Lauren Sallan

End-Devonian extinction and a bottleneck in the early evolution of modern jawed vertebrates

The Devonian marks a critical stage in the early evolution of vertebrates: It opens with an unprecedented diversity of fishes and closes with the earliest evidence of limbed tetrapods. However, the latter part of the Devonian has also been characterized as a period of global biotic crisis marked by two large extinction pulses: a “Big Five” mass extinction event at the Frasnian-Famennian stage boundary (374 Ma) and the less well-documented Hangenberg event some 15 million years later at the Devonian-Carboniferous boundary (359 Ma). Here, we report the results of a wide-ranging analysis of the impact of these events on early vertebrate evolution, which was obtained from a database of vertebrate occurrences sampling over 1,250 taxa from 66 localities spanning Givetian to Serpukhovian stages (391 to 318 Ma). We show that major vertebrate clades suffered acute and systematic effects centered on the Hangenberg extinction involving long-term losses of over 50% of diversity and the restructuring of vertebrate ecosystems worldwide. Marine and nonmarine faunas were equally affected, precluding the existence of environmental refugia. The subsequent recovery of previously diverse groups (including placoderms, sarcopterygian fish, and acanthodians) was minimal. Tetrapods, actinopterygians, and chondrichthyans, all scarce within the Devonian, undergo large diversification events in the aftermath of the extinction, dominating all subsequent faunas. The Hangenberg event represents a previously unrecognized bottleneck in the evolutionary history of vertebrates as a whole and a historical contingency that shaped the roots of modern biodiversity.

Persistent predator–prey dynamics revealed by mass extinction

Predator–prey interactions are thought by many researchers to define both modern ecosystems and past macroevolutionary events. In modern ecosystems, experimental removal or addition of taxa is often used to determine trophic relationships and predator identity. Both characteristics are notoriously difficult to infer in the fossil record, where evidence of predation is usually limited to damage from failed attacks, individual stomach contents, one-sided escalation, or modern analogs. As a result, the role of predation in macroevolution is often dismissed in favor of competition and abiotic factors. Here we show that the end-Devonian Hangenberg event (359 Mya) was a natural experiment in which vertebrate predators were both removed and added to an otherwise stable prey fauna, revealing specific and persistent trophic interactions. Despite apparently favorable environmental conditions, crinoids diversified only after removal of their vertebrate consumers, exhibiting predatory release on a geological time scale. In contrast, later Mississippian (359–318 Mya) camerate crinoids declined precipitously in the face of increasing predation pressure from new durophagous fishes. Camerate failure is linked to the retention of obsolete defenses or “legacy adaptations” that prevented coevolutionary escalation. Our results suggest that major crinoid evolutionary phenomena, including rapid diversification, faunal turnover, and species selection, might be linked to vertebrate predation. Thus, interactions observed in small ecosystems, such as Lotka-Volterra cycles and trophic cascades, could operate at geologic time scales and higher taxonomic ranks. Both trophic knock-on effects and retention of obsolete traits might be common in the aftermath of predator extinction.

Heads or tails: staged diversification in vertebrate evolutionary radiations

Adaptive radiations, bouts of morphological divergence coupled with taxonomic proliferation, underpin biodiversity. The most widespread model of radiations assumes a single round, or ‘early burst’, of elevated phenotypic divergence followed by a decline in rates of change or even stasis. A vertebrate-specific model proposes separate stages: initial divergence in postcranial traits related to habitat use, followed by diversification in cranial morphology linked to trophic demands. However, there is little empirical evidence for either hypothesis. Here, we show that, contrary to both models, separate large-scale radiations of actinopterygian fishes proceeded through distinct cranial and later postcranial stages of morphological diversification. Early actinopterygians and acanthomorph teleosts dispersed in cranial morphospace immediately following the end-Devonian extinction and the Cretaceous origin of the acanthomorph clade, respectively. Significant increases in postcranial morphological variation do not occur until one interval after cranial diversification commenced. Therefore, our results question the universality of the ‘general vertebrate model’. Based on the results of model-fitting exercises and application of the divergence order test, we find little evidence that the early onset of cranial diversification in these two radiations is due to elevated rates of cranial change relative to postcranial change early in their evolutionary histories. Instead, postcranial and cranial patterns are best fit by an Ornstein–Uhlenbeck model, which is characterized by constant evolutionary rates coupled with a strong central tendency. Other groups have been reported to show early saturation of cranial morphospace or tropic roles early in their histories, but it is unclear whether these patterns are attributable to dynamics similar to those inferred for our two model radiations.

