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

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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 111:50:451:50:45 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 111:50:511:50:51 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 111:50:511:50:51 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 phy- logenetic 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 111:50:511:50:51 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
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