THE EVOLUTIONARY ECOLOGY OF DEVELOPMENT

Authors


Review of : Gilbert, S. F., and D. Epel . 2009 . Ecological Developmental Biology: Integrating Epigenetics, Medicine, and Evolution . Sinauer Associates Inc. , 480 pp. , ISBN : 978-0-87893-299-3 . Paper. $49.95

I write these words a day after witnessing a historic moment, the inauguration of President Obama, in a year that celebrates the 150th anniversary of The Origin of Species. Yet that day in 1809 that saw the birth of both Charles Darwin and Abraham Lincoln went completely unnoted at the time. The importance of some events is obvious when they occur, others only long after. Some historical movements are captured in a single event, whereas others are the slow accumulation of many small actions. Often it is a bit of both. Obama's inauguration was the culmination of a decades long struggle. Over the course of three decades, the Modern Synthesis took the ideas first put forth by Darwin and joined them with genetics, ecology, systematics, and paleontology.

Certain events were milestones noted at the time, particularly the books of Dobzhansky, Mayr, Huxley, Simpson, and Stebbins. But the Synthesis was much more than those books. It consisted of numerous other publications, the importance of some was noted at the time and others only many decades later. Nor did that process halt in the 1950s. The Synthesis was being declared complete shortly after the publication of Watson and Crick's milestone paper. Recognized even at the time of the Synthesis, not all of biology participated, most pointedly developmental biology. But the seeds of the final synthesis were being planted even then. Over the next five decades, numerous papers and books would be published leading to a joining that is finally happening. The appearance of a textbook is often the culmination of a long process moving a subject from the fringes to the center of a discipline, or perhaps the coalescence of a discipline. Ecological Developmental Biology is such a milestone.

According to the title, this book is about how the external environment and ecological processes affect development, eco–devo in current parlance. However, it is really two books. The first two sections match the title. The third section is about evo–devo, the interaction of evolutionary and developmental processes. At very end are hints of the marriage of these two disciplines into eco–evo–devo.

The book is written as an upper-level undergraduate textbook. The authors claim that the book is readable by a student with just introductory biology, which I strongly doubt. The background knowledge assumed and the vocabulary used require a student with the sort of grounding in genetics, cell biology, and evolution that comes only with more advanced courses. This book would make an excellent supplemental text in a developmental biology course. Scott Gilbert is the author of a developmental biology textbook and this new book is aimed at topics not covered in that more traditional text. The book could also be the focus of an advanced topics or graduate-level course.

The book could profitably be read by researchers in developmental biology, ecology, and evolution and should be read by such a wide audience. The material is presented in a way that makes it very accessible to someone with just a smattering of background in the other fields. It does an excellent job of providing both depth and breadth while keeping the language from getting too technical.

The strengths of the book are the interdisciplinary scope and the engaging writing style. It conveys complex concepts in a straightforward fashion. The book is up to the usual visual standards of all Sinauer books with well-chosen photographs and well-designed illustrations that make each point clearly and complement the text nicely. The only unfortunate style choice was to have a separate bibliography for each chapter, making it hard to relocate citations. My only complaint with the writing is a tendency toward distracting asides. Some appear as throwaway lines in the text, while most are confined to footnotes1 or boxes. I got the sense that the authors felt compelled to tell us about every interesting fact learned in the process of assembling the book. Although all of those facts are fascinating, such asides can let major concepts get lost in the details. Both authors have received awards for excellence in teaching. These asides are probably ones that they pepper their students with in class to keep their attention. Although good in a classroom setting, they can become a distraction in a written text. The medium matters. This is a minor caveat, though.

In the title of the book, ecology is a modifier of development and this is definitely a book about developmental biology, rather than ecology. It also is firmly about Kingdom Animalia. Although the authors throw in some examples from Kingdom Plantae, without the complete context of plant developmental systems, the examples cannot be fully appreciated. Plant development has fundamental differences from animal development, for example, the lack of a distinction between somatic and germ cell lineages. The other multicellular kingdom, Fungi, is totally absent.

