Macroevolutionary Patterns and Processes During the Cambrian Radiation: Integrating Evidence from Fossils and Molecules

AÇOREANA, 2011, 7: 15-38

MACROEVOLUTIONARY PATTERNS AND PROCESSES DURING THE CAMBRIAN RADIATION: INTEGRATING EVIDENCE FROM FOSSILS AND MOLECULES

Bruce S. Lieberman1 & Paulyn Cartwright2

1 Department of Geology and Biodiversity Institute and 2 Department of Ecology and Evolutionary Biology, University of Kansas, Lawrence, KS 66045 e-mail: [email protected]

ABSTRACT The Cambrian radiation represents a key episode in the history of life when most of the major animal lineages appeared and diversiﬁ ed in the fossil record. Unravelling the pa erns and processes driving the Cambrian radiation has proven challenging. We discuss several lines of evidence that provide additional understanding about the Cambrian radiation including trilobite phylogeny and biogeography, cnidarian fossils and phylogenies, metazoan phylogenies and the molecular clock, genomics and evolutionary development, and palaeoecology. We argue that by integrating these disparate lines of evidence, a more comprehensive view of the Cambrian radiation emerges.

RESUMO A radiação Câmbrica representa um episódio-chave na história da vida, quando a maior parte das linhagens animais apareceu e se diversifi cou no registo fóssil. Descobrir os padrões e os processos que conduziram a radiação Câmbrica tem-se mostrado um desafi o. Discutimos aqui várias linhas de evidência que proporcionam entendimento adicional sobre a radiação Câmbrica incluindo fi logenia e biogeografi a das trilobites, fósseis e fi logenias de cnidários, fi logenias e relógio molecular dos metazoários, genómica e desenvolvimento evolutivo, e paleoecologia. Argumentamos que, integrando essas linhas de evidência variadas, emerge uma visão mais abrangente da radiação Câmbrica.

INTRODUCTION cesses relating to the birth, death, and persistence of spe- acroevolution is the study cies. As such, a special aspect Mof the pa erns and pro- of the study of macroevolution

PPaginação_21.inddaginação_21.indd 1515 119-01-20129-01-2012 11:50:4511:50:45 16AÇOREANA 2011, Suplemento 7: 15-38

has been a focus on investigat- netic precision about the taxa ing key episodes in the history involved. For instance, it is now of life that involve differential recognized that several animal proliferation or extinction of phyla proliferated well before species. The fossil record is our the start of the Cambrian includ- one true repository of species’ ing sponges and the Ediacaran births and deaths. One of the biota, which likely contains some most important episodes in the stem group cnidarians, or their history of life, at least in terms of relatives. However, establish- its placement in time and phylo- ing strong phylogenetic links be- genetic space, was the Cambrian tween elements of the Ediacaran radiation. Consideration of the biota and bilaterian animal phyla evolutionary significance of this has proven more diﬃ cult. key episode dates back at least Darwin’s (1859) perspective to Darwin (1859), and it will be on the Cambrian radiation is the focus of our contribution. worth considering. Notably, Since there is such a long history Darwin argued that the major of study, scientists‘ conclusions groups of taxa that appeared about the episode and its sig- in the fossil record at this time nificance have changed through must have evolved well back time (see Lieberman, 1999a, into the pre-Cambrian. It ap- 2003a; Knoll, 2003; Valentine, pears now that Darwin may 2004; Brasier, 2009). Originally have been partly inaccurate to this radiation was held to be the extent that he claimed the largely synonymous with the roots of Cambrian radiation taxa origins and diversification of extended way back into the pre- animals. However, more recent- Cambrian, but he was right to ly, a nuanced view has emerged, suggest that the Cambrian radi- and now it is more typically ation was not solely an explosive treated as the initial appearance evolutionary event writ large in and proliferation of abundant the fossil record. Instead, the metazoan remains in the fossil Cambrian radiation had some record (Knoll, 2003; Lieberman, pre-Cambrian fuse, where the 2003a; Valentine, 2004; Brasier, taxa had originated and started 2009). Part of the transition to evolving (a lit fuse) before the this more nuanced view has explosive radiation (the bang) involved increasing phyloge- appeared on the scene. Because

PPaginação_21.inddaginação_21.indd 1616 119-01-20129-01-2012 11:50:5111:50:51 LIEBERMAN & CARTWRIGHT: CAMBRIAN RADIATION 17

of this, a key question now is Information from palaeontol- how long before the radiation ogy and development in some re- did the component taxa actually spects played an important role evolve. This is fundamental be- in the formulation of what is re- cause it determines whether the ferred to as the Neo-Darwinian Cambrian radiation really is a synthesis (e.g., Simpson, 1944; key episode in the history of life, de Beer, 1940) as practitioners from an evolutionary perspec- from these areas were involved tive, and does indeed represent in what is treated as a hallmark a dramatic evolutionary prolif- event in evolutionary biology. eration or radiation, or instead However, by the same token it marks some set of changing eco- could be argued that when it logical or environmental condi- came to incorporating actual tions that allowed already ex- data or theoretical outlooks, tant organisms to become more neither of these disciplines was visible in the fossil record, either well represented in the body of through increases in abundance evolutionary theory that is as- or size or changes in fossiliza- sociated with that synthesis (see tion potential. Here we con- Eldredge, 1985; Gould, 2002). sider this issue in greater detail, Major advances in evolutionary marshalling various lines of evi- biology have come, and are apt dence from the fossil record and to continue to come, from more the extant biota. Then we con- fully incorporating information sider the specific set of changes, from palaeontology and com- genetic and environmental, that parative development. may have caused the radiation One important aspect of to happen. We conclude with studying any interval in the his- some discussion on how to forge tory of life is having information a synthesis between disparate about the pattern of evolution lines of evidence, from trilobite during that time period. Thus, phylogenies to genetic toolkits, phylogenies are a prerequisite and approaches, from palaeon- for any study that aims to ad- tology to evo-devo, to come up duce evolutionary processes or with a broader view of macro- mechanisms operating at the evolution both in general and grand scale. This is because during the Cambrian radiation “the most important connection interval in particular. between (pattern and process) …

