ESM for Ezcurra et al. - Proceedings of the Royal Society B

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SUPPLEMENTARY INFORMATION FOR EZCURRA “Biogeography of Triassic
tetrapods: evidence for provincialism and driven sympatric cladogenesis in the early
evolution of modern tetrapod lineages”.
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S1. ABBREVIATIONS FOR FIGURE 1.
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Node abbreviations: Ae, Aetosaurinae; Aet, Aetosauria; An, Anapsida; Ar,
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Archosauria; Arc, Archosauriformes; Arcs, Archosauromorpha; Av, Avemetatarsalia;
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Br, Brachyopidae; Ca, Capitosauroidea; Ch, Chigutisauridae; Cr, Crocodylomorpha;
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Cru, Crurotarsi; Cy, Cynognathia; De, Desmatosuchinae; Di, Dinosauria; Dia, Diapsida;
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Dic, Dicynodontia; Din, Dinosauromorpha; Dr, Drepanosauridae; Er, Erythrosuchidae;
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Eu, Eusaurischia; Euc, Eucynodontia; Gu, Guaibasauridae; He, Herrerasauria; Ic,
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Ictidosauria; Ka, Kannemeyerioidea; La, Lagerpetidae; Le, Leptopleuroninae; Ma,
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Massopoda; Ne, Neotheropoda; Or, Ornithischia; Orn, Ornithosuchidae; Ph,
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Phytosauria; Pl, Plateosauridae; Po, Poposauridae; Pr, Proterochampsidae; Pro,
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Probainognathia; Proc, Procolophonidae; Pt, Pterosauria; Ra, Rauisuchia; Rh,
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Rhynchosauria; Rio, Riojasauridae; Ry, Rhytidostea; Sa, Saurischia; Sh,
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Shansiodontidae; Si, Silesauridae; Sim, Simiosauria, Sp, Sphenodontia, St,
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Stereospondyli; Sy, Synapsida; Ta, Tanystropheidae; Te, Testudinata; Tem,
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Temnospondyli; Tr, Tritheledontidae; Tra, Traversodontidae; Tre, Trematosauroidea;
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Tri, Trirachodontidae; Ty, Typothoracisinae.
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Area abbreviations: AF, meridional Africa; AS, Asia; EU, Europe; IN, India; IS,
Ischigualasto; NA, North America; SM, Santa Maria.
Temporal abbreviations: Col, Coloradian; Isc, Ischigualastian.
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S2. PHYLOGENETIC RELATIONSHIPS OF MIDDLE AND LATE TRIASSIC
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TETRAPODS
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The present cladistic palaebiogeographic analysis was performed with the
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information provided by Middle and Late Triassic tetrapods. The employment of
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several independent phylogenies of tetrapod lineages would reduce sampling failures
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and weak phylogenetic signals for certain clades, which are potential causes of artificial
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results in a TRA (Turner et al. 2009). The phylogenetic evidence provided by Middle
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and Late Triassic tetrapods was introduced to this analysis through a composite tree
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(‘informal supertree’) constructed by hand of the group (figure 1). The topologies
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recovered by several independent cladistic analyses have been employed in order to
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perform this composite tree (see below). The terminals dating from non-Middle/Late
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Triassic beds were not considered. The phylogenetic relationships among the main
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lineages of Tetrapoda were reconstructed according to the analysis of Gauthier et al.
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(1988). Programs employed to perform TRA analyses (COMPONENT 2.0 and
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TreeMap 1.0; Page 1993, 1995) cannot deal with polytimized phylogenetic tress. Thus,
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the following data sources and pruning criteria for polytomized trees were applied for
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each tetrapod clade:
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(1) Temnospondyli: the supertree generated by Ruta et al. (2007) was used to
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consider the phylogenetic interrelationships among temnospondyls. The cladogram
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performed in this study presents a fully resolved topology, thus it was not necessary to
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prune any Middle or Late Triassic temnospondyl from the geographic areas considered
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here.
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(2) Procolophonidae: the phylogenetic analysis of Procolophonidae performed by
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Cisneros (2008) was used for this tetrapod clade. The strict consensus tree recovered by
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Cisneros (2008) exhibit fully resolved relationships for Middle and Late Triassic
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procolophonids, thus no taxon was pruned.
