Javier Ortega-Hernández

Hallucigenia ’s onychophoran-like claws and the case for Tactopoda

The Palaeozoic form-taxon Lobopodia encompasses a diverse range of soft-bodied ‘legged worms’ known from exceptional fossil deposits. Although lobopodians occupy a deep phylogenetic position within Panarthropoda, a shortage of derived characters obscures their evolutionary relationships with extant phyla (Onychophora, Tardigrada and Euarthropoda). Here we describe a complex feature in the terminal claws of the mid-Cambrian lobopodian Hallucigenia sparsa—their construction from a stack of constituent elements—and demonstrate that equivalent elements make up the jaws and claws of extant Onychophora. A cladistic analysis, informed by developmental data on panarthropod head segmentation, indicates that the stacked sclerite components in these two taxa are homologous—resolving hallucigeniid lobopodians as stem-group onychophorans. The results indicate a sister-group relationship between Tardigrada and Euarthropoda, adding palaeontological support to the neurological and musculoskeletal evidence uniting these disparate clades. These findings elucidate the evolutionary transformations that gave rise to the panarthropod phyla, and expound the lobopodian-like morphology of the ancestral panarthropod.

Specialized appendages in fuxianhuiids and the head organization of early euarthropods

The organization of the head provides critical data for resolving the phylogenetic relationships and evolutionary history of extinct and extant euarthropods. The early Cambrian-period fuxianhuiids are regarded as basal representatives of stem-group Euarthropoda, and their anterior morphology therefore offers key insights for reconstructing the ancestral condition of the euarthropod head. However, the paired post-antennal structures in Fuxianhuia protensa remain controversial; they have been interpreted as both ‘great appendages’ and as gut diverticulae. Here we describe Chengjiangocaris kunmingensis sp. nov. and Fuxianhuia xiaoshibaensis sp. nov. from a new early Cambrian (Stage 3) fossil Lagerstätte in Yunnan, China. Numerous specimens of both species show a unique ‘taphonomic dissection’ of the anterodorsal head shield, revealing the cephalic organization in detail. We demonstrate the presence of a pair of specialized post-antennal appendages (SPAs) in the fuxianhuiid head, which attach at either side of the posteriorly directed mouth, behind the hypostome. Preserved functional articulations indicate a well-defined but restricted range of limb movement, suggestive of a simple type of sweep feeding. The organization of the SPAs in fuxianhuiids is incompatible with the (deutocerebral) anterior raptorial appendages of megacheirans, and argue against the presence of protocerebral limbs in the fuxianhuiids. The positions of the fuxianhuiid antennae and SPAs indicate that they are segmentally homologous to the deutocerebral and tritocerebral appendages of crown-group Euarthropoda respectively. These findings indicate that antenniform deutocerebral appendages with many podomeres are a plesiomorphic feature of the ancestral euarthropod head.

Making sense of ‘lower’ and ‘upper’ stem‐group Euarthropoda, with comments on the strict use of the name Arthropoda von Siebold, 1848

The ever‐increasing number of studies that address the origin and evolution of Euarthropoda – whose extant representatives include chelicerates, myriapods, crustaceans and hexapods – are gradually reaching a consensus with regard to the overall phylogenetic relationships of some of the earliest representatives of this phylum. The stem‐lineage of Euarthropoda includes numerous forms that reflect the major morphological transition from a lobopodian‐type to a completely arthrodized body organization. Several methods of classification that aim to reflect such a complex evolutionary history have been proposed as a consequence of this taxonomic diversity. Unfortunately, this has also led to a saturation of nomenclatural schemes, often in conflict with each other, some of which are incompatible with cladistic‐based methodologies. Here, I review the convoluted terminology associated with the classification of stem‐group Euarthropoda, and propose a synapomorphy‐based distinction that allows ‘lower stem‐Euarthropoda’ (e.g. lobopodians, radiodontans) to be separated from ‘upper stem‐Euarthropoda’ (e.g. fuxianhuiids, Cambrian bivalved forms) in terms of the structural organization of the head region and other aspects of overall body architecture. The step‐wise acquisition of morphological features associated with the origins of the crown‐group indicate that the node defining upper stem‐Euarthropoda is phylogenetically stable, and supported by numerous synapomorphic characters; these include the presence of a deutocerebral first appendage pair, multisegmented head region with one or more pairs of post‐ocular differentiated limbs, complete body arthrodization, posterior‐facing mouth associated with the hypostome/labrum complex, and post‐oral biramous arthropodized appendages. The name ‘Deuteropoda’ nov. is proposed for the scion (monophyletic group including the crown‐group and an extension of the stem‐group) that comprises upper stem‐Euarthropoda and Euarthropoda. A brief account of common terminological inaccuracies in recent palaeontological studies evinces the utility of Deuteropoda nov. as a reference point for discussing aspects of early euarthropod phylogeny.