PPaginação_21.inddaginação_21.indd 1717 119-01-20129-01-2012 11:50:5111:50:51 18AÇOREANA 2011, Suplemento 7: 15-38

involves the comparison of both (Putnam et al., 2007; Chapman et intrinsic and extrinsic features al., 2010). of organisms predicted from theo- ries of process, with those actu- THE TEMPO AND MODE OF ally found in nature” (Eldredge EVOLUTION DURING THE and Cracra , 1980, p. 4). CAMBRIAN RADIATION Fortunately, a number of phylogenetic hypotheses for diff er- Trilobite phylogeny, biogeography, ent groups are available that can and the timing of the Cambrian prove useful in teasing apart radiation. the nature of the Cambrian ra- The earliest trilobites appear diation. One set of phylogenies in the fossil record in the lat- comes from Cambrian organ- ter part of the Lower Cambrian, isms themselves, specifi cally roughly 525 Ma (Lieberman & trilobites (e.g., Lieberman, 1998, Karim, 2010). When they appear 1999b, 2001a, 2002); these are it is eff ectively simultaneously in many respects the hallmark on several diff erent continents. Cambrian fossils in terms of Moreover, from their earliest the abundance and diversity in appearance they show signs of Cambrian strata. Another set signifi cant biogeographic dif- of phylogenies comes from mo- ferentiation (Fortey et al., 1996; lecular systematic analysis of an Lieberman, 1999a). This early early diverging animal group, biogeographic diff erentiation pro- the phylum Cnidaria (Collins et vides cogent evidence that trilo- al., 2006; Cartwright et al., 2008). bites may have been evolving for These phylogenies, taken in con- some period of time before they cert with the stratigraphic distri- actually appeared in the fossil re- bution of various cnidarian fos- cord. A key question of course is sils, can inform us about the evo- how long were trilobites around lutionary nature of the Cambrian before their appearance in the radiation (Cartwright & Collins, fossil record? Phylogenetic bio- 2007). Finally, our knowledge of geographic analysis provides a metazoan phylogeny, based on means of quantifying the dura- molecular systematic analyses of tion of this hidden evolutionary extant phyla, helps us recognize history. In particular, phylo- when and how the diff erent parts genetic biogeographic analy- of the genetic toolkit evolved sis can be used to determine if

PPaginação_21.inddaginação_21.indd 1818 119-01-20129-01-2012 11:50:5111:50:51 LIEBERMAN & CARTWRIGHT: CAMBRIAN RADIATION 19

there were any major tectonic ever dispersed before, during, events that may have infl uenced or a er 550-600 Ma; the biogeo- the early evolution of trilobites, graphic history of the majority through their eff ects on pa erns of Cambrian, and other trilobite of speciation. If there is evidence groups, has unfortunately not for congruent biogeographic dif- yet been investigated in a phylo- ferentiation that might be re- genetic framework. Still, based lated to such tectonic events, and on available evidence it does ap- further, if these tectonic events pear that for the key basal trilo- can be dated, it provides a mini- bite groups congruent dispersal mum age for the timing of bio- was absent and their diversifi - geographic diff erentiation and cation was most prominently thus evolutionary origins of the infl uenced by vicariance that group (Lieberman, 2003a). occurred sometime between 550- Phylogenetic biogeographic 600 Ma. Additional information analysis on basal trilobite line- about the biogeographic method ages suggests that pa erns of used is provided in Lieberman, early trilobite evolution show an 2000). This was a time of ma- episode of vicariance associated jor geological changes and for a with the breakup of a supercon- long time it had been generally tinent that occurred somewhere recognized that there was some in the interval 550-600 Ma (Meert association between these and & Lieberman, 2004). (The method the major biological changes of biogeographic analysis em- that were occurring, but phylo- ployed by Meert & Lieberman, genetic biogeographic analysis 2004 makes it possible to consid- provides a means of more rig- er pa erns of dispersal and does orously demonstrating that cor- not simply assume vicariance. relation. In particular and fore- In the particular case of these most, consider the fact that bio- Cambrian trilobites no evidence geographic pa erns reveal the for dispersal was uncovered. prominent stamp of vicariance Thus, the biogeographic pa erns recorded in congruent biogeo- cannot be explained by a subse- graphic pa erns. This suggests quent dispersal event that post- that earth history events exerted dated the breakup of the super- a signifi cant control on this key continent. Of course this does not episode in the history of life and imply that no Cambrian trilobites infl uenced the early evolution of

PPaginação_21.inddaginação_21.indd 1919 119-01-20129-01-2012 11:50:5111:50:51 20AÇOREANA 2011, Suplemento 7: 15-38

a major group of organisms, the and a er the bulk of diversifi ca- trilobites (Meert & Lieberman, tion has occurred (Lieberman et 2004). This provides evidence al., 2007; Abe & Lieberman, 2009). not only that the radiation is in For instance, the “Cenozoic” ra- some ways linked to changes in diation of mammals has roots the abiotic environment but that extending tens of millions of it was the opportunities for geo- years back into the Cretaceous graphic isolation that continen- (Archibald, 1996). (Further, pre- tal fragmentation aff orded that Cenozoic mammals are much helped spur speciation and the rarer than their Cenozoic breth- radiation (Lieberman, 2003a, b). ren, typically small, and on the A second key aspect of the whole morphologically homo- biogeographic pa erns is that geneous.) On the surface this they suggest that the origin of could simply imply an incom- trilobites occurred roughly 20- plete fossil record, but on closer 70 million years before their inspection this pa ern could fi rst appearance in the fossil actually be revealing something record. Given that trilobites about the nature of evolutionary are at least modestly derived radiations in general. (Notably, euarthropods, and arthropods Simpson, 1944 and Eldredge & are in turn a relatively derived Gould, 1972 also argued that bilaterian phylum, it suggests the relatively rapid appearance considerable metazoan, and even of higher taxa or species in the bilaterian, divergence must have fossil record told us something occurred before the start of the important about the nature of Cambrian. The meaning of these the evolutionary process.) The results is clear: the Cambrian very conditions that encourage radiation had a signifi cant fuse evolutionary radiations may also (Lieberman, 2003c; Meert & make groups less likely to be Lieberman, 2004). commonly retrieved as fossils. What happened during the This gains special meaning when Cambrian radiation refl ects a considered in light of punctuated more general pa ern associated equilibria (Eldredge & Gould, with other evolutionary radia- 1972); this theory posits that the tions in the fossil record. In par- very conditions that encourage ticular, many radiations appear speciation, rarity and a restric- in the fossil record fully formed, tion to marginal environments,

PPaginação_21.inddaginação_21.indd 2020 119-01-20129-01-2012 11:50:5111:50:51 LIEBERMAN & CARTWRIGHT: CAMBRIAN RADIATION 21

are likely to conspire to make ac- periods (Lieberman, 2001b, tual speciation events diffi cult to 2003c). The rate of speciation recover. Perhaps it should not be was found to be high during surprising then that groups un- the Cambrian radiation in the dergoing rapid speciation would trilobite groups considered by do so under conditions that make Lieberman (2001b), but it was them less likely to become pa- not found to be beyond the pale laeontologically emergent. Once of evolutionary rates witnessed groups do become commonplace at other times in the history of and distributed across a range of life. However, an important environmental se ings they are aspect of rapid evolution is likely to fossilize but the engine not just the speed with which of evolutionary radiation will speciation transpires but also mostly be shut off . Further, it is the amount of change that also worth noting that in the case occurs at each speciation event. of the Cambrian trilobites, al- Indeed, an important aspect of though we may be missing part Gould’s (1989) arguments about of their radiation in the fossil re- the pace of Cambrian evolution cord, the signature of that radia- have centered on the amount of tion is still preserved. morphological change occurring then and the greater genetic Tempo of trilobite evolution during fl exibility of Cambrian faunas. the Cambrian radiation. At least in the case of basal Early Information from trilobite Cambrian trilobites for which phylogenies can also be used to phylogenetic information exists, consider how rapidly speciation however, there does not seem was occurring during the ra- to be any statistical change in diation. It has been suggested the amount of morphological (e.g., Gould, 1989) that evolution change occurring at speciation at this time was operating un- events before and after the usually rapidly, but results Cambrian radiation interval from analyses of stochastic (Smith & Lieberman, 1999). This models suggest that, at least in is not to suggest that greater the case of trilobites, rates of genetic fl exibility plays no role speciation cannot be statistically in explaining what was unique distinguished from rates in about the Cambrian radiation, other groups and at other time and we will consider this issue

