sign in sign up
<<
Home , Agnostida, Cindarella, Emeraldella, Eoredlichia, Helmetia, Isoxys

San Jose State University SJSU ScholarWorks

Faculty Publications Geology

January 2007

Biogeography and the radiation of arachnomorph

Jonathan R. Hendricks University of Kansas, [email protected]

Bruce S. Lieberman University of Kansas

Follow this and additional works at: https://scholarworks.sjsu.edu/geol_pub

Part of the Geology Commons

Recommended Citation Jonathan R. Hendricks and Bruce S. Lieberman. "Biogeography and the Cambrian radiation of arachnomorph arthropods" Memoirs of the Association of Australasian Palaeontologists (2007): 29-39.

This Article is brought to you for free and open access by the Geology at SJSU ScholarWorks. It has been accepted for inclusion in Faculty Publications by an authorized administrator of SJSU ScholarWorks. For more information, please contact [email protected]. Biogeography and the Cambrian radiation of arachnomorph arthropods

JONATHAN R. HENDRICKS & BRUCE S. LIEBERMAN

HENDRICKS, J.R. & LIEBERMAN, B.S., 2007:12:21. Biogeography and the Cambrian radiation of arachnomorph arthropods. Memoirs of the Association of Australasian Palaeontologists 34, 461-471. ISSN 0810-8889.

Biogeographic patterns in primarily Cambrian arachnomorph taxa are investigated using a recently constructed phylogenetic hypothesis in to explore the biogeographic context of the Cambrian radiation. A modified version of Brooks Parsimony Analysis is employed to elucidate patterns of vicariance and geodispersal in taxa from six regions (Laurentia, Baltica, Siberia, Australia, Africa and China). Well resolved vicariance and geodispersal trees are very similar and reconstruct Laurentia and China as sister areas. This close area relationship between Laurentia and China provides extensive evidence for congruent vicariance and range expansion in Cambrian arachnomorphs, while data from do not show this pattern. Our results imply that cyclic events (such as sea-level change), in conjunction with dispersal ability, may have been more important than tectonic events in generating the biogeographic patterns we observed in Cambrian arachnomorphs. Further, the greater degree of dispersal in various non- arachnomorph lineages relative to trilobites is correlated with greater resistance across the early-Middle Cambrian boundary.

Jonathan R. Hendricks ([email protected]), Department of Geology, 1475 Jayhawk Boulevard, 120 Lindley Hall, University of Kansas, Lawrence, 66045-7613, USA; Bruce S. Lieberman (blieber@ ku.edu), Department of Geology and Natural History Museum and Biodiversity Research Center, 1475 Jayhawk Boulevard, 120 Lindley Hall, University of Kansas, Lawrence, 66045-7613, USA. Received 29 October 2007.

Keywords: Arachnomorpha, Arthropoda, Cambrian radiation, geodispersal, macroevolution, palaeobiogeography, phylogeny, tectonics, vicariance.

ONE of John Shergold’s abiding research interests, factors may have played in the Cambrian radiation and an area in which he made fundamental (Hoffman 1991; Knoll 1996; Dalziel 1997; contributions to the fields of palaeontology and Lieberman 1997; Veevers et al. 1997; Hoffman geology, was the study of Cambrian arthropods et al. 1998). The late Neoproterozoic to early in general, and trilobites in particular (e.g., Cambrian was a period of substantial tectonic Shergold 1977, 1988, 1991; Shergold et al. 1990; activity and Meert & Lieberman (2004; also see Shergold & Laurie 1997). Here we focus on references therein) provided a recent review of what Cambrian arthropods, including trilobites, these events, which are briefly recounted here. can tell us about the nature of evolutionary and The supercontinent Rodinia broke apart ca. biogeographic patterns, and their relationship to 750 Ma, with major rifting occurring between geological changes, during a key episode in the western Laurentia and Gondwana (Australia, East history of life, the Cambrian radiation. The first Antarctica and South China). Around 600 Ma, appearance of life in Cambrian strata has the ephemeral supercontinent Pannotia formed. stimulated the curiosity of naturalists ever since Pannotia rifted apart during the subsequent 50 Buckland (1836). A growing body of evidence, million years (550-600 Ma), resulting in four from studies of molecular sequence evolution to distinct land masses by the beginning of the trilobite biogeography, supports the hypothesis Cambrian: Laurentia; Baltica (Scandinavia that bilaterian lineages originated and began to and eastern Europe); Siberia; and Gondwana diverge at the end of the Neoproterozoic, perhaps (including South America, Africa, Antarctica, a few tens of millions of years before their first Australia, India, North and South China, Avalonia, appearance in the record (e.g., Meert & and western and central Europe). Lieberman 2004; Peterson et al. 2004). Of interest here are the roles that tectonic Much recent attention has focused on the factors may have played in the early evolution roles that extrinsic environmental or geological and radiation of arachnomorph arthropods, which 462 AAP Memoir 34 (2007) (1) (1) (2) (1) (1) (1,6) (6) (5) (4,6) (6) (6) (1) (6) (6) (1) (1) (5) (1,6) (6) (1,4,6) (2) Aglaspis Retifacies (6) Xandarella Kuamaia Saperion Nettapezoura Alalcomenaeus Dicranocaris Emeraldella Leanchoilia Helmetia Tegopelte Skioldia Soomaspis Sanctacaris (1) Liwia Weinbergina Trilobita (3) Trilobita Sinoburius Cindarella Tariccoia 3 5 6 9 11 12 14 15 17 18 20 22 24 25 28 29 31 33 34 37 38 40 42 43 Marrellomorpha (1,6)

4 1 10 1 16 1 23 6 27 1,6 32 5 36 1,6 41 6,9,1 16,13,1 22,18,1 46,40,1 61,59,1 73,69,1 8 1 21 6 30 1,2,3,5,6 39 1,6 1,3,1 44,36,1 52,45, 77,76,2 13 1 1 60,55, 17,16,1 1 26 1,2,3,5,6 35 1,6 57,54,1 84,84,3

