Xiaoya Ma

Complex brain and optic lobes in an early Cambrian arthropod

The nervous system provides a fundamental source of data for understanding the evolutionary relationships between major arthropod groups. Fossil arthropods rarely preserve neural tissue. As a result, inferring sensory and motor attributes of Cambrian taxa has been limited to interpreting external features, such as compound eyes or sensilla decorating appendages, and early-diverging arthropods have scarcely been analysed in the context of nervous system evolution. Here we report exceptional preservation of the brain and optic lobes of a stem-group arthropod from 520 million years ago (Myr ago), Fuxianhuia protensa, exhibiting the most compelling neuroanatomy known from the Cambrian. The protocerebrum of Fuxianhuia is supplied by optic lobes evidencing traces of three nested optic centres serving forward-viewing eyes. Nerves from uniramous antennae define the deutocerebrum, and a stout pair of more caudal nerves indicates a contiguous tritocerebral component. Fuxianhuia shares a tripartite pre-stomodeal brain and nested optic neuropils with extant Malacostraca and Insecta, demonstrating that these characters were present in some of the earliest derived arthropods. The brain of Fuxianhuia impacts molecular analyses that advocate either a branchiopod-like ancestor of Hexapoda or remipedes and possibly cephalocarids as sister groups of Hexapoda. Resolving arguments about whether the simple brain of a branchiopod approximates an ancestral insect brain or whether it is the result of secondary simplification has until now been hindered by lack of fossil evidence. The complex brain of Fuxianhuia accords with cladistic analyses on the basis of neural characters, suggesting that Branchiopoda derive from a malacostracan-like ancestor but underwent evolutionary reduction and character reversal of brain centres that are common to hexapods and malacostracans. The early origin of sophisticated brains provides a probable driver for versatile visual behaviours, a view that accords with compound eyes from the early Cambrian that were, in size and resolution, equal to those of modern insects and malacostracans.

Chelicerate neural ground pattern in a Cambrian great appendage arthropod

Preservation of neural tissue in early Cambrian arthropods has recently been demonstrated, to a degree that segmental structures of the head can be associated with individual brain neuromeres. This association provides novel data for addressing long-standing controversies about the segmental identities of specialized head appendages in fossil taxa. Here we document neuroanatomy in the head and trunk of a ‘great appendage’ arthropod, Alalcomenaeus sp., from the Chengjiang biota, southwest China, providing the most complete neuroanatomical profile known from a Cambrian animal. Micro-computed tomography reveals a configuration of one optic neuropil separate from a protocerebrum contiguous with four head ganglia, succeeded by eight contiguous ganglia in an eleven-segment trunk. Arrangements of optic neuropils, the brain and ganglia correspond most closely to the nervous system of Chelicerata of all extant arthropods, supporting the assignment of ‘great appendage’ arthropods to the chelicerate total group. The position of the deutocerebral neuromere aligns with the insertion of the great appendage, indicating its deutocerebral innervation and corroborating a homology between the ‘great appendage’ and chelicera indicated by morphological similarities. Alalcomenaeus and Fuxianhuia protensa demonstrate that the two main configurations of the brain observed in modern arthropods, those of Chelicerata and Mandibulata, respectively, had evolved by the early Cambrian.

Brain structure resolves the segmental affinity of anomalocaridid appendages

Despite being among the most celebrated taxa from Cambrian biotas, anomalocaridids (order Radiodonta) have provoked intense debate about their affinities within the moulting-animal clade that includes Arthropoda. Current alternatives identify anomalocaridids as either stem-group euarthropods, crown-group euarthropods near the ancestry of chelicerates, or a segmented ecdysozoan lineage with convergent similarity to arthropods in appendage construction. Determining unambiguous affinities has been impeded by uncertainties about the segmental affiliation of anomalocaridid frontal appendages. These structures are variably homologized with jointed appendages of the second (deutocerebral) head segment, including antennae and ‘great appendages’ of Cambrian arthropods, or with the paired antenniform frontal appendages of living Onychophora and some Cambrian lobopodians. Here we describe Lyrarapax unguispinus, a new anomalocaridid from the early Cambrian Chengjiang biota, southwest China, nearly complete specimens of which preserve traces of muscles, digestive tract and brain. The traces of brain provide the first direct evidence for the segmental composition of the anomalocaridid head and its appendicular organization. Carbon-rich areas in the head resolve paired pre-protocerebral ganglia at the origin of paired frontal appendages. The ganglia connect to areas indicative of a bilateral pre-oral brain that receives projections from the eyestalk neuropils and compound retina. The dorsal, segmented brain of L. unguispinus reinforces an alliance between anomalocaridids and arthropods rather than cycloneuralians. Correspondences in brain organization between anomalocaridids and Onychophora resolve pre-protocerebral ganglia, associated with pre-ocular frontal appendages, as characters of the last common ancestor of euarthropods and onychophorans. A position of Radiodonta on the euarthropod stem-lineage implies the transformation of frontal appendages to another structure in crown-group euarthropods, with gene expression and neuroanatomy providing strong evidence that the paired, pre-oral labrum is the remnant of paired frontal appendages.