PPaginação_21.inddaginação_21.indd 2121 119-01-20129-01-2012 11:50:5211:50:52 22AÇOREANA 2011, Suplemento 7: 15-38

more fully below, but such arthropods, nematodes, tardi- processes either did not leave grades and kinorhynchs. Within their signature upon basal Deuterostomia, the echinoderms trilobite speciation or the change and hemichordates form a clade in genetic fl exibility did not that is sister to the chordates. Less occur until some time a er the certainty is the relative place- Cambrian radiation. ment of several early diverging metazoan lineages. For instance, Metazoan phylogenies and the mo- Porifera is generally thought to lecular clock. be paraphyletic (Borchiellini et Molecular phylogenies of ex- al., 2001; Medina et al., 2001), tant metazoan phyla can provide although a recent phylogenomic important information with re- study has recovered a mono- gard to pa erns of evolution be- phyletic Porifera (Philippe et tween phyla and the relative tim- al., 2009). The pa ern of di- ing of their origination and diver- vergence between Ctenophora, sifi cation. By densely sampling Porifera and Cnidaria is also representatives from all major controversial. Most molecular phylum (Paps et al., 2009) and ap- phylogenies support Porifera plying phylogenomic techniques as the earliest diverging lineage to sample DNA sequences from (Glenner et al., 2004; Philippe et hundreds of genes (Dunn et al., al., 2009), whereas other recent 2008; Hejnol et al., 2009), a con- phylogenomic studies support sensus is emerging regarding the Ctenophora as sister to the rest phylogenetic relationships be- of the Metazoa (Dunn et al., 2008; tween major metazoan lineages. Hejnol et al., 2009). There is lit- We summarize this consensus tle consensus on the placement here. In particular, choanofl a- of Placozoa, although most evi- gellates are the sister taxon to all dence indicates they are an early Metazoa. Acoelomorpha (acoels diverging metazoan (Dellaporta + nemertodermatids) is the sister et al., 2006; Hejnol et al., 2009; clade to Bilateria. Protostomia Philippe et al., 2009). There ex- comprises two major clades: ist two confl icting hypotheses the Lophotrochozoa, which in- on the placement of the parasitic cludes molluscs, annelids, fl at- myxozoans: they could be de- worms and bryozoans; and rived cnidarians or the sister to the Ecdysozoa, which includes Bilateria (discussed in Evans et

PPaginação_21.inddaginação_21.indd 2222 119-01-20129-01-2012 11:50:5211:50:52 LIEBERMAN & CARTWRIGHT: CAMBRIAN RADIATION 23

al., 2010). Finally, the enigmatic sil dates were used as calibration Xenoturbella has been placed as points on relevant nodes of a the earliest diverging deutero- molecular phylogeny of Metazoa stome (Philippe et al., 2009) or (Cartwright & Collins, 2007). as sister to Acoelomorpha at Speciﬁ cally, the crown group the base of Bilateria (Hejnol et lineages were used to date the al., 2009). Over the next few minimum age of the clade that years, through the application includes that fossil taxon. In ad- of genomic technologies, there dition, sponge biomarker, cni- will be dramatic increases in darian stem fossil and bilaterian molecular sequence data from trace-fossil evidence were used a diverse sampling of metazoan to assign a maximum-age dates taxa. These new data will help (Table 1). A penalized likelihood to resolve many of the remaining model that uses a semi-paramet- questions in metazoan phylo- ric approach to relax the strin- geny. gency of a clock was employed Detailed molecular phylo- (Sanderson, 2002). The results genies, in conjunction with the of some of the dates recovered in fossil record, can be useful for the molecular clock analysis of estimating dates of the origin of Cartwright & Collins (2007) are major metazoan lineages. It is shown in Table 2. Although the well documented, however, that dates of these analyses should molecules do not actually evolve be viewed with an appropri- in a “clock-like” fashion and ate degree of skepticism given therefore dates from molecular that they are highly dependent clocks are highly dependent on on both the model of molecular the model of molecular evolu- evolution and the accuracy of the tion used and on the fossil cali- fossil calibration, it is interesting brations used to mark minimum to note that although metazoan and maximum time boundaries origins are indicated to extend at multiple nodes on the tree. way back (this is likely a problem Cartwright & Collins (2007) re- related to the available choices viewed the literature on some to root the tree), most of the ma- of the earliest fossils representa- jor metazoan clades (Cnidaria, tives of major metazoan lineages Deuterostomia, Ecdyso zoa and and Table 1 summarizes some of Lophotrochozoa) are predicted the key fossil dates. These fos- to have originated either towards

PPaginação_21.inddaginação_21.indd 2323 119-01-20129-01-2012 11:50:5211:50:52 24AÇOREANA 2011, Suplemento 7: 15-38

TABLE 1. Earliest Fossil Representative of Major Metazoan clades Earliest Fossil Date (Ma) Stem/ Reference representative Formation Crown Porifera, 710 Stem Love et al., 2006 Silicea (Biomarkers) Porifera 560 Crown Gehling & Rigby, 1996 Paleophragmodictya

Cnidaria 570 Stem Xiao et al., 2000

Scyphozoa, 500 Crown Cartwright et al., 2007 Semaestome Marjum Scyphozoa, 500 Crown Cartwright et al., 2007 Coronate Marjum Hydrozoa, 500 Crown Cartwright et al., 2007 Narcomedusae Marjum Hydrozoa, 500 Crown Cartwright et al., 2007 Filifera Marjum Cubozoa, 500 Crown Cartwright et al., 2007 Tripedalia Marjum Ctenophora 500 Stem Conway Morris & Collins, 1996 Fasciculus Burgess

Bilateria 560 Stem Narbonne & Aitken, 1990

Arthropoda 530 Stem Collins, 1996 Anomalocaris 525 Brachiopoda Crown cosmopolitan Urochordate 525 Stem Chen et al., 2003 Shankaouclava Chengjaing Chordate 525 Yunnanozoan Stem Chen et al., 1995; Shu et al., 1999 Chenjiang Haikouichthys Chordata 495 Crown Agnathan many

the very end of the pre-Cambrian does appear to approximate the (late Neoproteorozoic) or even in time when major metazoan line- the Early Cambrian. Thus, the ages start to appear and/or di- Cambrian radiation, according versify in the fossil record. This to the molecular clock analyses, introduces a bit of a disconnect

PPaginação_21.inddaginação_21.indd 2424 119-01-20129-01-2012 11:50:5211:50:52 LIEBERMAN & CARTWRIGHT: CAMBRIAN RADIATION 25

