Organ systems of a Cambrian euarthropod larva

Abstract

The Cambrian radiation of euarthropods can be attributed to an adaptable body plan. Sophisticated brains and specialized feeding appendages, which are elaborations of serially repeated organ systems and jointed appendages, underpin the dominance of Euarthropoda in a broad suite of ecological settings. The origin of the euarthropod body plan from a grade of vermiform taxa with hydrostatic lobopodous appendages ('lobopodian worms')^1,2 is founded on data from Burgess Shale-type fossils. However, the compaction associated with such preservation obscures internal anatomy^3-6. Phosphatized microfossils provide a complementary three-dimensional perspective on early crown group euarthropods⁷, but few lobopodians^8,9. Here we describe the internal and external anatomy of a three-dimensionally preserved euarthropod larva with lobopods, midgut glands and a sophisticated head. The architecture of the nervous system informs the early configuration of the euarthropod brain and its associated appendages and sensory organs, clarifying homologies across Panarthropoda. The deep evolutionary position of Youti yuanshi gen. et sp. nov. informs the sequence of character acquisition during arthropod evolution, demonstrating a deep origin of sophisticated haemolymph circulatory systems, and illuminating the internal anatomical changes that propelled the rise and diversification of this enduringly successful group.

Fig. 1. Anatomical overview of Youti yuanshi.

YKLP 12387. a, External scanning electron microscopy, right side. Damage to posterior epidermis exposes lining of perivisceral cavity, demonstrating blind gut. b, External scanning electron microscopy, left side. c,g–j, Median virtual dissection from X-ray computed tomography (XCT) data (c), showing location of transverse slices intersecting digestive glands (g,i) and transverse membrane (h,j). d, Semi-manual segmentation of internal chambers from XCT data, viewed from the left side. Dorsolateral aspects of the peripheral cavity are omitted for clarity. e,f, Virtual dissection parallel to coronal plane, looking ventrally (e) and dorsally (f), showing digestive glands, pericardial sinus, transverse membranes within perivisceral cavity, and oblique membranes within peripheral cavity. g–j, XCT sections at positions indicated in c at position of digestive glands (g,i) and at position of ventrolateral lacunae and transverse membrane (h,j). g,h, Sections close to the anterior trunk, reflecting segments at late developmental stage. i,j, Sections close to the posterior trunk, showing superior preservation of internal tissue. k, Segmentation of internal chambers from XCT data, viewed from the dorsal perspective at anterior, middle and posterior trunk. Aspects of peripheral cavity are omitted for clarity. a, appendage; cb, central body of brain; db, dorsolateral body of brain; dia, diagenetic grain; dg, digestive gland; dm, dorsal membrane; dp, dorsal projection; dv, dorsal vessel; fb, frontal body of brain; irr, irregular chamber; lig, ligament; om, oblique membrane; pc, pericardial sinus; pph, peripheral cavity; pn, perineural sinus; pv, perivisceral cavity; tm, transverse membrane; vl, ventrolateral sinus; vv, ventral vessel. Scale bars, 200 μm.

Fig. 2. Internal anatomy of Youti yuanshi.

YKLP 12387. a,b, Virtual dissections of dorsolateral trunk, looking posteriad, showing internal structure of tenth (a) and eighth (b) digestive glands, oblique membrane within peripheral cavity and ligaments associated with gut. c, Virtual dissection through 14th digestive gland, looking anteriad, showing connection of digestive glands to dorsal gut. d, Virtual dissection showing blind termination of posterior gut; dashed line marks anterior limit of gut preservation. e–g, Disposition of chambers within trunk appendages, showing extensions of perivisceral and peripheral cavities into appendage. Virtual dissections oriented parallel (e), oblique (f) and subperpendicular (g) to appendages. A, anterior; P, posterior. Colour scheme as in Fig. 1. dgp, digestive gland process; lac, lacuna of the ventrolateral sinus. Scale bars, 100 μm.

Fig. 3. Head structure in Youti yuanshi.

YKLP 12387. a–d, XCT sections from ventral (a,b) to dorsal (c,d) surface of dorsal lobe, showing internal structure of head and trunk. e–j, Transverse XCT sections from anterior (e) to posterior (j) of head. D, dorsal; V, ventral. k–m, Ventral view of head, showing external XCT volume render (k) and segmentation of chambers without (l) and with (m) ventral structures. n, Sublateral view. Colour scheme as in Fig. 1. an, anterior compartment of first appendage; cc, circumpharyngeal connective; co, circumoral ring; e, eye; mm, transverse medial membrane of the central body; po, posterior compartment of first appendage; sp, subpharyngeal gland; µb, microboring. Scale bars, 200 μm.

