[Palaeontology, Vol. 51, Part 6, 2008, pp. 1261–1288] CALIBRATED DIVERSITY, TREE TOPOLOGY AND THE MOTHER OF MASS EXTINCTIONS: THE LESSON OF TEMNOSPONDYLS by MARCELLO RUTA and MICHAEL J. BENTON Department of Earth Sciences, University of Bristol, Bristol BS8 1RJ, UK; e-mails [email protected]; [email protected] Typescript received 4 June 2007; accepted in revised form 14 January 2008 Abstract: Three family-level cladistic analyses of tem- closer to one another than they are when the observed num- nospondyl amphibians are used to evaluate the impact of ber of families is used; both values are also slightly higher taxonomic rank, tree topology, and sample size on diversity than the Carboniferous estimated diversity. The Guadalu- profiles, origination and extinction rates, and faunal turn- pian–Lopingian value is lower than raw data indicate, reflect- over. Temnospondyls are used as a case study for investigat- ing in part the depauperate land vertebrate diversity from ing replacement of families across the Permo-Triassic the late Cisuralian to the middle Guadalupian (Olson’s gap). boundary and modality of recovery in the aftermath of the The time-calibrated origination and extinction rate trajecto- end-Permian mass extinction. Both observed and inferred ries plot out close to one another and show a peak in the (i.e. tree topology-dependent) values of family diversity have Induan, regardless of the tree used to construct them. Origi- a negligible effect on the shape of the diversity curve. How- nation and extinction trajectories are disjunct in at least ever, inferred values produce both a flattening of the curve some Palaeozoic intervals, and background extinctions exert throughout the Cisuralian and a less pronounced increase in a significant role in shaping temnospondyl diversity in the family diversity from Tatarian through to Induan than do lowermost Triassic. Finally, species-, genus-, and family tra- observed values. Diversity curves based upon counts of gen- jectories consistently reveal a rapid increase in temnospondyl era and species display a clearer distinction between peaks diversity from latest Permian to earliest Triassic as well as a and troughs. We use rarefaction techniques (specifically, rar- decline near the end of the Cisuralian. However, during the efaction of the number of genera and species within families) rest of the Cisuralian family diversity increases slightly and to evaluate the effect of sampling size on the curve of esti- there is no evidence for a steady decline, contrary to previous mated family-level diversity during five time bins (Carbonif- reports. erous; Cisuralian; Guadalupian–Lopingian; Early Triassic; Middle Triassic–Cretaceous). After applying rarefaction, we Key words: cladogram, extinction, diversity, ghost lineages, note that Cisuralian and Early Triassic diversity values are origination, phylogeny, rarefaction. A large proportion of the literature on Phanerozoic dearth of quantitative macroevolutionary studies for the diversity draws from Sepkoski’s (1992, 2002) two monu- vast majority of fossil vertebrate groups (but see Benton mental compendia on families and genera of marine fossil 1985a, b, 1987, 1994, 1995, 1996a, b, 2003, Maxwell and animals. Modifications, additions, and refinements to Benton 1990, Benton and Simms 1995, and Benton and both compendia provide the foundations for analyses of Hitchin 1996). In addition, only a very small number of origination and extinction rates, reconstruction of trajec- papers have addressed specifically large-scale evolutionary tories of taxonomic diversity through time, and quantifi- patterns in early tetrapods (e.g. Pitrat 1973; Benton cation of biotic turnover. The development and 1985b, 1987; Olson 1989; Maxwell 1992; Benton et al. enrichment of databases for macroevolutionary investiga- 2004; Laurin 2004; Ruta et al. 2006; Wagner et al. 2006). tions have a prestigious and long tradition in palaeo- As the most species-rich and widespread of all groups biology. As a result, data on diversity are now available of early tetrapods, temnospondyl amphibians are suitable for several groups (e.g. Benton 1993; see also online for macroevolutionary studies. In an early account of this resources such as The Paleobiology Database: http:// group’s diversity, Carroll (1977) provided a stratigraphic paleodb.org/cgi-bin/bridge.pl and FossilPlot: http:// plot of family ranges, but offered no qualitative or quan- geology.isu.edu/FossilPlot/Index.htm). However, there is a titative frameworks for investigating faunal turnover or ª The Palaeontological Association doi: 10.1111/j.1475-4983.2008.00808.x 1261 1262 PALAEONTOLOGY, VOLUME 51 extinction ⁄ origination rates. More recently, Milner (1990) synonymy to the amount of effort and time required for