TABLE 2. Results of molecular-clock While these analyses provide analysis for estimated dates of origin insight into the relative timing of several metazoan lineages from Cartwright & Collins (2007) of the origin of these lineages, there is likely a fair amount of Estimated Taxon date of origin error in the estimation of actual Metazoa 1147 dates, because of the depend- ency on a model of molecular Choanoﬂ agellates 837 evolution and accuracy in fossil Ctenophores 390 calibrations. Ultimately, syn- Silicea 710 thesis in science in general, and Cnidarians 570 evolutionary biology in particu- Bilaterians 560 lar, will come not from decid- ing which result is right, but ex- Deuterostomes 540 plaining how and why there are Hemichordates 361 diﬀ erences between the two. Chordates 495 Protostomes 543 MEDUSOZOAN FOSSILS AND PHYLOGENIES AND Ecdysozoa 530 THEIR BEARING ON THE Lophotrochozoa 537 CAMBRIAN RADIATION

Cnidarians are an impor- relative to the trilobite results al- tant metazoan group because of ready discussed, and we are not their exceptional diversity, their sure yet how to square these two prominent role in marine eco- disparate data sets. In particu- systems and their place as one lar, the pa erns from trilobite of the earliest diverging animal biogeography suggested that this lineages. Thus, understanding euarthropod clade had begun their evolutionary history, and to diversify by 550-600 Ma. By also their distribution in the fos- contrast, the molecular clock sil record, can provide important results suggest that Ecdysozoa, clues about the nature of evolu- which is down the tree relative tionary pa erns and processes, to Euarthropoda, originated at especially during the Cambrian 530 Ma. This discrepancy il- radiation interval. Associated lustrates the inherent problems with the Cnidarian Tree of Life with molecular clock analyses. project (http://cnidtol.com/)

PPaginação_21.inddaginação_21.indd 2525 119-01-20129-01-2012 11:50:5211:50:52 26AÇOREANA 2011, Suplemento 7: 15-38

there have been signifi cant ad- One diffi culty with interpret- vances in our understanding of ing early cnidarian fossils, es- cnidarian phylogeny (McFadden pecially those belonging to the et al., 2006; Cartwright et al., Medusozoa, which includes 2008; Collins et al., 2008; Daly those with a medusae stage (jel- et al., 2008; Evans et al., 2008; lyfi sh) in their life cycle, com- Bentlage et al., 2010; Nawrocki et prising the classes Cubozoa, al., 2010). A summary of our cur- Scyphozoa, Staurozoa and rent understanding of cnidarian Hydrozoa (Daly et al., 2007) is relationships is shown in Figure that they are o en poorly pre- 1. This information, along with served. Sometimes the “syna- newly discovered cnidarian fos- pomorphy” used to identify a sils from the Cambrian, can be medusozoan basically amounted put together to provide a picture to “rounded blob”, and o en of evolution at this time, and to with early putative medusozoan add to the perspective from tri- fossils that is all that is visible lobites already presented. (Hagadorn et al., 2002). Although such an assignment may in general be valid, it makes it diffi cult to say much more about these sorts of fossils and especially to determine whether or not they represent stem or crown medu- sozoans. Recently, we were fortunate enough to be able to study and describe new and exquisitely detailed Middle Cambrian medusozoan fossils (Cartwright et al., 2007). One of these fossils is shown in Figure 2. These fossils FIGURE 1. Medusozoan phylogeny provided enough character data summarizing our current understanding to allow them to be assigned of cnidarian relationships based on Collins not only to extant medusozoan et al. (2006), Cartwright et al. (2008), classes but also to extant orders, Collins et al. (2008), and Evans et al. (2008). Those taxa with Middle Cambrian fossil families, and in one case a ge- representatives are denoted by an “*”. nus. One of these genera, the

PPaginação_21.inddaginação_21.indd 2626 119-01-20129-01-2012 11:50:5211:50:52 LIEBERMAN & CARTWRIGHT: CAMBRIAN RADIATION 27

sent by the Middle Cambrian. This implies that not only all of the extant medusozoan higher taxa, but even many of the extant orders and perhaps families and genera had begun to diversify by the Middle Cambrian, shortly after the Cambrian radiation. The implications seem clear, and are akin to what was discovered with the trilobites: it is likely that the early Cambrian FIGURE 2. Fossil cnidarian identiﬁ ed as a crown group scyphozoan jellyﬁ sh that represents an interval of rapid belongs to the extant order Semaeostomae. diversification. The fossil is from the Middle Cambrium The record from fossils and Marjum Formation (approximately 500 phylogeny is also informative million years old) in Utah, U. S. A.; see about the nature of Cambrian Cartwright et al. (2007) for additional ecosystems. For a long time it details. was thought that these were relatively simple, but the presence cubozoan Tripedalia, today has of a diverse variety of pelagic or- an advanced visual system and ganisms provides a cautionary complex reproductive behavior. tale. Today jellyfish are domi- Although these structures are nant predatory forms (and also not visible on the Cambrian fos- prey items) in open ocean envi- sils, phylogenetic evidence indi- ronments. Their presence and cates that the character complex- diversity back in the Cambrian es associated with these would suggests that these environ- have also originated back in the ments were occupied; further- Cambrian. more, there must have been In Figure 1, the medusozoan prey for the jellyfish to feed on taxa that have Middle Cambrian in the pelagic environments. It fossil representatives are de- appears that Cambrian ecosys- picted with an asterisk. As illus- tems were not as simple as once trated in this figure, nearly the thought and in particular pelag- entire breadth of medusozoan ic ecosystems were occupied by phylogenetic diversity was pre- a diverse array of taxa.

PPaginação_21.inddaginação_21.indd 2727 119-01-20129-01-2012 11:50:5311:50:53 28AÇOREANA 2011, Suplemento 7: 15-38

ANCESTRAL GENETIC both Hydra and Nematostella TOOLKITS AND EVOLUTION- possess a complex genome that ARY DEVELOPMENT IN contains many developmental RELATION TO THE CAMBRIAN regulatory genes/gene families RADIATION previously thought to be specific to vertebrates (Ball et al., 2004; Recently, entire genomes have Kusserow et al., 2005; Technau been sequenced from a diverse et al., 2005; Ryan et al., 2006; array of metazoan taxa. Most Chapman et al., 2010) (mean- notably for our discussion here, ing that these genes were lost in the first complete, assembled Drosophila and Caenorhabditis). genome from the sea anemone Prominent signaling pathways Nematostella vectensis (Putnam shared between bilaterians and et al., 2007) and the hydrozoan cnidarians include Hedgehog, Hydra magnipapillata have been the receptor for tyrosine kinase, published (Chapman et al., 2010). Notch, transforming growth In addition, genome sequencing factor-B and Wnt (Technau et projects from the demosponge al., 2005; Chapman et al., 2010). Amphimedon queenslandica, the Thus, the ancestor to cnidarians placozoan Trichoplax, the cteno- and bilaterians must have been phore Mnemiopsis leidyi and the equipped with a diverse genom- coral Acropora millepora are ex- ic toolkit necessary for the speci- pected to be released in the near fication of complex body plans. future. Comparisons of cnidari- It is likely that before the evo- an genomes with those of bilate- lution of multicellular animals, rians have revealed unexpected many of these genes were per- insights into the genetic makeup forming entirely different func- of early-diverging animals. Prior tions, and were subsequently to the availability of genomic co-opted for signaling the de- data in non-bilaterian animals, velopment of complex and di- it was thought that many of the verse metazoan body plans. For complex, signaling pathways example, the cellular adhesion were unique to vertebrates, gene family cadherins that is im- because the model organisms portant for mediating cell-cell Drosophila and Caenorhabditis signaling in metazoans, is pre- elegans lacked these genes. sent in single celled protists such However, it is now known that as the choanoflagellates (King et