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(3) Testudinata: the phylogenetic relationships of basal testudinates recovered by
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the analysis of Joyce et al. (2009) were followed in this contribution. The topology
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recovered by these authors presents two trichotomies, one composed of Chinlechelys,
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Proganochelys, and more crown-ward forms, and the other constituted by
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Palaeochersis, Australochelys, and more derived taxa. The latter polytomy is not
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problematic, because Australochelys is Early Jurassic in age and goes beyond the time
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span considered in this study. However, the more basal trichotomy is composed of Late
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Triassic taxa and a pruning criterion was adopted. For the sake of increase the available
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geographic area information, Proganochelys was excluded from the composite tree of
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Tetrapoda, because this taxon and Proterochersis come from European beds and
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Chinlechelys will provide information of the North American fauna.
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(4) Dicynodontia: the phylogenetic relationships of Middle Triassic dicynodonts
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were reconstructed after the analysis of Damiani et al. (2007). The most parsimonious
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tress recovered by these authors exhibit fully resolved relationships among Middle
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Triassic dicynodonts (i.e., Kannemeyeriiformes). For the Late Triassic time slice,
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although they were not included in the analysis of Damiani et al. (2007), the South
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American dicynodont genera Ischigualastia and Jachaleria (composed of two species)
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were included for the sake of increasing geographic data (Cox 1962; Bonaparte 1970;
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Araújo & Gonzaga 1980).
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(5) Cynognathia: the phylogenetic relationships of cynongnathian cynodonts found
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by Abdala et al. (2006) were followed in this contribution. The majority rule consensus
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of this study depicted two politomies, a trichotomy at the base of Traversodontidae
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composed of Luangwa, Scalenodon angustifrons, and more derived forms, and the other
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is a fourth order polytomy constituted by “Scalenodon” hirschsoni, Pascualgnathus,
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Traversodon, and more derived taxa. The trichotomy was avoided pruning Scalenodon
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angustifrons, because this species comes from central Africa (Tanzania) (Parrington
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1946) and Luangwa provides more geographic data, coming from South America and
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meridional Africa (Brink 1963, Abdala & Sa-Texeira 2004; Abdala & Smith 2009). In
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the other polytomy, “Scalenodon” hirschsoni and Traversodon were excluded from the
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analysis, and Pascualgnathus was included in order to increase the data coming from
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the “Ischigualasto” geographic area.
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(6) Probainognathia: the analysis of Martinelli & Rougier (2007) was followed
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regarding the phylogenetic relationships of probainognathian eucynodonts. The
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topology recovered by these authors is fully resolved.
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(7) Sphenodontia: the phylogenetic analysis of Evans (2003) was followed for
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sphenodontian interrelationships. This phylogeny presents a trichotomy composed of
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the European clade (Brachyrhinodon + Polysphenodon), Clevosaurus, and more crown-
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ward taxa. However, no pruning was implemented, because the taxa more derived than
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Clevosaurus in this study are recorded in post-Triassic rocks.
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(8) Simiosauria: the phylogenetic relationships among simiosaurians were followed
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according to the analysis of Senter (2004). No polytomy was found by this author.
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(9) Tanystropheidae: the phylogenetic relationships of tanystropheids and their
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position as basal archosauromorphs were followed from Senter (2004). No polytomy
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was found by this author.
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(10) Rhynchosauria: the phylogenetic analysis of Langer & Schultz (2000) was
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adopted for rhynchosaur interrelationships. This analysis recovered a polytomy
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composed of Hyperodapedon mariensis, Hyperidapedon gordoni + Hyperodapedon
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huxleyi, and Hyperodapedon sanjuanensis. In order to avoid this polytomy,
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Hyperodapedon mariensis was pruned from the analysis, because it presents the same
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geographic information as the sister-taxon of this entire group, Hyperodapedon huenei.
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(11) Non-archosaurian Archosauriformes: the phylogenetic relationships of non-
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archosaurian archosauriforms recently found by Nesbitt et al. (2009a) were followed,
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but with some changes. In order to include a “proterosuchid”, the Middle Triassic
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Sarmatosuchus (sensu Gower & Sennikov 1997) was included instead of the Early
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Triassic Proterosuchus. The information provided by the erythrosuchids was enlarged
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adding the Russian species Vjushkovia triplicostata, a widely accepted close relative of
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Erythrosuchus africanus (von Huene 1960; Parrish 1992). In the Middle Triassic time
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slice, the type species of the proterochampsid genus Chanaresuchus was included
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(Romer 1971) together with a Chanaresuchus sp. from the Santa Maria Formation
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(Dornelles 1992, 1995). Besides, a Chanresuchus sp. from the Ischigualasto Formation
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(Sill et al. 1994) and the two species of Proterochampsa (Sill 1967; Barberena 1982)
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were incorporated to the Late Triassic tetrapod tree.
