Author’s Accepted Manuscript Eric, Evolution and Bodyplans Douglas H. Erwin
www.elsevier.com/locate/developmentalbiology
PII: DOI: Reference:
S0012-1606(16)00019-1 http://dx.doi.org/10.1016/j.ydbio.2016.01.024 YDBIO6994
To appear in: Developmental Biology Cite this article as: Douglas H. Erwin, Eric, Evolution and Bodyplans, Developmental Biology, http://dx.doi.org/10.1016/j.ydbio.2016.01.024 This is a PDF file of an unedited manuscript that has been accepted for publication. As a service to our customers we are providing this early version of the manuscript. The manuscript will undergo copyediting, typesetting, and review of the resulting galley proof before it is published in its final citable form. Please note that during the production process errors may be discovered which could affect the content, and all legal disclaimers that apply to the journal pertain.
Eric, Evolution and Bodyplans Douglas H. Erwin, Dept. of Paleobiology MRC-121, Smithsonian Institution, PO Box 37012, Washington, DC 20013-7012 E-mail: [email protected] “Good to see you, man” So began each conversation with Eric, as I walked into his office in the basement of Church at Cal Tech. Although the piles on his desk changed with each project, interspersed with the ubiquitous blue sheets upon which Eric scrawled notes, the rest of the office was comfortably constant: the Chinese couch and chair in a corner to the right, the coffee pot to the left, usually overseen by Eric’s long-time majordomo Jane Rigg, a photo of Eric in a Cal Tech football uniform. There were occasional additions of course: a bottle of Ancient Age Bourbon with a photo of Vernanimacula gracing the front and additions to the collection of fossil echinoids on a side table. Eric and I began collaborating in the late 1990s, after he visited the National Museum of Natural History to see our collection of fossils of the Burgess Shale. As we looked at some of the remarkable morphologies found we talked about the evolution of body plans during the Cambrian Explosion of animal life about 540 million years ago (Ma). Through Kevin Peterson, a paleontologist and evolutionary developmental biologist who had worked in Eric’s lab, Eric knew of my interests the Cambrian and in comparative developmental studies. He was surprised to learn that I had read his 1969 and 1971 gene regulatory model papers with Roy Britten and that they had deeply influenced my interests in evolution. Eric had a deep and abiding interest in the history of life and the role fossils played in documenting that history, but even at his most charitable he was never entirely convinced that paleontologists were scientists – too few mechanisms and too many theories for Eric to abide. But evidently Eric decided that in my case there was some hope because he invited me to visit him later that year. Eric and I shared an interest in the origins and early evolution of animal body plans. I had been interested in the subject since I was a graduate student (although my dissertation was on a completely different topic) and Eric began thinking about the topic by the early 1970s. The explosion of comparative developmental data from the mid-1990s onward led to the recognition that many apparently key developmental genes were conserved between flies and vertebrates, and thus must have been present in the last common bilaterian ancestor (LCBA) (and more recent studies have shown that many appeared much earlier in metazoan history). I had co-authored a couple of papers on this topic with my paleontological colleagues Jim Valentine and David Jablonski, but I had become convinced that some of the ‘evo-devo’ interpretations of highly conserved genes were a bit overly enthusiastic. As Eric and I began talking at CalTech we recognized that we might be able to make some progress by combining Eric’s deep understanding of the developmental issues with my knowledge of the Ediacaran and Cambrian fossil record. We began by focusing on the interpretations of these highly conserved genes and the nature of the LCBA. To a paleontologist the complexity of the LCBA was of great interest because it informed the probability that we might be able to find evidence of fossils of this level of phenotypic complexity in the fossil record. To a developmental biologist the issue was critical to understanding how GRNs evolved and how they influenced the evolution of body plans. Our discussions led to our first paper (Erwin and Davidson, 2002) in which we advanced
the view that the LCBA may have had far less morphological complexity than others had argued: no true segmentation or appendages, no image forming eyes, etc. As the GRN structure of the Strongylocentrotus embryo was revealed experimentally in Eric’s lab our discussions increasingly focused on GRN evolution. In 2003 Veronica Hinman and Eric published a paper showing the conservation of a GRN subnet required for endoderm specification (Hinman et al., 2003). Further work progressively revealed the hierarchical structure of the GRN network and the differing evolutionary lability of different network components. Eric and I began discussing the evolutionary implications, particularly the importance of what Eric had termed ‘kernels’, the recursively wired subnets that were responsible for regional