EVOLUTION & DEVELOPMENT 7:6, 498–514 (2005) Terminal addition, the Cambrian radiation and the Phanerozoic evolution of bilaterian form David K. Jacobs,a,Ã Nigel C. Hughes,b Sorel T. Fitz-Gibbon,c and Christopher J. Winchella aDepartment of Ecology and Evolutionary Biology, University of California, Los Angeles, 621 Young Drive South, Los Angeles, CA 90095-1606, USA bDepartment of Earth Sciences, University of California, Riverside, CA 92521, USA cIGPP Center for Astrobiology, University of California Los Angeles, CA 90095-1567, USA ÃAuthor for correspondence (email: [email protected]) SUMMARY We examine terminal addition, the process of evolution evident in the fossil record. These trends appear to addition of serial elements in a posterior subterminal growth be the product of departure from the initial terminal addition zone during animal development, across modern taxa and state, as is evident in evolutionary patterns within-fossil groups fossil material. We argue that terminal addition was the basal such as trilobites, but is also more generally related to shifts in condition in Bilateria, and that modification of terminal addition types of morphologic change through the early Phanerozoic. was an important component of the rapid Cambrian evolu- Our argument is contingent on dates of metazoan divergence tion of novel bilaterian morphology. We categorize the that are roughly convergent with the first appearance of often-convergent modifications of terminal addition from the metazoan fossils in the latest Proterozoic and Cambrian, as presumed ancestral condition. Our focus on terminal addition well as on an inference of homology of terminal addition and its modification highlights trends in the history of animal across bilaterian Metazoa. INTRODUCTION struction and from fossil data; and (3) the fossil record should document broad changes in the classes of morphologic tran- We argue that bilaterian evolution began with, and evolved sitions observed in evolution following departure from the from, a shared ancestral condition that included terminal ad- initial terminal addition condition near the base of the Cam- dition as a critical component of development. Terminal ad- brian. Here we make a preliminary assessment of the con- dition here refers to growth and patterning in a posterior (or sistency of the data with these predictions. in the case of echinoderms, distal) subterminal growth zone. For this perspective on metazoan evolution to have broad Terminal addition is more obvious morphologically when re- explanatory value, two premises must hold. First, the peated pattern elements are added in the growth zone and has bilaterian component of metazoan evolution must have been been most extensively discussed in segmented taxa. Our more relatively abrupt in terms of morphologic and phyletic evo- general definition of ‘‘growth and patterning’’ permits an ex- lution, consistent with the sudden appearance of most phyla amination of the course of modification of terminal addition in the Cambrian record. We presume that rapid cladogenesis across the range of bilaterian morphology. In our view, de- in combination with evolution of disparate morphology con- parture from an initial mode of terminal addition provided a tributes to this phase of departure from an ancestral ‘‘set of avenues’’ for body plan modification. Thus, we are bilaterian. Second, the ancestor of all (or nearly all) living singling out one, very critical, component of body-plan ev- Bilateria must have used some form of terminal addition in- olution for an initial examination. volving subterminal posterior growth and patterning during Inferring terminal addition as a starting condition in development. Both these premises are controversial, but when bilaterian evolution constrains evolutionary interpretation, considered together, they provide a new lens through which yielding the following predictions: (1) departure from the an- one can view the morphologic evolution of Metazoa. cestral terminal addition state should be evident in the evo- Below we examine our premises, that a sudden radiation lutionary transitions among modern bilaterian groups; (2) occurred at the base of the Cambrian, and that a terminal early phanerozoic patterns of evolutionary departure from a addition mechanism is ancestral in the Bilateria; we also dis- terminal addition condition should be evident in the mor- cuss caveats to the argument. We then classify the possible phologic history of lineages inferred from phylogeny recon- evolutionary modifications of terminal addition and discuss 498 & BLACKWELL PUBLISHING, INC. Jacobs et al. Terminal addition and the Cambrian radiation 499 each of these modification types, providing examples of each Table 1. Results of a Blast/Z statistic analysis of typeFmany of which appear to have evolved in parallel in sponge genes. If there is no lineage-specific bias in rate of multiple lineages. Lastly, we relate the process of modification evolution, then individual