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(12) Phytosauria: the analysis of Parker & Irmis (2006) was followed regarding the
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phylogenetic relationships of phytosaur crurotarsans. The topology recovered by these
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authors is fully resolved. Additionally, the relationships among the main lineages of
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crurotarsans (i.e., phytosaurs, aetosaurs, ornithosuchians, rauisuchians,
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crocodylomorphs) were reconstructed according to Brusatte et al. (2008).
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(13) Aetosauria: the phylogenetic relationships of aetosaurs recovered by the
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analysis of Parker (2007) were followed in this contribution. The phylogenetic
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relationships among desmatosuchins and typothoracisins are fully resolved. By contrast,
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the relationships among aetosaurins exhibit two politomies. In order to avoid these
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ambiguities, Coahomasuchus and both species of Stagonolepis were pruned from the
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analysis, leaving the taxa that provide more geographic information (i.e.,
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Neoaetosauroides, Aetosaurus, Aetosauroides).
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(14) Rauisuchia: the phylogenetic relationships among rauisuchians were
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reconstructed according to the phylogenetic analysis of Brusatte et al. (2008). No
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poltimies were recovered by these authors within Rauisuchia, and ornithosuchians were
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found as members of this group as the sister-taxon of Poposauroidea.
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(15) Pterosauria: the phylogenetic relationships of pterosaurs were reconstructed
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after the analysis of Brusatte et al. (2008), which does not recover politomies within this
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clade.
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(16) Non-dinosaurian Dinosauromorpha: the cladistic analysis performed by
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Nesbitt et al. (2009b) was used for the phylogenetic relationships of non-dinosaurian
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dinosauromorphs. No politomies were obtained in this analysis.
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(17) Ornithischia: the extremely poor Triassic record of ornithischians (Irmis et al.
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2007) is reflected in the present analysis, in which the only two currently valid Triassic
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species of the group are included. The ornithischian nature of this species is followed
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according to Casamiquela (1967) and Butler et al. (2007).
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(18) Herrerasauria: the phylogenetic relationships among herrerasaurians were
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considered following the analyses of Novas et al. (2009) and Ezcurra et al. (in review),
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in which a specimen from the Late Triassic of India (ISI R282) is found as the sister-
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taxon of Herrerasauridae.
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(19) Sauropodomorpha: the phylogenetic analyses performed by Novas et al.
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(2009) and Ezcurra et al. (in review) were used to consider the phylogenetic
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interrelationships among basal sauropodomorphs. Some politomies were found in this
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analyses, as consequence Panphagia, Agnosphytis and Pantydraco were pruned with
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the goal of avoiding such ambiguities but maintaining the maximum of geographic data.
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(20) Non-neotheropod Theropda: Nesbitt et al. (2009c) performed the most recent
cladistic analysis of basal theropods, which includes the recently described basal
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theropod Tawa. Accordingly, this analysis was selected here. No polotimies were found
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by these authors among non-neotheropod theropods.
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(21) Neotheropoda: the analysis of Ezcurra & Novas (2007) was chosen for the
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phylogenetic relationships within Neotheropoda. The European Procompsognathus was
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pruned from the analysis in order to avoid the polytomy found by these authors within
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Coelophysoidea.
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S3. GEOGRAPHIC AREAS AND TIME SLICES SELECTION
Key Middle and Late Triassic tetrapod-bearing assemblages have been selected as
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geographic areas because of their abundant and/or diverse fossil content. Seven
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geographic areas were designated to conduct the present cladistic palaeobiogeographic
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analysis:
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(1) Ischigualasto-Cuyo (western Argentina: Ischigualasto-Villa Unión, Sierra
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Pintada, and Cuyo basins): the Cuyo Basin, cropping out in central western Argentina,
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bears rich tetrapod-bearing assemblages of Middle and Late Triassic age (Marsicano et
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al. 2001). The Sierra Pintada Basin has rich tetrapod faunas of Early and early Middle
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Triassic age (Bonaparte 1981; Martinelli et al. 2009). The Ischigualasto-Villa Unión
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Basin is located in northwestern Argentina, and it is famous for its abundant and diverse
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late Middle and Late Triassic fossil content, including one of the oldest known dinosaur
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faunas (Rogers et al. 1993). These geological basins of western Argentina have been
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considered as a single geographic area (Ischigualasto-Cuyo) because they document a
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quite continuous temporal sequence in the southwestern extreme of the supercontinent
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of Pangaea.
