Developmental Biology ∎ (∎∎∎∎) ∎∎∎–∎∎∎

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Editorial

Eric Davidson’s career as a paleontologist

Much of what has been written on Eric Davidson is about his pioneering achievements in developmental molecular biology, through his studies of the gene regulatory network of the purple sea urchin. These activities were driven by a deep interest in wanting to understand how evolution works. In his fearless way this intellectual goal also led him to the fossil record and how that could further inform our understanding of the evolutionary process. I worked with Eric for 15 years on our joint interest in evolution and how combining the information from molecular biology and the fossil record could lead to insights on the evolutionary process. Throughout this time Andy Cameron also partnered and led on many of these activities. I wasn’t the only paleontologist who Eric collaborated with on these issues. Most notably, Doug Erwin and Eric wrote a number of seminal papers on the gene regulatory network and evolution. Other North American paleontologists who collaborated with Eric are Kevin Peterson and James Hagadorn. My work with Eric was initially spurred by our mutual interest in understanding how early animals had evolved. I first met Eric in the spring of 1999 at a CalPaleo conference at Caltech, where Eric was the featured evening speaker. We talked only briefly, chiefly about the upcoming meeting that we were both going to that June in China on the evolutionary origin of animals. This CalPaleo conference, primarily for paleontology graduate students and faculty in California, had among its organizers Kevin Peterson and James Hagadorn, then post-docs at Caltech. Eric and I were both attracted towards attending the meeting in China because it was to feature aspects of the newly discovered Doushantuo biota of late Precambrian (  600 million years old) microfossils interpreted as embryos of early animals. The main organizer of this meeting was Jun-Yuan Chen of the Nanjing Institute of Geology and Paleontology (Academia Sinica), and was held at a resort hotel on Fuxian Lake near Chengjiang in Yunnan Province, China. Chen had recently been co-author of a paper in Science on the Doushantuo fossils with others including Chia-Wei Li of the National Tsing Hua University in Taiwan (Li et al., 1998). This area in Yunnan also hosts rocks containing the famous Chengjiang fossil fauna (  515 million years old), an early Cambrian biota that contains the remains of soft-bodied marine organisms, much like the somewhat younger Middle Cambrian Burgess Shale fauna (  508 million years old) from British Columbia, both of which exemplify animal diversity during the Cambrian explosion. I and Steve Dornbos, then a graduate student with me at USC, arrived a few days early for the meeting in Yunnan. We had come to do some field work on the Chengjiang fauna, and stayed with http://dx.doi.org/10.1016/j.ydbio.2016.01.026 0012-1606/& 2016 Published by Elsevier Inc.

Jun-Yuan Chen and his research group at his laboratory in nearby Jinning. We then went on a pre-meeting field trip to adjacent Guizhou Province to see, among other things, the rocks containing the Doushantuo biota. While we were on that field trip Eric and Jane Rigg arrived at Jinning so that he could examine thin sections of the Doushantuo biota embryos, of which Chen’s group had many. When we arrived back from the field trip for the start of the meeting I immediately ran into Eric and we had much to discuss about the topics for presentation at the meeting. Unexpectedly, a number of individuals attending the meeting were affiliated with the Discovery Institute in Seattle, and we were faced with some interesting talks emphasizing the topic of intelligent design. Our interactions with this group at the meeting gained some notoriety and they have been written up in a book about the creationist movement (Forrest and Gross, 2004). At this meeting in a delightful locale along Fuxian Lake, Eric, Jane, Steve and I got to know well our host, Jun-Yuan Chen, as well as his then Ph.D. students including Feng Gao and Maoyan Zhu. During the meeting we also interacted significantly with Chia-Wei Li. It turned out that we all had deep interests in understanding the early evolution of animals, and the evolutionary mechanisms which brought about their evolution. We left that meeting knowing that we would be working together in the future on the fascinating fossils of the Doushantuo and Chengjiang biotas. Upon return to southern California Eric began work on the fossil embryos in the Doushantuo biota with Jun-Yuan Chen and Chia-Wei Li, together also with others including Kevin Peterson, James Hagadorn, Feng Gao, and Paola Oliveri, then a post-doc in his lab (Chen et al., 2000). Meanwhile, Steve Dornbos and I commenced work with Chen on the Chengjiang biota. We all stayed in touch and as things developed Eric asked me if I would like to join on a grant proposal to NASA to collaborate with Chen and Li and also John Eiler of Caltech, for a study of the Doushantuo biota. Our goals were to document the animals that were represented by these fossils, how they were preserved, and what environments they lived in. That grant was funded and led to an exciting time of interaction with our Chinese collaborators. We made several trips to work at the Early Life Research Center of the Nanjing Institute of Geology and Palaeontology in Chengjiang. There, Chen had overseen construction of a multistory building in which research was conducted on the Chengjiang and Doushantuo biotas. We would spend a week at the Center, working day and night on Doushantuo microfossils and their meaning. For a break we would stroll the picturesque streets of Chengjiang to buy tea and observe the street life, or take a drive along the beautiful shores of Fuxian Lake. One