At times this book comes across as a buffet of related topics, rather than a coherent whole. The subtitle of the book—Integrating Epigenetics, Medicine, and Evolution-–gives some sense of this eclectic mix. The book has a very strong human medical viewpoint, with some attention paid to environmental issues of other vertebrates. As such, the book is well-suited to reaching the typical premedical undergraduate, who desperately needs to think more broadly, at the risk, though, of making eco–devo seem to be primarily about public health. There is extensive content dealing with health, conservation, and regulatory issues, often in those footnotes and boxes. Such material follows in the footsteps of today's textbooks that feel compelled to convince students that the material is relevant and important to their everyday existence. To the extent that developmental biology and medicine have ignored these issues, making students and researchers aware of them is important, and the authors are obviously passionate about these topics.

The book is strong testament that developmental biology needs to pay attention to ecology, but it does little to argue the reverse. The closest it comes to showing how more attention to development would benefit ecologists is the discussion of the effects of UV irradiance on early embryos as an explanation for night-time spawning. Currently, most ecological models treat development as a black box, ignoring developmental limitations and constraints. It will not be until models of age- and stage-structured demographics embrace those mechanistic details that a truly interdisciplinary eco–devo will emerge.

In contrast, evolutionary biology has long been aware of the importance of development, despite the book's claims. The field of evo–devo is truly interdisciplinary, providing complementary understanding of evolutionary and developmental processes. Which brings me to the two major failings of this book, its portrayal of the history of evolutionary biology and its discussion of evolutionary and developmental theory.

The historical errors are of lesser importance, almost entirely sins of omission rather than commission. As my own work is part of what is omitted, you are welcome to discount these complaints. This is a textbook, not a review article. Science textbooks of necessity give history short shrift. In this case, however, because the authors go out of their way to give a historical account (e.g., Appendix C), it is proper to call them on any errors.

My complaint is not the claim that the Modern Synthesis failed to encompass developmental biology. That is demonstrably true. The problem is the claim that this failure was due to a rejection of developmental biology as important to understanding evolutionary processes. Even at the culmination of the Synthesis, the leading thinkers noted the need for a better understanding of development (Smocovitis 1996). The authors' claim for an antipathy to development is made through a single quote by Bruce Wallace (1986). Many from that same period said the opposite.

As presented, the story of the marriage between development and evolution jumps from the 1950s to the 2000s (e.g., pp. 427–428, The Return of Plasticity), ignoring the extensive literature on the evolution of phenotypic plasticity in the 1980s and 1990s (Pigliucci 2001; DeWitt and Scheiner 2003; West-Eberhard 2003). For example, the cited experiments on selection of plasticity are from the 2000s, ignoring work done more than 15 years earlier (Hillesheim and Stearns 1991; Scheiner and Lyman 1991). Although Stephen Gould's attempt in the 1970s to raise developmental constraints above natural selection in determining evolutionary trajectories led to a decade of vociferous debate, I heard few say that development could be completely ignored. It is true that when I began my work on the evolution of plasticity in the early 1980s, environmental effects were mostly treated as just noise. But by the end of that decade, the debates were not about whether genotype–environment interactions were important, but about genetic models of plasticity. All of us were keenly aware that developmental biology could greatly inform that debate. Most important, all of that work was done within the paradigm of the Modern Synthesis and accepted by the community as a whole, evidenced by the fact that Mary Jane West-Eberhard was the president of the Society for the Study of Evolution in 1992.

Both authors are developmental biologists, and it shows. The level of detail, assumed background knowledge, and use of jargon is much greater when dealing with topics in developmental and molecular biology. The ecology contains no obvious errors, probably because it consists of a series of examples with no discussion of the underlying theory. Similarly, the evolutionary examples are correct, it is when they deal with evolutionary theory that they get into trouble. The problems come from a tangle of the pedagogical approach taken, the authors' misunderstandings of evolutionary theory, and the lack of a well-articulated theory of development.