Fig. 4. Interpretative drawings of Youti yuanshi.

a, Organ system disposition in sagittal view. Dotted lines denote location of sections shown in e,f. b, Organ system disposition in transverse view. c,d, Head, from lateral perspective (c) and as medial transverse section (d). e,f, Transverse sections through trunk at location of digestive glands (e) and transverse membranes (f). g–j, Coronal sections through head, from ventral (g) to dorsal (j) planes. Colour scheme as in Fig. 1.

Fig. 5. Proposed homology of brain components in early panarthropods.

Phylogenetic analysis situates Youti yuanshi within the AOPK clade containing Anomalocaris, Opabinia, Pambdelurion and Kerygmachela. Under our preferred model, the circumoral brain ring of cycloneuralians corresponds to the panarthropod prosocerebrum, which innervates the first appendage pair (onychophoran antennae, tardigrade stylets or euarthropod labrum). We interpret the archicerebrum as a distinct development dorsal to the prosocerebrum, associated with sensory receptors: specifically the eyes, and the dorsal projections (Kerygmachela rostral spines, tardigrade cirri, crustacean frontal filaments or anterior paired projections of stem euarthropods; homology with the anteriormost onychophoran lip papillae is plausible, but may not be parsimonious). The taxa depicted in this figure are selected in order to depict the evolutionary context of Youti; the relationships shown are recovered under all analytical conditions.

Extended Data Fig. 1. Structure and relationship of major body cavities within Youti yuanshi.

Location of major organ systems within YKLP 12387, lateral view. a, perivisceral cavity; b, pericardial sinus; c, digestive glands, showing relationship to perivisceral cavity; d, gut and subpharyngeal gland; absence of medial gut represents non-preservation; e, ventrolateral sinus, showing relationship to perivisceral cavity; f, perineural sinus; g, peripheral cavity; h, dorsolateral body of brain with associated vessel. Abbreviations: co, circumoral ring; dv, dorsal vessel; pn, perineural sinus; sp, subpharyngeal gland.

Extended Data Fig. 2. Structure and relationship of major body cavities within Youti yuanshi.

Location of major organ systems in YKLP 12387, dorsal views. a, perivisceral cavity; b, pericardial sinus; c, digestive glands; d, preserved extent of gut; absence of medial gut represents non-preservation; e, ventrolateral sinus; f, perineural sinus; g, dorsolateral body of brain with associated vessel; h, central body of brain; i, irregular chamber, interpreted as dorsal extra-embryonic ectoderm. Abbreviations: cc, circumpharyngeal connective, co, circumoral ring; db, dorsolateral body of brain; dp, dorsal projection; dv, dorsal vessel; pn, perineural sinus.

Extended Data Fig. 3. Coronal sections through anterior of Youti yuanshi.

a–o, Virtual dissections of YKLP 12387 rendered from XCT data, from dorsal to ventral. Coloured regions identify organ systems. Raw images available at FigShare. Abbreviations: a, appendage; an, anterior compartment of first appendage; cb, central body of brain; cc, circumpharyngeal connective; co, circumoral ring; db, dorsolateral body of brain; dg, digestive gland; dp, dorsal projection; dv, dorsal vessel; e, eye; fb, frontal body of brain; irr, irregular chamber; lac, lacuna; mm, transverse medial membrane of the central body; po, posterior compartment of first appendage; pph, peripheral cavity; sep, membrane separating compartments of the first appendage; sp, subpharyngeal gland; tm, transverse membrane; vl, ventrolateral sinus.

Extended Data Fig. 4. Transverse sections through anterior of Youti yuanshi.

a–t, Virtual dissections of YKLP 12387 rendered from XCT data, from anterior to posterior. Coloured regions identify organ systems; colours as for Extended Data Fig. 3. Raw images available at FigShare. Abbreviations: an, anterior compartment of first appendage; cb, central body of brain; cc, circumpharyngeal connective; db, dorsolateral body of brain; dg, digestive gland; dv, dorsal vessel; e, eye; fen, fenestra; irr, irregular chamber; lac, lacuna; pc, pericardial sinus; pn, perineural sinus; po, posterior compartment of first appendage; pv, perivisceral sinus; sp, subpharyngeal gland; vl, ventrolateral sinus.

Extended Data Fig. 5. Virtual dissection of Youti yuanshi.

Enlargement of Fig. 1e–f, Rendered from XCT data parallel to coronal plane, looking a, ventrally; b, dorsally. Abbreviations: a, appendage; dg, digestive gland; dgp, digestive gland process; fen, fenestra; lig, ligament; om, oblique membrane; pc, pericardial sinus; pph, peripheral cavity; tm, transverse membrane; vv, ventral vessel.