Grand challenges in evolutionary developmental biology

Abstract

EVO-DEVO’S IDENTITY There is a widespread consensus on the view that evolutionary developmental biology (evo-devo) is the discipline eventually borne to fill the gap between evolutionary biology and developmental biology, following a divorce between these two fields that extended over more than half a century (Amundson, 2005). On closer inspection, however, this broadly acceptable perspective discloses a wealth of questions, if looked at retrospectively, and of potentially divergent possibilities, if looked at prospectively. The slow pace of integration between the different threads that were converging into evo-devo was well expressed by Raff (2000) in a survey of the main issues in this field. Some 15 years ago Raff, one of the discipline’s founding fathers, remarked that “What constitutes the fundamental problems for a science of evolutionary developmental biology (evo-devo) depends on whether the scientist is a developmental biologist, a paleontologist or an evolutionary biologist” and drafted a list of at the time hot issues. Evo-devo has answered these questions only in part. However, this discipline is now mature for addressing a number of more precise, and more challenging questions, as I will argue in this article. To date, two sets of problems have been primarily floated in discussions about the identity and research targets of evo-devo. On the one hand are those centered around the (controversial) notions of evolvability, robustness and constraint in connection with the increasing appreciation of the intricacies of the genotype→phenotype map (Alberch, 1991; Altenberg, 1995; West-Eberhard, 2003; Pigliucci, 2010; Wagner and Zhang, 2011). On the other hand are those centered around the notions of origination, innovation, and novelty, the so-called “innovation triad.” To Hendrikse et al. (2007), for example, evolvability is the key issue that justifies recognizing evo-devo as an autonomous discipline. Others, e.g., Muller and Newman (2005), focus instead on the innovation triad. Unfortunately, for all these candidates to core concept of evo-devo, too many alternative definitions have been proposed (or, more dangerously, implicitly assumed), thus adding new items to the dramatically increasing series of biological terms on whose definition there seem to be more and more disagreement. Eventually, we should probably learn to accept that multiple notions associated with each of these terms deserve to be retained and perhaps recognized by adjectival specifications. Similar terminological refinement is applied to other biological terms such as species (e.g., Claridge et al., 1997), homology (e.g., Minelli and Fusco, 2013a), and gene (e.g., Beurton et al., 2000). In discussing the concept of gene in historical perspective, Muller-Wille and Rheinberger (2009) have sensibly recalled Friedrich Nietzsche’s (1887; second essay, para. 13) dictum, that “all concepts in which an entire process is semiotically concentrated elude definition; only that which has no history is definable.” In addition to terminological ambiguity, there is an another problem with the “innovation triad”—the problem that these terms are all framed in terms of “origins.” Framing definitions in terms of origin requires splitting the evolutionary sequence in two contiguous segments, “before” and “after” the origination of a new feature. This splitting is a natural consequence if origination indeed “refers to the specific causality of the generative conditions that underlie both the first origins and the later innovations of phenotypes” and especially “the very first beginnings of phenotypes, e.g., the origin of multicellular assemblies, of complex tissues, and of the generic forms that result from the self-organizational and physical principles of cell interaction (Newman, 1992, 1994). In contrast, innovation [evolutionary modes and mechanisms] and novelty [their phenotypic outcome] designate the processes and results of introducing new characters into already existing phenotypic themes of a certain architecture (bodyplans)” (Muller and Newman, 2005, p. 490). This separation, however, is artificial. The better we know a process, the less we are able to identify its exact origins, these instead being determined by arbitrary choice. In science, and especially in biological disciplines with a strong historical dimension such as evolutionary biology and developmental biology, we should frame questions in terms of transitions rather than origins.