PPaginação_21.inddaginação_21.indd 2828 119-01-20129-01-2012 11:50:5311:50:53 LIEBERMAN & CARTWRIGHT: CAMBRIAN RADIATION 29

al., 2003; Abedin & King, 2008). NA gene families become more The increased availability of diverse through time, the to- genomes from other early-di- tal number of microRNAs does verging lineages will allow for not. That is, there is no correla- a more precise reconstruction of tion between the number of total the metazoan ancestral genome. microRNAs and morphological Thus far, evidence from genom- complexity in extant metazoan ics indicates that the ancestral taxa. For example, Peterson et metazoan genetic toolkit was al. (2009) reports that the sea complex and enabled the rapid anemone Nematostella has 29 to- diversification of body plans tal microRNAs, whereas mouse during the Cambrian radiation. has only 16. Moreover, pattern Although the complex meta- and process could be conflated zoan ancestral genomic toolkit in Peterson et al.’s (2009) argu- can in part explain rapid diver- ment because of the existence of sification of animal body plans, a “left wall” sensu Gould (1996). it cannot explain why these That is to say, the number of mi- body plans appear to become croRNA families start out low more canalized through time. and through time has to increase Peterson et al. (2009) proposed because the only direction avail- that the evolution of microR- able for change is for the num- NAs, because of their key role in ber to increase (gene families transcriptional regulation, may that went extinct and were elim- explain the increasing morpho- inated could not be sampled). logical conservativism of body This argument was originally plans through time. Specifically, developed by Gould (1996) to Peterson et al. (2009) note that explain why apparent biological the evolution of additional mi- complexity increases through croRNA gene families through time. However, any time there time means that development is a trend that occurs in a system becomes more tightly regulated. that involves an originally mini- While this hypothesis is conceiv- mal value that increases through able, it seems a bit premature as time, one has to be careful not very little is known about the to prematurely invoke a driven role of the diverse microRNA trend; the pattern could just in- families that exist in metazoans. volve a random walk, with pas- In addition, although microR- sive diffusion away from a re-

PPaginação_21.inddaginação_21.indd 2929 119-01-20129-01-2012 11:50:5311:50:53 30AÇOREANA 2011, Suplemento 7: 15-38

fl ecting barrier or minimum value. & Lieberman, 2004). These were Moreover, diversification of not, however, the only profound gene families through time is not set of environmental changes unique to microRNAs. Hox genes transpiring at the time. During also show gene duplications and the very end of the Proterozoic diversifi cation in many separate there were also a series of ma- lineages. (The same “le wall” jor climatic changes, informally argument might explain some of grouped under the rubric of the these pa erns as well.) In sum- Snowball Earth (Hoffman et al., mation, it is likely that there is 1998). There may have been as no single explanation for the ca- many as four episodes when nalization of body plans in meta- the Earth experienced near total zoans, but instead it was due to a glaciation, being completely en- number of complex changes both cased in ice; the intervening in- in the genomes themselves and in tervals also witnessed extreme the regulations and interactions environments as the ice melted amongst the diff erent signaling away only to be followed by epi- pathways. sodes of near broiling warmth where global temperatures hov- CHANGES IN THE ABIOTIC ered at close to 50 °C. Given the ENVIRONMENT AND THE inhospitable environments, at TIMING OF THE RADIATION least for large multicellular organisms, it may be no surprise As we have already de- that it was only after these con- scribed, there is some evidence ditions ameliorated that such that changes in the abiotic envi- organisms evolved (Hoffman et ronment at least partly triggered al., 1998; Knoll, 2003). In this the Cambrian radiation. In par- case, environmental conditions ticular, the geological changes might well have served as a at the end of the Proterozoic as- check on evolution, with envi- sociated with the fragmentation ronmental moderation creating of a supercontinent expanded fodder for evolutionary change. the opportunities for vicariant Another critical aspect in the differentiation and allopatric abiotic environment and evo- speciation, thereby increased lutionary equation, at least re- the tempo of evolution at the garding large organisms, are time (Lieberman, 2003a; Meert oxygen concentrations. These

PPaginação_21.inddaginação_21.indd 3030 119-01-20129-01-2012 11:50:5411:50:54 LIEBERMAN & CARTWRIGHT: CAMBRIAN RADIATION 31

seem to have been generally in- In addition, the biotic en- creasing towards the end of the vironment as manifest in eco- Proterozoic, perhaps then reach- logical interactions in the ing 10% of present atmospheric Proterozoic world would have levels (Fike et al., 2006; Canfield been impoverished relative to et al., 2007; Li et al., 2010). This those that prevail today, or even might have been an important relative to those that prevailed threshold especially for the gen- by the late Cambrian. There is eration of key proteins found in some general sense that minimal many organisms, such as col- competition early in the history lagen, and also facilitating the of animal life in the Proterozoic building of rigid exoskeletons might have served to facilitate that make organisms more like- the evolution of animals early ly to fossilize (Schopf & Klein, on. As competition inevita- 1992; Bengtson et al., 1994). It bly increased with increasing also would have facilitated the diversity in the Phanerozoic, evolution of large body size evolution might have later be- because of the issue of surface come constrained. However, area to volume constraints (see the evolutionary mechanisms Bonner, 1988). Again, these en- whereby these ecological differ- vironmental changes involve re- ences would become translated, moving a constraint that would specifically from the ecological have kept a lid on the evolution to the genealogical hierarchies, of animals. The changes do are not as yet clear and must appear to have occurred some remain nebulous at this time time before animals actually are (Lieberman, 2008). found in the fossil record. Thus, the changes might not have pre- CONCLUSIONS cipitated evolution instantane- ously. However, it is worth Unravelling the patterns adding that this difference in and processes involved in the timing lessens when one takes Cambrian radiation is one of the into account the evidence from grand challenges in evolution trilobites, which indicates evo- because these events occurred lution might have significantly rapidly and in deep time. A preceded first appearance in the comprehensive understanding fossil record. of the origin and diversification