patterning in the developing embryo. The nature of kernels and suggestions about their role in the formation of animal body plans was the focus of the next paper we wrote (Davidson and Erwin, 2006). The empirical data on GRNs was growing rapidly and our discussions, sandwiched in among other priorities increasingly focused on the topologies of GRNs. We produced a few more papers on this topic in 2009 and 2010. I think we were really stuck on this issue over the past few years, however, and it wasn’t until Isabelle Peter and Eric developed a more robust computational approach to GRNs in the past couple of years that it began to become a bit clearer how we could attach the evolutionary problem with more rigor. Beyond our ongoing discussions on the role of cis-regulation and developmental gene networks in the evolution of animal body plans Eric had interests in the early fossil record of animals, and of course in the fossil history of echinoids. Although Eric often showed me the data and manuscripts for these projects before publication they were not ones with which I was directly involved. His collaborations with Chinese paleontologist Chen Jun-Yuan began with a meeting in China in 1999 on the origin of animal body plans. Eric wondered if the recently discovered fossilized metazoan embryos found in the Doushantuo formation in southern China might not reveal something of the early history of animal development. In particular, Eric was interested in finding evidence of embryos of bilaterians. This developed into a fairly extensive ‘side-project’ applying new techniques and intensive scanning of thin-sections of rock in search of preserved Doushantuo embryos. Eric, Chen and their colleagues, including paleontologist Dave Bottjer of the University of Southern California formed one of several international collaborations trying to understand these fossils. Before the mid-1990s paleontologists had not anticipated that embryos could be preserved as fossils, and there remain many question about how this occurs and what biological information we can glean from these fossils. Collaboration with Eric was often one long argument (and not quite in the way meant by Darwin). Eric possessed a keenly logical mind and a driving curiosity about development, evolution and anything even tangentially related to them (and much else besides). As we wrote our 2010 paper (Davidson and Erwin, 2010) we got into a long debate over the age of the Doushantuo embryos. I had been collaborating with MIT geochronologist Sam Bowring for over a decade by this time and was reasonably well versed in the evaluation of age estimates from the geological record. Eric favored estimates of about 600 Ma while I was more comfortable with age estimates of about 580 Ma or younger, roughly coincident with the oldest Ediacaran fossils. Someone who did not know Eric might expect that he would accept the views of a colleague (me) who was, after all, a geologist with some experience with geochronology. And someone who did not understand Eric might think that given his interest in the Doushantuo embryo fossils Eric was pushing for an older age. But Eric had visited the one of the Doushantuo
localities on a trip to China and had read as many of the geological papers on the Doushantuo as I had. He had zeroed in on the greatest weakness of a 2005 paper in Science with some U-Pb dates from Sam’s lab (Condon et al., 2005): problems with the correlation between rocks in the Yangtze gorges and those in the Weng’an area in southern China. So around and around we went arguing about the relative reliability of different age estimates, correlations and the amount of time missing from the geological sections. And Eric cared passionately about each of these details, as passionately as he did about patterns of gene interactions. The details mattered to Eric because the details were the only data through which we could make sense of this little piece of the history of life. Compromise was of course anathema but we eventually settled the issue and finished the paper. But the denouement came last summer. I spent several weeks in China and discovered that recent work pointed to an older estimate for the age of the Doushantuo fossils. Eric’s intuition (although he would never have accepted the term) had been right all along – the age of the embryos is close to 600 Ma. He was good enough not to gloat (too much) when I gave him the news. A fragment from the Greek poet Atchilochus: “The fox knows many things, but the hedgehog knows one big thing” was the foundation of Isaiah Berlin’s famous essay about the fox and the hedgehog. Berlin suggested that many writers and thinkers could be separated into foxes and hedgehogs (although Berlin knew that we all have elements of the fox and the hedgehog). He evidently meant this as sort of an intellectual parlor game, although it has been taken more seriously. Many would unhesitatingly classify Eric as a hedgehog -- incredibly driven to explore cis-regulation and its implications for development and evolution. This persistent drive was the source of his remarkable successes and his most profound contributions to science. Eric was fond of the following syllogism: 1) morphology is a product of development; 2) development is controlled by