Trilobite body patterning and the evolution of arthropod tagmosis

Preservation permitting patterns of developmental evolution can be reconstructed within long extinct clades, and the rich fossil record of trilobite ontogeny and phylogeny provides an unparalleled opportunity for doing so. Furthermore, knowledge of Hox gene expression patterns among living arthropods permit inferences about possible Hox gene deployment in trilobites. The trilobite anteroposterior body plan is consistent with recent suggestions that basal euarthropods had a relatively low degree of tagmosis among cephalic limbs, possibly related to overlapping expression domains of cephalic Hox genes. Trilobite trunk segments appeared sequentially at a subterminal generative zone, and were exchanged between regions of fused and freely articulating segments during growth. Homonomous trunk segment shape and gradual size transition were apparently phylogenetically basal conditions and suggest a single trunk tagma. Several derived clades independently evolved functionally distinct tagmata within the trunk, apparently exchanging flexible segment numbers for greater regionally autonomy. The trilobite trunk chronicles how different aspects of arthropod segmentation coevolved as the degree of tagmosis increased.     

Head segmentation of trilobites

Although trilobites have provided research subjects for more than two centuries, their head segmentation has remained unresolved. Four glabellar furrows (SO and S1–S3) marking the segmental boundaries are generally present in the cephalic axis, but there are trilobites with one more pair of furrows, the so‐called S4, in the cephalic axis, causing confusion in understanding trilobite head segmentation. Recent advances in developmental biology and palaeontology have shed light on the arthropod head problem, and thus, trilobite head segmentation can be reviewed in the light of this knowledge. Based on the information from the anatomy of exceptionally preserved trilobites and artiopodans closely related to trilobites, it is inferred that trilobite head contains five segments: the anteriormost ocular segment potentially associated with the hypostome, the antennal segment and the following three segments with walking legs. When present, the S4 furrows are situated where the eye ridges meet the cephalic axis of trilobites, indicating that the furrows are incised ‘within’ the anteriormost segment in trilobites with an anteriorly enlarged frontal lobe. Trilobites of the Order Redlichiida, the most primitive stock, show variable conditions in the frontal glabellar conditions, while in other more derived groups, the condition is rather constant. The frontal glabellar condition, therefore, could provide a clue to elucidate the unresolved Cambrian trilobite phylogeny and the Cambrian roots of the post‐Cambrian trilobites.     

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.     

The Phylogeny and Systematics of Blind Cambrian Ptychoparioid Trilobites

The paraphyletic trilobite suborder Ptychopariina includes a large proportion of Cambrian trilobite diversity and is probably ancestral to most groups of post-Cambrian trilobites. Resolution of the phylogenetic relationships within the group is therefore crucial to a better understanding of the initial radiation of trilobites. The recognition of approaches that can successfully resolve the relationships of ptychoparioid taxa is an important first step towards this aim. Cladistic analysis was used to determine relationships within the Cambrian ptychoparioid trilobite family Conocoryphidae, and to test claims that the family is polyphyletic. Ninety-seven characters were coded for 40 conocoryphid species and nine non-conocoryphids. The results indicate that the family consists of four distantly related clades. Three are recognized here as distinct families, including an extensively revised Conocoryphidae, and the families Holocephalidae and Atopidae. The fourth clade is referred to the subfamily Acontheinae (Corynexochida) as the new Tribe Hartshillini. Analysis of the disparity of these four clades shows that they are significantly less morphologically variable than the original polyphyletic taxon, demonstrating the possible effects of taxonomic error on macroevolutionary studies of morphological disparity.     

Thoracic structure and enrolment style in middle Cambrian Eccaparadoxides pradoanus presages caudalization of the derived trilobite trunk

Abstract: The ability to enrol effectively evolved several times among trilobites. Here, we show that, unlike most redlichiid trilobites that could not enrol, both morphotypes of Eccaparadoxides pradoanus from the middle Cambrian of Spain enrolled so as to enclose most of the ventral surface beneath the exoskeleton and possessed specialized articulating devices that facilitated this behaviour. The holaspid thorax of all E. pradoanus was divided into two principal regions. The boundary between these marked a transition from anterior segments with short pleural spines, fulcra and ridge‐and‐groove inner pleural regions to posterior segments with longer, acuminate pleural spines that lack fulcra and inner pleural regions. Devices that aid articulation, such as fulcra with short articulating pleural surfaces, the petaloid articulating facet and long articulating half rings, are concentrated in the anterior region. These features, and the large number of specimens preserved in various degrees of enrolment, suggest an enrolment procedure in which the rear part of the trunk, containing both the posterior thorax and the pygidium, rotated as a single unit without significant internal flexure. As these posterior trunk articulations were apparently not required to permit enrolment, concentrating flexure in the anterior may have presaged the caudalized condition seen in many derived trilobite groups that encapsulated, in which a larger proportion of the trunk segments were allocated to the mature pygidium, and therefore unable to articulate.     