PPaginação_21.inddaginação_21.indd 3131 119-01-20129-01-2012 11:50:5411:50:54 32AÇOREANA 2011, Suplemento 7: 15-38

of major metazoan lineages will LITERATURE CITED likely come from the integra- tion of several fields of inquiry, ABE, F.R., & B.S. LIEBERMAN, 2009. including a careful study of di- The nature of evolutionary ra- versification in the fossil record, diations: A case study involving detailed paleobiogeographic Devonian trilobites. Evolutionary analyses, paleoecological stud- Biology, 36: 225-234. ies, molecular phylogenetic ABEDIN, M., & N. KING, 2008. The studies, and studies of genomics premetazoan ancestry of cadherins. and evolutionary development. Science, 319:946-948. We predict that from these dis- ARCHIBALD, J.D., 1996. Fossil evi- parate lines of evidence a mac- dence for a Late Cretaceous origin roevolutionary synthesis will of “Hoofed” mammals. Science, 272: emerge where paleontology, 1150-1153. phylogenetics and evolutionary BALL, E.E., D.C. HAYWARD, R. SAINT development are the key areas & D.J. MILLER, 2004. A simple plan of study for understanding this - cnidarians and the origins of de- important episode (as well as velopmental mechanisms. Nature other important episodes) in the Reviews of Genetics, 5: 567-577. history of life. BENGTSON, S. (ed.), 1994. Early Life on Earth, 630 pp. Columbia University ACKNOWLEDGEMENTS Press, New York. BENTLAGE, B., P. CARTWRIGHT, We gratefully thank António A.A. YANAGIHARA, C. LEWIS, G. Manuel de Frias Martins for in- RICHARDS & A.G. COLLINS, 2010. viting us to participate in the Evolution of box jellyﬁ shes (Cnidaria: symposium in the Azores that Cubozoa), a group of highly toxic this paper was based on. We invertebrates. Proceedings of the also thank one anonymous re- Royal Society of London, Series B, 277: viewer for comments on an ear- 493-501. lier version of this paper. This BONNER, J.T., 1988. The Evolution research was supported by NSF of Complexity by Means of Natural DEB-0716162 to BSL and NSF Selection, 272 pp. Princeton Uni- AtoL EF-0531779 and NSF DEB- versity Press, Princeton, NJ. 0953571 to PC. BORCHIELLINI, C., M. MANUEL, E. ALIVON, N. BOURY-ESNAULT, J. VACELET & Y. LE PARCO, 2001.

PPaginação_21.inddaginação_21.indd 3232 119-01-20129-01-2012 11:50:5411:50:54 LIEBERMAN & CARTWRIGHT: CAMBRIAN RADIATION 33

Sponge para-phyly and the origin N. SUMIN, G.G. SUTTON, L.D. of Metazoa. Journal of Evolutionary VISWANATHAN, B. WALENZ, D. Biology, 14: 171-179. M. GOODSTEIN, U. HELLSTEN, BRASIER, M., 2009. Darwin’s Lost T. KAWASHIMA, S.E. PROCHNIK, World, 304 pp. Oxford University N.H. PUTNAM, S. SHU, B. Press, Oxford, UK. BLUMBERG, C.E. DANA, L. CANFIELD, D.E., S.W. POULTON GEE, D.F. KIBLER, L. LAW, D. & G.M. NARBONNE, 2007. Late LINDGENS, D.E. MARTINEZ, J. Neoproterozoic deep-ocean oxy- PENG, P.A. WIGGE, B. BERTULAT, genation and the rise of animal life. C. GUDER, Y. NAKAMURA, Science, 315: 92-95. S. OZBEK, H. WATANABE, K. CARTWRIGHT, P., & A. COLLINS, KHALTURIN, G. HEMMRICH, 2007. Fossils and phylogenies: inte- A. FRANKE, R. AUGUSTIN, S. grating multiple lines of evidence to FRAUNE, E. HAYAKAWA, S. investigate the origin of early major HAYAKAWA, M. HIROSE, J.S. metazoan lineages. Integrative and HWANG, K. IKEO, C. NISHIMIYA- Comparative Biology, 47(5): 744-751. FUJISAWA, A. OGURA, T. CARTWRIGHT, P., N.M. EVANS, TAKAHASHI, P.R.H. STEINMETZ, C.W. DUNN, A.C. MARQUES, M.P. X. ZHANG, R. AUFSCHNAITER, MIGLIETTA & A.G. COLLINS, M.-K. EDER, A.-K. GORNY, W. 2008. Phylogenetics of Hydroidolina SALVENMOSER, A.M. HEIMBERG, (Cnidaria, Hydrozoa). Journal of the B.M. WHEELER, K.J. PETERSON, A. Marine Biological Association, 88(8): BOTTGER, P. TISCHLER, A. WOLF, 1163-1672. T. GOJOBORI, K.A. REMINGTON, CARTWRIGHT, P., S.L. HALGEDAHL, R.L. STRAUSBERG, J.C. VENTER, J.R. HENDRICKS, R.D. JARRARD, U. TECHNAU, B. HOBMAYER, A.C. MARQUES, A.G. COLLINS T.C.G. BOSCH, T.W. HOLSTEIN, & B.S. LIEBERMAN, 2007. T. FUJISAWA, H.R. BODE, C.N. Exceptionally Preserved Jellyﬁ shes DAVID, D.S. ROKHSAR & R.E. from the Middle Cambrian. PLoS STEELE, 2010. The dynamic genome ONE, 2: e1121. of Hydra. Nature, 464: 592-596. CHAPMAN, J.A., E.F. KIRKNESS, CHEN, J.-Y., J. DZIK, G.D. EDGE- O. SIMAKOV, S.E. HAMPSON, T. COMBE, L. RAMSKOLD & G.Q. MITROS, T. WEINMAIER, T. RATTEI, ZHOU, 1995. A possible Early Cam- P.G. BALASUBRAMANIAN, bian chordate. Nature, 377: 720-222. J. BORMAN, D. BUSAM, K. CHEN, J.-Y., D.-Y. HUANG, Q.-Q. DISBENNETT, C. PFANNKOCH, PENG, H.-M. CHI, X.-Q. WANG &

PPaginação_21.inddaginação_21.indd 3333 119-01-20129-01-2012 11:50:5411:50:54 34AÇOREANA 2011, Suplemento 7: 15-38

M. FENG, 2003. The fi rst tunicate C.S. MCFADDEN, D.M. OPRESKO, from the Early Cambrian of South E. RODRIGUEZ, S. ROMANO & J. China. Proceedings of the National STAKE, 2007. The phylum Cnidaria: Academy of Sciences, U S A, 100: 8314- A review of phylogenetic pa erns 8318. and diversity three hundred years COLLINS, A.G., B. BENTLAGE, D. a er Linneaeus. Zootaxa, 166(8): 127- LINDSAY, S.H.D. HADDOCK, A. 182. LINDNER, J.L. NORENBURG, DALY, M., A. CHAUDHURI, L. G. JARMS, T. JANKOWSKI & P. GUSMO & E. RODRÌGUEZ, 2008. CARTWRIGHT, 2008. Phylogenetics Phylogenetic relationships among of Trachylina (Cnidaria, Hydrozoa). sea anemones (Cnidaria: Anthozoa: Journal of the Marine Biological Actiniaria). Molecular Phylogenetics Association, 88: 1671-1684. and Evolution, 48: 292-301. COLLINS, A.G., P. SCHUCHERT, A.C. DARWIN, C., 1859. On the Origin MARQUES, T. JANKOWSKI, M. of Species by Means of Natural MEDINA & B. SCHIERWATER, Selection (Reprinted 1st edition), 2006. Medusozoan phylogeny and 540 pp. Harvard University Press, character evolution clarifi ed by Cambridge, MA. new large and small subunit rDNA DE BEER, G., 1951. Embryos and data and an assessment of the util- Ancestors, 159 pp. Clarendon Press, ity of phylogenetic mixture models. Oxford, UK. Systematic Biology, 55: 97-115. DELLAPORTA, S.L., A. XU, S. COLLINS, D., 1996. The “Evolution” SAGASSER & W. JAKOB, 2006. of Anomalocaris and Its Classifi cation Mitochondrial genome of Trichoplax in the Arthropod Class Dinocarida adhaerens supports Placozoa as the (nov.) and Order Radiodonta (nov.). basal lower metazoan phylum. Journal Paleontology, 70: 280-293. Proceedings of the National Academy of CONWAY MORRIS, S., & D.H. Sciences, U.S.A., 103(23): 8751-8756. COLLINS, 1996. Middle Cambrian DUNN, C.W., A. HEJNOL, D.Q. MATUS, Ctenophores from the Stephen L. PANG, W.E. BROWNE, S.A. Formation, British Columbia, SMITH, E. SEAVER, G.W. ROUSE, Canada. Philosophical Transactions of M. OBST, G.D. EDGECOMBE, M.V. the Royal Society, Biological Sciences, SØRENSEN, S.H.D. HADDOCK, 351: 279-308. A. SCHMIDT-RHAESA, A. DALY, M., M.R. BRUGLER, P. OKUSU, R.M. KRISTENSEN, W.C. CARTWRIGHT, A.G. COLLINS, WHEELER, M.Q. MARTINDALE & M.N. DAWSON, S.C. FRANCE, G.N. GIRIBET, 2008. Broad phylo-

