On comparisons and causes in evolutionary developmental biology

gerhard scholtz

Denn mit dem Warum der Dinge kommt niemand zu Ende. Die Ursachen alles Geschehens gleichen den Dünenkulissen am Meere: eine ist immer der anderen vorgelagert, und das Weil, bei dem sich ruhen ließe, liegt im Unendlichen.

[For once you begin with the Why you can never get to the end. It is like the dunes by the sea, where behind each dune lies still another and the Because where you might come to final rest lies somewhere in infinity.]

Thomas Mann, Joseph und seine Brüder

Comparison is fundamental to any evolutionary developmental analysis (e.g. Alberch 1985, Rieppel 1988, Dohle 1989, Minelli 2003, Scholtz 2005, Deutsch 2006, Jenner 2006, Breidbach and Ghiselin 2007). However, evo-devo as a discipline evolved from a mix of experimental and descriptive approaches to development. Accordingly, different weight is put on the method of studying development in an evolutionary framework depending on a researcher's scientific background. Here I want to evaluate the different approaches and their contribution to addressing evolutionary questions. I stress that only the comparative approach offers a direct method of studying development with respect to evolutionary changes. Descriptive and comparative approaches are often interpreted as being less 'exact' than experimental studies because they deal with untestable scenarios. Here I want to show

1 This work is dedicated to my teacher and mentor Wolfgang Dohle on the occasion of his 70th birthday.

Evolving Pathways: Key Themes in Evolutionary Developmental Biology, ed. Alessandro Minelli and Giuseppe Fusco. Published by Cambridge University Press. # Cambridge University Press 2008.

that comparative approaches are a direct means to study evolution if the latter is accepted as the general framework for reasoning about causality and changes and the link between the two. The experimental approach alone, dealing with mechanisms, does not help with respect to evolutionary considerations because developmental mechanisms are not evolutionary mechanisms. In contrast, in comparative approaches to development, ontogenetic mechanisms analysed in terms of independence of developmental steps might reveal the kind of causes operating in evolutionary mechanisms.

comparison as a general tool for the study of development

Comparisons are always involved in developmental biology and the differences lie only in the theoretical and practical frameworks under which the results are interpreted. Even in an experimental approach using a model organism, comparison of the development of a number of individuals is the prerequisite to conceptualising the normal development of the species and to establish the stages etc. on which the experiments will be carried out. Only against this background can the results be generalised. Focus is not on comparison between species, but rather on comparison between normal development and the results of experimental manipulation or naturally occurring mutants. From these comparisons the mechanisms are inferred within a theoretical framework centred on the question of how we interpret developmental causes. The developmental experimentalist knows what he or she did to achieve the result. Nevertheless, a rest of unknown and unexplained elements remains - that is, the results have to be interpreted!

It is obvious that the role of comparison is even greater in the comparative evolutionary approach to development. Here the comparison is used as a direct means to interpret the observed similarities and differences in the theoretical framework of evolution. There is no contrast of normal versus disturbed development because all observed, existing normal developmental pathways are successful.

causation

With the advent of experimental developmental biology (Entwicklungsmechanik) at the end of the nineteenth century, the term 'causal morphology' (Kausale Morphologie) was coined (Mocek 1998). Causal morphology claimed to find causal explanations of animal form by performing experiments, in contrast to comparative morphological approaches which, according to the causal morphologists' view, lead only to descriptions of phenomena but not to explanations (Mocek 1998). Since then development has often been conceptualised in terms of causation. Alberch (1985), for instance, discriminates between 'causal developmental sequences' in which every stage is the prerequisite for the next stage, and 'temporal developmental sequences' in which stages lack a causal connection. Mayr (1997) introduced the distinction between functional 'proximate causes' and evolutionary 'ultimate causes' in the explanation of change in biological systems. Because all biological objects are the products of history, only the two levels of causes together explain biological features completely. For instance, the horizontal orientation and the up and down movements of the whale fluke, as opposed to the vertical tail fin of a fish with lateral movements, can be explained in terms of developmental and physiological processes (proximate causes) but to gain a full understanding of these features, the descent of whales from terrestrial placentalian mammals with their characteristic anatomy and movement (ultimate cause) has to be considered as well.

However, causality is a highly problematic issue and a great debate about causality forms a major part of (bio-) philosophy (see e. g. Schopenhauer 1847, Wuketits 1981, Rieppel 1988, Jonas 1997, Mahner and Bunge 1997). The concept of causality has often been used in a broad sense covering most things that produce differences. In contrast to this, Mahner and Bunge (1997) restrict causation to events in a temporal sequence accompanied by energy transfer. According to this narrower concept, other differences in time (e.g. between states or properties) are interpreted in terms of determinants and conditions rather than causes. Furthermore, this view implies that historical (evolutionary) conditions that determine actual biological structures are not causes either. Hence the expression 'ultimate cause' (Mayr 1997) should be abandoned. I acknowledge the merits in these distinctions, but in a developmental biological context the discrimination between causes, determinants and conditions is problematic. Thus, I use developmental causation in a broader sense covering all three of these terms. Furthermore, I know that the occurrence of consecutive or otherwise correlated events does not automatically imply causal relation, i.e. post hoc does not automatically mean propter hoc (Wuke-tits 1981). Nevertheless, for the sake of clarity in the following I use causality between time-ordered events and states in developmental sequences (as defined by Alberch 1985) as given. Moreover, for the same reason I use formalised linear sequences as examples despite the fact that the relationships between developmental events are often best represented as complex networks.

developmental steps

Biological studies are conceptually divided into those dealing mainly with processes and those dealing with patterns. The distinction between these categories is not always straightforward - this seems evident for the tension between evolutionary process and resulting pattern (e.g. Rieppel 1985, Arthur 2000). Development is almost universally considered as being a continuous process and thus contrasted to things we can categorise as patterns (Cracraft 2005). However, as soon as we deal with development, in particular in a comparative and evolutionary framework, we are forced to use descriptions of discrete steps in time such as stages, instars or phases (Alberch 1985, Rieppel 1988, Scholtz 2004, 2005), and these entities are conceptualised as processes in a theory- and assumption-laden framework as has been discussed by Cracraft (2005). Hence, I do not endorse the distinction made by Alberch (1985) between more static and more dynamic approaches to development, the latter not implying stages. I think it is just a question of perspective and of level of the subdivision of processes - in any case one has to deal with some kind of discrete developmental entity.