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Editorial / Developmental Biology ∎ (∎∎∎∎) ∎∎∎–∎∎∎

Fig. 1. The NASA team at the Early Life Research Center in Chengjiang Yunnan, China. Top, from left: Chia-Wei Li, David Bottjer, Eric Davidson, Jun-Yuan Chen, Stephen Dornbos, Jane Rigg. Bottom, from left: Paola Oliveri, Feng Gao.

spring it was Eric’s birthday while we were in Chengjiang and Chen arranged for a memorable birthday party at a resort along the lakeshore. This was an exciting time for the “NASA team”, as Chen called us (Fig. 1), and we produced a number of important publications on the early animals represented by the Doushantuo biota (e.g., Chen et al., 2002; Chen et al., 2004; Dornbos et al., 2005; Chen et al., 2006; Dornbos et al., 2006). During this time we began weaving threads from this paleontological work together with work on sequencing the genome of the purple sea urchin, Strongylocentrotus purpuratus, that Eric and Andy Cameron were organizing with others. We talked at many meetings in Eric’s office at Caltech on the use of fossil data to show when in time important characters in evolution were evolving, combined with an understanding of the genes that produce these characters in modern organisms, as a way to understand when these specific genes first evolved. Calling this approach “paleogenomics”, we used as an example the first appearance in the early Cambrian of the echinoderm biomineralized tissue stereom, with our understanding of modern echinoid biomineralization genes, as a way to determine when these biomineralization genes first evolved (Bottjer et al., 2006). While we were not the first to coin the term paleogenomics, which has come to represent a variety of approaches, we were the first to formulate this particular kind of paleogenomic analysis. Meanwhile, Chen had forged a collaboration with Paul Tafforeau, a paleontologist at the European Synchrotron Radiation Facility, in Grenoble, France. This led us to do synchrotron x-ray microtomography of the Doushantuo microfossils. This technique allowed much finer resolution of these tiny fossils, and most importantly, the ability to do virtual sectioning of specimens. This opened our eyes to many important features of these early animal embryos. During the summer of 2008 Bill Schopf of UCLA organized a “World Summit on Ancient Microscopic Fossils” at UCLA. Eric, Chen, Feng Gao (then a Research Fellow with Eric), I, and others, used this as inspiration to spend several weeks at Caltech that summer looking at synchrotron images of the Doushantuo microfossils. The results of this work were presented at the UCLA conference and then ultimately published with input from others including Andy Cameron and Mike Hadfield of the University of Hawaii (Chen et al., 2009a). Other complimentary studies on the complex and sometimes controversial fossils of the Doushantuo biota were also pursued during this time (e,g, Chen et al., 2009b; Petryshyn et al., 2013).