gene regulation; 3) therefore evolutionary changes in morphology depend upon changes in developmental GRNs. This is true as far as it goes, but the challenge is that evolutionary changes in morphology depend upon much more than developmental GRNs: ecological interactions, environmental changes and other sorts of genetic changes all play a role in the success or failure of morphological changes. Eric recognized these complexities of course, but it was that remarkable drive, his inate hedgehoginess, if you will, that was the source of his power as a developmental biologist. There were so many questions Eric and I never had a chance to discuss. Our last conversation, just a few days before he died was on how we could push further on the mechanisms underlying evolutionary changes in gene regulatory patterning. This past summer we submitted a preliminary research proposal to re-engineer the developmental GRN of a cidaroid to test ideas about the changes in GRN topology that led to euechinoids. There were many more conceptual papers waiting to be written as well, exploring the implications for evolution of the work Eric and Isabelle Peter had done on GRN control processes. And I never got around to asking how Eric managed his remarkable depth of knowledge of developmental patterning and genetic control mechanisms across the animal kingdom. Early in our collaboration I occasionally mused about searching out some obscure fact about the development of kinorhynchs in order to stump Eric. But I realized that Eric would already know that fact AND why the experiments that uncovered it were flawed AND he would have just seen a paper by another group showing … You get the idea. It wasn’t that Eric knew everything
about development, but he certainly seemed to know everything relevant. And it was all stored away in that supremely logical brain, pieces of a puzzle he never gave up trying to solve. References Condon, D., Zhu, M., Bowring, S., Wang, W., Yang, A., Jin, Y., 2005. U-Pb ages from the neoproterozoic Doushantuo Formation, China. Science 308, 95-98. Davidson, E.H., Erwin, D.H., 2006. Gene regulatory networks and the evolution of animal body plans. Science 311, 796-800. Davidson, E.H., Erwin, D.H., 2010. An integrated view of precambrian eumetazoan evolution. Cold Spring Harbor Symposium on Quantitative Biology 79, 65-80. Erwin, D.H., Davidson, E.H., 2002. The last common bilaterian ancestor. Development 129, 30213032. Hinman, V.F., Nguyen, A.T., Cameron, R.A., Davidson, E.H., 2003. Developmental gene regulatory network architecture across 500 million years of echinoderm evolution. Proceedings of the National Academy of Sciences, USA 100, 13356-13361.
www.elsevier.com/locate/developmentalbiology
PII: DOI: Reference:
S0012-1606(16)00019-1 http://dx.doi.org/10.1016/j.ydbio.2016.01.024 YDBIO6994
To appear in: Developmental Biology Cite this article as: Douglas H. Erwin, Eric, Evolution and Bodyplans, Developmental Biology, http://dx.doi.org/10.1016/j.ydbio.2016.01.024 This is a PDF file of an unedited manuscript that has been accepted for publication. As a service to our customers we are providing this early version of the manuscript. The manuscript will undergo copyediting, typesetting, and review of the resulting galley proof before it is published in its final citable form. Please note that during the production process errors may be discovered which could affect the content, and all legal disclaimers that apply to the journal pertain.
Eric, Evolution and Bodyplans Douglas H. Erwin, Dept. of Paleobiology MRC-121, Smithsonian Institution, PO Box 37012, Washington, DC 20013-7012 E-mail: [email protected] “Good to see you, man” So began each conversation with Eric, as I walked into his office in the basement of Church at Cal Tech. Although the piles on his desk changed with each project, interspersed with the ubiquitous blue sheets upon which Eric scrawled notes, the rest of the office was comfortably constant: the Chinese couch and chair in a corner to the right, the coffee pot to the left, usually overseen by Eric’s long-time majordomo Jane Rigg, a photo of Eric in a Cal Tech football uniform. There were occasional additions of course: a bottle of Ancient Age Bourbon with a photo of Vernanimacula gracing the front and additions to the collection of fossil echinoids on a side table. Eric and I began collaborating in the late 1990s, after he visited the National Museum of Natural History to see our collection of fossils of the Burgess Shale. As we looked at some of the remarkable morphologies found we talked about the evolution of body plans during the Cambrian Explosion of animal life about 540 million years ago (Ma). Through Kevin Peterson, a paleontologist and evolutionary developmental biologist who had worked in Eric’s lab, Eric knew of my interests the Cambrian and in comparative developmental studies. He was surprised to learn that I had read his 1969 and 1971 gene regulatory model papers with Roy Britten and that they had deeply influenced my interests in evolution. Eric had a deep and abiding interest in the history of life and the role fossils played in documenting that history, but even at his most charitable he was never entirely convinced that paleontologists were scientists – too few mechanisms and