I can only speculate why the authors get their history wrong. It may be that their background in developmental biology has them battling that discipline's ruling paradigm of laboratory-based studies focused on a very short list of model organisms. Such a paradigm has never existed within evolutionary ecology; if anything it has an antimodel organism bias. Thus, the authors tout eco–evo–devo as a new paradigm, rather than the beginning of the end of a decades long processes. It is true that evolutionary and developmental biologists did not talk to each other for a long time. It is fair to say, though, that evolutionary biologists bemoaned this gap and tried to reach across it well before the developmental biologists.

The book's problems are exacerbated by a lack of a coherent theoretical framework, starting with a failure to provide a definition of development. From that font of all wisdom, Wikipedia, we get: “Developmental biology is the study of the process by which organisms grow and develop. Modern developmental biology studies the genetic control of cell growth, differentiation and ‘morphogenesis,’ which is the process that gives rise to tissues, organs and anatomy.” In some places in this book, development is equated with body construction, consistent with both Wikipedia and what I would have given as a definition. At other times, though, development seems to be equated with changes in gene expression. While such changes are clearly necessary for development, they are not sufficient. For example, if E. coli is given a new carbon source, gene expression changes, but no one would call this development.

The lack of a definition ramifies throughout the book. Chapter 3 on developmental symbiosis states that “all development is co-development” (p. 114). However, nearly all of the examples are interactions between a multicellular species and a unicellular species, mostly bacteria. They describe how one organism affects the development of another, but fail to demonstrate co-development, the reciprocal control of development.

The definitional lack intersects with the focus on human health when they get to the story of malaria. As presented, it nicely links molecular evolution and natural selection. However, the authors attempt to tie it to the evolution of developmental regulatory genes. While it does demonstrate how the regulation of gene expression can respond to natural selection, this is not development. More attention could have been given to their three-spine stickleback story, which is about development. That example could have been used in their chapter on the success of the Modern Synthesis, instead of malaria. However, this would have required a change in focus from population and molecular genetics to quantitative genetics. It is unfortunate that quantitative genetics is given short shrift as that is where linkages between development and evolution have been the most fruitful (Berrigan and Scheiner 2004).

The authors attempt to make development a central part of evolutionary theory. “The explananda (that which needs to be explained) of evolutionary biology must include both a theory of change and a theory of body construction.” (p. 411) Body construction, however, has relevance for multicellular organisms only. As such, any theory that combined both would be a special case of a more general theory of evolution. As presented, this theory is built primarily on information about animal development. The relevance to plants and fungi, which have fundamentally different developmental processes, makes the scope of such a theory an open question.

To answer the question of what a theory of the evolution of development might encompass, examine the current state of evolutionary theory. Contrary to the book's claim that, “the Modern Synthesis is mostly a set of theories about adults competing for reproductive success…” (p. 318), it is much more. The theory of natural selection combined with quantitative genetic theory have been very successful in explaining the evolution of existing morphological, physiological, and behavioral traits at all life stages. Contra this book (p. 292), natural selection consists of the following syllogism:

If individuals within a population vary in their characteristics, and if that phenotypic variation leads to differences in fitness, and if that phenotypic variation has a genetic basis, then the population will change its characteristics over generations.

Described in this way, we see that natural selection depends on the intersection of development (phenotypic variation), ecology (fitness differences), and genetics (genetic variation). The authors are correct that, “[n]atural selection can only work on existing variation…” (p. 318–9). Much work has been done, though, to integrate multitrait mutational variation into evolutionary models (e.g., Wagner and Misof 1993; Hansen and Houle 2008). What the Modern Synthesis lacks, however, is a theory of phenotypic novelties.

Here is where the book can be hailed as an important milestone. It puts forth, although disjointedly, a theory of phenotypic novelties:

  • 1Development across all lineages uses a small set of related molecules (pp.326–327).
  • 2Genetic novelties come about through gene duplication and divergence (pp. 327–334).
  • 3Development occurs through discrete, interacting modules (pp. 336–341).
  • 4Developmental change occurs through changes in the location, time, amount and kind of gene expression2 (pp. 342–362).
  • 5Novel phenotypes become fixed through genetic assimilation, genetic accommodation, and phenotypic accommodation (pp. 375–391).