Eric and I had been yearning to do more paleogenomics work, but the possibility of funding such interdisciplinary work has always been daunting. This situation changed in the fall of 2011, when we learned that the new NSF Director, Subra Suresh, had instituted a new program called CREATIV which would fund research combining approaches from traditionally disparate areas in science. Eric and I immediately applied for CREATIV funding and were successful and began work later in 2012. The goals of this research have been to understand how the two types of modern echinoids, the cidaroids and euechinoids, evolved from their last common ancestor  270 million years ago. This has quite naturally involved extensive paleontological and molecular biology studies of cidaroids and euechinoids. We assembled a team including USC graduate students Elizabeth Petsios and Jeff Thompson, Caltech graduate student Eric Erkenbrack, and Feng Gao. Plunging into the various aspects of this research, we made great progress, discussing our results every few months at late afternoon meetings in the coffee room of Eric’s lab, which we called “Archaeocidaris meetings”, after a prominent ancestral echinoid. This research has been very stimulating and from it we have learned a tremendous amount in the lab on the reorganization of echinoid gene regulatory networks that occurred as euechinoids and cidaroids diverged, and when this occurred through study of the fossil record (Gao et al., 2015; Erkenbrack and Davidson, 2015; Thompson et al., 2016). Meanwhile, Jun-Yuan Chen, although he still holds a position at Nanjing University, had retired from the Nanjing Institute of Geology and Paleontology, with Maoyan Zhu replacing him. Maoyan and his research group have continued working on the Doushantuo biota, and have continued to find fossil specimens that are greatly informative on early animal evolution. Maoyan and his then Ph.D. student Zongjun Yin pursued this work with Eric and I on Doushantuo fossils, and our last joint effort in this area was on an exceptional fossil that, along with Fangchen Zhao and Paul Tafforeau, we have interpreted as the best-preserved oldest adult fossil sponge (Yin et al., 2015). The presence of this sponge 600 million years ago implies that eumetazoan ancestors were also present at this time, and that the shared metazoan genetic toolkit must have originated much earlier. We all thoroughly enjoyed our work together on this remarkable fossil specimen! All of these various research projects were accompanied by much pleasure by all as we discussed science under favorable circumstances. For Eric and I, mixed in with science discussions were conversations about football, one of his acknowledged obsessions. These would usually occur on the way to lunch at Full House, a dim sum restaurant in Arcadia. For these lunch meetings, at the arranged time I would show up at Eric’s office, to be met by Jane Rigg, where Jane and I would discuss the issues of the day. After ten or fifteen minutes Jane would get a call from Eric that he was out back in his Acura waiting for me. I would join Eric with some of his traditional Appalachian music pouring out of the car speakers. Off we headed to Full House, with the requisite initial conversation on football, usually beginning with USC football, unless it was that brief period of the year when football news was lacking. Eric was well-known at Full House, and as we sat down we would order up many more dishes that we would be able to eat. Soon the talk was on our research which continued for as much as an hour. Then we would bundle up the leftovers to be taken back to his lab, and head over to Caltech. If we had a paper or grant we were writing we would spend additional time in his office doing that before I headed back to USC later in the afternoon. We did this every month or so for many years, interspersed with more intensive meetings caused by deadlines and in the past few years by our Archaeocidaris meetings. We were always amazed at how many ideas we had and how much work got done, apparently due to the presence of the dim sum!

Editorial / Developmental Biology ∎ (∎∎∎∎) ∎∎∎–∎∎∎

We shared a lot of adventures at a lot of places and with a lot of other people. I know that many other people interacted with Eric in this way, too. His career as a paleontologist, as I have outlined, was but one of many facets of his life. Perhaps most importantly, he was among the best of friends, and we all had a great time pursuing science with him in the deepest ways, while also enjoying every minute of it!

