The Permian–Triassic mass extinction interval was an important time in the evolutionary history of the echinoderms. Details of the extinction and, in particular the immediate post-extinction recovery in the Early Triassic, are seldom addressed because of a perception that the Permian–Triassic echinoderm fossil record is too poor. However, only the Holothuroidea and Asteroidea lack any Early Triassic fossil representatives. Even in these groups, details of the extinction and recovery can be inferred from recent cladistic analyses. The Holothuroidea are unique amongst the echinoderms in showing no family level extinction through the Permian–Triassic interval, possibly due to their deposit-feeding lifestyle. In contrast, the Echinoidea, Crinoidea and probably the Asteroidea underwent severe evolutionary bottlenecks during that time. In the echinoids, significant post-Permian radiation occurred from the Late Triassic (Carnian), although it may have begun in the Early Triassic. In the Crinoidea, fossil diversity increases dramatically from the Late Ladinian, although cladistic analyses suggest that initial diversification took place in the Earliest Triassic (Induan). Many undescribed crinoid remains from Lower Triassic strata worldwide also imply that the post-Permian radiation in this group may have been more rapid than currently thought. Locally in the Spathian, crinoid ossicles may approach rock-building densities. The presence of at least seven Early Triassic fossil ophiuroid species may indicate rapid post-Permian radiation in the Ophiuroidea, although the higher level affinities of these taxa are presently unresolved and the Late Permian record is poorly known. Ophiuroid remains are the most diverse echinoderm fossils during the Early Triassic, comprising both complete body fossils and disarticulated ossicles. Holothuroids possibly radiated in the Early Triassic, but current evidence from cladistic analysis favours a largely Anisian age for the post-Permian radiation in this group. All known Early Triassic echinoderms were small-sized animals that inhabited very shallow, oxygenated, low palaeolatitude environments within wave base. .
The Permian–Triassic (P–Tr) interval witnessed the largest extinction event of the Phanerozoic, which heralded a dramatic reorganisation of the marine biosphere. The extinction crisis was demonstrably selective, with many groups suffering complete, or very near, annihilation, while others escaped relatively unscathed
While this remains true for some taxa (e.g., the Asteroidea) it is not true for others (e.g., the Ophiuroidea). In addition, echinoderms are one of the few invertebrate groups whose skeletal remains possess enough morphological characters to provide meaningful cladistic analyses. A rigorous cladistic phylogeny can provide details on the timing and nature of extinction and radiation even if the actual fossil record is relatively sparse (e.g.,
Understanding changes in diversity is only half the story, Droser et al.
Our aim is to detail the Late Permian and Early Triassic fossil records of the individual classes of the Echinodermata and to review the current data pertaining to their initial post-extinction recovery in the immediate aftermath of the Late Permian crisis. The most recent cladistic analyses will be discussed. In addition, we will describe the palaeoenvironmental distribution of the fossils and discuss the palaeoecology and life habits of the Early Triassic echinoderms in order to provide a more detailed understanding of the survival and initial recovery of these animals.
Crinoids were one of the major constituents of Palaeozoic benthic communities. However, they suffered a severe bottleneck at or near the P–Tr boundary, recording the most striking decline of all the echinoderm groups (e.g.,
According to Simms et al.