Morphology of Luolishania longicruris (Lower Cambrian, Chengjiang Lagerstätte, SW China) and the phylogenetic relationships within lobopodians

New material of the lobopodian Luolishania longicruris has been recovered from the Lower Cambrian Chengjiang Lagerstätte, southwest China. The specimens throw new light on several morphological features of the species, including the paired antenniform outgrowths, eyes, head shield, setae and other cuticular projections, as well as the differentiated sclerites, appendages, claws, and lobopod interspaces. L. longicruris shows well developed tagmosis: a distinct head and a trunk divided into two sections. The new data allow a revised comparison with other lobopodians. Miraluolishania haikouensis Liu et al., 2004 is considered to be a junior synonym of L. longicruris Hou and Chen, 1989. Evidence from gut filling and specialized morphological characters indicates that L. longicruris may have had a filter feeding lifestyle. A new cladistic analysis suggests that fossil lobopodians are paraphyletic or even polyphyletic and L. longicruris may be an important representative of the stem lineage leading to arthropods.

The lobopodian Paucipodia inermis from the Lower Cambrian Chengjiang fauna, Yunnan, China

New specimens of Paucipodia inermis Chen, Zhou & Ramskold, 1995, are described from the Lower Cambrian Chengjiang Lagerstatte in Haikou, Kunming. Details not previously seen in the Chengjiang material appear to be caused by early diagenetic processes. Some features not previously observed in Palaeozoic lobopodians include details of the dermomuscular sac, body cavities, contents of the gut, possible paired ventral nerve ganglia, and a rasping or biting apparatus with teeth. The latter implies a fundamental difference from onychophorans and rules out an ancestral position for Palaeozoic lobopodians. The supposed tail is shown to be the head, and it is shown that this animal possessed nine pairs of lobopods rather than six, as originally stated. The family Paucipodiidae n. fam. is introduced.

Cambrian anemones with preserved soft tissue from the Chengjiang biota, China

Hou, X.-G., Stanley Jr, G.D., Zhao, J. & Ma, X.-Y. 2005 09 12: Cambrian anemones withpreserved soft tissue from the Chengjiang biota, China. Lethaia, Vol. 38, pp. 193–203.Oslo. ISSN 0024-1164.The group Cnidaria includes ‘jellyfish’, soft-bodied anemone and anemone-like formsand calcified corals. These diploblastic organisms have a fossil record extending back tothe earliest metazoans of the Neoproterozoic; however certain cnidarians of the subclassZoantharia, characterized by soft-bodied anemone-like forms, are absent or poorlyrepresented in the fossil record. Despite the paucity of fossils, it is thought that calcifi-cation by soft anemone-like animals was responsible for producing the skeleton thatallowed the preservation of the first corals. We report discovery of an abundant assem-blage of in situ soft-bodied polyps with tissues. They are preserved in exquisite detail andcome from the well-known Lower Cambrian Chengjiang biota of Yunnan, China. Thesoft-bodied polyps display a simple anatomy that is comparable to some extant anemonesof the order Actinaria. The new fossils are assigned to Archisaccophyllia kunmingensis n.gen. et n. sp. Their simple and conservative form suggests that these fossils may representsome kind of ancestral rootstock. The preserved life assemblage provides a uniquesnapshot of Lower Cambrian anemone life and provides clues for relationships withextant actiniarians as well as calcified corals. & Actiniaria, anemone, Chengjiang biota,China, Lower Cambrian, soft-bodied fossils.Xian-guang Hou (corresponding author) [xghou@ynu.edu.cn], Jie Zhao [biofeature@hotmail.com] and Xiao-ya Ma [littleya@vip.sina.com], Yunnan Key Laboratory forPalaeobiology, Yunnan University, Kunming 650091, China; George D. Stanley, Jr.[george.stanley@umontana.edu], Department of Geology, The University of Montana,Missoula, MT 59812, USA; 19th August 2004, revised 11th April 2005.

Arthropod eyes: The early Cambrian fossil record and divergent evolution of visual systems

