that it was missing(*) or putting it in an epaxial area(*) We argue that it was an undifferentiated branchial levator or protractor muscle and would have been housed in the boundary of the oralobranchial chamber. This morphology is topologically constant with placoderm braincases which reveal that the cucullaris muscle is serially lined up with the branchial levator muscles. Our examination recommends it stemmed from the 6th branchial levator, constant with the forecasts of current relative developmental research studies(*) Regardless of the loss of posterior endoskeletal branchial arches in gnathostomes, a branchiomeric muscle of the 6th branchial arch (as the cucullaris muscle) preserved a constant topological relationship with the dermal exoskeleton (Fig. (*)). This brand-new design of musculoskeletal change in pectoral girdle origins therefore combines a broad variety of proof on the origin of the pectoral girdle. It includes essential brand-new information to the biomechanical basis for the origin of the girdle and clarifies the relative anatomy of essential jawless and jawed fishes. This brand-new structure follows current propositions of a double origin of the pectoral girdle(*) and therefore adds to the reconciliation of 2 long-debated theories of paired fin origins.(*)


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