7 1 6 63,58, 3,4,1 1

19 1,3,6 23,27,2

2 1,6 1 1,6

Fig. 1. Combined phylogenetic hypothesis (Hendricks & Lieberman in press) of arachnomorph relationships (strict consensus of 12 most parsimonious trees, each of 78 steps and with CI = 0.62 and RI = 0.75; the consensus has 82 steps) and area cladogram resulting from substituting biogeographic character states for taxon names and mapping biogeographic characters to ancestral nodes. Numbers adjacent to taxon names refer to geographic occurrence records (also see Table 1): 1) Laurentia; 2) Baltica; 3) Siberia; 4) Australia; 5) Africa; and 6) China. Geographic data for “Marrellomorpha” are derived from Marrella and geographic data for Weinbergina are derived from Eolimulus and Paleomerus (see text for details); further, “Trilobita” represents a sister-group relationship found for Eoredlichia and Olenoides by Hendricks & Lieberman (in press). Numbers in boxes are biogeographic regions reconstructed at ancestral nodes using Fitch (1971) optimisation as described by Lieberman (2000). Numbers in circles refer to nodes or terminals developed into biogeographical characters shown in Tables 2 and 3. Numbers in boxes are support values [normal , bootstrap support (Felsenstein 1985); italicised type, jackknife support (Farris et al. 1996); bold type, Bremer support (Bremer 1988, 1994)] calculated for the phylogenetic hypothesis of Hendricks & Lieberman (in press, fig. 3). include trilobites, chelicerates and many poorly to Cambrian arachnomorphs and crown-group scleritised, enigmatic arthropods only known chelicerates. Biogeographic patterns in these from -type deposits. Our study other taxa are outside the scope of this paper, and considers over 20 relevant, early Palaeozoic the interested reader is referred to discussions on arachnomorph taxa. It was not possible, however, the phylogenetic status of the arachnomorphs to consider every taxon that has been treated by Wills et al. (1998), Edgecombe & Ramsköld as an arachnomorph (or close relative) in our (1999), Budd (2002), Cotton & Braddy (2004), study. For example, we did not explore the Scholtz & Edgecombe (2006) and Hendricks & phylogenetic position of the pycnogonids relative Lieberman (in press), and references therein. AAP Memoir 34 (2007) 463

It has been previously demonstrated (Lieberman episodes of vicariance; the other designed to 2003a, b; Lieberman & Meert 2004; Meert & retrieve congruent episodes of geodispersal. Each Lieberman 2004) that vicariant biogeographic data matrix is then individually analysed using a patterns (those involving the fragmentation parsimony algorithm. The results are expressed of geographic areas, with subsequent lineage as a most parsimonious tree (or consensus diversification and range contraction) in early tree) depicting, respectively, the best supported Cambrian trilobites are congruent with the congruent patterns of vicariance and the best 600-550 Ma breakup of Pannotia. Further, analyses supported congruent patterns of geodispersal of patterns of geodispersal (those involving the in the data. A recently constructed phylogenetic joining of geographic areas, with subsequent range hypothesis for mostly Cambrian, Palaeozoic expansion) in early Cambrian trilobites show little arachnomorph taxa (Hendricks & Lieberman evidence for significant amounts of congruent in press) forms the basis of this study. Our dispersal or range expansion between tectonic phylogenetic hypothesis (see Fig. 1) was built regions (Lieberman 2003a; Lieberman & Meert by modification of, and addition to, a character 2004; Meert & Lieberman 2004). Indeed, many matrix previously published by Edgecombe early Cambrian trilobites are highly endemic. For & Ramsköld (1999) and included a total of 26 example, among more than 100 of early terminal taxa. The topology shown (Fig. 1) is Cambrian olenelline trilobites, all were confined the strict consensus (with all unsupported nodes to a single craton and only one species occurred collapsed) of 12 most parsimonious trees, each in more than one tectonic basin (Lieberman 1997, of 78 steps. 1999, 2001, 2003c). On the face of it, however, Some changes were made to the phylogenetic this pattern of endemicity is not present in many of hypothesis of Hendricks & Lieberman (in the Cambrian Burgess Shale-type taxa, press) for the purposes of the present study. including many non-trilobite arachnomorphs; for In particular, because the goal of the present instance, some of these taxa are known to occur study was to deduce patterns of biogeography in in multiple tectonic basins (Lieberman 2003c). Cambrian arachnomorphs (see Table 1), two of Here we use new analyses to study biogeographic the -aged terminal taxa were replaced patterns of vicariance and geodispersal in on the tree by Cambrian taxa considered to primarily Cambrian arachnomorphs in order be either nearly equivalent or closely related. to better understand the biogeographic context These two changes included: 1) replacing the of the Cambrian radiation and to consider how composite outgroup terminal “Marrellomorpha”, these patterns compare to those that have been which comprises both the Cambrian taxon previously observed in trilobite taxa. Marrella and the Devonian taxon Mimetaster, with just Marrella; and 2) substituting either METHODS AND MATERIALS Eolimulus or Paleomerus, both Cambrian taxa, A variety of methods have been developed to for the Devonian chelicerate Weinbergina. We explore phylogenetic biogeographic patterns acknowledge that because information about (e.g., Ebach & Edgecombe 2001). Our study the appendages of Eolimulus and Paleomerus utilised a modified version of Brooks Parsimony are lacking, their phylogenetic positions cannot Analysis (BPA) to consider biogeographic be confidently established. For the purposes patterns in Cambrian arachnomorphs; this method of the present study, however, we assume that was chosen because it allows examination of one (or both) may be on the xiphosuran stem both patterns of vicariance and patterns of lineage and are thus appropriate placeholders for geodispersal. The modified BPA methodology Weinbergina, especially because all three taxa used here has been described in detail previously share a similar palaeogeographic provenance (Lieberman & Eldredge 1996; Lieberman 1997, (Baltica). Additionally, the trilobite genera 2000). The method relies on first constructing Eoredlichia and Olenoides, found to be sister an area cladogram by replacing the terminal taxa in the earlier analysis, were fused into a taxa from a phylogenetic hypothesis with the single terminal labeled here simply as “Trilobita” geographic regions occupied by those taxa. (as shown in Fig. 1). With the exceptions of Geographic occurrences are then reconstructed the taxa Tariccoia and Soomaspis, at the nodes of the cladogram using Fitch (1971) these changes resulted in all terminal taxa being optimisation (see Lieberman, 2000, p. 121-123), Cambrian in age. a parsimony algorithm. Once constructed, Global geographic occurrence data for all taxa information from the area cladogram is used to considered in this study were collected from a explore how the geographic distributions of taxa comprehensive review of the relevant literature, changed during cladogenesis by creating two especially the work of Raasch (1939), Bergström data matrices: one designed to retrieve congruent (1968), Dzik & Lendzion (1988), Hammann et 464 AAP Memoir 34 (2007)