Burgess Shale-type microfossils from the middle Cambrian Kaili Formation, Guizhou Province, China

Diverse carbonaceous microfossils, including exceptionally preserved remains of non-biomineralizing metazoans, are reported from a basal middle Cambrian interval of the Kaili Formation (Guizhou Province, China). The application of a gentle acid maceration technique complements previous palynological studies by revealing a larger size-class of acritarchs, a richer assemblage of filamentous microfossils, and a variety of previously unrecovered forms. Metazoan fossils include Wiwaxia sclerites and elements derived from biomineralizing taxa, including chancelloriids, brachiopods and hyolithids, in common with previously studied assemblages from the early and middle Cambrian of Canada. In addition, the Kaili Formation has yielded pterobranch remains and an assemblage of cuticle fragments representing “soft-bodied” worms, including a priapulid-like scalidophoran. Our results demonstrate the wide distribution and palaeobiological importance of microscopic “Burgess Shale-type” fossils, and provide insights into the limitations and potential of this largely untapped preservational mode.

Fuxianhuiid ventral nerve cord and early nervous system evolution in Panarthropoda.

Significance Understanding the evolution of the CNS is fundamental for resolving the phylogenetic relationships within Panarthropoda (Euarthropoda, Tardigrada, Onychophora). The ground pattern of the panarthropod CNS remains elusive, however, as there is uncertainty on which neurological characters can be regarded as ancestral among extant phyla. Here we describe the ventral nerve cord (VNC) in Chengjiangocaris kunmingensis, an early Cambrian euarthropod from South China. The VNC reveals extraordinary detail, including condensed ganglia and regularly spaced nerve roots that correspond topologically to the peripheral nerves of Priapulida and Onychophora. Our findings demonstrate the persistence of ancestral neurological features of Ecdysozoa in early euarthropods and help to reconstruct the VNC ground pattern in Panarthropoda. Panarthropods are typified by disparate grades of neurological organization reflecting a complex evolutionary history. The fossil record offers a unique opportunity to reconstruct early character evolution of the nervous system via exceptional preservation in extinct representatives. Here we describe the neurological architecture of the ventral nerve cord (VNC) in the upper-stem group euarthropod Chengjiangocaris kunmingensis from the early Cambrian Xiaoshiba Lagerstätte (South China). The VNC of C. kunmingensis comprises a homonymous series of condensed ganglia that extend throughout the body, each associated with a pair of biramous limbs. Submillimetric preservation reveals numerous segmental and intersegmental nerve roots emerging from both sides of the VNC, which correspond topologically to the peripheral nerves of extant Priapulida and Onychophora. The fuxianhuiid VNC indicates that ancestral neurological features of Ecdysozoa persisted into derived members of stem-group Euarthropoda but were later lost in crown-group representatives. These findings illuminate the VNC ground pattern in Panarthropoda and suggest the independent secondary loss of cycloneuralian-like neurological characters in Tardigrada and Euarthropoda.

A superarmored lobopodian from the Cambrian of China and early disparity in the evolution of Onychophora

Significance Paleozoic lobopodians constitute a diverse assemblage of worm-like organisms that are known from various exceptional fossil deposits and were among the earliest animals to develop skeletonized body parts for protection. Here, we describe Collinsium ciliosum gen. et sp. nov., an armored lobopodian from the early Cambrian Xiaoshiba Lagerstätte (South China). Collinsium belongs to an extinct clade of superarmored lobopodians characterized by supernumerary dorsal spines, and specialized limbs for filter feeding; collectively, these fossil taxa represent a well-defined group within the lineage leading to extant velvet worms (Onychophora). Despite their greater morphological variety and appendage complexity compared with other lobopodians and extant velvet worms, Collinsium and its close relatives embodied a unique, yet ultimately failed, autoecology during the Cambrian explosion. We describe Collinsium ciliosum from the early Cambrian Xiaoshiba Lagerstätte in South China, an armored lobopodian with a remarkable degree of limb differentiation including a pair of antenna-like appendages, six pairs of elongate setiferous limbs for suspension feeding, and nine pairs of clawed annulated legs with an anchoring function. Collinsium belongs to a highly derived clade of lobopodians within stem group Onychophora, distinguished by a substantial dorsal armature of supernumerary and biomineralized spines (Family Luolishaniidae). As demonstrated here, luolishaniids display the highest degree of limb specialization among Paleozoic lobopodians, constitute more than one-third of the overall morphological disparity of stem group Onychophora, and are substantially more disparate than crown group representatives. Despite having higher disparity and appendage complexity than other lobopodians and extant velvet worms, the specialized mode of life embodied by luolishaniids became extinct during the Early Paleozoic. Collinsium and other superarmored lobopodians exploited a unique paleoecological niche during the Cambrian explosion.