genes should show higher of terminal addition to the fossil record, considering Ediaca- similarity as a consequence of random gene-specific ran and trilobite lineages where evolutionary changes in the processes. Thus considering homologous genes sampled terminal addition process can be observed, as well as consid- from sponges, Human and Nematode the null expecta- ering the broader implications of these changes for the evo- tion is that in half the genes the sponge example should lution of bilaterian form in the Phanerozoic record. be more similar in sequence to Human (Hs) half to Nematode (Ce). Similarly, in the comparison of sponge to human and fly (Dm) half the sponge genes are expected to be similar to Human and half to Fly JUSTIFICATION OF PREMISES (comparisons that are equally similar are tabulated under 0 and are dropped from the analysis). Length of aligned The Cambrian radiation was rapid amino acid sequence as well as number and percent Darwin (1859) suggested that the absence of Precambrian identity of amino acid residues in the alignment are animal fossils was an artifact of the fossil record. However, used in comparisons. As can be seen there is a broad extensive subsequent investigation of the rock record provides bias in the data and the null of equal rates between no strong evidence of any animal life prior to the Maranoan lineages can be rejected. Thus the nematode and fly glaciation 600 Myr, less than 60 Myr before the fossil record lineages are substantially and pervasively higher in of the Cambrian radiation (e.g., Knoll 2000). Despite this lack rate than the human lineage as is discussed further of fossil evidence, a recently developed neo-gradualist school in the text. maintains that animals including taxa within the Bilateria be- Comparison of sponge/nematode and sponge/human gan diversifying a billion years or more before the first fossil evidence of Metazoa (e.g., Wray et al. 1996; Gu 1998; Wang Aligned AA Identical AA %Identity et al. 1999). This interpretation involves a protein ‘‘clock’’ Hs 0 Ce Hs 0 Ce Hs 0 Ce based on aligned amino-acid sequences from many genes 80 8 53 106 2 33 98 0 43 combined in a single analysis. This type of approach allows Z 5 2.3 Z 5 6.2 Z 5 4.6 for gene-specific differences in evolutionary rate, but neces- Significant Off table V. H. Significant sarily presumes that lineage-specific differences in rate that Comparison of sponge/fly and sponge/human influence the evolution of the whole genome are insignificant. If such an assumption were to hold, precise dates of diver- Aligned AA Identical AA %Identity gence would be calculable, given the accumulation of protein Hs 0 Dm Hs 0 Dm Hs 0 Dm data from genome sequencing and several well-dated fossil 70 14 59 97 4 48 89 3 57 divergences for calibration. However, as discussed below, a Z 5 0.97 Z 5 4.1 Z 5 2.6 priori biological evidence and reasoning suggest that the pu- Suggestive V. H. Signficant Highly Significant rifying selection that most proteins experience should yield significantly different rates of change across genomes in dif- ferent lineages, violating the assumptions of the analysis. Fly and nematode models are of special concern as they Multi-gene calculation of metazoan divergence dates has have been the focus of several early analyses because of come under attack from a number of authors for reasons availability of genome sequence (e.g., Wray et al. 1996; Wang related to those discussed here (e.g., Ayala 1999; Jacobs 2002; et al. 1999). However, these taxa were originally selected for Smith and Peterson 2002), as well as from concerns regarding short generation time, an attribute associated with smaller data alignment and concatenation (e.g., Nei et al. 2001), un- genome size and high rate of deletion (Petrov et al. 2000). warranted claims of precision (e.g., Graur and Martin 2004), There appears to be a deletion mechanism that maintains the and insufficient fossil calibration (e.g., Peterson et al. 2004). small size of genomes in high generation rate taxa, thus con- Here we present a brief analysis showing that the first se- tributing to a higher mutation rate. This is corroborated by quenced genomes from the fly and nematode model systems the extreme genome evolution of Oikopleura (Seo et al. 2001), are pervasively biased toward high rates of evolution. Studies a larvacean urochordate with a 5-day generation time and the that use these and other ‘‘high-rate’’ taxa in multi-gene/pro- smallest genome known to date for animals (72 Mb). tein approaches to calculating divergence times (Table 1) are Our simple analyses of the fly and the nematode data show expected to yield early dates as a product of this bias. Con- that they have pervasively higher rates of evolution than the sequently, they do not provide evidence of early metazoan human lineage (Fig. 1; Table 1). Our analyses use compar- divergence as discussed below. isons of sequence data from Porifera (sponges), a universally 500 EVOLUTION&DEVELOPMENT Vol.