Taxon Laurentia (1) Baltica (2) Siberia (3) Australia (4) Africa (5) China (6) Aglaspis Hall, 1862 Raasch 1939 Robison 1991; Briggs Alalcomenaeus Simonetta, 1970 et al. 1994 Cindarella Chen, Ramsköld, Edgecombe & Zhou in Chen et Hou et al. 2004 al. , 1996 Dicranocaris Briggs et al. , in Briggs et al. in press press Robison 1991; Briggs Emeraldella Walcott, 1912 et al. 1994 Eolimulus Bergström, 1968 Bergström (Placeholder for Weinbergina ) 1968 Helmetia Walcott, 1918 Briggs et al. 1994 Kuamaia Hou, 1987 Hou et al. 2004 Robison 1991; Briggs Zhao et al. 2002; Hou Leanchoilia Walcott, 1912 et al. 1994 et al. 2004 Dzik & Liwia Dzik & Lendzion, 1988 Lendzion 1988 Marrella Walcott, 1912 Briggs et al. 1994 Zhao et al. 2002 (Placeholder for Marrellomorpha) Hou et al. 2004; Misszhouia Chen et al. , 1997 Steiner et al. 2005 Hou et al. 2004; Robison 1991; Briggs Steiner et al. 2005; Naraoia Walcott, 1912 et al. 1994; Zhang et Nedin 1999 Lin 2006; Zhang et al. al. 2007 2007 Nettapezoura Briggs et al. , in Briggs et al. in press press Paleomerus Størmer, 1956 Tetlie & (Placeholder for Weinbergina ) Moore 2004 Retifacies Hou et al. , 1989 Hou et al. 2004 Sanctacaris Briggs & Collins, Briggs et al. 1994 1988 Saperion Hou et al. , 1991 Hou et al. 2004 Sidneyia Walcott, 1911 Briggs et al. 1994 Hou et al. 2004 Sinoburius Hou et al. , 1991 Hou et al. 2004 Hou et al. 2004; Skioldia Hou & Bergström, 1997 Steiner et al. 2005 Soomaspis Fortey & Theron, Fortey & Theron 1994 1994 Hammann et al. Tariccoia Hammann et al. , 1990 1990 Tegopelte Simonetta & Delle Briggs et al. 1994 Cave, 1975 Trilobita (Placeholder for Lieberman 2002 Eoredlichia and Olenoides ) Xandarella Hou et al. , 1991 Hagadorn 2002 Hou et al. 2004 Table 1. Regional biogeographic occurrence data (presence indicated by reference) for the arachnomorph taxa considered in this study. Presence in a region is indicated by a recent reference. al. (1990), Robison (1991), Briggs et al. (1994), These occurrence data are summarised in Table 1. Fortey & Theron (1994), Nedin (1999), Hagadorn The assignment of the biogeographic state of the (2002), Zhao et al. (2002), Hou et al. (2004), Tetlie Trilobita to Siberia is based upon the phylogenetic & Moore (2004), Steiner et al. (2005), Lin (2006), biogeographic analysis of Lieberman (2002), Zhang et al. (2007) and Briggs et al. (in press). which reconstructed Siberia as the region We grouped these occurrence records into six where eutrilobites originated. Additionally, a major tectonic provinces or areas of endemism: 1) hypothetical, ancestral outgroup region (0) was Laurentia (including taxa from present day British created to provide polarity for the biogeographic Columbia, Greenland, Pennsylvania, Utah and character data in the six ingroup regions; see Wisconsin); 2) Baltica (Poland and Sweden); further details below. 3) Siberia; 4) Australia (in this case the lower Some geographical assignments of taxa remain Cambrian deposits from Kangaroo Island); 5) controversial. Relevant examples include the Africa (in this case South Africa and Sardinia, occurrence records for Alalcomenaeus, Sidneyia which sat close to the margins of the African and Naraoia. It has been suggested (e.g., craton; Meert & Lieberman 2004); and 6) China Briggs & Collins 1999) that a small number of (in this case Yunnan and Guizhou provinces). Chengjiang specimens referred to Leanchoilia AAP Memoir 34 (2007) 465

1 1 1 1 1 1 1 1 1 1 2 2 2 2 2 2 2 2 2 2 3 3 3 3 3 3 3 3 3 3 4 4 4 4 1 2 3 4 5 6 7 8 9 0 1 2 3 4 5 6 7 8 9 0 1 2 3 4 5 6 7 8 9 0 1 2 3 4 5 6 7 8 9 0 1 2 3 Ancestor (0) 0000000000000000000000000000000000000000 0 0 0 Laurentia (1) 111211210111111111111000012111110021121 2 1 0 0 Baltica (2) 000000001000000000000000011001210000000 0 0 0 0 Siberia (3) 000000000000000000121000011001110010000 0 0 0 0 Australia (4) 000000000000000000000000100010000000000 0 0 0 0 Africa (5) 000000000000000000000000011001121100000 0 0 0 0 China (6) 112100100010010000112111112211110021211 1 2 1 1 Table 2. Matrix of biogeographical characters and character states used in the analysis of vicariance. State 0 signifies the primitive condition (absent) and states 1 and 2 signify the derived conditions (present). All characters treated as ordered (additive). Characters 5, 6, 8-10, 12, 13, 15-18, 22-24, 33, 34, 42 and 43 are uninformative and were deactivated prior to cladistic analysis. may be Alalcomenaeus, though this assignment easily tested, further evaluated and modified, if has not yet been conclusively determined and need be, as new fossil discoveries are made. several recent publications do not recognise We replaced the terminal taxon names on our this taxon as occurring in China (Hou et al. phylogenetic hypothesis (Hendricks & Lieberman 2004; Steiner et al. 2005). Therefore, we do not in press) with their associated geographic treat Alalcomenaeus as occurring in China in occurrence data (tectonic provinces 1-6); see this study. Sidneyia—first described from the Figure 1. Next, unordered Fitch optimisation Burgess Shale of Laurentia by Walcott (1911) (Fitch 1971) was used to optimise the geographic as S. inexpectans—has been reported (Zhang states on the tree topology, as described by et al. 2002) to occur in the Chengjiang as S. Lieberman (2000, p. 121-123). This resulted sinica, though Briggs et al. (in press) challenge in an area cladogram (see Fig. 1) that could this generic assignment. Nevertheless, Briggs be used to construct a vicariance matrix and et al. (in press) argue that S. sinica is similar to a geodispersal matrix, which are respectively Sidneyia inexpectans in many respects and was designed to discover congruent historical episodes likely closely related. Hence, we have chosen of vicariance and range expansion (Lieberman to include an occurrence record for Sidneyia in 2003a). These matrices were constructed and China. Recently, Lin et al. (2006) and Zhang et al. coded from the area cladogram (Fig. 1) following (2007) challenged Nedin’s (1999) identification of the methodology described by Lieberman (2000, Naraoia in the , claiming instead p. 144-150). All characters were treated as ordered that Nedin’s material may represent Primicaris or (=additive), with a vicariant transition between Skania. Nedin’s (1999, fig. 2a) figured specimen a region denoted by a transition from state ‘1’ is somewhat poorly preserved and in general form to state ‘2’ in the vicariance matrix; similarly, a could be compatible with an interpretation either transition involving range expansion would be as Naraoia, Primicaris or Skania. Specimens denoted by a transition from state ‘1’ to state ‘2’ of Naraoia tend to be larger than specimens of in the geodispersal matrix. The vicariance matrix Primicaris and Skania (see sizes for these taxa is shown in Table 2 and the geodispersal matrix is presented by Zhang et al. 2003; Lin et al. 2006), shown in Table 3. In both cases, all biogeographic however, and the size of Nedin’s (1999, fig. 2a) characters for the hypothetical ancestral outgroup figured specimen (ca. 12 mm) from the Emu Bay region (0) were coded as absent in order to Shale is within the range of Naraoia, but appears provide polarity to the characters in the ingroup to be too large for the other two taxa. Thus, until regions. These matrices were used to reconstruct decisive Emu Bay Shale specimens present the best supported vicariance and geodispersal themselves to the contrary, we follow Nedin’s topologies using the parsimony criterion, which (1999) identification of his material from the Emu may be interpreted as follows: on a vicariance Bay Shale, South Australia. tree (or a consensus of multiple trees), the closer We acknowledge the possibility that potential two regions sit on the tree, the more recently they biases may have led to some true taxon occurrence were separated (Lieberman 2003a); the closer records going unrecognised due to either their two regions sit on the geodispersal tree, the more missing fossil record (not being fossilised due recently they were joined (Lieberman 2003a). to taphonomic biases) or their lack of collection Significant amounts of similarity between the two to date. This is a challenging problem without trees may suggest that the same environmental a simple solution: how should one weigh processes responsible for vicariance were negative occurrence evidence? We argue that the also responsible for geodispersal (e.g., cyclic distributional patterns considered here could be processes such as sea-level change). By contrast, 466 AAP Memoir 34 (2007)

