Tectonic trigger to the first major extinction of the Phanerozoic: The early Cambrian Sinsk event.

The Cambrian explosion, one of the most consequential biological revolutions in Earth history, occurred in two phases separated by the Sinsk event, the first major extinction of the Phanerozoic. Trilobite fossil data show that Series 2 strata in the Ross Orogen, Antarctica, and Delamerian Orogen, Australia, record nearly identical and synchronous tectono-sedimentary shifts marking the Sinsk event. These resulted from an abrupt pulse of contractional supracrustal deformation on both continents during the Pararaia janeae trilobite Zone. The Sinsk event extinction was triggered by initial Ross/Delamerian supracrustal contraction along the edge of Gondwana, which caused a cascading series of geodynamic, paleoenvironmental, and biotic changes, including (i) loss of shallow marine carbonate habitats along the Gondwanan margin; (ii) tectonic transformation to extensional tectonics within the Gondwanan interior; (iii) extrusion of the Kalkarindji large igneous province; (iv) release of large volumes of volcanic gasses; and (v) rapid climatic change, including incursions of marine anoxic waters and collapse of shallow marine ecosystems.

Gill function in an early arthropod and the widespread adoption of the countercurrent exchange mechanism.

Rising but fluctuating oxygen levels in the Early Palaeozoic provide an environmental context for the radiation of early metazoans, but little is known about how mechanistically early animals satisfied their oxygen requirements. Here we propose that the countercurrent gaseous exchange, a highly efficient respiratory mechanism, was effective in the gills of the Late Ordovician trilobite Triarthrus eatoni. In order to test this, we use computational fluid dynamics to simulate water flow around its gills and show that water velocity decreased distinctly in front of and between the swollen ends, which first encountered the oxygen-charged water, and slowed continuously at the mid-central region, forming a buffer zone with a slight increase of the water volume. In T. eatoni respiratory surface area was maximized by extending filament height and gill shaft length. In comparison with the oxygen capacity of modern fish and crustaceans, a relatively low weight specific area in T. eatoni may indicate its low oxygen uptake, possibly related to a less active life mode. Exceptionally preserved respiratory structures in the Cambrian deuterostome Haikouella are also consistent with a model of countercurrent gaseous exchange, exemplifying the wide adoption of this strategy among early animals.

Developmental and functional controls on enrolment in an ancient, extinct arthropod.

Three-dimensional models reveal how the mechanics of exoskeletal enrolment changed during the development of a model organism for insights into ancient arthropod development, the 429-million-year-old trilobite Aulacopleura koninckii. Changes in the number, size and allocation of segments within the trunk, coupled with the need to maintain effective exoskeletal shielding of soft tissue during enrolment, necessitated a transition in enrolment style about the onset of mature growth. During an earlier growth phase, enrolment was sphaeroidal, with the venter of the trunk fitting exactly against that of the head. In later growth, if lateral exoskeletal encapsulation was to be maintained trunk length proportions did not permit such exact fitting, requiring an alternative, non-sphaeoridal enrolment style. Our study favours the adoption of a posture in later growth in which the posterior trunk extended beyond the front of the head. This change in enrolment accommodated a pattern of notable variation in the number of mature trunk segments, well known to characterize the development of this species. It suggests how an animal whose early segmental development was remarkably precisely controlled was able to realize the marked variation in mature segment number that was related, apparently, to life in a physically challenging, reduced oxygen setting.

Revision of F. R. C. Reeds Ordovician trilobite types from Myanmar (Burma) and western Yunnan Province, China.