Ancestral patterning of tergite formation in a centipede suggests derived mode of trunk segmentation in trilobites.

Trilobites have a rich and abundant fossil record, but little is known about the intrinsic mechanisms that orchestrate their body organization. To date, there is disagreement regarding the correspondence, or lack thereof, of the segmental units that constitute the trilobite trunk and their associated exoskeletal elements. The phylogenetic position of trilobites within total-group Euarthropoda, however, allows inferences about the underlying organization in these extinct taxa to be made, as some of the fundamental genetic processes for constructing the trunk segments are remarkably conserved among living arthropods. One example is the expression of the segment polarity gene engrailed, which at embryonic and early postembryonic stages is expressed in extant panarthropods (i.e. tardigrades, onychophorans, euarthropods) as transverse stripes that define the posteriormost region of each trunk segment. Due to its conservative morphology and allegedly primitive trunk tagmosis, we have utilized the centipede Strigamia maritima to study the correspondence between the expression of engrailed during late embryonic to postembryonic stages, and the development of the dorsal exoskeletal plates (i.e. tergites). The results corroborate the close correlation between the formation of the tergite borders and the dorsal expression of engrailed, and suggest that this association represents a symplesiomorphy within Euarthropoda. This correspondence between the genetic and phenetic levels enables making accurate inferences about the dorsoventral expression domains of engrailed in the trunk of exceptionally preserved trilobites and their close relatives, and is suggestive of the widespread occurrence of a distinct type of genetic segmental mismatch in these extinct arthropods. The metameric organization of the digestive tract in trilobites provides further support to this new interpretation. The wider evolutionary implications of these findings suggest the presence of a derived morphogenetic patterning mechanism responsible for the reiterated occurrence of different types of trunk dorsoventral segmental mismatch in several phylogenetically distant, extinct and extant, arthropod groups.

Origin and evolution of the panarthropod head - A palaeobiological and developmental perspective.

The panarthropod head represents a complex body region that has evolved through the integration and functional specialization of the anterior appendage-bearing segments. Advances in the developmental biology of diverse extant organisms have led to a substantial clarity regarding the relationships of segmental homology between Onychophora (velvet worms), Tardigrada (water bears), and Euarthropoda (e.g. arachnids, myriapods, crustaceans, hexapods). The improved understanding of the segmental organization in panarthropods offers a novel perspective for interpreting the ubiquitous Cambrian fossil record of these successful animals. A combined palaeobiological and developmental approach to the study of the panarthropod head through deep time leads us to propose a consensus hypothesis for the intricate evolutionary history of this important tagma. The contribution of exceptionally preserved brains in Cambrian fossils - together with the recognition of segmentally informative morphological characters - illuminate the polarity for major anatomical features. The euarthropod stem-lineage provides a detailed view of the step-wise acquisition of critical characters, including the origin of a multiappendicular head formed by the fusion of several segments, and the transformation of the ancestral protocerebral limb pair into the labrum, following the postero-ventral migration of the mouth opening. Stem-group onychophorans demonstrate an independent ventral migration of the mouth and development of a multisegmented head, as well as the differentiation of the deutocerebral limbs as expressed in extant representatives. The anterior organization of crown-group Tardigrada retains several ancestral features, such as an anterior-facing mouth and one-segmented head. The proposed model aims to clarify contentious issues on the evolution of the panarthropod head, and lays the foundation from which to further address this complex subject in the future.

Occurrence of the Ordovician-type aglaspidid Tremaglaspis in the Cambrian Weeks Formation (Utah, USA)

The Guzhangian Weeks Formation preserves a diverse, yet virtually unstudied, non-trilobite arthropod fauna. Here we describe Tremaglaspis vanroyi sp. nov., the oldest representative of an enigmatic group of extinct arthropods, the Aglaspidida. Tremaglaspis was previously known from the Lower Ordovician and its morphology was regarded as particularly derived within the clade. Its occurrence in the Cambrian of Utah suggests that much of the early evolutionary history of the Aglaspidida remains unknown. A review of the environmental settings of previous aglaspidid findings suggests that these arthropods preferentially inhabited shallow-water environments, which may partially explain their limited fossil record.

The first aglaspidid sensu stricto from the Cambrian of China (Sandu Formation, Guangxi)

Aglaspidids represent an obscure group of lower Palaeozoic arthropods with a patchy biogeographic distribution. Before the recent description of a representative from Tasmania, these arthropods were exclusively known from Laurentia during the late Cambrian. Here we describe a new species, Aglaspella sanduensis sp. nov., from the Furongian of China, confirming that aglaspidids sensu stricto were already widely distributed worldwide by the late Cambrian; this demonstrates that some aglaspidids had great dispersal capabilities. A new diagnosis of the genus Aglaspella is proposed and the species formerly known as Aglaspella eatoni is assigned to a new taxon, Hesselbonia gen. nov.