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(2) Santa Maria (southern Brazil: Santa María Supersequence): this sequence crops
out in southern Brazil and documents abundant Early, Middle, and Late Triassic
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tetrapod faunas (Langer et al. 2007). The tetrapod faunas of the Santa Maria (late
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Middle and early Late Triassic) and Caturrita (middle Late Triassic) formations were
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considered in this analysis (Langer 2005a).
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(3) Africa (meridional Africa depocenters): several localities from meridional
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Africa, most of them corresponding to the Karoo Basin, were considered as composing
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a single geographic area (Africa). The Ischigualastian Triassic record of meridional
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Africa is quite biased, so this geographic area was not considered in the analysis of this
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time slice (Anderson et al. 1998; Lucas & Hancox 2001).
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(4) Asia: several Asiatic tetrapod-bearing sedimentary units of Middle and Late
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Triassic age have been included in this analysis and all grouped in the geographic area
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of Asia. The Late Triassic record from this geographic area is strongly patched, and it
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was not considered in the analyses of the Ischigualastian and Coloradian time slices
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(Benton 1983).
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(5) Europe: in this geographic area the tetrapod-bearing beds of Middle and Late
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Triassic age of the West European depocenters and the Keuper Group were included
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(Benton 1983).
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(6) North America (meridional North America): in this geographic area the basins of
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the Newark Supergroup and the Chinle Group were considered. These beds preserve an
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abundant and diverse sample of tetrapods that inhabited the northwestern extreme of
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Pangaea during the Middle and Late Triassic (e.g., Long & Murry 1995; Irmis 2005).
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(7) India (central India: Pranhita-Gondavari and Son-Mahanadi basins): the Middle
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and Late Triassic tetrapod record of India is well-represented in the Pranhita-Gondavari
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and Son-Mahanadi basins (Bandyopadhyay & Sengupta 2006). Accordingly, the
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tetrapods collected from these sedimentary basins have been grouped in the geographic
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area of India.
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The time slicing protocol introduced by Upchurch et al. (2002) for TRAs was
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implemented here. Three time-frames were selected to conduct the palaeobiogeographic
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analysis: Middle Triassic, Ischigualastian (early Late Triassic), and Coloradian (late
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Late Triassic) (Bonaparte 1973; Langer 2005a, b). The Reptile-Ages Ischigualastian and
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Coloradian were chosen over stratigraphical ages (i.e., Carnian-Rhaetian), because they
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are defined by key tetrapod taxa among Triassic continental tetrapod faunas which seem
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to be of global extent (Bonaparte 1973; Langer 2005a, b). By contrast, the
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stratigraphical ages are largely determined by marine conodont biozones (Muttoni et al.
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2001), and absolute age assessments and correlations among continental Triassic rock
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units are notoriously difficult (Muttoni et al. 2004). Accordingly, Reptile-Ages are more
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adequate as time-slices in order to conduct a TRA of Triassic continental biotas.
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S4. TREATMENT OF THE “WIDESPREAD TAXA” PROBLEM
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When a taxon is found in two or more of the employed geographic areas this is
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considered a “widespread taxon”. Such distributions would be consequence of several
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different reasons, including missing data and biotic dispersal. Cladistic biogeographers
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have coped with this problem following three different alternative assumptions
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(assumption 0, 1 or 2), which differ in the allowed cladogenetic relationships among the
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areas in which the taxon is distributed (Nelson & Platnick 1981; Zandee & Roos 1987;
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Sanmartin & Ronquist 2002). The use of these assumptions allows widespread taxa to
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be included in these analyses (Upchurch et al. 2002).