The Articulata was once considered to include only Triassic to Recent crinoids. However, now the Articulata also includes some Palaeozoic families, such as the Ampelocrinidae, Cymbiocrinidae, Calceolispongiidae, and Tribrachyocrinidae
Until now,
Prior to the first occurrence of
After the Holocrinidae, the next families to appear in the fossil record are the Dadocrinidae, recorded from the very Latest Olenekian, followed by the Encrinidae in the Early Anisian
Morphological cladistic analysis by Simms
Only three ophiuroid taxa have been described from Upper Permian strata, all from China:
In contrast to the sparse and relatively localised Late Permian record, ophiuroid fossils are quite abundant in Lower Triassic strata worldwide (
Despite these common and well-preserved specimens, phylogenetic relationships between Palaeozoic and Mesozoic ophiuroids remain obscure. The current classification of fossil Ophiuroidea is so unsatisfactory that most taxa at genus level and above are probably paraphyletic or even polyphyletic
Despite these taxonomic and phylogenetic problems, the high diversity of Early Triassic ophiuroids is probably good evidence that they did not suffer any evolutionary bottleneck during the P–Tr interval, in contrast to the Crinoidea and Echinoidea. Modern ophiuroids are known to be very tolerant of low salinities and low oxygen levels
Lower Triassic strata also contain abundant trace fossil evidence for the presence of ophiuroids, namely the resting trace (cubichnium)
The palaeoenvironmental distribution of
Morphological analysis of the known Early Triassic ophiuroids shows them to be small-bodied animals (maximum disk diameters of 10 mm, typically less than 5 mm) with relatively short arms of less than 3x the disk diameter
The P–Tr fossil record of the Asteroidea is very poor indeed. Only two genera of asteroid (
Only three genera (
Many extant asteroids are voracious predators. The radiation of the crown group Asteroidea would have had important consequences for many benthic invertebrates and has been implicated as the major reason for the failure of articulate brachiopods to regain their pre-Mesozoic dominance and diversity
Current evidence indicates that an initial post-Permian diversification of the Neoasteroidea occurred near the Olenekian-Anisian boundary (
The only other Triassic asteroid is
The P–Tr evolutionary history of echinoids is often cited as an example of the dramatic and far-reaching effects of the Late Permian mass extinction event (e.g.,
Two echinoid families are recorded as fossils in the Late Permian: the Lepidocentridae and Miocidaridae
Two fossil genera assigned to the Miocidaridae have been recorded from Lower Triassic strata.
No new families appear in the fossil record until the Carnian and very low levels of diversity were apparently maintained for at least the duration of the Early and Middle Triassic. However, as with the crinoid fossil record, numerous undescribed echinoid spines and other remains have been noted in Early Triassic fossil assemblages: e.g., from the Griesbachian of Oman
Post-Permian echinoids are divided into two subclasses: the Cidaroidea (comprising the families Miocidaridae and Cidaridae) and the Euechinoidea (comprising all the remaining echinoid taxa). Morphological data from tooth construction and stereom microstructure indicate that these two sister taxa must have diverged before the Late Permian
When calibrated to the fossil record, the recent phylogenetic analyses (e.g.,
Compared to other echinoderm classes, holothuroids have low preservation potential and the fossil record of this class is poor. For example, Gilliland
Simply counting the presence or absence of fossil taxa indicates that there was no diversity decline at the family level through the P–Tr boundary
Sheehan et al
From their phylogenetic analysis, Kerr and Kim
The different echinoderm classes appear, on the often-limited evidence available, to have experienced different patterns of evolution through the Permian–Triassic interval. Significant evolutionary bottlenecks are recorded in the Crinoidea, Echinoidea and possibly Asteroidea, whereas in the Holothuroidea no family-level extinction is evident. The preferential survival of the Holothuroidea may be due to their deposit-feeding mode of life, which may have conferred a selective advantage during primary productivity collapse. In the Early Triassic, the relative high diversity of the Ophiuroidea may indicate rapid post-Permian recovery and radiation, or may simply be due to biases in the fossil record. In the Holothuroidea and Asteroidea, phylogenetic analyses imply that radiation most likely occurred in the very Latest Spathian and Anisian. Current evidence suggests that significant radiation did not occur in the Echinoidea or Crinoidea until later in the Triassic, although the presence of many undescribed crinoid and echinoid fossils from Lower Triassic rocks worldwide suggests that this view may be revised in the future. Details of the P–Tr evolutionary history of the Holothuroidea and Asteroidea are masked by a lack of Early Triassic fossils and a large number of Early Triassic Lazarus taxa in these clades. In contrast, despite the presence of an abundant Early Triassic fossil record, understanding the evolution of the Ophiuroidea through this interval is hampered by unresolved taxonomic problems. Echinoderm taxa that are present in Lower Triassic strata are invariably smaller than Palaeozoic or later Mesozoic taxa. Small body size is a characteristic of Early Triassic marine organisms and is likely due to prevailing environmental conditions, such as anoxia or low primary productivity levels (i.e. low food supply). There are still many unresolved questions concerning the Permian–Triassic evolutionary history of the Echinodermata. Future fossil discoveries and advances in phylogenetic analysis will surely increase our understanding of this important episode in echinoderm evolution.