too many theories for Eric to abide. But evidently Eric decided that in my case there was some hope because he invited me to visit him later that year. Eric and I shared an interest in the origins and early evolution of animal body plans. I had been interested in the subject since I was a graduate student (although my dissertation was on a completely different topic) and Eric began thinking about the topic by the early 1970s. The explosion of comparative developmental data from the mid-1990s onward led to the recognition that many apparently key developmental genes were conserved between flies and vertebrates, and thus must have been present in the last common bilaterian ancestor (LCBA) (and more recent studies have shown that many appeared much earlier in metazoan history). I had co-authored a couple of papers on this topic with my paleontological colleagues Jim Valentine and David Jablonski, but I had become convinced that some of the ‘evo-devo’ interpretations of highly conserved genes were a bit overly enthusiastic. As Eric and I began talking at CalTech we recognized that we might be able to make some progress by combining Eric’s deep understanding of the developmental issues with my knowledge of the Ediacaran and Cambrian fossil record. We began by focusing on the interpretations of these highly conserved genes and the nature of the LCBA. To a paleontologist the complexity of the LCBA was of great interest because it informed the probability that we might be able to find evidence of fossils of this level of phenotypic complexity in the fossil record. To a developmental biologist the issue was critical to understanding how GRNs evolved and how they influenced the evolution of body plans. Our discussions led to our first paper (Erwin and Davidson, 2002) in which we advanced
the view that the LCBA may have had far less morphological complexity than others had argued: no true segmentation or appendages, no image forming eyes, etc. As the GRN structure of the Strongylocentrotus embryo was revealed experimentally in Eric’s lab our discussions increasingly focused on GRN evolution. In 2003 Veronica Hinman and Eric published a paper showing the conservation of a GRN subnet required for endoderm specification (Hinman et al., 2003). Further work progressively revealed the hierarchical structure of the GRN network and the differing evolutionary lability of different network components. Eric and I began discussing the evolutionary implications, particularly the importance of what Eric had termed ‘kernels’, the recursively wired subnets that were responsible for regional patterning in the developing embryo. The nature of kernels and suggestions about their role in the formation of animal body plans was the focus of the next paper we wrote (Davidson and Erwin, 2006). The empirical data on GRNs was growing rapidly and our discussions, sandwiched in among other priorities increasingly focused on the topologies of GRNs. We produced a few more papers on this topic in 2009 and 2010. I think we were really stuck on this issue over the past few years, however, and it wasn’t until Isabelle Peter and Eric developed a more robust computational approach to GRNs in the past couple of years that it began to become a bit clearer how we could attach the evolutionary problem with more rigor. Beyond our ongoing discussions on the role of cis-regulation and developmental gene networks in the evolution of animal body plans Eric had interests in the early fossil record of animals, and of course in the fossil history of echinoids. Although Eric often showed me the data and manuscripts for these projects before publication they were not ones with which I was directly involved. His collaborations with Chinese paleontologist Chen Jun-Yuan began with a meeting in China in 1999 on the origin of animal body plans. Eric wondered if the recently discovered fossilized metazoan embryos found in the Doushantuo formation in southern China might not reveal something of the early history of animal development. In particular, Eric was interested in finding evidence of embryos of bilaterians. This developed into a fairly extensive ‘side-project’ applying new techniques and intensive scanning of thin-sections of rock in search of preserved Doushantuo embryos. Eric, Chen and their colleagues, including paleontologist Dave Bottjer of the University of Southern California formed one of several international collaborations trying to understand these fossils. Before the mid-1990s paleontologists had not anticipated that embryos could be preserved as fossils, and there remain many question about how this occurs and what biological information we can glean from these fossils. Collaboration with Eric was often one long argument (and not quite in the way meant by Darwin). Eric possessed a keenly logical mind and a driving curiosity about development, evolution and anything even tangentially related to them (and much else besides). As we wrote our 2010 paper (Davidson and Erwin, 2010) we got into a long debate over the age of the Doushantuo embryos. I had been collaborating with MIT geochronologist Sam Bowring for over a decade by this time and was reasonably well versed in the evaluation of age estimates from the geological record. Eric favored estimates of about 600 Ma while I was more comfortable with age estimates of about 580 Ma or younger, roughly coincident with the oldest Ediacaran fossils. Someone who did not know Eric might expect that he would accept the views of a colleague (me) who was, after all, a geologist with some experience with geochronology. And someone who did not understand Eric might think that given his interest in the Doushantuo embryo fossils Eric was pushing for an older age. But Eric had visited the one of the Doushantuo