PPaginação_21.inddaginação_21.indd 3434 119-01-20129-01-2012 11:50:5411:50:54 LIEBERMAN & CARTWRIGHT: CAMBRIAN RADIATION 35

genomic sampling improves resolu- ity. Biological Journal of the Linnaean tion of the animal tree of life. Nature, Society, 57: 13-33. 452: 745-749. GEHLING, J.G., & J.K. RIGBY, 1996. ELDREDGE, N., 1985. Unfinished Long expected sponges from the ne- Synthesis, 237 pp. Oxford University oproterozoic ediacara fauna of South Press, New York. Australia. Journal of Paleontology, ELDREDGE, N., & J. CRACRAFT, 70(2): 185-195. 1980. Phylogenetic Pa erns and the GLENNER, H., A.J. HANSEN, M.V. Evolutionary Process, 349 pp. Colum- SØRENSEN & F. RONQUIST, 2004. bia University Press, New York. Bayesian Inference of the Metazoan ELDREDGE, N., & S.J. GOULD, 1972. Phylogeny: A Combined Molecular Punctuated equilibria: an alternative and Morphological Approach. to phyletic gradualism. In: SCHOPF, Current Biology, 14(18): 1644-1649. T.J.M. (ed.), Models in Paleobiology, GOULD, S.J., 1989. Wonderful Life, 352 pp. 82-115. Freeman, Cooper, San pp. W.W. Norton, New York. Francisco, CA. GOULD, S.J., 1996. Full House, 244 pp. EVANS, N., A. LINDNER, E. RAIKOVA, Harmony Books, New York. A. COLLINS & P. CARTWRIGHT, GOULD, S.J., 2002. The Structure of 2008. Phylogenetic placement of the Evolutionary Theory, 1464 pp. Harvard enigmatic parasite, Polypodium hydri- University Press, Cambridge, MA. forme, within the Phylum Cnidaria. HAGADORN, J.W., R.H.J. DOTT & BMC Evolutionary Biology, 8: 139. D. DAMROW, 2002. Stranded on a EVANS, N.M., M.T. HOLDER, M.S. Late Cambrian shoreline: Medusae BARBEITOS, B. OKAMURA & P. from central Wisconsin. Geology, 3 0 : CARTWRIGHT, 2010. The phyloge- 147-150. netic position of Myxozoa: Exploring HEJNOL, A., M. OBST, A. STAMA- Conﬂ icting Signals in Phylogenomic TAKIS, M. OTT, G.W. ROUSE, G.D. and Ribosomal Datasets. Molecular EDGECOMBE, P. MARTINEZ, J. Biology and Evolution, 50(3): 456-472. BAGUÑÀ, X. BAILLY, U. JONDE- FIKE, D.A., J.P. GROTZINGER, L.M. LIUS, M. WIENS, W.E.G. MÜLLER, PRATT & R.E. SUMMONS, 2006. E. SEAVER, W.C. WHEELER, M.Q. Oxidation of the Ediacaran ocean. MARTINDALE, G. GIRIBET & C.W. Nature, 444: 744-747. DUNN, 2009. Assessing the root of FORTEY, R.A., D.E.G. BRIGGS & M.A. bilaterian animals with scalable phy- WILLS, 1996. The Cambrian evolu- logenomic methods. Proceedings of tionary ‘explosion’: decoupling clad- the Royal Society of London, Series B, ogenesis from morphological dispar- 276: 4261-4270.

PPaginação_21.inddaginação_21.indd 3535 119-01-20129-01-2012 11:50:5411:50:54 36AÇOREANA 2011, Suplemento 7: 15-38

HOFFMAN, P.F., A.J. KAUFMAN, G.P. University Peabody Museum of Natural HALVERSON & D.P. SCHRAG, History, 45: 1-150. 1998. A Neoproterozoic Snowball LIEBERMAN, B.S., 2000. Paleobiogeo- Earth. Science, 281: 1342-1346. graphy: Using Fossils to Study Global KING, N., C.T. HITTINGER & S.B. Change, Plate Tectonics, and Evolution, CARROLL, 2003. Evolution of key 208 pp. Kluwer Academic/Plenum cell signalling and adhesion protein Publishing, New York. families predated the origin of ani- LIEBERMAN, B.S., 2001a. Phylogenetic mals. Science, 301: 361-363. analysis of the Olenellina (Trilobita, KNOLL, A.H., 2003. Life on a Young Cambrian). Journal of Paleontology, Planet, 277 pp. Princeton University 75: 96-115. Press, Princeton, NJ. LIEBERMAN, B.S., 2001b. A proba- KUSSEROW, A., K. PANG, C. STURM, bilistic analysis of rates of specia- M. HROUDA, J. LENTFER, H.A. tion during the Cambrian radia- SCHMIDT, U. TECHNAU, A. VON tion. Proceedings of the Royal Society, HAESELER, B. HOBMAYER, M.Q. Biological Sciences, 268: 1707-1714. MARTINDALE & T.W. HOLSTEIN, LIEBERMAN, B.S., 2002. Phylogenetic 2005. Unexpected complexity of the analysis of some basal Early Cam- Wnt gene family in a sea anemone. brian trilobites, the biogeographic Nature, 433: 156-160. origins of the eutrilobita, and the LI, C., G.D. LOVE, T.W. LYONS, D.A. timing of the Cambrian radiation. FIKE, A.L. SESSIONS X. CHU, 2010. Journal of Paleontology, 76: 672-688. A stratiﬁ ed redox model for the LIEBERMAN, B.S., 2003a. Biogeogra- Ediacaran ocean. Science, 328: phy of the Cambrian radiation: de- 80-83. ducing geological processes from LIEBERMAN, B.S., 1998. Cladistic anal- trilobite evolution. Special Papers in ysis of the Early Cambrian olenelloid Palaeontology, 70: 59-72. trilobites. Journal of Paleontology, LIEBERMAN, B.S., 2003b. Paleobiogeo- 72:59-78. graphy: The relevance of fossils to LIEBERMAN, B.S., 1999a. Testing the biogeography. Annual Review of Eco- Darwinian legacy of the Cambrian logy and Systematics, 34: 51-69. radiation using trilobite phylog- LIEBERMAN, B.S., 2003c. Taking the eny and biogeography. Journal of pulse of the Cambrian radiation. Paleontology, 73:176-181. Journal of Integrative and Comparative LIEBERMAN, B.S., 1999b. Systematic Biology, 43: 229-237. revision of the Olenelloidea (Trilo- LIEBERMAN, B.S., 2008. The Cambrian bita, Cambrian). Bulletin of the Yale radiation of bilaterians: Evolutionary