1 1 1 1 1 1 1 1 1 1 2 2 2 2 2 2 2 2 2 2 3 3 3 3 3 3 3 3 3 3 4 4 4 4 1 2 3 4 5 6 7 8 9 0 1 2 3 4 5 6 7 8 9 0 1 2 3 4 5 6 7 8 9 0 1 2 3 4 5 6 7 8 9 0 1 2 3 Ancestor (0) 0000000000000000000000000000000000000000 0 0 0 Laurentia (1) 110111111111111111100000011011000011011 1 0 0 0 Baltica (2) 000000002000000000000000020001100000000 0 0 0 0 Siberia (3) 000000000000000000210000010001000000000 0 0 0 0 Australia (4) 000000000000000000000000200020000000000 0 0 0 0 Africa (5) 000000000000000000000000020001011100000 0 0 0 0 China (6) 111000000020020000101111111111000011101 0 1 1 1 Table 3. Matrix of biogeographical characters and character states used in the analysis of geodispersal. State 0 signifies the primitive condition (absent) and states 1 and 2 signify the derived conditions (present). All characters treated as ordered (additive). Characters 3-8, 10, 12, 13, 15-18, 20-24, 28, 31-34, 37, 38 and 40-43 are uninformative and were deactivated prior to cladistic analysis. significant differences between the two trees may tree is well resolved. Note, however, that no suggest that tectonic events, a single profound characters support separation of Africa from episode of sea-level rise (or fall), or chance Baltica, resulting in a collapsed node; thus, it is dispersal events may have played more important not clear whether Baltica is positioned basal to roles in influencing the observed biogeographic Africa, or vice-versa. patterns in a given group (Lieberman 2003a); see The analysis of the geodispersal matrix resulted Lieberman & Eldredge (1996) and Lieberman in the discovery of a single most parsimonious tree (1997, 2000) for additional discussion. of length 24 steps (CI = 0.87, RI = 0.82), which The vicariance and geodispersal matrices were is shown in Figure 2B. This well resolved tree managed using WinClada (Nixon 1999-2002) and features two major groupings: 1) a monophyletic heuristic parsimony analyses were independently area composed of Siberia, Laurentia and China; carried out on each matrix using NONA 2.0 and 2) a sister-area relationship for Baltica and (Goloboff 1999). Prior to each parsimony Africa. These two groupings in turn have a sister- analysis, all uninformative characters were group relationship, with Australia positioned selected and deactivated using WinClada. The (relatively) one node down the tree. matrices were then submitted to NONA for The vicariance (Fig. 2A) and geodispersal (Fig. analysis. The tree-bisection reconnection (TBR) 2B) trees are very similar in appearance. Both algorithm of Swofford & Olsen (1990) was used show a derived sister-area relationship between in NONA to search for most parsimonious tree Laurentia and China and show Siberia one node (MPT) topologies. Each analysis involved 2,500 “down the tree” from this grouping. Further, both replications (during each replication, 15 trees show a basal position for Australia. As described were stored in memory for branch-swapping) and above, and shown in Figure 2A-B, the vicariance space was held in memory to store up to 10,000 and geodispersal trees differ only in their relative trees. After this search, the shortest MPT’s were placements of Baltica and Africa. swapped to completion and only unique trees were saved. The command line for this search DISCUSSION AND CONCLUSIONS sequence in NONA is “h10000; h/15; mult*2500; The results from the analysis of phylogenetic max*; unique; sv* filename.tre sv/;”. Ensemble biogeographic patterns in predominantly Cambrian consistency index (CI; Kluge & Farris 1969) and arachnomorphs are rather different from the results retention index (RI; Farris 1989) values were then that have been observed previously in Cambrian computed using NONA’s “fit;” command. Saved trilobites (Lieberman 2002, 2003a). In particular, trees were imported into WinClada for study and the most parsimonious patterns of geodispersal nodes lacking character support were collapsed. are well resolved for the arachnomorphs (Fig. 2B), Additionally, bootstrap (Felsenstein 1985) and whereas the patterns from the trilobites showed jackknife support (Farris et al. 1996) values were relatively little resolution. This suggests that the calculated for each matrix using NONA (executed arachnomorphs experienced significantly more through WinClada). congruent episodes of range expansion during the Cambrian than trilobites did. Another fundamental RESULTS difference between the biogeographic patterns The parsimony analysis of the vicariance matrix in arachnomorphs and trilobites involves the resulted in the discovery of a single most association between the faunas of Laurentia and parsimonious tree of length 41 steps (CI = 0.95; China. These regions are sister areas in both RI = 0.93), which is shown in Figure 2A. The the arachnomorph vicariance and geodispersal AAP Memoir 34 (2007) 467