Major issues in the origins of ray-finned fish (Actinopterygii) biodiversity

Ray‐finned fishes (Actinopterygii) dominate modern aquatic ecosystems and are represented by over 32000 extant species. The vast majority of living actinopterygians are teleosts; their success is often attributed to a genome duplication event or morphological novelties. The remainder are ‘living fossils’ belonging to a few depauperate lineages with long‐retained ecomorphologies: Polypteriformes (bichirs), Holostei (bowfin and gar) and Chondrostei (paddlefish and sturgeon). Despite over a century of systematic work, the circumstances surrounding the origins of these clades, as well as their basic interrelationships and diagnoses, have been largely mired in uncertainty. Here, I review the systematics and characteristics of these major ray‐finned fish clades, and the early fossil record of Actinopterygii, in order to gauge the sources of doubt. Recent relaxed molecular clock studies have pushed the origins of actinopterygian crown clades to the mid‐late Palaeozoic [Silurian–Carboniferous; 420 to 298 million years ago (Ma)], despite a diagnostic body fossil record extending only to the later Mesozoic (251 to 66 Ma). This disjunct, recently termed the ‘Teleost Gap’ (although it affects all crown lineages), is based partly on calibrations from potential Palaeozoic stem‐taxa and thus has been attributed to poor fossil sampling. Actinopterygian fossils of appropriate ages are usually abundant and well preserved, yet long‐term neglect of this record in both taxonomic and systematic studies has exacerbated the gaps and obscured potential synapomorphies. At the moment, it is possible that later Palaeozoic‐age teleost, holostean, chondrostean and/or polypteriform crown taxa sit unrecognized in museum drawers. However, it is equally likely that the ‘Teleost Gap’ is an artifact of incorrect attributions to extant lineages, overwriting both a post‐Palaeozoic crown actinopterygian radiation and the ecomorphological diversity of stem‐taxa.

Body-size reduction in vertebrates following the end-Devonian mass extinction.

The small will inherit the Earth… Understanding how communities and ecosystems recovered from the previous five global extinction events sheds light on how extinctions shape broad patterns of biodiversity. Sallan et al. looked across vertebrate species during and after the Devonian extinction (see the Perspective by Wagner). Small-bodied species, with rapid reproductive rates, dominated post-extinction communities, despite the presence of many successful large-bodied species before the extinction. This pattern mimics, to some degree, current patterns of extinction, suggesting that we might expect similar loss of large-bodied species if we continue along our current path. Science, this issue p. 812; see also p. 736 Similar to ongoing extinctions, the end-Devonian extinction resulted in the loss of most large-bodied vertebrates. [Also see Perspective by Wagner] Following the end-Devonian mass extinction (359 million years ago), vertebrates experienced persistent reductions in body size for at least 36 million years. Global shrinkage was not related to oxygen or temperature, which suggests that ecological drivers played a key role in determining the length and direction of size trends. Small, fast-breeding ray-finned fishes, sharks, and tetrapods, most under 1 meter in length from snout to tail, radiated to dominate postextinction ecosystems and vertebrae biodiversity. The few large-bodied, slow-breeding survivors failed to diversify, facing extinction despite earlier evolutionary success. Thus, the recovery interval resembled modern ecological successions in terms of active selection on size and related life histories. Disruption of global vertebrate, and particularly fish, biotas may commonly lead to widespread, long-term reduction in body size, structuring future biodiversity.

The long-rostrumed elasmobranch Bandringa Zangerl, 1969, and taphonomy within a Carboniferous shark nursery

ABSTRACT The shark Bandringa (Elasmobranchii, Chondrichthyes), from the Pennsylvanian (Moscovian) Lagerstätte of Mazon Creek, Illinois, is notable for an elongated snout constituting up to half of total body length. This genus formerly contained two distinct species (B. rayi and B. herdinae). However, reexamination of all cataloged material from Mazon Creek and similarly aged North American coal measure localities shows that characteristics previously considered diagnostic at the species level can be attributed to differential taphonomy in adjacent marine and non-marine deposits. We find no evidence of morphologically distinct populations. A monospecific Bandringa exhibiting complementary data sets from localities with different modes of preservation provides a more complete picture of hard- and soft-tissue anatomy than resident taxa from a single deposit. Our new reconstruction of Bandringa incorporates several previously unreported features, including ventrally directed jaws, stellate squamation, a branched lateral line, and fin spines bearing smooth costae. Bandringa occupies an unresolved position within total-group Elasmobranchii, but displays similarities with sphenacanthids, hybodontiforms, and other member clades of the stem group. Bandringa is most simply interpreted as a freshwater, benthic, suction-feeding shark, and as a plausible analogue of modern sawfish (Pristidae). Juveniles of the Carboniferous Bandringa appear to have inhabited one of the earliest known shark nurseries at the brackish and marine Mazon Creek before migrating to freshwaters elsewhere.

Tetrapod-like axial regionalization in an early ray-finned fish

Tetrapods possess up to five morphologically distinct vertebral series: cervical, thoracic, lumbar, sacral and caudal. The evolution of axial regionalization has been linked to derived Hox expression patterns during development and the demands of weight-bearing and walking on land. These evolutionary and functional explanations are supported by an absence of similar traits in fishes, living and extinct. Here, I show that, Tarrasius problematicus, a marine ray-finned fish from the Mississippian (Early Carboniferous; 359–318 Ma) of Scotland, is the first non-tetrapod known to possess tetrapod-like axial regionalization. Tarrasius exhibits five vertebral regions, including a seven-vertebrae ‘cervical’ series and a reinforced ‘sacrum’ over the pelvic area. Most vertebrae possess processes for intervertebral contact similar to tetrapod zygapophyses. The fully aquatic Tarrasius evolved these morphologies alongside other traits convergent with early tetrapods, including a naked trunk, and a single median continuous fin. Regional modifications in Tarrasius probably facilitated pelagic swimming, rather than a terrestrial lifestyle or walking gait, presenting an alternative scenario for the evolution of such traits in tetrapods. Axial regionalization in Tarrasius could indicate tetrapod-like Hox expression patterns, possibly representing the primitive state for jawed vertebrates. Alternately, it could signal a weaker relationship, or even a complete disconnect, between Hox expression domains and vertebrate axial plans.