There is a long tradition of subdividing development into stages (Richardson et al. 2001, Fürst von Lieven 2005, Minelli et al. 2006, Hopwood 2007). However, many people associate the term 'stage' with a specific shape taken by an embryo or larva (e.g., nauplius, pharyngula, gastrula). Such stages are often too imprecise to be used for comparison of developmental events and can thus be misleading (Richardson et al. 2001, Hopwood 2007). Hence, in contrast to a stage-based approach, I will use in the following the term 'developmental step'. I define a developmental step as a describable and comparable (homologisable) pattern at any moment of development. The word step is chosen because of its twofold meaning: as a structure (a step of a ladder) and as an event with a temporal aspect (a walking step). Accordingly, the term developmental step comprises spatial patterns ('frozen' moments of development such as the 16-cell stage, the initial limb bud, a distinct gene expression pattern or early gastrulation) and units within developmental processes and developmental events (e.g. regulation of segmentation genes, gastrulation, cell division sequences) which are also treated as patterns, i.e. patterns in time (Scholtz 2005). A developmental step can correspond to a traditional stage but it also can be just a part of it. Developmental steps can be described and analysed at the morphogenetic, cellular, gene expression or molecular levels. According to this view, development is characterised by complex temporal sequences and interactions of developmental steps.

For the identification of developmental steps a distinct element of comparison is always involved. Furthermore, the recognition of corresponding and similar developmental steps in two or more individuals of one or several species implies their homology. The concept of developmental steps has its basis in empirical observation since it deals with describable patterns. Hence, a developmental step is an ontological entity and not just an artificial construct to subdivide a continuous process into slices. Nevertheless, unavoidable arbitrary elements are involved. These concern, for instance, the temporal and spatial limits of the developmental steps. However, this partial restriction is a problem common to many entities in biology in general (e.g. character, homologue, organ, population, species), and in developmental biology in particular.

It is evident that the concept of developmental steps is related to the character concept in phylogenetics (e.g. Cracraft 2005, Richter 2005). Correspondingly, there is a hierarchy of nested developmental steps with nested homologies: individual steps as well as a sequence of steps can be homologous (see Scholtz 2005). The evolutionary independence of individual developmental steps can be shown in comparative analyses (see below) and, based on this possible independence, a mosaic distribution of homologous developmental steps occurs among taxa. Hence, transformation, insertion, deletion or replacement of developmental steps are the kinds of evolutionary change of developmental processes.

A recent discussion centres on whether developmental processes are modular and whether modules form some sort of functional elements of development (e.g. Wagner 1996, Minelli 2003, Schlosser and Wagner 2003). At first sight this approach seems similar to what I describe here in terms of developmental steps. However, developmental steps in my sense are different from modules insofar as the former are not intended as functional entities. For a critical view of modularity, see Mitchell (2006).

In the following I use letters to represent developmental steps: I am aware of the fact that this is a gross simplification. But if the reader accepts that a letter can stand for a morphological structure, a cell arrangement, a gene expression or a regulatory network, then I think that this simplification is appropriate to clarify what I want to discuss. Each letter represents an observable, comparable and homologisable developmental step.

descriptive studies of single species

The purely descriptive approach to the study of development without any interspecies comparisons leads to an analysis of the temporal sequence of developmental steps. The result is a description of the events of the normal development (normogenesis) of a given species. The descriptive approach leads to a finalistic view because normogenesis is observed to lead to the final and differentiated stage, namely the adult. However, this does not imply any causal relationship between developmental steps. Nevertheless, the regularity of the developmental process observed again and again in every embryo at each generation makes it tempting to infer strict causal connections between subsequent development steps. That this kind of conclusion cannot be legitimately drawn has been already discussed by Roux (1907) and has been shown by classical experiments which revealed the regulatory capacity of development (Müller 1996, Sander 1996).

Nevertheless, exact descriptions of developmental processes are the necessary prerequisite for all following approaches to development as well as for interpreting evidence such as the recently found fossils of Cambrian embryos (e.g. Chen et al. 2004, Donoghue et al 2006). This is true in particular of taxa thus far neglected.

the experimental m o de l-o rg a nis m approach

Experiments are designed to show the independence or dependence of developmental steps or mechanisms, and they sort out what could have an influence on subsequent steps by experimental manipulations (Roux 1907). In other words, this approach is largely an analysis of malformations. Given that there is a sequence of developmental steps ABCDE, an experimental developmental biologist would say that A causes B, B causes C etc. if he or she has proven this experimentally, e.g. by deletion experiments or gene silencing. If B is taken away and C does not occur in development as is the case in normal (i.e. not manipulated) development it has been shown that B causes C (Figure 8.1). This is of course a simplification because the causal link between B and C can be quite indirect, but as a general principle this

Observation

A^B^C^D^E Manipulation

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