Ancestor (0) Shergold & Laurie 1997)]. By contrast, the Vicariance Cambrian Burgess Shale-type faunas of Laurentia Australia (4) and China share many elements in common, including arachnomorphs. Baltica (2) Still, on tectonic grounds, it is somewhat Africa (5) unexpected to find such a close area relationship 99,99 between Laurentia and China (Fig. 2A): these 0,0 Siberia (3) two regions were last in tectonic contact about 98,97 Laurentia (1) 750 Ma (see Meert & Lieberman 2004, but also 100,100 see Veevers et al. 1997 for an alternative breakup A China (6) time). The close association between Laurentia and China in our area cladograms may be partly related to the fact that the most diverse and well known Cambrian arthropod faunas occur in Laurentia (for example, the Middle Cambrian Burgess Shale biota [e.g., Briggs et al. 1994] and Geodispersal Ancestor (0) biotas of similar age from Utah [e.g., Robison Australia (4) 1991; Briggs et al. in press]) and China (for example the Chengjiang biota [e.g., Hou et al. Baltica (2) 2004]). It has been shown previously that low 61,60 diversity faunas can sometimes map “down the Africa (5) tree” in phylogenetic biogeographic analyses, 100,100 73,72 Siberia (3) causing high diversity faunas to potentially group together (Fortey & Cocks 1992). We acknowledge 53,54 Laurentia (1) this potential bias. However, it is worth noting B 99,99 China (6) that the close area relationship we recovered here Fig. 2. Single most parsimonious area cladograms between Laurentia and China does seem to reflect resulting from modified Brooks Parsimony Analyses a truly different pattern from the one uncovered in of the vicariance (2A; see Table 2) and geodispersal the trilobites. In particular, while the non-trilobite (2B; see Table 3) matrices. Values at nodes are faunas of Laurentia and China share many bootstrap (normal type) and jackknife (italicised type) elements in common (e.g., see discussion above), support values. The vicariance tree (2A) is 41 steps the trilobites that co-occur in the early Cambrian in length (CI = 0.95; RI = 0.93); one node is collapsed Chengjiang biota and other early Cambrian or due to lack of character support. The geodispersal Middle Cambrian Burgess Shale-type faunas in tree is 24 steps in length (CI = 0.87, RI = 0.82) and is Laurentia share very few elements in common. completely resolved. Further, many non-trilobite arthropod genera (for instance, the arachnomorphs Leanchoilia and trees (Fig. 2A-B); by contrast, the trilobite Naraoia, as well as , Branchiocaris, faunas of Laurentia and China do not have a Canadaspis, Isoxys, Marrella, Tuzoia and Waptia) close area relationship. Our recovered pattern are widely distributed, and occur in both Laurentia is part of a more general pattern that other and China. This too, as mentioned above, is authors have recognised. For instance, of the 112 very different from the trilobites, which tend to early Cambrian trilobite taxa from the western be much more narrowly distributed, except in Gondwanan margin considered in the study the case of the agnostoids (Shergold & Laurie by Álvaro et al. (2003, fig. 5), only one 1997). We are not alone in recognising a biotic () is found in both Laurentia and association between Laurentia and China near the China. Similarly, of 94 Middle Cambrian trilobite beginning of the Phanerozoic: Waggoner (1999) genera (also from western Gondwana), Álvaro et recovered a biogeographic association between al. (2003, fig. 6) reported only eight (Centropleura, some taxa from southwestern Laurentia Diplagnostus, Doryagnostus, Hypagnostus, and south China, although our data are based on Lejopyge, Oidalagnostus, Peratagnostus and different methods, and other aspects of our results ) common to Laurentia and China. are very different. [Of these nine Cambrian trilobite genera, only When dispersal is minimal or absent, the Centropleura belongs to the polymeroid trilobite timing of tectonic events—for example, the age ; the other eight taxa are ‘miomeroids’. when two regions that are now separated were The latter likely had a pelagic lifestyle and last joined and homogeneous—can potentially consequently were more widely distributed than be used to constrain the age of origination of polymeroids (Laurie 1988; Shergold et al. 1990; monophyletic groups. For example, studies of 468 AAP Memoir 34 (2007)