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In the present cladistic palaeobiogeographic analysis some widespread taxa are
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present, including Aetosauroides, Hyperodapedon sanjuanensis, Exaeretodon spp.,
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Metoposaurus, Massetognathus, Luangwa, Diademodon, Cynognathus, Kannemeyeria,
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and Cyclotosaurus. With the exception of the genus Exaeretodon, all the other taxa are a
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single widespread species or no sufficient information is currently available to separate
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specimens at an alfa-taxonomic level. Accordingly, these taxa were treated following
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the assumption 2 of Nelson & Platnick (1981), which allows a failure to vicariate,
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extinction, dispersal, or any combination of these events as an explanation for the origin
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of widespread distributions (van Veller et al. 1999). By contrast, Exaeretodon has four
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distinct species recognized in three geographic areas (i.e., Exaeretodon major: Santa
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Maria; Exaeretodon riograndensis; Exaeretodon statisticae: India; Exaeretodon
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frenguelli: Ischigualasto; Cabrera 1943; Chatterjee 1982; Abdala et al. 2002). This
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genus should be treated following the assumption 0 of Zandee & Roos (1987), in which
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the widespread distribution of the taxon is result of a failure to speciate in response to
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vicariant events affecting other lineages and it is considered as a synapomorphy of the
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areas in which it occurs (Sanmartin & Ronquist 2002). However, no currently available
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analysis successfully reconstructed the phylogenetic relationships among the species of
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Exaeretodon, and since the programs used here to conduct the TRAs cannot deal with
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politomies, the assumption 2 has been also used for the genus Exaeretodon.
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S5. OPTIMAL AREA CLADOGRAMS (OACs) SEARCH PARAMETERS
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The OACs have been reconstructed with the program COMPONENT 2.0 (Page
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1993) based on the information provided by the composite tree of Middle and Late
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Triassic tetrapods performed here. The geographic areas (hosts) without associates were
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interpreted as missing information. A heuristic search employing nearest-neighbor
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interchanges as branch swapping algorithm was conducted and “losses” was used as the
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optimal criterion instead of the optimization of “leaves added”.
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The use of “leaves added” as the optimal criterion during the search of the OACs
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maximizes the number of codivergences among the geographic areas. However, when
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some of the employed geographic areas have a poor taxonomic sample, usual when we
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are working with palaeontological evidence, the leaves added optimization will tend to
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recover these areas closer to the root of the tree or clade. This is result of the low
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number of taxa sampled from these areas, which result in a lower probability of
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codivergences with other areas than it would be recovered between two well-sampled
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territories. By contrast, the optimization of “losses” during the search is less sensitive to
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these poorly sampled geographic areas, and will be more effective to reconstruct their
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palaeobiogeographic affinities. Accordingly, I have used the latter optimal criterion in
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order to perform the search of the OACs.
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In order to compare the two optimal criteria, the following results are found when
the “leaves added” criterion is used:
(1) Middle Triassic: in this time slice almost the same topology is recovered for the
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single OAC. The difference relapses in the position of India, the worst sampled
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geographic area of this time slice (an unsurprising result because of the sensitive of the
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algorithm for poorly sampled areas). In this analysis, India is found as the sister-area of
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the clade which includes Asia, Europe, and North America. The randomization test
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found a significant statistical support (p < 0.05) for the TRA of this time slice.
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(2) Ischigualastian: the same OAC has been recovered for the Ischigualastian
employing either of the two optimal criteria.
(3) Coloradian: this time slice exhibits the greater difference between the
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employments of the two optimal criteria. The optimization of “leaves added” found a
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single OAC of the following topology: (Santa Maria, (India, (South Africa,
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(Ischigualasto, (Europe, North America))))). It must be noted that Ischigualasto and the
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Europe + North America clade share several codivergent events, but Santa Maria and
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India seem to be found artificially outside all the other geographic areas because of the
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poor sample of their Coloradian tetrapod record (Langer et al. 2007, 2009; Kutty &
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Sengupta 1989; Bandyopadhyay & Sengupta 2006). The randomization test recovered
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that the reconstruction generated by the TRA in this time slice was not statistically
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significant (p > 0.05).