The field collections made from Burma (Myanmar) by the Geological Survey of India, and described by F.R.C. Reed more than a century ago, still provide the only ground truthing for an important region of the Ordovician marginal terranes fringing Gondwana. A revision of these faunas is overdue, particularly as it is likely that further collections cannot be made in the northern Shan State in the near future. The specimens, stored in the Geological Survey of India collections in Kolkata, cannot be loaned. Sixteen species are fully revised herein; another twelve species are left under open nomenclature because of inadequacies in the material. Several of Reeds species subsequently became type species of genera that have proved to be widespread: Birmanites Sheng, 1934, Encrinurella Reed, 1915, Neseuretinus Dean, 1967, and Pliomerina Chugaeva, 1956. Reeds Ordovician trilobite collections came from two main areas: northern Shan State (Myanmar), and westernmost Yunnan (China). The Burmese (Myanmar) collections are from the Upper Ordovician (Katian) while Yunnan specimens are from the Middle Ordovician (Darriwilian), though Upper Ordovician trilobites also occur in the area. Both collections are predominantly from clastic strata. Based on a small new Katian collection from Pupiao, we report Neseuretinus birmanicus (Reed, 1906) in common between the northern part of the Shan State and western Yunnan. A few genera (Dionide Barrande, 1847, Phorocephala Lu, 1957, Lonchodomas Angelin, 1854, Nileus Dalman, 1827) are distributed worldwide, and include pelagic (Phorocephala) or deeper benthic (Dionide) taxa. The palaeogeographic comparisons offered by the other taxa are mostly peri-Gondwanan and extend from southwest China westwards (present geography) as far as the Iberian Pennsula. Birmanites is the type genus of a subfamily (Birmanitinae Kobayashi, 1960, revived herein) widely distributed over Ordovician Gondwana, and absent from Laurentia, Baltica and North China/Siberia. Mioptychopyge Zhou, Dean, Yuan Zhou, 1998, probably belongs with the same group and is otherwise known from South China. Parillaenus Jaanusson, 1954, is also peripheral Gondwanan, as is Prionocheilus Rouault, 1847. The Reedocalymeninae Kobayashi, 1951 (Neseuretinus, Reedocalymene Kobayashi, 1951) are similarly diagnostic of periGondwanan sites. However, some genera (Pliomerina, Encrinurella, Ovalocephalus Koroleva, 1959) have been associated with other oriental and Australian occurrences in particular, with outliers in certain terranes in Kazakhstan, i.e. palaeotropical Gondwana.

Enduring evolutionary embellishment of cloudinids in the Cambrian.

The Ediacaran-Cambrian transition and the following Cambrian Explosion are among the most fundamental events in the evolutionary history of animals. Understanding these events is enhanced when phylogenetic linkages can be established among animal fossils across this interval and their trait evolution monitored. Doing this is challenging because the fossil record of animal lineages that span this transition is sparse, preserved morphologies generally simple and lifestyles in the Ediacaran and Cambrian commonly quite different. Here, we identify derived characters linking some members of an enigmatic animal group, the cloudinids, which first appeared in the Late Ediacaran, to animals with cnidarian affinity from the Cambrian Series 2 and the Miaolingian. Accordingly, we present the first case of an animal lineage represented in the Ediacaran that endured and diversified successfully throughout the Cambrian Explosion by embellishing its overall robustness and structural complexity. Among other features, dichotomous branching, present in some early cloudinids, compares closely with a cnidarian asexual reproduction mode. Tracking this morphological change from Late Ediacaran to the Miaolingian provides a unique glimpse into how a primeval animal group responded during the Cambrian Explosion.

The trilobite upper limb branch is a well-developed gill.

Whether the upper limb branch of Paleozoic "biramous" arthropods, including trilobites, served a respiratory function has been much debated. Here, new imaging of the trilobite Triarthrus eatoni shows that dumbbell-shaped filaments in the upper limb branch are morphologically comparable with gill structures in crustaceans that aerate the hemolymph. In Olenoides serratus, the upper limb's partial articulation to the body via an extended arthrodial membrane is morphologically comparable to the junction of the respiratory book gill of Limulus and differentiates it from the typically robust exopod junction in Chelicerata or Crustacea. Apparently limited mechanical rotation of the upper branch may have protected the respiratory structures. Partial attachment of the upper branch to the body wall may represent an intermediate state in the evolution of limb branch fusion between dorsal attachment to the body wall, as in Radiodonta, and ventral fusion to the limb base, as in extant Euarthropoda.

Positional specification in the segmental growth pattern of an early arthropod.

In many arthropods, there is a change in relative segment size during post-embryonic development, but how segment differential growth is produced is little known. A new dataset of the highest quality specimens of the 429 Myr old trilobite Aulacopleura koninckii provides an unparalleled opportunity to investigate segment growth dynamics and its control in an early arthropod. Morphometric analysis across nine post-embryonic stages revealed a growth gradient in the trunk of A. koninckii. We contrastively tested different growth models referable to two distinct hypotheses of growth control for the developing trunk: (i) a segment-specific control, with individual segments having differential autonomous growth progression, and (ii) a regional control, with segment growth depending on their relative position along the main axis. We show that the trunk growth pattern of A. koninckii was consistent with a regional growth control producing a continuous growth gradient that was stable across all developmental stages investigated. The specific posterior-to-anterior decaying shape of the growth gradient suggests it deriving from the linear transduction of a graded signal, similar to those commonly provided by morphogens. A growth control depending on a form of positional specification, possibly realized through the linear interpretation of a graded signal, may represent the primitive condition for arthropod differential growth along the main body axis, from which the diverse and generally more complex forms of growth control in subsequent arthropods have evolved.