This work was undertaken during tenure of a Japanese Society for the Promotion of Science (JSPS) Research Fellowship to RJT. We thank Andrew Smith (Natural History Museum, London) and Mike Simms (Ulster Museum, Belfast) for thorough and very helpful reviews.
Permian–Triassic evolutionary history of the Crinoidea. Thick solid lines show actual taxon ranges from first appearance in the fossil record. Thin solid lines indicate phylogenetic relationships. Dashed lines indicate ghost ranges of known taxa, inferred from the phylogeny. Note, the phylogenetic relationships of the Millericrinidae, Dadocrinidae, Isocrinidae, Holocrinidae and Encrinidae derive from cladistic analysis
Fig. 1. Histoire de l'évolution des crinoïdes au cours du Permo-Trias. Les traits épais continus donnent la distribution des taxons depuis leur première apparition dans les annales paléontologiques. Les traits minces continus indiquent les relations phylogénétiques. Les tirets indiquent la distribution supposée des taxons connus, déduite de la phylogénie. Remarquer que les relations phylogénétiques des Millericrinidae, des Dadocrinidae, des Isocrinidae, des Holocrinidae et des Encrinidae sont déduites des analyses cladistiques
Permian–Triassic fossil record of the Ophiuroidea. Thick solid lines show ranges of described fossil genera (see text for details). Dashed lines show Lazarus intervals. Thin solid line shows possible range extension of
Fig. 2. Distribution des Ophiuroidea fossiles du Permo-Trias. Les traits épais continus donnent la distribution des genres fossiles cités (détails dans le texte). Les tirets représentent les intervalles correspondant aux formes Lazare. Le trait fin continu indique l'intervalle de distribution possible de Preaplocoma, dans la mesure où les ossicules désarticulés des couches sous-jacentes peuvent effectivement être rapportés à ce taxon (voir détails dans le texte). Remarquer qu'aucune relation phylogénétique n'est proposée, parce qu'aucun des taxons fossiles mentionné du Permien supérieur ou du début du Trias n'a été inclus dans une analyse phylogénétique récente (cf., par exemple,
Late Permian to Early Jurassic evolutionary history of the Asteroidea. Thick solid lines show actual taxon ranges from the first appearance in the fossil record. Thin solid lines indicate phylogenetic relationships. Dashed lines indicate ghost ranges of known taxa, inferred from the phylogeny. The generic-level cladistic analysis of Blake and Hagdorn
Fig. 3. Histoire de l'évolution des Asteroidea du Permien supérieur au Jurassique inférieur. Les traits épais continus donnent la distribution des taxons depuis leur première apparition dans les annales paléontologiques. Les traits minces continus indiquent les relations phylogénétiques. Les tirets indiquent la distribution supposée des taxons connus, déduite de la phylogénie. La représentation phylogénétique a utilisé les résultats de l'analyse cladistique au niveau générique réalisée par Blake et Hagdorn
Permian–Triassic evolutionary history of the Echinoidea. Thick solid lines indicate actual taxon ranges from the first appearance in the fossil record. Thin solid lines indicate the phylogenetic relationships of the majority rule consensus tree from the total evidence analysis of Littlewood and Smith
Fig. 4. Histoire de l'évolution des Echinoidea au cours du Permo-Trias. Les traits épais continus donnent la distribution des taxons depuis leur première apparition dans les annales paléontologiques. Les traits minces continus indiquent les relations phylogénétiques, objets d'un large consensus, d'après les analyses de Littlewood et Smith
Permian–Triassic evolutionary history of the Holothuroidea. Thick solid lines show actual family ranges from the first appearance in the fossil record. Thin solid lines indicate the phylogenetic relationships of Kerr and Kim
Fig. 5. Histoire de l'évolution des Holothuroidea au cours du Permo-Trias. Les traits épais continus donnent la distribution des familles depuis leur première apparition dans les annales paléontologiques. Les traits minces continus indiquent les relations phylogénétiques d'après Kerr et Kim