An inverse latitudinal gradient in speciation rate for marine fishes

Far more species of organisms are found in the tropics than in temperate and polar regions, but the evolutionary and ecological causes of this pattern remain controversial1,2. Tropical marine fish communities are much more diverse than cold-water fish communities found at higher latitudes3,4, and several explanations for this latitudinal diversity gradient propose that warm reef environments serve as evolutionary ‘hotspots’ for species formation5–8. Here we test the relationship between latitude, species richness and speciation rate across marine fishes. We assembled a time-calibrated phylogeny of all ray-finned fishes (31,526 tips, of which 11,638 had genetic data) and used this framework to describe the spatial dynamics of speciation in the marine realm. We show that the fastest rates of speciation occur in species-poor regions outside the tropics, and that high-latitude fish lineages form new species at much faster rates than their tropical counterparts. High rates of speciation occur in geographical regions that are characterized by low surface temperatures and high endemism. Our results reject a broad class of mechanisms under which the tropics serve as an evolutionary cradle for marine fish diversity and raise new questions about why the coldest oceans on Earth are present-day hotspots of species formation.Contrary to previous hypotheses, high-latitude fish lineages form new species at much faster rates than their tropical counterparts especially in geographical regions that are characterized by low surface temperatures and high endemism.

The nearshore cradle of early vertebrate diversification

Shallow-water diversification Most of what we know about the relationship between diversification and environment in ancient marine environments has come from invertebrates. The influence of habitat on vertebrate diversification thus remains a persistent question. Sallan et al. studied fossil vertebrates spanning the mid-Paleozoic, including both jawed and jawless fish (see the Perspective by Pimiento). They found that diversification occurred primarily in nearshore environments, with diversified forms later colonizing deeper marine or freshwater habitats. Furthermore, more robust forms remained in the nearshore, whereas more gracile forms moved to deeper waters. This split is similar to current relationships between form and environment in aquatic habitats. Science, this issue p. 460; see also p. 402 Nearshore environments hosted diversification among mid-Paleozoic vertebrates. Ancestral vertebrate habitats are subject to controversy and obscured by limited, often contradictory paleontological data. We assembled fossil vertebrate occurrence and habitat datasets spanning the middle Paleozoic (480 million to 360 million years ago) and found that early vertebrate clades, both jawed and jawless, originated in restricted, shallow intertidal-subtidal environments. Nearshore divergences gave rise to body plans with different dispersal abilities: Robust fishes shifted shoreward, whereas gracile groups moved seaward. Fresh waters were invaded repeatedly, but movement to deeper waters was contingent upon form and short-lived until the later Devonian. Our results contrast with the onshore-offshore trends, reef-centered diversification, and mid-shelf clustering observed for benthic invertebrates. Nearshore origins for vertebrates may be linked to the demands of their mobility and may have influenced the structure of their early fossil record and diversification.

An examination of the Devonian fishes of Michigan

We surveyed the taxa, ecosystems, and localities of the Devonian fishes of Michigan to provide a framework for renewed study, to learn about the diversity and number of these fishes, and to investigate their connection to other North American faunas. Nineteen genera of fishes have been found in the Middle and Late Devonian deposits of Michigan, of which thirteen are ‘placoderms’ represented by material ranging from articulated head shields to ichthyoliths. As expected from the marine nature of these deposits, ‘placoderms’ are overwhelmingly arthrodire in nature, but two genera of ptyctodonts have been reported along with less common petalichthyid material. The remaining fish fauna consists of fin-spines attributed to ‘acanthodians’, two genera of potential crown chondrichthyans, an isolated dipnoan, and onychodont teeth/jaw material. There was an apparent drop in fish diversity and fossil abundance between Middle and Late Devonian sediments. This pattern may be attributed to a paucity of Late Devonian sites, along with a relative lack of recent collection efforts at existing outcrops. It may also be due to a shift towards open water pelagic environments at Late Devonian localities, as opposed to the nearshore reef fauna preserved in the more numerous Middle Devonian localities. The Middle Devonian vertebrate fauna in Michigan shows strong connections with same-age assemblages from Ohio and New York. Finally, we document the presence of partially articulated vertebrate remains associated with benthic invertebrates, an uncommon occurrence in Devonian strata outside of North America. We anticipate this new survey will guide future field work efforts in an undersampled yet highly accessible region that preserves an abundance of fishes from a critical interval in marine vertebrate evolution.