Developmental trait evolution in trilobites.

We performed a tree-based analysis of trilobite postembryonic development in a sample of 60 species for which quantitative data on segmentation and growth increments between putative successive instars are available, and that spans much of the temporal, phylogenetic, and habitat range of the group. Three developmental traits were investigated: the developmental mode of trunk segmentation, the average per-molt growth rate, and the conformity to a constant per-molt growth rate (Dyar's rule), for which an original metric was devised. Growth rates are within the normal range with respect to other arthropods and show overall conformity to Dyar's rule. Randomization tests indicate statistically significant phylogenetic signal for growth in early juveniles but not in later stages. Among five evolutionary models fit via maximum likelihood, one in which growth rates vary independently among species, analogous to Brownian motion on a star phylogeny, is the best supported in all ontogenetic stages, although a model with a single, stationary peak to which growth rates are attracted also garners nontrivial support. These results are not consistent with unbounded, Brownian-motion-like evolutionary dynamics, but instead suggest the influence of an adaptive zone. Our results suggest that developmental traits in trilobites were relatively labile during evolutionary history.

The magnitude and duration of Late Ordovician-Early Silurian glaciation.

Understanding ancient climate changes is hampered by the inability to disentangle trends in ocean temperature from trends in continental ice volume. We used carbonate "clumped" isotope paleothermometry to constrain ocean temperatures, and thereby estimate ice volumes, through the Late Ordovician-Early Silurian glaciation. We find tropical ocean temperatures of 32° to 37°C except for short-lived cooling by ~5°C during the final Ordovician stage. Evidence for ice sheets spans much of the study interval, but the cooling pulse coincided with a glacial maximum during which ice volumes likely equaled or exceeded those of the last (Pleistocene) glacial maximum. This cooling also coincided with a large perturbation of the carbon cycle and the Late Ordovician mass extinction.

Strength in numbers: High phenotypic variance in early Cambrian trilobites and its evolutionary implications.

Analysis of the degree of intraspecific morphological polymorphism during the evolutionary history of trilobites using an informatic approach(1) provides striking evidence of a long-suspected but previously unsubstantiated pattern: degrees of polymorphism are markedly higher in phylogenetically basal, stratigraphically early species. This unequivocal pattern prompts further exploration of the relationship between microevolutionary variance and macroevolutionary history. It demonstrates that the 'traditional' fossil record of skeletonized organisms can provide unique insight into questions of major evolutionary interest.

Evaluating paedomorphic heterochrony in trilobites: the case of the diminutive trilobite Flexicalymene retrorsa minuens from the Cincinnatian Series (Upper Ordovician), Cincinnati region.

Flexicalymene retrorsa minuens from the uppermost 3 m of the Waynesville Formation of the Cincinnatian Series (Upper Ordovician) of North America lived approximately 445 Ma and exhibited marked reduction in maximum size relative to its stratigraphically subjacent sister subspecies, Flexicalymene retrorsa retrorsa. Phylogenetic analysis is consistent with the notion that F. retrorsa retrorsa was the ancestor of F. retrorsa minuens. F. retrorsa minuens has been claimed to differ from F. retrorsa retrorsa"in size alone," and thus presents a plausible example of global paedomorphic evolution in trilobites. Despite strong similarity in the overall form of the two subspecies, F. retrorsa minuens is neither a dwarf nor a simple progenetic descendant of F. retrorsa retrorsa. More complex patterns of global heterochronic paedomorphosis, such as a neotonic decrease in the rate of progress along a common ontogenetic trajectory with respect to size, coupled with growth cessation at a small size, "sequential" progenesis, or non-uniform changes in the rate of progress along a shared ontogenetic trajectory with respect to size, can also be rejected. Rather, differences between these subspecies are more consistent with localized changes in rates of character development than with a global heterochronic modification of the ancestral ontogeny. The evolution of F. retrorsa minuens from F. retrorsa retrorsa was largely dominated by modifications of the development of characters already evident in the ancestral ontogeny, not by the origin of novel structures. Factors promoting size reduction in F. retrorsa minuens appear to have been specific to this subspecies, because other co-occurring taxa, including other trilobite species, do not show marked differences in mean size.