Four types of eyes serve the visual neuropils of extant arthropods: compound retinas composed of adjacent facets; a visual surface populated by spaced eyelets; a smooth transparent cuticle providing inwardly directed lens cylinders; and single-lens eyes. The first type is a characteristic of pancrustaceans, the eyes of which comprise lenses arranged as hexagonal or rectilinear arrays, each lens crowning 8-9 photoreceptor neurons. Except for Scutigeromorpha, the second type typifies Myriapoda whose relatively large eyelets surmount numerous photoreceptive rhabdoms stacked together as tiers. Scutigeromorph eyes are facetted, each lens crowning some dozen photoreceptor neurons of a modified apposition-type eye. Extant chelicerate eyes are single-lensed except in xiphosurans, whose lateral eyes comprise a cuticle with a smooth outer surface and an inner one providing regular arrays of lens cylinders. This account discusses whether these disparate eye types speak for or against divergence from one ancestral eye type. Previous considerations of eye evolution, focusing on the eyes of trilobites and on facet proliferation in xiphosurans and myriapods, have proposed that the mode of development of eyes in those taxa is distinct from that of pancrustaceans and is the plesiomorphic condition from which facetted eyes have evolved. But the recent discovery of enormous regularly facetted compound eyes belonging to early Cambrian radiodontans suggests that high-resolution facetted eyes with superior optics may be the ground pattern organization for arthropods, predating the evolution of arthrodization and jointed post-protocerebral appendages. Here we provide evidence that compound eye organization in stem-group euarthropods of the Cambrian can be understood in terms of eye morphologies diverging from this ancestral radiodontan-type ground pattern. We show that in certain Cambrian groups apposition eyes relate to fixed or mobile eyestalks, whereas other groups reveal concomitant evolution of sessile eyes equipped with optics typical of extant xiphosurans. Observations of fossil material, including that of trilobites and eurypterids, support the proposition that the ancestral compound eye was the apposition type. Cambrian arthropods include possible precursors of mandibulate eyes. The latter are the modified compound eyes, now sessile, and their underlying optic lobes exemplified by scutigeromorph chilopods, and the mobile stalked compound eyes and more elaborate optic lobes typifying Pancrustacea. Radical divergence from an ancestral apposition type is demonstrated by the evolution of chelicerate eyes, from doublet sessile-eyed stem-group taxa to special apposition eyes of xiphosurans, the compound eyes of eurypterids, and single-lens eyes of arachnids. Different eye types are discussed with respect to possible modes of life of the extinct species that possessed them, comparing these to extant counterparts and the types of visual centers the eyes might have served.

An exceptionally preserved arthropod cardiovascular system from the early Cambrian

The assumption that amongst internal organs of early arthropods only the digestive system withstands fossilization is challenged by the identification of brain and ganglia in early Cambrian fuxianhuiids and megacheirans from southwest China. Here we document in the 520-million-year-old Chengjiang arthropod Fuxianhuia protensa an exceptionally preserved bilaterally symmetrical organ system corresponding to the vascular system of extant arthropods. Preserved primarily as carbon, this system includes a broad dorsal vessel extending through the thorax to the brain where anastomosing branches overlap brain segments and supply the eyes and antennae. The dorsal vessel provides segmentally paired branches to lateral vessels, an arthropod ground pattern character, and extends into the anterior part of the abdomen. The addition of its vascular system to documented digestive and nervous systems resolves the internal organization of F. protensa as the most completely understood of any Cambrian arthropod, emphasizing complexity that had evolved by the early Cambrian.

Unlocking the early fossil record of the arthropod central nervous system.

Extant panarthropods (euarthropods, onychophorans and tardigrades) are hallmarked by stunning morphological and taxonomic diversity, but their central nervous systems (CNS) are relatively conserved. The timing of divergences of the ground pattern CNS organization of the major panarthropod clades has been poorly constrained because of a scarcity of data from their early fossil record. Although the CNS has been documented in three-dimensional detail in insects from Cenozoic ambers, it is widely assumed that these tissues are too prone to decay to withstand other styles of fossilization or geologically older preservation. However, Cambrian Burgess Shale-type compressions have emerged as sources of fossilized brains and nerve cords. CNS in these Cambrian fossils are preserved as carbon films or as iron oxides/hydroxides after pyrite in association with carbon. Experiments with carcasses compacted in fine-grained sediment depict preservation of neural tissue for a more prolonged temporal window than anticipated by decay experiments in other media. CNS and compound eye characters in exceptionally preserved Cambrian fossils predict divergences of the mandibulate and chelicerate ground patterns by Cambrian Stage 3 (ca 518 Ma), a dating that is compatible with molecular estimates for these splits.

A New Exceptionally Preserved Cambrian Priapulid From The Chengjiang Lagerstätte

Abstract A fossil priapulid, Eximipriapulus globocaudatus new genus new species, is described from the Cambrian Chengjiang Lagerstätte of Yunnan, China. The exceptional preservation of the animal reveals morphological details that allow direct comparison with extant priapulids. The body is divisible into a partially eversible pharynx, a smooth collar, a scalid-bearing introvert, a neck with triangular scalids, an unsegmented trunk with annulations, and a distinctly expanded terminal region. Several specialized regions of the alimentary canal are recognized: a pharynx (lined by cuticle and bearing teeth), esophagus, midgut, hindgut, and a terminal anus. The sample includes a putative juvenile. The animal is inferred to have been an active burrower using a double-anchor strategy, practicing both deposit feeding and carnivory. Inclusion of Eximipriapulus in the most recent character matrix for cladistic analysis of fossil and Recent priapulids resolves the new genus within the priapulid crown group.