localities on a trip to China and had read as many of the geological papers on the Doushantuo as I had. He had zeroed in on the greatest weakness of a 2005 paper in Science with some U-Pb dates from Sam’s lab (Condon et al., 2005): problems with the correlation between rocks in the Yangtze gorges and those in the Weng’an area in southern China. So around and around we went arguing about the relative reliability of different age estimates, correlations and the amount of time missing from the geological sections. And Eric cared passionately about each of these details, as passionately as he did about patterns of gene interactions. The details mattered to Eric because the details were the only data through which we could make sense of this little piece of the history of life. Compromise was of course anathema but we eventually settled the issue and finished the paper. But the denouement came last summer. I spent several weeks in China and discovered that recent work pointed to an older estimate for the age of the Doushantuo fossils. Eric’s intuition (although he would never have accepted the term) had been right all along – the age of the embryos is close to 600 Ma. He was good enough not to gloat (too much) when I gave him the news. A fragment from the Greek poet Atchilochus: “The fox knows many things, but the hedgehog knows one big thing” was the foundation of Isaiah Berlin’s famous essay about the fox and the hedgehog. Berlin suggested that many writers and thinkers could be separated into foxes and hedgehogs (although Berlin knew that we all have elements of the fox and the hedgehog). He evidently meant this as sort of an intellectual parlor game, although it has been taken more seriously. Many would unhesitatingly classify Eric as a hedgehog -- incredibly driven to explore cis-regulation and its implications for development and evolution. This persistent drive was the source of his remarkable successes and his most profound contributions to science. Eric was fond of the following syllogism: 1) morphology is a product of development; 2) development is controlled by gene regulation; 3) therefore evolutionary changes in morphology depend upon changes in developmental GRNs. This is true as far as it goes, but the challenge is that evolutionary changes in morphology depend upon much more than developmental GRNs: ecological interactions, environmental changes and other sorts of genetic changes all play a role in the success or failure of morphological changes. Eric recognized these complexities of course, but it was that remarkable drive, his inate hedgehoginess, if you will, that was the source of his power as a developmental biologist. There were so many questions Eric and I never had a chance to discuss. Our last conversation, just a few days before he died was on how we could push further on the mechanisms underlying evolutionary changes in gene regulatory patterning. This past summer we submitted a preliminary research proposal to re-engineer the developmental GRN of a cidaroid to test ideas about the changes in GRN topology that led to euechinoids. There were many more conceptual papers waiting to be written as well, exploring the implications for evolution of the work Eric and Isabelle Peter had done on GRN control processes. And I never got around to asking how Eric managed his remarkable depth of knowledge of developmental patterning and genetic control mechanisms across the animal kingdom. Early in our collaboration I occasionally mused about searching out some obscure fact about the development of kinorhynchs in order to stump Eric. But I realized that Eric would already know that fact AND why the experiments that uncovered it were flawed AND he would have just seen a paper by another group showing … You get the idea. It wasn’t that Eric knew everything
about development, but he certainly seemed to know everything relevant. And it was all stored away in that supremely logical brain, pieces of a puzzle he never gave up trying to solve. References Condon, D., Zhu, M., Bowring, S., Wang, W., Yang, A., Jin, Y., 2005. U-Pb ages from the neoproterozoic Doushantuo Formation, China. Science 308, 95-98. Davidson, E.H., Erwin, D.H., 2006. Gene regulatory networks and the evolution of animal body plans. Science 311, 796-800. Davidson, E.H., Erwin, D.H., 2010. An integrated view of precambrian eumetazoan evolution. Cold Spring Harbor Symposium on Quantitative Biology 79, 65-80. Erwin, D.H., Davidson, E.H., 2002. The last common bilaterian ancestor. Development 129, 30213032. Hinman, V.F., Nguyen, A.T., Cameron, R.A., Davidson, E.H., 2003. Developmental gene regulatory network architecture across 500 million years of echinoderm evolution. Proceedings of the National Academy of Sciences, USA 100, 13356-13361.