Terminal addition, the Cambrian radiation and the Phanerozoic evolution of bilaterian form.

We examine terminal addition, the process of addition of serial elements in a posterior subterminal growth zone during animal development, across modern taxa and fossil material. We argue that terminal addition was the basal condition in Bilateria, and that modification of terminal addition was an important component of the rapid Cambrian evolution of novel bilaterian morphology. We categorize the often-convergent modifications of terminal addition from the presumed ancestral condition. Our focus on terminal addition and its modification highlights trends in the history of animal evolution evident in the fossil record. These trends appear to be the product of departure from the initial terminal addition state, as is evident in evolutionary patterns within-fossil groups such as trilobites, but is also more generally related to shifts in types of morphologic change through the early Phanerozoic. Our argument is contingent on dates of metazoan divergence that are roughly convergent with the first appearance of metazoan fossils in the latest Proterozoic and Cambrian, as well as on an inference of homology of terminal addition across bilaterian Metazoa.

Development of the caudal exoskeleton of the pliomerid trilobite Hintzeia plicamarginis new species.

The later juvenile ontogeny of the caudal plate of the early Ordovician pliomerid trilobite Hintzeia plicamarginis new species likely comprised an initial phase during which the rate of appearance of new segments subterminally exceeded that of segment release into the thorax, a short phase of constant segment numbers, and a later phase during which release occurred but in which no new segments appeared. A distinct terminal region became manifest in the second phase. During the second and third phases growth coefficients for individual segments were about 1.1--1.2 per instar. Although the shapes of segments varied during growth, the pattern of ontogenetic shape change appears to have been broadly similar among segments. This suggests an homonomous trunk segment morphology regardless of thoracic or caudal identity in maturity. These results imply that control of trunk exoskeletal segment appearance and articulation were decoupled in this trilobite, and that the terminal region had a distinct mature morphology. H. plicamarginis is described as a new species.

Exploring developmental modes in a fossil arthropod: growth and trunk segmentation of the trilobite Aulacopleura konincki.

Trilobites offer the opportunity to explore postembryonic development within the fossil record of arthropod evolution. In contrast to most trilobites, the Silurian proetid Aulacopleura konincki from the Czech Republic exhibits marked variation in the mature number of thoracic segments, with five morphs with 18-22 thoracic segments. The combination of abundant articulated specimens available from a narrow stratigraphic interval and segmental intraspecific variation makes this trilobite singularly useful for studying postembryonic growth and segmentation. Trunk segmentation followed a hemianamorphic pattern, as seen in other arthropods and as characteristic of the Trilobita; during a first anamorphic phase, segments were accreted, while in the subsequent epimorphic phase, segmentation did not proceed further despite continued growth. Size increment during the anamorphic phase was targeted and followed Dyar's rule, a geometric progression typical of many arthropods. We consider alternative hypotheses for the control of the switch from anamorphic to epimorphic phases of development. Our analysis favors a scenario in which the mature number of thoracic segments was determined quite early in development rather than at a late stage in association with a critical size threshold. This study demonstrates that hypotheses concerning developmental pattern and control can be tested in organisms belonging to an extinct clade.

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.

Trilobite tagmosis and body patterning from morphological and developmental perspectives.

The Trilobita were characterized by a cephalic region in which the biomineralized exoskeleton showed relatively high morphological differentiation among a taxonomically stable set of well defined segments, and an ontogenetically and taxonomically dynamic trunk region in which both exoskeletal segments and ventral appendages were similar in overall form. Ventral appendages were homonomous biramous limbs throughout both the cephalon and trunk, except for the most anterior appendage pair that was antenniform, preoral, and uniramous, and a posteriormost pair of antenniform cerci, known only in one species. In some clades trunk exoskeletal segments were divided into two batches. In some, but not all, of these clades the boundary between batches coincided with the boundary between the thorax and the adult pygidium. The repeated differentiation of the trunk into two batches of segments from the homonomous trunk condition indicates an evolutionary trend in aspects of body patterning regulation that was achieved independently in several trilobite clades. The phylogenetic placement of trilobites and congruence of broad patterns of tagmosis with those seen among extant arthropods suggest that the expression domains of trilobite cephalic Hox genes may have overlapped in a manner similar to that seen among extant arachnates. This, coupled with the fact that trilobites likely possessed ten Hox genes, presents one alternative to a recent model in which Hox gene distribution in trilobites was equated to eight putative divisions of the trilobite body plan.