Marrellomorpha otherwise, in trilobite lineages. By contrast, the congruent patterns of vicariance and geodispersal Retifacies observed here in arachnomorphs (particularly Emeraldella between Laurentia and China) mean that the tectonic vicariance between these regions does Aglaspis not equate to the last time of contact between Weinbergina their respective faunas. This is because dispersing lineages could recolonise regions after they were Sidneyia no longer in contact geologically. Still, the fact Nettapezoura that biogeographic patterns indicate that trilobites likely originated somewhere in the interval of Leanchoilia 600-550 Ma (Lieberman 2003a; Lieberman Sanctacaris & Meert 2004) can be used as a phylogenetic constraint on the origination time of a whole host Alalcomenaeus of arachnomorph lineages. In particular, these Dicranocaris lineages—including the true chelicerates—must have minimally also commenced diverging by Eoredlichia 600-550 Ma (Fig. 3). >550 Olenoides The failure of Australia to biogeographically group with China also differs from the inferred >550 Sinoburius sequence of late Neoproterozoic and early Cambrian tectonic events (Lieberman & Meert Cindarella 2004; Meert & Lieberman 2004). This, and Xandarella the fact that there are very strong similarities between our vicariance and geodispersal trees Misszhouia (Fig. 2A-B), may suggest that in the case of these arachnomorphs, tectonics was not the primary Naraoia factor that governed diversification. Instead, the >550 Liwia processes producing the pattern in the vicariance tree may have been those driving the patterns in Tariccoia the geodispersal tree (Lieberman 2000) and likely Soomaspis included cyclic processes including repeated episodes of sea-level rise and fall. Kuamaia The palaeobiogeographic patterns described Helmetia herein also have the potential to inform our understanding of macroevolutionary processes Tegopelte operating during (and immediately prior to) the Skioldia Cambrian radiation. This is because Cambrian trilobites and many non-trilobite arthropods show Saperion not only differing biogeographical patterns, but Fig. 3. Strict consensus of the 12 most parsimonious also different patterns of extinction across the trees found in the analysis of Hendricks & Lieberman early-Middle Cambrian boundary, as has been (in press) with minimum ages of origination (in noted previously (Conway Morris & Robison millions of years ago) mapped at some nodes. 1986; Conway Morris 1989; Lieberman 2003c). Biogeographic data suggest that trilobites (represented These two aspects may be related. Highly endemic here by Eoredlichia and Olenoides) originated by early Cambrian trilobites show significant 550-600 Ma. The derived position of the trilobites in taxonomic turnover at the early-Middle Cambrian this tree implies that many other arachnomorph taxa boundary (Palmer 1998; Lieberman 2003c), while must also have originated by no later than 550 Ma. many other non-trilobite taxa cross this boundary unscathed. This extinction resistance is in fact trilobite palaeobiogeography were used to make reflected in the faunal similarities between the inferences about the timing of the Cambrian early Cambrian Chengjiang fauna of China and radiation (e.g., Lieberman 2003b; Meert & other Cambrian faunas in Laurentia, including the Lieberman 2004). This was possible because not Middle Cambrian Burgess Shale fauna of British only did the vicariance patterns in trilobites match Columbia and the Middle Cambrian Pioche Shale the pattern predicted for the 600-550 Ma breakup of Nevada (e.g., Lieberman 2003c). The topic of of Pannotia, but also there was very limited the causal link between broad geographic range evidence for any kind of dispersal, congruent or and extinction resistance has been frequently AAP Memoir 34 (2007) 469 supported (Eldredge 1979; Stanley 1979; considered with reference to natural theology. Vrba 1980; Hansen 1982; Gould 2002) and William Pickering, London, Vol. 1, 618 p., Vol 2, we hypothesise that such an association may 128 p. have been important for the early evolution and Bu d d , G.E., 2002. A palaeontological solution to the persistence of many metazoan taxa. In particular, arthropod head problem. Nature 417, 271-275. the relatively endemic nature of certain early Ch e n J.-Y., Ed ge c o m be , G.D. & Ra m s k ö l d , L., 1997. Cambrian trilobites, especially the olenellines, Morphological and ecological disparity in naraoiids would have made them more susceptible to (Arthropoda) from the Early Cambrian Chengjiang extinction, whereas by contrast, more broadly Fauna, China. Records of the Australian Museum distributed Cambrian non-trilobite arthropod taxa 49, 1-24. would have been naturally extinction resistant. Ch e n J.-Y., Zh o u G.-Q., Zh u M.-Y. & Ye h K.-Y., 1996. This, however, remains to be studied in greater The Chengjiang Biota. A Unique Window of the detail. . National Museum of Natural Science, Taichung, 222 p. ACKNOWLEDGEMENTS Co n w a y Mo r r i s , S., 1989. The persistence of Burgess We thank the Gunther family, Sue Halgedahl, Shale-type faunas: implications for the evolution Richard Jarrard and Dick Robison for access to of deeper-water faunas. Transactions of the fossil material that proved highly useful to this Royal Society of Edinburgh: Earth Sciences 80, study. Thanks also go to , Greg 271-283. Edgecombe, Rachel Moore and Dick Robison for Co n w a y Mo r r i s , S. & Ro b i s o n , R.A., 1986. Middle scientific discussions on Cambrian arthropods. Cambrian priapulids and other soft-bodied We also thank John Paterson and two anonymous from Utah and Spain. University of Kansas reviewers, whose comments improved this Paleontological Contributions 117, 1-22. manuscript. This research was supported by Co t t o n , T.J. & Br a d d y , S.J., 2004. The phylogeny NSF EAR-0518976, NSF DEB-0716162, NASA of arachnomorph arthropods and the origin of the Astrobiology NNG04GM41G, and a Madison and . Transactions of the Royal Society of Lila Self Faculty Scholar Award. Edinburgh: Earth Sciences 94, 169-193. Da l z i e l , I.W.D., 1997. Neoproterozoic-Paleozoic REFERENCES geography and tectonics: review, hypothesis, Ál v a r o , J.J., El i c k i , O., Ge y e r , G., Ru s h t o n , A.W.A. environmental speculation. Bulletin of the Geological & Sh e r g o l d , J.H., 2003. Palaeogeographical Society of America 190, 16-42. controls on the Cambrian trilobite immigration Dz i k , J. & Le n d z i o n , K., 1988. The oldest arthropods of and evolutionary patterns reported in the the East European Platform. Lethaia 21, 29-38. western Gondwana margin. Palaeogeography, Eb a c h , M.C. & Ed ge c o m be , G.D., 2001. Biogeography Palaeoclimatology, Palaeoecology 195, 5-35. and the nature and timing of the Cambrian radiation. Be r g s t r ö m , J., 1968. Eolimulus, a lower Cambrian 235-289 in Adrain, J.M., Edgecombe, G.D. & xiphosurid from Sweden. Geologiska Föreningens Lieberman, B.S. (eds), Fossils, phylogeny, and i Stockholm Förhandlingar 90, 489-503. form: an analytical approach. Kluwer Academic/ Br e m e r , K., 1988. The limits of amino acid sequence Plenum Publishers, New York. data in angiosperm phylogenetic reconstruction. Ed ge c o m be , G.D. & Ra m s k ö l d , L., 1999. Relationships Evolution 42, 795-803. of Cambrian Arachnata and the systematic position Br e m e r , K., 1994. Branch support and tree stability. of Trilobita. Journal of 73, 263-287. 10, 295-304. El d r e d ge , N., 1979. Alternative approaches to Br i gg s , D.E.G. & Co l l i n s , D., 1988. A Middle evolutionary theory. Bulletin of the Carnegie Cambrian chelicerate from Mount Stephen, British Museum of Natural History 13, 7-19. Columbia. Palaeontology 31, 779-798. Fa r r i s , J.S., 1989. The retention index and rescaled Br i gg s , D.E.G. & Co l l i n s , D., 1999. The arthropod consistency index. Cladistics 5, 417-419. Alalcomenaeus cambricus Simonetta, from Fa r r i s , J.S., Al be r t , V.A., Kä l l e r s j ö , M., Li p s c o m b , the Middle Cambrian Burgess Shale of British D. & Kl u ge , A.G., 1996. Parsimony jackknifing Columbia. Palaeontology 42, 953-977. outperforms neighbor-joining. Cladistics 12, Br i gg s , D.E.G., Er w i n , D.H. & Co l l i e r , F.J., 1994. The 99-124. fossils of the Burgess Shale. Smithsonian Institution, Fe l s e n s t e i n , J., 1985. Confidence limits on phylogenies: Washington, 238 p. an approach using the bootstrap. Evolution 39, Br i gg s , D.E.G., Li ebe r m a n , B.S., He n d r i c k s , J.R., 783-791. Ha l ge d a h l , S.L. & Ja r r a r d , R.D., in press. Soft- Fi t c h , W.M., 1971. Toward defining the course of bodied arthropods from the Middle Cambrian of evolution: minimum change for a specific tree Utah. Journal of Paleontology 82, 238-254. topology. Systematic Zoology 20, 406-416. Bu c k l a n d , W., 1836. Geology and mineralogy Fo r t e y , R.A. & Co c k s , L.R.M., 1992. The early 470 AAP Memoir 34 (2007)

