[Palaeontology, Vol. 55, Part 4, 2012, pp. 707–742] FIVE HUNDRED MILLION YEARS OF EXTINCTION AND RECOVERY: A PHANEROZOIC SURVEY OF LARGE-SCALE DIVERSITY PATTERNS IN FISHES by MATT FRIEDMAN1* and LAUREN COLE SALLAN2 1Department of Earth Sciences, University of Oxford, Oxford OX1 3AN, UK; e-mail: [email protected] 2Department of Organismal Biology and Anatomy, University of Chicago, Chicago, IL 60637, USA; e-mail: [email protected] *Corresponding author. Typescript received 1 December 2011; accepted in revised form 26 February 2012 Abstract: Fishes include more than half of all living intervals of turnover, evolutionary radiation, and extinc- animals with backbones, but large-scale palaeobiological tion. In particular, we provide in-depth reviews of changes patterns in this assemblage have not received the same during, and ecological and evolutionary recovery after, the attention as those for terrestrial vertebrates. Previous sur- end-Devonian (Hangenberg) and Cretaceous–Palaeogene veys of the fish record have generally been anecdotal, or (K–Pg) extinctions. limited either in their stratigraphic or in their taxonomic scope. Here, we provide a broad overview of the Phanero- Key words: adaptive radiation, biodiversity, Chondrich- zoic history of fish diversity, placing a special emphasis on thyes, durophagy, Hangenberg, K–Pg, Osteichthyes. ‘Fishes’, the paraphyletic assemblage of primitively 2011; Sallan et al. 2011). Ignorance of historical patterns aquatic backboned animals, comprise over half of all of fish diversity, therefore, impedes a general under- living vertebrate species (Nelson 2006), with a fossil standing of aquatic biodiversity and evolutionary record extending to the early Cambrian (Shu et al. 1999, processes. 2003). Compared with marine invertebrates (Sepkoski Several factors have prevented a synoptic picture of 2002) and many other vertebrate groups (e.g. Alroy 1996; macroevolutionary patterns in fishes from materializing. Lloyd et al. 2008), our understanding of large-scale Key among these is the sheer scope of the problem: no diversity patterns in fossil fishes is limited. This is some- other vertebrate assemblage encompasses as much taxo- what surprising, because fishes were the first group for nomic richness and morphological disparity, distributed which patterns of palaeobiodiversity were systematically over such a long geological interval and represented by documented, more than a century and a half ago by Louis such a diverse range of preservational styles as fishes. Agassiz in his monumental Recherches sur les Poissons But this extensive record remains relatively understud- fossiles (1833–1844). Fishes should represent a obvious ied, as a review of the table of contents in any issue of study system for exploring macroevolutionary contrasts a palaeontological journal will illustrate. Since the time between freshwater and marine environments within a of Agassiz, the small community of fish palaeontologists single group (e.g. McKinney 1998; Vega and Wiens 2012), has focused primarily on taxonomy, description and and the considerable body of work dissecting form–func- interrelationships. As a result, fish workers were among tion relationships in living forms generally, and teleosts the early adopters and innovators of cladistic methods specifically (e.g. Wainwright and Bellwood 2002), make late in the 20th century (e.g. Nelson 1969) and among fishes a particularly attractive system for exploring ques- the first to apply then novel ‘tree-thinking’ approaches tions related to ecology over geological timescales (e.g. to the fossil record (Patterson and Rosen 1977). By Bellwood 2003; Friedman 2010; Anderson et al. 2011; contrast, the coincident ‘Palaeobiological Revolution’ Sallan et al. 2011; Sallan and Friedman 2012). Addition- (Sepkoski and Ruse 2009), with its emphasis on com- ally, the impact of fishes as predators, competitors and mon macroevolutionary trends among disparate clades, prey on the long-term macroevolution and macroecology was barely noted. of other clades in the same ecosystems (e.g. invertebrates Macroevolutionary studies have been perceived as of and tetrapods) has likely been substantial (Vermeij 1977; secondary importance by most fish workers for many rea- Brett and Walker 2002; Stanley 2008; Bush and Bambach sons: the very real need to catalogue available and newly ª The Palaeontological Association doi: 10.1111/j.1475-4983.2012.01165.x 707 708 PALAEONTOLOGY, VOLUME 55 discovered material, assumptions of scarcity relative to that should be the target of future research. While we the invertebrate record, and unfamiliarity with palaeobio- have attempted to present a balanced picture of Phan- logical methods. In addition, systematic and palaeobiolog- erozoic fish diversity patterns, this