Abstract
“Functional homology” appears regularly in different areas of biological research and yet it is apparently a contradiction in terms—homology concerns identity of structure regardless of form and function. I argue that despite this conceptual tension there is a legitimate conception of ‘homology of function’, which can be recovered by utilizing a distinction from pre-Darwinian physiology (use versus activity) to identify an appropriate meaning of ‘function’. This account is directly applicable to molecular developmental biology and shares a connection to the theme of hierarchy in homology. I situate ‘homology of function’ within existing definitions and criteria for structural assessments of homology, and introduce a criterion of ‘organization’ for judging function homologues, which focuses on hierarchically interconnected interdependencies (similar to relative position and connection for skeletal elements in structural homology). This analysis of biological concepts has at least three broad philosophical consequences: (1) it provides the grounds for the study of behavior and psychological categories as homologues; (2) it demonstrates that philosophers who take selected effect function as primary effectively ignore large portions of comparative, structural, and experimental research, thereby misconstruing biological reasoning and knowledge; and, (3) it underwrites causal generalizations, which illuminates inferences made from model organisms in experimental biology.
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Notes
Many biological cases are tricky to interpret and the line between homology and analogy can be difficult to draw in practice, especially because of the hierarchical relationships among homologues and analogues (Hall 1994). The contrast class for homology is often taken to be more than analogy (convergent similarity of function due to selection). ‘Homoplasy’ encompasses analogy, reversal, parallelism, and other non-homologous phenomena (Hall 2003).
Strictly parallel language displays this dependence: ‘an organismal innovation is a function that is neither homologous to any function in the ancestral species nor operational elsewhere (serially homologous) in the functional context of the same organism’.
Bock and von Wahlert (1965) made a similar distinction between ‘activity’ (what something does) and ‘biological role’ (what something is used for). I originally took their ‘activity’ to correspond to causal role functions (Love 2005, 2006), but now concur that they are distinct (see Wouters 2003: 642–3).
This distinction came to my attention via an unpublished paper by Jim Lennox entitled “Biological function: a brief slice of history”. There is a third aspect, ‘movement’, which I am ignoring here.
“Explanations of use and explanations of activity will refer to quite different sets of facts; and this is as true today as it was for Galen” (Furley and Wilkie 1984: 63).
It should be stressed that the use vs. activity distinction is epistemological, which means that there need not be ‘bare’ activity-functions with no use-function. Rather, activity-functions can be described and investigated as such apart from their use-functions, whether causal role, viability, or selected effect. There can also be different descriptions of the same activity-function that may be more or less germane depending on which use-functions are in view.
Activity-function homology and the nature of functional hierarchies are related to explorations of ‘process homology’ by Evo-devo researchers: “By a ‘process’ we refer to an action (what happens), not to its functional outcome (why it happens)” (Gilbert and Bolker 2001: 445; see also Brigandt, this issue).
There is no privileged level of analysis; only the requirement that one is explicit about where you are trying to discern activity-function homologues. Thus, even though rhythmic muscular contraction is an activity that contributes to the causal role capacity of the heart pumping, heart pumping could be considered as an activity-function homologue in the causal role context of the cardiovascular system.
One key explanation for this divergence in developmental role despite activity-function homology of DNA binding is that Hox genes work in tandem with other cofactors (Svingen and Tonissen 2006). Change in sequence outside of the DNA binding domain can lead to altered cofactor interaction, which implies that a regulatory gene can retain one activity-function homology and lose another.
This is also congruent with the argument that non-arbitrary individuations of causal role functions are secured by ascribing them only to systems exhibiting hierarchical organization (Davies 2001, ch. 4).
Some candidates for activity-function homology are directly tied to particular structurally homologous features, such as homeodomain DNA sequence and the activity of DNA binding. A different asymmetry between structure and function arises in phylogenetic reconstruction, which leans heavily on structural data (e.g. skeletal anatomy or DNA sequences), even though activity-function character states can also be scored (i.e. functional characters can provide good phylogenetic data). This is a result of the greater difficulty in obtaining functional data as opposed to structural data (Lauder 1990). The dependence of homology of function on structural characters in this sense is indirect, mediated through the identification of structural synapomorphies required to construct a necessary but insufficient phylogenetic context.
The success of activity-function homology is due in part to treating activities structurally (‘structure’=df “The mutual relation of the constituent parts or elements of a whole as determining its peculiar nature or character”; OED). I am intentionally skirting the ontological issue of whether there are both entities (structures) and activities (functions) or, alternatively, whether activities can be reduced to the interactions of entities (cf. Tabery 2004).
“Every biologically interesting structure is labeled by the term that expresses its selected effect; how a structure is ‘individuated’—how the border between it and other structures in the same animal or plant (or fungi) are drawn—depends on its selected effect, its function” (Rosenberg 2006: 137).
“Amundson and Lauder and perhaps also Griffiths seem to maintain that there are not functional categories of any scientific significance in biology, with the exception of the analogous categories being categories of traits that have evolved independently to serve the same function” (Neander 2002: 391). This is a strange assertion because all three of these authors clearly state that causal role functional categories are ubiquitous in experimental biology. Only selected effect functional categories are identified with evolutionary analogies, which follows the mainstream neo-Darwinian tradition.
“We investigated functional conservation among the Drosophila zinc-finger homeodomain protein 1 (zfh1) and its mouse functional homologue Smad-interacting protein 1 (SIP1)” (Liu et al. 2006: 683).
Vertebrate lens crystallins could be used to explore some of these issues (Piatigorsky 2007). The enzymatic activity of aldehyde dehydrogenase in different taxa can be activity-function homologous but its role as a transparent, refractive globular protein in the eye usually is not. This is because different metabolic enzymes (e.g. transketolase) and stress protection proteins (e.g. heat shock) were recruited into the role of lens crystallins in different vertebrate taxa because they also could play the role of a transparent, refractive globular protein, and thus lens crystallins as a class are most likely to be activity-function analogues.
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This paper benefited greatly from the feedback of participants at the 2006 Philosophy and Developmental Biology Workshop in Vancouver and those attending the ‘The Importance of Homology for Biology and Philosophy’ session at the 2007 ISHPSSB in Exeter. Ingo Brigandt, Marc Ereshefsky, Paul Griffiths, Mohan Matthen, and Karola Stotz provided helpful suggestions on many aspects of an earlier version of the paper. I am also grateful to Marc Ereshefsky for organizing these symposia on homology, which spurred me to work on this material.
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Love, A.C. Functional homology and homology of function: biological concepts and philosophical consequences. Biol Philos 22, 691–708 (2007). https://doi.org/10.1007/s10539-007-9093-7
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DOI: https://doi.org/10.1007/s10539-007-9093-7