Palaeozoic of the North Atlantic region as a test case 22, 1-7. for the use of fossils in continental reconstruction. La u r i e , J.R., 1988. Revision of some Australian Tectonophysics 206, 147-158. Ptychagnostinae (, Cambrian). Alcheringa Fo r t e y , R.A. & Th e r o n , J.N., 1994. A new Ordovician 12, 169-205. arthropod, Soomapsis, and the agnostid problem. Li ebe r m a n , B.S., 1997. Early Cambrian paleogeography Palaeontology 37, 841-861. and tectonic history: a biogeographic approach. Go l o b o ff , P., 1999. NONA, version 2.0. Published by Geology 25, 1039-1042. the author, Tucumán. Li ebe r m a n , B.S., 1999. Systematic revision of the Go u l d , S.J., 2002. The structure of evolutionary theory. Olenelloidea (Trilobita, Cambrian). Bulletin of Belknap Press, Cambridge, 1432 p. the Yale University Peabody Museum of Natural Ha g a d o r n , J.W., 2002. Burgess Shale-type localities: History 45, 1-150. the global picture. 91-116 in Bottjer, D.J., Etter, Li ebe r m a n , B.S., 2000. Paleobiogeography: using W., Hagadorn, J.W. & Tang, C. (eds), Exceptional fossils to study global change, plate tectonics, Fossil Preservation: A Unique View on the Evolution and evolution. Kluwer Academic Press/Plenum of Marine Life. Columbia University Press, New Publishing, New York, 208 p. York. Li ebe r m a n , B.S., 2001. Phylogenetic analysis of the Ha l l , J., 1862. A new from the Potsdam Olenellina Walcott, 1890 (Trilobita, Cambrian). Sandstone. Canadian Naturalist 7, 443-445. Journal of Paleontology 75, 96-115. Ha m m a n n , W., La s k e , R. & Pi l l o l a , G.L., 1990. Li ebe r m a n , B.S., 2002. Phylogenetic analysis of some Tariccoia arrusensis n. g. n. sp., an unusual trilobite- basal early Cambrian trilobites, the biogeographic like arthropod. Rediscovery of the “phyllocarid” origins of the Eutrilobita, and the timing of the beds of Taricco (1922) in the Ordovician “Puddinga” Cambrian radiation. Journal of Paleontology 76, sequence of Sardinia. Bolletino della Società 692-708. Paleontologica Italiana 29, 163-178. Li ebe r m a n , B.S., 2003a. Biogeography of the Trilobita Ha n s e n , T.A., 1982. Modes of larval development during the Cambrian radiation: deducing geological in early Tertiary neogastropods. 8, processes from trilobite evolution. Special Papers 367-377. in Palaeontology 70, 59-72. He n d r i c k s , J.R. & Li ebe r m a n , B.S., in press. Li ebe r m a n , B.S., 2003b. Taking the pulse of the New phylogenetic insights into the Cambrian Cambrian radiation. Integrative and Comparative radiation of arachnomorph arthropods. Journal of Biology 43, 229-237. Paleontology. Li ebe r m a n , B.S., 2003c. A new soft-bodied fauna: Ho ff m a n , P.F., 1991. Did the breakout of Laurentia turn the Pioche Formation of Nevada. Journal of Gondwana inside out? Science 252, 1409-1412. Paleontology 77, 674-690. Ho ff m a n , P.F., Ka u f m a n , A.J., Ha l v e r s o n , G.P. & Li ebe r m a n , B.S. & El d r e d ge , N., 1996. Trilobite Sc h r a g , D.P., 1998. A Neoproterozoic snowball biogeography in the Middle Devonian: geological Earth. Science 281, 1342-1346. processes and analytical methods. Paleobiology Ho u X.-G., 1987. Three new large arthropods from the 22, 66-79. Lower Cambrian, Chengjiang, eastern Yunnan. Acta Li ebe r m a n , B.S. & Mee r t , J.G., 2004. Biogeography Palaeontologica Sinica 26, 272-285. and the nature and timing of the Cambrian radiation. Ho u X.-G., Al d r i d ge , R.J., Be r g s t r ö m , J., Si v e t e r , 79-90 in Lipps, J.H. & Waggoner, B.M. (eds), D.J., Si v e t e r , D.J. & Fe n g X.-H., 2004. The Neoproterozoic-Cambrian biological revolutions. Cambrian Fossils of Chengjiang, China: The Paleontological Society Papers, Volume 10. Flowering of Early Animal Life. Blackwell Science Li n J.-P., 2006. Taphonomy of naraoiids (Arthropoda) Ltd., Malden, 233 p. from the Middle Cambrian Kaili biota, Guizhou Ho u X.-G. & Be r g s t r ö m , J., 1997. Arthropods of the Province, south China. Palaios 21, 15-25. Lower Cambrian Chengjiang fauna, southwest Li n J.-P., Go n III, S.M., Ge h l i n g , J.G., Ba b c o c k , L.E., China. Fossils and Strata 45, 1-116. Zh a o Y.-L., Zh a n g X.-L., Hu S.-X., Yu a n J.-L., Ho u X.-G., Ch e n J.-Y. & Lu H.-Z., 1989. Early Yu M.-Y. & Pe n g , J., 2006. A -like Cambrian new arthropods from Chengjiang, arthropod from the Cambrian of south China. Yunnan. Acta Palaeontologica Sinica 28, 42-57. Historical Biology 18, 33-45. Ho u X.-G., Ra m s k ö l d , L. & Be r g s t r ö m , J., 1991. Mee r t , J.G. & Li ebe r m a n , B.S., 2004. A palaeomagnetic Composition and preservation of the Chengjiang and palaeobiogeographic perspective on latest fauna - a Lower Cambrian soft-bodied biota. Neoproterozoic and early Cambrian tectonic events. Zoologica Scripta 20, 395-411. Journal of the Geological Society of London 161, Kl u ge , A.G. & Fa r r i s , J.S., 1969. Quantitative 1-11. phyletics and the evolution of anurans. Systematic Ne d i n , C., 1999. Anomalocaris on Zoology 18, 1-32. nonmineralized and mineralized trilobites. Geology Kn o l l , A.H., 1996. Daughter of time. Paleobiology 27, 987-990. AAP Memoir 34 (2007) 471