Trunk segmentation of Cambrian eodiscoid trilobites

SUMMARY Here we report, from Cambrian Series 2 of Chongqing, southern China, on some three-dimensionally phosphatized exoskeletons representing a series of instars of a specialized eodiscoid trilobite Badiscus spinosus gen. et sp. nov. The preservation is unusual and its protaspides (the youngest juveniles) belonging to different growth stages markedly exhibit some "embryonic trunk segments," which imply the specification of all body segments during embryogenesis. This previously unknown style of tagmosis, as being inconsistent with the conventional view of sequential segmentation during postembryonic anamorphosis, emphasizes the complexity of trilobite trunk segmentation during ontogeny and indicates for the first time that epimorphic development, like other known patterns during postembryonic development, may have already been adopted by some of the earliest trilobites.     

Enrolment and trunk segmentation of a Cambrian eodiscoid trilobite

Completely enrolled, phosphatized, 3‐D specimens of the eodiscinid trilobite Tsunyidiscus yanjiazhaiensis from Cambrian Stage 3 of South China exhibit much morphological detail and show variation in delicate coaptative structures associated with their trunk segmentation. The relationship between enrolment mechanism and trunk segmentation during ontogeny confirms a unique developmental pattern among the early Cambrian eodiscoid trilobites, revealing how these animals controlled the rate of segment increase and release during post‐embryonic development in their life cycles.     

An early Cambrian chelicerate from the Emu Bay Shale,South Australia

The Emu Bay Shale Lagerstätte (Cambrian Series 2, Stage 4) occurs on the north coast of Kangaroo Island, South Australia. Over 50 species are known from here, including trilobites and non‐biomineralized arthropods, palaeoscolecids, a lobopodian, a polychaete, vetulicolians, nectocaridids, hyoliths, brachiopods, sponges and chancelloriids. A new chelicerate, Wisangocaris barbarahardyae gen. et sp. nov., is described herein, based on a collection of some 270 specimens. It is up to 60 mm long, with the length of the cephalic shield comprising about 30% that of the exoskeleton. The cephalic margin has three pairs of bilaterally‐symmetrical small triangular spines. A pair of small eyes is placed well forwards on the ventral margin of the cephalic shield. The trunk comprises 11 segments that increase in length while narrowing posteriorly, each possibly bearing a pair of biramous appendages; the most posterior segment is almost square whereas the others are transversely elongated. The spatulate telson is proportionately longer than in taxa such as Sanctacaris, Utahcaris and Leanchoilia. Up to eight (?four pairs) of 3 mm‐long elements bearing alternating inward‐curving short and long spines beneath the cephalic shield are interpreted as basipodal gnathobases, part of a complex feeding apparatus. A well‐developed gut includes a stomach within the cephalic shield; it extends to the base of the telson. In a few specimens there are shell fragments within the gut, including those of the trilobite Estaingia bilobata (the most common species in the biota); these fragments have sharp margins and extend across the gut lumen. The species may have been a predator or a scavenger, ingesting material already broken up by a larger predator/scavenger. The morphology of this taxon shares many overall body features with Sanctacaris, and some with Sidneyia, particularly its gnathobasic complex. These chelicerate affinities are corroborated by phylogenetic analyses.     

Varied development of trunk segmentation in three related Upper Devonian phacopine trilobites

In many arthropods, the development of the trunk region is a complex part of post-embryonic development. Consideration of fossil ontogeny provides an additional source of data and a broader evolutionary perspective on the evolution of arthropod body patterning. Here, I examine the development of the thoraco-pygidial exoskeleton of three related phacopine trilobites from the Upper Devonian according to the integrated ontogenetic scheme proposed by Hughes et al. Pygidial shields assigned to three ontogenetic series gave us the opportunity to further explore the evolutionary pattern of the trilobite segmentation. The analysis showed a different mode of development in two of three species and thus reveals variability between the related taxa. Comparison of the boundaries of different aspects of ontogenesis ratifies the diversity of the segmentation process among trilobites and even among related phacopine species. Results include (i) in a synarthromeric trunk condition recorded to date, there has consistently been a preceding ‘equilibrium’ phase for the late meraspid pygidium and (ii) two developmental modes, i.e. both hypoprotomeric development and synarthromeric development, occur contemporaneously in closely related taxa. Such developments suggest that aspects of segmental development such as segment accretion and segment articulation were able to vary in a labile manner.     

