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How to Compare Homology Concepts: Class Reasoning About Evolution and Morphology in Phylogenetics and Developmental Biology

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Abstract

Many of the current comparisons of taxic phylogenetic and biological homology in the context of morphology focus on what are seen as categorical distinctions between the two concepts. The first, it is claimed, identifies historical patterns of conservation and variation relating taxa; the second provides a causal framework for the explanation of this conservation and variation. This leads to the conclusion that the two need not be placed in conflict and are in fact compatible, having non-competing epistemic purposes or mapping the same extensions in the form of monophyletic groupings (see Roth, The biological basis of homology 1–26, 1988; Sluys, J Zool Syst Evol Res 34:145–152, 1996; Abouheif, Trends Ecol Evol 12:405–408, 1997; Brigandt, J Exp Zool 299:9–17, 2003, Biol Philos 22:709–725, 2007; Assis and Brigandt, Evol Biol 36:248–255, 2009). This article argues that moves in this direction miss the essential disagreement between these concepts as they have been developed in the context of the debate concerning the best concept for evolutionary investigation. We should rather see these concepts employing a common fundamental methodological approach to homology, but disagreeing about how to apply the methodology effectively. Both concepts employ class reasoning, which pursues homologies as units of generalization—more precisely, as sources of reliable and relevant group-bound information in the form of shared underlying causes. The dispute can be better understood by two poles that structure such reasoning: the need for a reliable basis for projections about the causal history of shared structures, and the desire to identify homologous characters with more informative and specific causal information relevant to generalizing about evolutionary processes. Judgments in favor of one or the other in turn have affected the scope or extension of these competing homology concepts.

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Notes

  1. This debate begins with the papers of van Valen (1982) and Patterson (1982) setting forward the different biological and phylogenetics perspectives respectively, and involves developmental biologists and phylogenists such as Roth (1984, 1988, 1991), Wagner (1989a, b, 1994, 1999), Rieppel (1992, 1994), Hall (1994, 2007), Müller (2003), Abouheif (1997), and recently, very provocatively, Cracraft (2005).

  2. West-Eberhard (2003) takes there to be universal agreement on this point. That would be nice if it were true but there are certainly many authors who have questioned the association between similarity and homology, such as Bock (1963), Mayr (1969), or in more modern contexts, Lauder (1994) and Kluge (2003), for different reasons. The taxic homology stream I focus on here, which begins with Patterson (1982) and includes authors such as Rieppel and Kearney (2007) and Franz (2005), argues strongly, citing practice itself against the impracticability of removing similarity assessments from primary homology judgments. There has to be some basis for deciding which structures to relate for testing. On this basis, sameness as criterion for homology, which is often asserted by developmental biologists (see Müller 2003) as principal, seems to mean no more than similarity due to common ancestry, both sharing the implication that there is shared information or similarities underlying the grouping as a result of this ancestry. I do not see any principal need to be critical of the use of “similarity” rather than “sameness” here.

  3. I will make a distinction between transformational and strict transformational here, since the notion is ambiguous in the literature. Transformational is often used to mean that elements of process are used as criteria for homology. It is often applied to biological homology. This does not, however, deny treatment of homologies as classes or kinds, as we shall see. Strict transformational I take to be the position asserting an “individualist” ontology, treating homologies as parts of a whole, which need not share any similarities other than historical relations. It fits a particular phylogenetic approach that is popular in the molecular context but is argued with strongly when it comes to morphology.

  4. This association was made earlier by Peters (1973) and Wiley (1975). Patterson is usually cited, however, as the first to rigorously argue for it. Synapomorphies are traits shared by two or more taxa and their most recent common ancestor. There is no gap in the expression or presence of the trait throughout the clade.

  5. See, for instance, as just a selection of literature on this: Assis and Brigandt 2009; Brigandt 2003, 2007; Müller 2003; Minelli 1996, 1999, 2009; West-Eberhard 2005; Haszprunar 1992; Abouheif 1997; Wagner 1989a, b, 1994, 1999; Sluys 1996; Roth 1988; Rieppel 1992, 1994, 2006; Cracraft 2005; Laubichler 2000; Young 1993; Butler and Saidel 2000; Donoghue 1992; de Pinna 1991; Hall 1994, 1999; Roth 1988, 1994; Janies and DeSalle 1999; Striedter 1998, 1999; Striedter and Northcutt 1991; Wake 1994.

  6. Of course, this is not uncontroversial among phylogenists, some of whom would rather disconnect cladistics from any evolutionary interpretation; but it again reflects the views of those taking part in this debate, who are principally concerned with generating platforms for evolutionary study.

  7. A symplesiomorphy is a trait shared between two or more taxa, but also shared with other taxa that have an earlier last common ancestor with the taxa under consideration. Parallelisms are traits arising independently in different lineages. A recurrent trait is a trait that disappears and reappears sporadically amongst related taxa.

  8. This concept is also applied in Newman and Müller (2010).

  9. As an anonymous reviewer pointed out to me, Arendt and Reznick (2007) do not explicitly discuss monophyletic groups or synapomorphic characters. They work to show that the distinction between convergent and parallel evolution is a false dichotomy, representing rather a continuum. But they do pick out examples of features amongst closely related taxa. Such features ordinarily would be considered the result of homologous developmental or gene pathways (p. 27). There is in fact a steady record of discoveries of homologous features that do not map to shared developmental mechanisms. See de Beer (1971), Wagner and Misof (1993), and West-Eberhard (2003).

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Acknowledgments

This research was funded with a postdoctoral fellowship at the Konrad Lorenz Institute for Evolution and Cognition Research (Altenberg, Austria).

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    Miles MacLeod

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MacLeod, M. How to Compare Homology Concepts: Class Reasoning About Evolution and Morphology in Phylogenetics and Developmental Biology. Biol Theory 6, 141–153 (2011). https://doi.org/10.1007/s13752-012-0020-z

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