The Intellectual Challenge of Morphological Evolution: A Case for Variational Structuralism

Throughout the history of evolutionary biology, as well as many other sciences, there has been a conflict between two styles of thinking (Mayr 1982; Hughes and Lambert 1984; Ghiselin 1997; Amundson 2005). One is conventionally called functionalism, although in evolutionary biology the term "adaptationism" is more frequently used today because a trait's "functional fit for its office" is produced through adaptation by natural selection (i.e., function is explained by adaptation through natural selection). The functionalist stance is one that explains organismal traits through their functional and adaptive values.

The alternative style of thinking does not have a generic name in biology, although in other areas of study it is called "structuralist." In evolutionary biology, the most influential structuralist manifesto is "The Spandrels of San Marco and the Panglossian Paradigm" by Gould and Lewontin (Gould and Lewontin 1978). In their essay, Gould and Lewontin attacked the adaptationist assumption that each feature of an organism had to have an adaptive explanation. The "spandrels" of the Basilica di San Marco were not built to accept an angel picture; rather, they were a geometric consequence of a structure that was built with arches. Similarly, the protruding "chin" of the human lower jaw was a consequence of the progressive reduction of the tooth row relative to the body of the mandible rather than a directly selected character.

The differences in perspective between these two styles of thinking was best expressed by Rudy Raff in his quip, "They [the population geneticists] are interested in species while we [devo-evo researchers] are interested in bodies." I hasten to add that this contrast is most often exemplified by the different perspectives of population geneticists and developmental biologists; however, there is no scientific or conceptual reason for a substantial conflict between population genetics and a structuralist view.

The tension between functionalist and structuralist views of nature is as pervasive as the tension between explanations based on nature or nurture, and probably as unnecessary and unproductive in the long term. With respect to the nature/nurture debate, any serious biologist or psychologist understands that organisms and their traits (including behaviors) are the product of the interactions between genes (nature) and the environment (nurture). Hence, the contrast "nature or nurture" does not make any sense, because we are always faced with the combined effects of both "nature and nurture."

In contrast, the conflict between functionalist and structuralist accounts of organisms has not been resolved, and will likely be more difficult to resolve than that between nature and nurture. The reason is that form (i.e., structure) and function (i.e., adaptation) are intertwined during the life and evolution of organisms in a complex manner such that each party, both structuralists and functionalists, can make a legitimate claim to a certain amount of truth. This book is about a project to overcome this conflict by addressing a specific biological phenomenon for which the conflict often crystallizes: the question of homology (i.e., the existence of the same body parts in different and often distantly related organisms—aka homologs). At its core, the question is whether homologs exist—that is, whether they are natural members of the "furniture of the world" or whether they are only transient traces of the phylogenetic past. In the latter case, they would have no biological, conceptual, or causal significance. In the former case, homologs would have to play a central role among the concepts of evolutionary theory.

To some this question may seem quaint and irrelevant, as the dominant school of evolutionary thinking during the twentieth century was thought to have disposed of this topic for good. This was ostensibly achieved by excluding issues of body organization, development, morphology, and, for a long time, even phylogeny from the research program of the New Synthesis (Mayr 1982). Yet this situation has changed due to the maturation of phylogenetic inference (Donoghue 1992), as well as that of developmental biology and the subsequent emergence of developmental evolution as a new branch of biology (Carroll, Grenier et al. 2001; Wilkins 2002). In developmental evolution, questions regarding the nature of homology have resurfaced and have come into sharp focus (Hall 1994). Our ability to identify those genes responsible for the development of morphological characters opened up new avenues to address questions that were, for the most part, abandoned at the end of the nineteenth century (Abouheif 1997; Wray and Abouheif 1998; Abouheif 1999; Wang, Young et al. 2011). In the nineteenth century, however, the program of evolutionary morphology collapsed under the weight of these questions, which, at the time, where unmatched by scientific methodology (Nyhart 1995; Nyhart 2002).

After Origin of Species (1859) was published, the study of comparative anatomy experienced a revolution in which comparisons of anatomical structures were pursued in order to infer the phylogenetic relationships among species and higher taxa, and to explain the evolutionary origin of body plans and the characters that make up the bodies of animals and plants (Nyhart 1995; Laubichler and Maienschein 2003). However, at that time, there was neither a proper comparative methodology to infer phylogenetic relationships nor was there another source of phylogenetic information other than morphology, such as that provided now by molecular sequence data. Also, any understanding regarding the developmental mechanisms that create morphological characters during embryogenesis was virtually absent, and genes had not been (re)discovered. In retrospect, the program of evolutionary morphology was premature.

This situation, however, has changed dramatically during the last 20 to 30 years. Data at the molecular level have greatly improved the amount and quality of phylogenetic information. Conceptual progress and the availability of cheap computing power have vastly increased our ability to infer phylogenetic relationships. The discovery of conserved...