Crustacean (malacostracan) Hox genes and the evolution of the arthropod trunk

Representatives of the Insecta and the Malacostraca (higher crustaceans) have highly derived body plans subdivided into several tagma, groups of segments united by a common function and/or morphology. The tagmatization of segments in the trunk, the part of the body between head and telson, in both lineages is thought to have evolved independently from ancestors with a distinct head but a homonomous, undifferentiated trunk. In the branchiopod crustacean, Artemia franciscana, the trunk Hox genes are expressed in broad overlapping domains suggesting a conserved ancestral state (Averof, M. and Akam, M. (1995) Nature 376, 420-423). In comparison, in insects, the Antennapedia-class genes of the homeotic clusters are more regionally deployed into distinct domains where they serve to control the morphology of the different trunk segments. Thus an originally Artemia-like pattern of homeotic gene expression has apparently been modified in the insect lineage associated with and perhaps facilitating the observed pattern of tagmatization. Since insects are the only arthropods with a derived trunk tagmosis tested to date, we examined the expression patterns of the Hox genes Antp, Ubx and abd-A in the malacostracan crustacean Porcellio scaber (Oniscidae, Isopoda). We found that, unlike the pattern seen in Artemia, these genes are expressed in well-defined discrete domains coinciding with tagmatic boundaries which are distinct from those of the insects. Our observations suggest that, during the independent tagmatization in insects and malacostracan crustaceans, the homologous 'trunk' genes evolved to perform different developmental functions. We also propose that, in each lineage, the changes in Hox gene expression pattern may have been important in trunk tagmatization.     

Rusophycus carleyi (James, 1885), Trace Fossils from the Lower Ordovician of Southern Morocco,and the Trilobites that Made Them

Thin-bedded, pyrite-rich, fine sandstones and mudstones of the Floian-Dapingian Upper Fezouata Formation contain abundant trace fossils Rusophycus carleyi in close association with a species of the asaphid trilobite Asaphellus. The sizes and shapes of this trilobite and the traces match closely. Five specimens have even been found where an articulated specimen of Asaphellus appears to be directly located over a specimen of Rusophycus carleyi within a thin bed of sandstone, suggesting that the trilobite animal may have been trapped on top of a trace that it had just made. Such intimate associations between a putative tracemaker and a trace are rare in the fossil record and particularly rare for Trilobita. The number of coxal impressions that form part of R. carleyi, eleven, matches the number expected for an asaphid trilobite (one for each of eight thoracic segments and one for each of three post-oral cephalic appendages). Impressions of the hypostome, thoracic tip impressions, cephalic margin, and pygidial margin in a few of the traces also match those of this asaphid trilobite. R. carleyi has been found in Ordovician strata of other parts of the world in association with asaphid trilobites.     

Early Cambrian phytoplankton diversification and appearance of trilobites in the Swedish Caledonides with implications for coupled evolutionary events between primary producers and consumers

The newly examined Lower Cambrian strata in the Laisvall-Storuman area, central Swedish Caledonides, yield diverse and stratigraphically significant phytoplanktic organic-walled microfossils (acritarchs) associated with the olenellid trilobites of Holmia sp. that appear to be at the lowermost horizon ever recorded in the Caledonides. The acritarchs, recovered throughout the Grammajukku Formation, are taxonomically reviewed in the context of regional and global trends of phytoplankton diversity. The assemblages are assigned to acritarch zones Skiagia ornata-Fimbriaglomerella membranacea and Heliosphaeridium dissimilare-Skiagia ciliosa , corresponding to the Schmidtiellus mickwitzi and Holmia kjerulfi trilobite zones. The records of acritarch radiations and appearances of trilobites and other faunas in Baltica, and on a more interregional scale, are biochronologically correlated, revealing tightly coupled evolutionary events among primary producers and consumers. The timing of early diversifications of trilobites in various faunal provinces is discussed and the relative age of the oldest known non-mineralized arthropods from the Zawiszyn Formation in Poland is estimated.     

Phylogenetic support for the monophyly of proetide trilobites

The monophyly of the order Proetida, the only trilobite group to survive the end‐Devonian mass extinction, has been regularly questioned since its erection almost three decades ago. Through analysis of a novel phylogenetic data set comprising 114 characters coded for 55 taxa, including both traditional members of the Proetida along with a number of other trilobite groups, the monophyly of proetide trilobites is rigorously tested for the first time. Proetida is shown to be monophyletic, united by the initial compound eye formation in early protaspids occurring at the lateral margin rather than the anterior margin, and the form of the protaspid glabella being tapering with a pre‐glabellar field. A number of adult characters, including the possession of a quadrate or shield‐shaped hypostome with angular posterior margins, the hypostome median body being divided by a deep groove that entirely traverses the median body, the presence of an enlarged thoracic spine on the sixth tergite and a tergite count of between 7 and 10, also define the basal node. Hystricurid and dimeropygoid trilobites are shown to resolve at the base of the group, while the remaining proetide taxa are divided between large proetoid and aulacopleuroid clades. Some taxa previously allied with Aulacopleuroidea, such as rorringtoniids and scharyiids, are retrieved as basal members of the Proetoidea.     