built a large-scale (albeit not a computer-assisted) cladis- data collection at a low taxonomic level, and from precision tic analysis of family-level relationships for temnospondyls in dating to sampling bias. However, in the case of temno- as a whole. This analysis was employed to assess timing spondyls the number of species is ‘manageable’, not least and magnitude of the main diversification and extinction because recent compendia cover the majority of described events in temnospondyl history as well as patterns of species and include detailed reviews of their synonymy. biogeographic dispersal and ecological partitioning. Dating and sampling problems are certainly more difficult In this paper, we undertake a new analysis of tem- to tackle. However, for the main purposes of the present nospondyl diversity. This study is certainly timely, given paper, the assignment of species to stages will suffice. the large number of temnospondyl species described since Although certain species pose difficulties in this respect (i.e. Milner’s (1990) paper (representing an increase of almost their precise assignment to a stage is dubious), they repre- 20 per cent) and the availability of analytical techniques sent only a small fraction of the total number. As far as for macroevolutionary inference. Specifically, we address sampling is concerned, we assume that the group’s record the following issues: forms an unbiased collection from its entire stratigraphic 1. the impact of different taxonomic ranks on trajectories range. This may seem unwarranted, given the fact that sev- of raw (i.e. observed) diversity; eral temnospondyl assemblages (e.g. in the Carboniferous) 2. the influence of cladogram shape, ghost lineages, and show characteristic ecological fingerprints (see Milner range extensions on these trajectories; 1990). For this reason, their probability of preservation 3. the correlation (if any) between rates of family extinc- would be higher than that of species living in environments tions and originations (i.e. faunal turnover); that are not conducive to preservation. The impact of eco- 4. the effect of sample size on diversity profiles, in partic- logical and ⁄ or biogeographic factors on the trajectories of ular during periods of depauperate taxonomic richness observed diversity will be considered in a separate publica- (especially Olson’s gap; see below); tion (but see also Benton 1985a, b, 1987). 5. the impact of the end-Permian mass extinction on tem- As far as the topology of phylogenetic trees is con- nospondyl diversification near the Palaeozoic-Mesozoic cerned, we seek to assess differences in profiles of family- boundary and the pattern of taxonomic recovery in the level temnospondyl diversity when ghost lineages and aftermath of that extinction. range extensions (e.g. Norell 1992; Smith 1994) are taken Taxonomic rank is an important, yet often neglected into account. To this end, we use three recently published component of any macroevolutionary analysis. Empirical temnospondyl phylogenies. The use of families is dictated work demonstrates that diversity trajectories produced by the fact that species- or genus-level phylogenies for using a variety of ranks may differ to a considerable temnospondyls are not available, despite the number of extent. These differences ultimately result in different cladistic data sets published so far. Only some of these models of diversity expansion and contraction during a data sets have considered a significant proportion of all group’s history, including the fitting of appropriate curves major temnospondyl clades (see Yates and Warren 2000 for assessing patterns of increasing taxonomic growth and Ruta and Bolt 2006); many others (e.g. see Schoch (e.g. see Bambach 1989 and Lane and Benton 2003). The and Rubidge 2005; Damiani et al. 2006; Laurin and Soler- use of different ranks can alter profoundly models of Gijo´n 2006; Witzmann and Schoch 2006 and Schoch recovery in the aftermath of large-scale extinctions, e.g. et al. 2007) have tackled small sections of the tem- by either diluting or exaggerating the magnitude of the nospondyl tree, e.g. to assess the phylogenetic placement latter. Similarly, ranks can impact our perception of rates of a few key species. of originations (e.g. a gradual increase in taxonomic rich- Our use of the expressions ‘range extension’ and ‘ghost ness as opposed to a burst of diversification). lineage’ conform strictly to Smith (1994). A range exten- Jablonski (2007) provided a detailed treatment of the sion of a taxon is the minimum stratigraphic range added scale effect in macroevolutionary studies while Benton and to (or extended below) the earliest occurrence of that taxon Emerson (2007) discussed some problems associated with in order to join an older