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S6. RECONSTRUCTION OF BIOGEOGRAPHIC EVENTS AND
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RANDOMISATION TEST ANALYSES
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Reconstructions of biogeographic events for each time-slice were conducted in
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TreeMap 1.0 (Page 1995) through heuristic searches. Regarding the statistical analyses,
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a randomisation test which generates random area cladograms and reconciles each of
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them with the phylogenetic cladogram was performed (Page 1991). This test has the
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goal of determining the probability that the observed biogeographical pattern could have
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occurred only by chance (Page 1994a, 1995). The area cladograms were randomized
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instead of the tetrapod phylogeny, because in this analysis I wanted to test which was
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the effect in the reconciliation analysis of alternative random OACs onto a steady
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phylogenetic framework. Besides, it was considered here that the size of the OACs (the
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smaller one with 5 terminals) was sufficient to provide a good statistical test for the
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TRA. Accordingly, for each time slice, 10,000 randomised replications were conducted
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using the “proportional to distinguishable” algorithm. This randomisation test was
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conducted in TreeMap 1.0. The topology recovered in the OACs was considered as
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statistically significant if less than 5% of the replicates (p < 0.05) reached the number of
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codivergences found in the original TRA.
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S7. SSf CALCULATION
The TRAs performed in TreeMap 1.0 recover the number of codivergences
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(coespeciations), sympatric splits (duplications), extinctions (sorting events), and
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dispersals (host switches) present at each data frame (Sanmartin & Ronquist 2002). In
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the present contribution, the frequency of sympatric splits (SSf) was calculated
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following equation 1, in order to compare the importance that had this
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macroevolutionary event at each time slice.
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SSf = (SS/CE)*100
(1)
SSf: frequency of sympatric split events over the total of cladogenetic events present
in the taxon cladogram.
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SS: number of sympatric events found by the TRA.
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CE: number of cladogenetic events document by the phylogenetic tree.
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S8. PALAEOLATITUDINAL OPTIMIZATION ON THE OACs,
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PALAEOLATITUDINAL CONSISTENCY INDEX, AND STATISTICAL
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SUPPORT.
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In order to obtain a quantitative measure of the relationships between
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palaeolatitudinal distinctions and the topology obtained in the OACs, a
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“palaeolatitudinal consistency index” was calculated. First, the palaeolatitudes of the
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respective geographic areas were scored in the continuous character “palaeolatitude”,
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treated as such (Goloboff et al. 2006). This character was treated a priori polarization.
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Then, this character was optimized on the topologies of the recovered OACs of each
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time slice using the program TNT 1.1. (Goloboff et al. 2008). Finally, the consistency
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index of the character “palaeolatitude” (PltCI) was calculated (see equation 2). A closer
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value of the consistency index to 1 indicates less degree of homoplasy for the character
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(Kluge & Farris 1969) (Fig. S9). Accordingly, a stronger palaeolatitudinal signal in the
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reconstructed OAC is indicated as closer the PalCI is to 1.
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PltCI = Pltm/Plts (2)
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PltCI: palaeolatitudinal consistency index.
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Pltm: number of states of the palaeolatitudinal character – 1 (i.e. minimum number
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of changes in any tree).
Plts: number of steps recovered in the optimization of the palaeolatitudinal character
on the OACs.
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Finally, a statistical analysis generating P-values was performed through a sample
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of randomized trees in order to test the likelihood of recovering the Ischigualastian
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palaeolatitudinal signal by chance alone. 10,000 random rooted trees of the same
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number of leaves recovered in the Ischigualastian OAC (i.e., 5 geographic areas) were
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generated with the program COMPONENT 2.0. This program generates random trees
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through an algorithm which uses the numbering scheme of Furnas (1984). It establishes
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a one-to-one correspondence between the integers 1 to k, where k is the number of
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unlabelled trees for n taxa (Page 1993). Using a uniform random number generator a
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random number between 1 and k is obtained, and employed to recover a random tree
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(Page 1993). The character palaeolatitud was optimized onto this set of random
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cladograms and the consistency index of the character was calculated with TNT 1.1. A p
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value was generated with the number of random trees which recovered the same
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palaeobiogeographic signal as the original OAC (i.e., the same PltCI). Through these
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proceeding a significant statistical support was found (p = 0.0094), indicating that the
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Ischigualastian palaeolatitudinal signal is very unlikely to have occurred by chance.
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Figure S9. Optimization of the palaeolatitud of each geographic area as a continuous
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character onto the OACs of each time slice. The palaeolatitud of each terminal was
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divided by 10 in order to work with smaller values (e.g., for Africa during the
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Coloradian: 55°/10 = 5.5). Abbreviations: CI, consistency index.
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