Ni x o n , K.C., 1999-2002. WinClada, version 1.00.08. associations of South China. Palaeogeography, Published by the author, Ithaca. Palaeoclimatology, Palaeoecology 220, 129-152. Pa l m e r , A.R., 1998. Terminal early Cambrian St ø r m e r , L., 1956. A Lower Cambrian merostome from extinction of the Olenellina: documentation from the Sweden. Arkiv för Zoologi, serie 2, 9, 507-514. Pioche Formation, Nevada. Journal of Paleontology Sw o ff o r d , D.L. & Ol s e n , G.J., 1990. Phylogeny 72, 650-672. reconstruction. 411-501 in Hillis, D.M. & Moritz, Pe t e r s o n , K.J., Ly o n s , J.B., No w a k , K.S., Ta k a c s , C. (eds), Molecular Systematics. Sinauer Associates, C.M., Wa r g o , M.J. & McPee k , M.A., 2004. Inc., Sunderland. Estimating metazoan divergence times with a Te t l i e , O.E. & Mo o r e , R.A., 2004. A new molecular clock. Proceedings of the National specimen of Paleomerus hamiltoni (Arthropoda; Academy of Sciences of the United States of America Arachnomorpha). Transactions of the Royal Society 101, 6536-6541. of Edinburgh: Earth Sciences 94, 195-198. Ra a s c h , G.O., 1939. Cambrian Merostomata. Vee v e r s , J.J., Wa l t e r , M.R. & Sc h e i b n e r , E., 1997. Geological Society of America, Special Papers Neoproterozoic tectonics of Australia-Antarctica 19, 1-146. and Laurentia and the 560 Ma birth of the Pacific Ro b i s o n , R.A., 1991. Middle Cambrian biotic diversity: Ocean reflect the 400 m.y. Pangean supercycle. examples from four Utah Lagerstätten. 77-98 in Journal of Geology 105, 225-242. Simonetta, A. & Conway Morris, S. (eds), The Vr b a , E.S., 1980. Evolution, species and fossils: how Early Evolution of Metazoa and the Significance does life evolve? South African Journal of Science of Problematic Taxa. Cambridge University Press, 76, 61-84. Cambridge. Wa gg o n e r , B., 1999. Biogeographic analyses of Sc h o l t z , G. & Ed ge c o m be , G.D., 2006. The evolution the Ediacara biota: a conflict with paleotectonic of arthropod heads: reconciling morphological, reconstructions. Paleobiology 25, 440-458. developmental and palaeontological evidence. Wa l c o t t , C.D., 1911. Cambrian Geology and Development Genes and Evolution 216, 395-415. Paleontology II. Middle Cambrian Merostomata. Sh e r g o l d , J.H., 1977. Classification of the trilobite Smithsonian Miscellaneous Collections 57, 17-40. Pseudagnostus. Palaeontology 20, 69-100. Wa l c o t t , C.D., 1912. Cambrian Geology and Sh e r g o l d , J.H., 1988. Review of trilobite biofacies Paleontology II. Middle Cambrian Branchiopoda, distributions and the Cambrian-Ordovician Malacostraca, Trilobita and Merostomata. Smith- boundary. Geological Magazine 125, 363-380. sonian Miscellaneous Collections 57, 145-228. Sh e r g o l d , J.H., 1991. Protaspid and early meraspid Wa l c o t t , C.D., 1918. Geological explorations in the growth stages of the eodiscid trilobite Canadian Rockies. Explorations and fieldwork of ocellata Jell, and their implication for classification. the Smithsonian Institution in 1917. Smithsonian Alcheringa 15, 65-86. Miscellaneous Collections 68, 4-20. Sh e r g o l d , J.H. & La u r i e , J.R., 1997. Introduction to Wi l l s , M.A., Br i gg s , D.E.G., Fo r t e y , R.A., Wi l k i n s o n , the Suborder Agnostina. 331-384 in Kaesler, R.L. M. & Sn e a t h , P.H.A., 1998. An arthropod phylogeny (ed.), Treatise on Invertebrate Paleontology, Part based on fossil and recent taxa. 33-105 in Edgecombe, O, Arthropoda 1, Trilobita, Revised. Geological G.D. (ed.), Arthropod Fossils and Phylogeny. Society of America, Boulder and University of Columbia University Press, New York. Kansas Press, Lawrence. Zh a n g X.-L., Ha n J. & Sh u D., 2002. New occurrence Sh e r g o l d , J.H., La u r i e , J.R. & Su n X., 1990. of the Burgess Shale arthropod Sidneyia in the Classification and review of the trilobite order Early Cambrian Chengjiang Lagerstätte (South Agnostida Salter, 1864: an Australian perspective. China), and revision of the arthropod Urokodia. Bureau of Mineral Resources, Geology and Alcheringa 26, 1-8. Geophysics, Report 296, 1-92. Zh a n g X.-L., Ha n J., Zh a n g Z.-F., Li u H.-Q. & Sh u Si m o n e t t a , A.M., 1970. Studies on non trilobite D.-G., 2003. Reconsideration of the supposed arthropods of the Burgess Shale (Middle Cambrian). naraoiid larva from the Early Cambrian Chengjiang Palaeontographica Italica 56, 35-45. lagerstätte, south China. Palaeontology 46, Si m o n e t t a , A.M. & De l l e Ca v e , L., 1975. The 447-465. Cambrian non trilobite arthropods from the Zh a n g X.-L., Sh u D.-G. & Er w i n D.H., 2007. Cambrian Burgess Shale of British Columbia. A study of naraoiids (Arthropoda): morphology, ontogeny, their comparative morphology, , and systematics, and evolutionary relationships. evolutionary significance. Palaeontographica Paleontological Society Memoir 68, 1-52. Italica 69, 1-37. Zh a o Y., Yu a n J., Zh u M., Ya n g R., Qu o Q., Pe n g St a n l e y , S.M., 1979. Macroevolution. W.H. Freeman, J. & Ya n g X., 2002. Progress and significance in San Francisco, 332 p. research on the early Middle Cambrian Kaili biota, St e i n e r , M., Zh u M., Zh a o Y. & Er d t m a n n , B.-D., Guizhou Province, China. Progress in Natural 2005. Lower Cambrian Burgess Shale-type fossil Science 12, 649-654.