Trilobites in Paleozoic carbonate buildups

The trilobite faunas found in carbonate buildups throughout much of the Paleozoic are remarkably similar in both composition and general morphological characteristics. This is primarily the result of the domination of these faunas by a limited number of trilobite families which are long-ranging in the buildup environment. Illaenids are the dominant trilobites in Ordovician-Devonian buildups and are generally accompanied by members of the Lichidae and Cheiruridae. Proetid trilobites are characteristic of Ordovician-Permian buildups but are seldom common. The number of trilobite families found in carbonate buildups is highest in the late Ordovician, with most of the important families persisting into the Devonian. After the Devonian only proetids are found in this environment. The conservative nature of these trilobite faunas suggests that the environmental characteristics of normal-marine Paleozoic carbonate buildups are similar. Trilobita, palaeoecology, faunistics, morphology. carbonate buildups. Palaeozoic .     

The stability of thoracic segmentation in trilobites: a case study in developmental and ecological constraints

The decline in origination rate of new metazoan body plans following the Cambrian radiation has been suggested to reflect developmental canalization in derived taxa, limiting their ability to evolve forms with radically different morphotypes. Segmentation is a fundamental aspect of arthropod body plan, and here we show that a derived trilobite that secondarily converged on a morphotype characteristic of basal members of the clade also reverted to a pattern of segmental variability common among basal trilobites. Hence a secular trend in loss of variability of the trilobite thorax was not due to the evolution of an inviolable developmental constraint. This result challenges the notion of developmental canalization in phylogenetically derived taxa. Rather, early variability in trilobites may be the result of ecological factors that promoted segment-rich thoracic morphotypes during Cambrian time.     

Patterning mechanisms in the body trunk and the appendages of Drosophila.

During evolution, many animal groups have developed specialised outgrowths of the body wall, limbs or appendages. The type of appendage depends on the identity of the segment where they appear, indicating that the Hox genes contribute to appendage specification. Moreover, work carried out principally in Drosophila has identified the gene products and the mechanisms involved in pattern formation in the appendages. In this essay, we compare the morphogenetic processes in the appendages and the body wall; the function of the Hox genes and the response to the signalling molecules involved in local patterning. We speculate that, although the basic mechanisms are similar, there are significant differences in the manner the body trunk and appendages respond to them.     

Gut content fossilization and evidence for detritus feeding habits in an enrolled trilobite from the Cambrian of China

Enrolment was a major defensive strategy for trilobites that significantly contributed to their evolutionary success. The ability to enrol also helped to constrain the morphological evolution of trilobites, which in part was driven by the need to improve this capability to encapsulate the soft parts of the body within the mineralized dorsal exoskeleton. Here, we describe a unique example of gut content fossilization in an enrolled trilobite from the Cambrian of China, and we propose a taphonomic scenario that considers the possible implication of enrolment in this exceptional preservation. A micro‐facies analysis indicates that the specimen was entombed during an obrution event and remained intact due to limited infaunal activity. The encapsulation of the body did not prevent the decay of soft tissues, but it permitted the delicate gut content to be protected during diagenesis. In isolating the decaying soft tissues from the external environment, enrolment might also have favoured the establishment of microenvironmental conditions conducive to the precipitation of pyrite framboids. Within the gut, the formation of such crystals may have led to the consolidation of the ingested material. These results suggest that fossilized gut contents might be quite common in enrolled trilobites. Textural and compositional analyses reveal that the gut content is similar to the sediment surrounding the fossil except for the presence of pyrite framboids that indicate higher initial organic matter content. The complete enrolment of the body argues against an accidental ingestion of this material or a diagenetic origin for it. Accordingly, detritus feeding habits are inferred for this ptychopariid trilobite.     

Humble origins for a successful strategy: complete enrolment in early Cambrian olenellid trilobites

Trilobites are typified by the behavioural and morphological ability to enrol their bodies, most probably as a defence mechanism against adverse environmental conditions or predators. Although most trilobites could enrol at least partially, there is uncertainty about whether olenellids—among the most phylogenetically and stratigraphically basal representatives—could perform this behaviour because of their poorly caudalized trunk and scarcity of coaptative devices. Here, we report complete—but not encapsulating—enrolment for the olenellid genus Mummaspis from the early Cambrian Mural Formation in Alberta, the earliest direct evidence of this strategy in the fossil record of polymerid trilobites. Complete enrolment in olenellids was achieved through a combination of ancestral morphological features, and thus provides new information on the character polarity associated with this key trilobite adaptation.