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

Abstract

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.T he rise of jawed vertebrates (gnathostomes) throughout the Devonian (416 to 359 Ma) (1) and into the post-Devonian is one of the key episodes in vertebrate evolution (2, 3). This interval encompasses well-known early diversification events, including those of Osteichthyes (bony fishes: ray-finned Actinopterygii and lobe-finned Sarcopterygii, including tetrapods), Chondrichthyes (cartilaginous fishes: Elasmobranchii and Holocephalii), and Placodermi and Acanthodii (extinct groups of debated affinity to extant gnathostomes) (2-5). What is less well known, although apparent from cursory surveys, is that the gnathostome biota underwent major changes over the Devonian-Mississippian divide (3, 5). Placoderms, sarcopterygians, and acanthodians are replaced by chondrichthyans, actinopterygians, and tetrapods, occupying a wider range of ecological roles and dominating all succeeding biotas (3,5,6). This faunal transformation has been subjected to few analyses, and explanations have tended to focus on gradual replacement (2, 7) and competitive displacement (8).However, the Devonian-Mississippian vertebrate succession also fits a characteristic pattern of large-scale mass extinction and subsequent refilling of niche space (9). The impact of global events on biodiversity has been established by studies of dinosaurmammal turnover at the end-Cretaceous (3, 5, 9) and the decimation and restructuring of...

Persistent predator–prey dynamics revealed by mass extinction

“…The Paleozoic apex of crinoid diversity likely required the separate mass extinction of predatory fishes at the Hangenberg event (Figs. 1 and 2) (11,12). This pattern of suppression and release supports hypotheses of significant vertebrate-crinoid trophic interaction during the MPMR interval of prey escalation (2,6,9).…”

“…In contrast, the Mississippian vertebrate radiation was defined by crushing predators. Crushers represent 57% (40 of 71) of all chondrichthyans by the end of the Tournaisian vs. 21% (8 of 37) of the smaller Famennian shark fauna (11).…”

“…This resulted in 671 camerate and advanced cladid occurrences and 416 vertebrate occurrences (SI Appendix, Supporting Methods and Discussion and Table S2). Serpukhovian 2 was excluded from results presented in the text because of poor sampling of crinoids, as well as vertebrates outside the Lagerstätten of Bear Gulch, Montana (11). This phenomenon reflects the relative lack of preserved marine rocks from the upper Serpukhovian.…”

“…This has been linked to increased predation from nektonic ammonoids, arthropods, and especially jawed vertebrates-all devastated by the Hangenberg extinction (6,10,11,(15)(16)(17). Among vertebrates, a number of unique novel fish lineages appeared in the postextinction Mississippian subsystem of the Carboniferous period (11).…”

“…The end-Devonian Hangenberg event (359 Mya) provides a natural experiment in which potential predators are both removed (via extinction) and introduced (in the form of unspecialized survivors) to a prey biota with stable diversity trends (10)(11)(12)(13). During the Mid-Paleozoic Marine Revolution (MPMR), crinoids and other benthic invertebrates exhibited signs of escalation, including greater armature and spinosity (2,6,14).…”