topic is vast and our ical analyses impose distinct demands on the worker. review is inevitably biased towards our own areas of Cladistic analysis requires detailed investigations of a expertise, centred on the end-Devonian (Sallan) and small set of exemplars, selected on the basis of group end-Cretaceous (Friedman) extinctions. Our taxonomic membership and phylogenetically informative characters. scope encompasses the vertebrate total group exclusive Macroevolutionary analysis requires large-scale surveys of of tetrapods (Fig. 1). There is mounting evidence that diverse taxa selected on the basis of factors generally not cyclostomes are monophyletic (Heimberg et al. 2010; specific to a particular group (e.g. faunal membership, Janvier 2011; Ota et al. 2011), meaning that the verte- ecology and age or environment). brate crown group includes hagfishes in addition to As a result of this dichotomy, the literature concern- gnathostomes and lampreys. In contrast to most previ- ing patterns of extinction and recovery in fishes is ous surveys of fish diversity in the fossil record, we small and diffuse, making it difficult for workers both include conodonts in our review. There is some conflict within and outside the field to make meaningful state- concerning the precise systematic position of the group ments about patterns of diversity. Under the theme of (e.g. Turner et al. 2010), but all explicit hypotheses of extinction and recovery, our goal is to provide a broad conodont relationships place them as members of the overview of major patterns of turnover in the fossil vertebrate total group. A summary of hypothesized rela- record of fishes, so far as they can be discerned at tionships between major groups discussed elsewhere in present, and highlight areas of persistent uncertainty this paper is given in Figure 1. FIG. 1. A composite hypothesis of deuterostome phylogeny, with an emphasis on the interrelationships among vertebrates. Taxa preceeded by the dagger symbol (‘ ’) are extinct, while those enclosed in inverted commas are possibly or likely paraphyletic. Here, ‘Anaspida’ includes problematic naked taxa (e.g. Euphanerops) typically associated with this ostracoderm assemblage. Uncertain phylogenetic placements are marked by question marks. Placoderms appear to be a grade of stem gnathostomes (Friedman 2007; Brazeau 2009), while the paraphyletic acanthodians branch from the chondrichthyan, osteichthyan and possibly gnathostome stems (the first two are shown by Brazeau’s 2009 consensus topologies, while the latter is present in some source trees). Abbreviations: ATG, actinopterygian total group; ChCG, chondrichthyan crown group; ChTG, chondrichthyan total group; CoTG, chordate total group; DTG, deuterostome total group; GCG, gnathostome crown group; GTG, gnathostome total group; HTG, holostean total group; NTG, neopterygian total group; OCG, osteichthyan crown group; OTG, osteichthyan total group; STG, sarcopterygian total group; VTG, vertebrate total group. Topology based on local solutions presented by: Janvier (1996), Donoghue et al. (2000), Coates and Sequeira (2001), Blieck and Turner (2003), Sansom et al. (2005), Hurley et al. (2007), Friedman (2007), Brazeau (2009). FRIEDMAN AND SALLAN: EXTINCTION AND RECOVERY IN FISHES 709 AN OVERVIEW OF THE HISTORY OF richness: one in the Late Devonian and another FISH DIVERSITY approaching the Recent. Actinopterygians, specifically te- leosts, are responsible for the latter. A shallow trough, A detailed picture of diversity patterns in the fossil record extending from the Carboniferous to mid-Cretaceous, lies of fishes is lacking, despite synoptic attempts dating back between these two intervals of apparently high richness. to the 19th century (Agassiz 1833–1844; Marsh 1877). This long span is punctuated by a series of minor peaks Broad overviews are presented as range charts in relevant and valleys that, for the most part, are not consistent chapters of The Fossil Record (Andrews et al. 1967) and between the three datasets. The Fossil Record 2 (Aldridge and Smith 1993; Cappetta Using Foote’s (2000) expressions, we made estimates of et al. 1993; Gardiner 1993a, b; Halstead 1993; Patterson per capita rates of extinction and origination from all of 1993a; Schultze 1993; Zidek 1993). Richness-through-time Sepkoski’s (2002) fish data, as well as calculating these plots have been produced for different fish groups (Fig. 1) rates separately for the two major groups of living fishes, during all (osteichthyans, or bony fishes: Patterson 1994) chondrichthyans (cartilaginous fishes, or sharks, chima- or part (Jurassic-Recent neoselachians (anatomically mod- eras and their relatives) and osteichthyans (actinoptery- ern sharks and rays): Cappetta 1987a; Late Cretaceous- gians and lobe-finned