References Bottjer, D.J., Davidson, E.H., Peterson, K.J., Cameron, R.A., 2006. Paleogenomics of echinoderms. Science 314, 956–960. Chen, J.-Y., Oliveri, P., Li, C.-W., Zhou, G.-Q., Gao, F., Hagadorn, J.W., Peterson, K.J., Davidson, E.H., 2000. Precambrian animal diversity: putative phosphatized embryos from the Doushantuo Formation of China. Proc. Natl. Acad. Sci. USA 97, 4457–4462. Chen, J.-Y., Oliveri, P., Gao, F., Dornbos, S.Q., Li, C.W., Bottjer, D.J., Davidson, E.H., 2002. Precambrian animal life: probable developmental and adult cnidarian forms from southwest China. Dev. Biol. 248, 182–196. Chen, J.-Y., Bottjer, D.J., Oliveri, P., Dornbos, S.Q., Gao, F., Ruffins, S., Chi, H., Li, C.-W., Davidson, E.H., 2004. Small bilaterian fossils from 40 to 55 million years before the Cambrian. Science 305, 218–222. Chen, J.-Y., Bottjer, D.J., Davidson, E.H., Dornbos, S.Q., Gao, X., Yang, Y.-H., Li, C.W., Li, G., Wang, X.-Q., Xian, D.-C., Wu, S.H., Hwu, Y.-K., Tafforeau, P., 2006. Phosphatized polar lobe-forming embryos from the Precambrian of southwest China. Science 312, 1644–1646. Chen, J.-Y., Bottjer, D.J., Davidson, E.H., Li, G., Gao, F., Cameron, R.A., Hadfield, M.G., Xian, D.-C., Tafforeau, P., Jia, Q.-J., Sugiyama, H., Tang, R., 2009a. Phase contrast synchrotron X-ray microtomography of Ediacaran (Doushantuo) metazoan microfossils: phylogenetic diversity and evolutionary implications. Precambr. Res. 173, 191–200. Chen, J.-Y., Bottjer, D.J., Li, G., Hadfield, M.G., Gao, F., Cameron, A.R., Zhang, C.-Y., Xian, D.-C., Tafforeau, P., Liao, X., Yin, Z.-J., 2009b. Complex embryos displaying

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bilaterian characters from Precambrian Doushantuo phosphate deposits, Weng’an, Guizhou, China. Proc. Natl. Acad. Sci. USA 106, 19056–19060. Dornbos, S.Q., Bottjer, D.J., Chen, J.-Y., Oliveri, P., Gao, F., Li, C.-W., 2005. Precambrian animal life: taphonomy of phosphatized metazoan embryos from southwest China. Lethaia 38, 101–109. Dornbos, S.Q., Bottjer, D.J., Chen, J.-Y., Gao, F., Oliveri, P., Li, C.-W., 2006. Environmental controls on the taphonomy of phosphatized animals and animal embryos from the Neoproterozoic Doushantuo Formation, southwest China. Palaios 21, 3–14. Erkenbrack, E.M., Davidson, E.H., 2015. Evolutionary rewiring of gene regulatory network linkages at divergence of the echinoid subclasses. Proc. Natl. Acad. Sci. USA 112, E4075–E4084. Forrest, B., Gross, P.R., 2004. Creationism’s Trojan Horse: The Wedge of Intelligent Design. Oxford University Press, New York, USA. Gao, F., Thompson, J.R., Petsios, E., Erkenbrack, E., Moats, R.A., Bottjer, D.J., Davidson, E.H., 2015. Juvenile skeletogenesis in anciently diverged sea urchin clades. Dev. Biol. 400, 148–158. Li, C.-W., Chen, J.-Y., Hua, T.-E., 1998. Precambrian sponges with cellular structures. Science 279, 879–882. Petryshyn, V.A., Bottjer, D.J., Chen, J.-Y., Gao, F., 2013. Petrographic analysis of new specimens of the putative microfossil Vernanimalcula guizhouena (Doushantuo Formation, South China). Precamb. Res. 225, 58–66. Thompson, J.R., Petsios, E., Davidson, E.H., Erkenbrack, E., Gao, F., Bottjer, D.J., 2016. Reorganization of sea urchin gene regulatory networks at least 268 million years ago as revealed by oldest fossil cidaroid echinoid. Sci. Rep 5, 15541, http:// dx.doi.org/10.1038/srep15541. Yin, Z., Zhu, M., Davidson, E.H., Bottjer, D.J., Zhao, F., Tafforeau, P., 2015. Sponge grade body fossil with cellular resolution dating 60 Myr before the Cambrian. Proc. Natl. Acad. Sci. USA 112, E1453–E1460.

David J. Bottjer Department of Earth Sciences, University of Southern California, Los Angeles, CA 90089-0740, United States

Eric Davidson's career as a paleontologist.

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