PPaginação_21.inddaginação_21.indd 3636 119-01-20129-01-2012 11:50:5411:50:54 LIEBERMAN & CARTWRIGHT: CAMBRIAN RADIATION 37

origins and palaeontological emer- rRNA. Proceedings of the National gence; earth history change and bi- Academy of Sciences, U. S. A., 98: 9707- otic factors. Palaeogeography, Palaeo- 9712. climatology, Palaeoecology, 258: 180- MEERT, J.G., & B.S. LIEBERMAN, 188. 2004. A palaeomagnetic and palaeo- LIEBERMAN, B.S., & T.S. KARIM, 2010. biogeographic perspective on latest Tracing the trilobite tree from the root Neoproterozoic and early Cambrian to the tips: a model marriage of fossils tectonic events. Journal of the Geological and phylogeny. Arthropod Structure Society of London, 161: 1-11. & Development, 39(3): 111-123. NARBONNE, G.M., & J.D. AITKEN, LIEBERMAN, B.S., W. MILLER. III & N. 1990. Ediacaran fossils from the ELDREDGE, 2007. Paleontological Sekwi Brook area, Mackenzie pa erns, macroecological dynam- Mountains, north-western Canada. ics and the evolutionary process. Paleontology, 33: 945-980. Evolutionary Biology, 34: 28-48. NAWROCKI, A.M., P. SCHUCHERT LOVE, G.D., D.A. FIKE, E. GROSJEAN, & P. CARTWRIGHT, 2010. Phylo- C. STALVIES, J. GROTZINGER, genetics and evolution of Capitata A.S. BRADLEY, S. BOWRING, D. (Cnidaria: Hydrozoa), and the sys- CONDON & R.E. SUMMONS, 2006. tematics of Corynidae. Zoologica Constraining the timing of basal Scripta, 39(3): 290-304. metazoan radiation using molecular PAPS, J., J. BAGUÑÀ & M. RIUTORT, biomarkers and U-Pb isotope dat- 2009. Lophotrochozoa internal phy- ing. Geochimica et Cosmochimica Acta, logeny: new insights from an up-to- 70(18): A371-A371. date analysis of nuclear ribosomal MCFADDEN, C.S., S.C. FRANCE, J.A. genes. Proceedings of the Royal Society SANCHEZ & P. ALDERSLADE, of London, Series B, 276:1245-1254. 2006. A molecular phylogenetic anal- PETERSON, K.J., M.R. DIETRICH & ysis of the Octocorallia (Cnidaria: M.A. MCPEEK, 2009. MicroRNAs Anthozoa) based on mitochondrial and metazoan macroevolution: in- protein-coding sequences. Molecular sights into canalization, complex- Phylogenenetics and Evolution, 41: 513- ity, and the Cambrian explosion. 527. Bioessays, 31: 736-747. MEDINA, M., A.G. COLLINS, J.D. PHILIPPE, H., R. DERELLE, P. LOPEZ, SILBERMAN & M.L. SOGIN, 2001. K. PICK, C. BORCHIELLINI, N. Evaluating hypotheses of basal ani- BOURY-ESNAULT, J. VACELET, mal phylogeny using complete se- E. RENARD, E. HOULISTON, quences of large and small subunit E. QUÈINNEC, C. DA SILVA, P.

PPaginação_21.inddaginação_21.indd 3737 119-01-20129-01-2012 11:50:5411:50:54 38AÇOREANA 2011, Suplemento 7: 15-38

WINCKER, H. LE GUYADER, SCHOPF, J.W, & C. KLEIN (eds.), S. LEYS, D. J. JACKSON, F. 1992. The Proterozoic Biosphere, 1374 SCHREIBER, D. ERPENBECK, B. pp. Cambridge University Press, MORGENSTERN, G. WORHEIDE & Cambridge, UK. M. MANUEL, 2009. Phylogenomics SHU, D.-G., H.-L. LUO, S. CONWAY revives traditional views on deep an- MORRIS, X.-L. ZHANG, S.-X. HU, J. imal relationships. Current Biology, HAN, M. ZHU, Y. LI & L.-Z. CHEN, 19: 706-712. 1999. Lower Cambrian vertebrates PUTNAM, N.H., M. SRIVASTAVA, from south China. Nature, 402: 42-46. U. HELLSTEN, B. DIRKS, J. SIMPSON, G.G., 1944. Tempo and Mode CHAPMAN, A. SALAMOV, in Evolution, 237 pp. Columbia A. TERRY, H. SHAPIRO, E. University Press, New York. LINDQUIST, V.V. KAPITONOV, SMITH, L.H., & B.S. LIEBERMAN, J. JURKA, G. GENIKHOVICH, 1999. Disparity and constraint in ole- I.V. GRIGORIEV, S.M. LUCAS, nelloid trilobites and the Cambrian R.E. STEELE, J.R. FINNERTY, U. radiation. Paleobiology, 25:459-470. TECHNAU, M.Q. MARTINDALE & TECHNAU, U., S. RUDD, P. D.S. ROKHSAR, 2007. Sea anemone MAXWELL, P.M.K. GORDON, genome reveals ancestral eumeta- M. SAINA, L.C. GRASSO, D.C. zoan gene repertoire and genomic HAYWARD, C.W. SENSEN, R. organization. Science, 317: 86-94. SAINT, T.W. HOLSTEIN, E.E. BALL RYAN, J.F., P.M. BURTON, M.E. & D.J. MILLER, 2005. Maintenance MAZZA, G.K. KWONG, J.C. of ancestral complexity and non- MULLIKIN & J.R. FINNERTY, 2006. metazoan genes in two basal cnidar- The cnidarian-bilaterian ancestor ians. Trends in Genetics, 21: 633-639. possessed at least 56 homeoboxes: VALENTINE, J.W., 2004. On the Origin evidence from the starlet sea anem- of Phyla, 608 pp. University of one, Nematostella vectensis. Genome Chicago Press, Chicago. Biology, 7: R64-R64. XIAO, S., X. YUAN & A.H. KNOLL, SANDERSON, M.J., 2002. Estimating 2000. Eumetazoan fossils in ter- absolute rates of molecular evolu- minal Proterozoic phosphorites? tion and divergence times: a penal- Proceedings of the National Academy of ized likelihood approach. Molecular Sciences, U.S.A., 97: 13684-13689. Biology and Evolution, 19: 101-109.

PPaginação_21.inddaginação_21.indd 3838 119-01-20129-01-2012 11:50:5411:50:54