Summarized thusly, it is clear that the components of a theory of phenotypic novelties now exist. The long post-Synthesis march linking evolution and development is on the crux of completion. Articulating this theory makes clearer the context of the current debate over the relative importance of the evolution of regulatory versus structural genes (Pennisi 2008). Such debates are important in shaping the propositions and fundamental principles of theories (Scheiner and Willig 2008), such as those listed above.

Formalizing the theory leads to new questions. Is phenotypic accommodation, the ability to adjust development to accommodate environmentally induced changes, something inherent to biological systems? Or does it exist because over the long run evolution favors flexibility? The authors miss an opportunity to ask this question by stating that epigenetic variation is something separate from the standard assumption that “all evolutionarily significant variation is heritable” (p. 370). What is heritable is the ability to create epigenetic variation, that is what is selected. The notion that plasticity is heritable and selectable goes back to Woltereck (1909), was reiterated by Bradshaw (1965) and was formalized by Scheiner and Lyman (1989).

The evolution of phenotypic novelties should not be confused, as is done in this book, with either the evolution of reproductive isolation or evolution above the species level. Because phenotypic novelties are often used to define taxonomic differences at the level of genus, family, or above, these are often conflated. Evolution is clearly occurring at the level that it always does, populations and species. While phenotypic novelties might lead to reproductive isolation through hybrid incompatibilities, they need not, depending on the robustness of the developmental system.

Finally, this book demands a few comments about the pedagogical paradigm around which it, and most textbooks in biology, are built. First is the problem that we tend to teach biology from anecdote, rather than theory. Chapter 1 is emblematic of this problem. It consists of a series of examples about the intersection of ecology and development from which it is assumed that the students will be able to induce general principles. Not until Chapter 7 is there a discussion of short-, intermediate-, and long-term responses to environmental change, exactly the sort of framing device that should be in Chapter 1. Part 3, which focuses on evolution, does a much better job in this regard, most likely because evolution is the area of biology with the best articulated general theory. Recently, Michael Willig and I published a general theory of ecology (Scheiner and Willig 2008). Open up any ecology textbook and you will find all of the pieces of that theory. As I have done here, we simply took those scattered pieces and codifying them. There is a general need for the building of such theories across all of biology.

The second problem is a clear math phobia. The book contains not a single equation. Reaction–diffusion models are cited as a key to understanding morphogenetic constraints (p. 360), yet the models themselves are never detailed. All of the models presented in this book are visual, rather than analytic. Nor is this problem confined to organismal and molecular biology. The recent edition of the leading textbook on evolutionary biology (Futuyma 2005) is notable for how much less math it contains compared to earlier editions. We must properly prepare our students by increasing math content across the entire biology curriculum. While general theories should not be confused with models (Scheiner and Willig 2008), it is through specific models that linkages are made across domains.

Which brings us to the evolutionary ecology of development. If evo–devo has almost exclusively been about deep phylogenetic patterns and the appearance of phenotypic novelties, then eco–evo–devo is about how the ecology of organisms combines with developmental processes to shape natural selection. The final chapter ends with a call for a theory of eco–evo–devo. It is unfortunate that the authors ignored the literature on quantitative genetics and the evolution of phenotypic plasticity. That theory can rightly be called a theory of the evolutionary ecology of development (Sultan 2007). None of those papers when they were published had the impact of the milestones of the Modern Synthesis, but the importance of their accumulated affect is now obvious.


Book Review Editor: J. Thompson

Footnotes

  • 1

    I am compelled to correct one very minor error (p. 358). Dorothy meets the Wheelers in the Land of Ev, not Oz.

  • 2

    The authors have a fondness for jargon, including the coining of a new term for these types of changes: heterocyberny, a change in governance (p. 373). Jargon should always be minimized, especially in a textbook, besides which this is a truly ugly word.

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