Abstract
This paper explores an important type of biological explanation called ‘homology thinking.’ Homology thinking explains the properties of a homologue by citing the history of a homologue. Homology thinking is significant in several ways. First, it offers more detailed explanations of biological phenomena than corresponding analogy explanations. Second, it provides an important explanation of character similarity and difference. Third, homology thinking offers a promising account of multiple realizability in biology.
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Notes
This paper focuses on an important use of the concept of homology in biology, one that relies on the historicity of homologues. However, no claim is made that a historical approach to homology is the only valuable approach to homology. Nor is it claimed that every type of explanation a biologist offers concerning a homologue is historical. The aim of this paper is more modest, namely to explore one way, a significant way, that biologists use the concept of homology to understand biological phenomena.
The significant differences between the taxic and transformational approaches are twofold. For cladists homologues only mark the boundaries of monophyletic taxa, whereas for evolutionary taxonomists they mark the boundaries of monophyletic and paraphyletic taxa. Furthermore, for cladists new homologues arise only when character lineages branch, whereas for evolutionary taxonomists new homologues can arise within character lineages. The idea that a homologue can occur in different states does not distinguish the taxic and transformational accounts: cladists recognize that homologues can occur in multiple states (Donoghue 1992).
Compare with speciation. Not all isolated populations become new species. It depends on what happens to those populations later (Ereshefsky 2001).
Another tension between the developmental and phylogenetic accounts concerns serial homology. Supporters of the developmental approach argue that the phylogenetic account is inadequate because it does not treat serial homologues (such as the bristles of a fly) as homologous (Wagner 1989; Roth 1994). In fact, some supporters of the phylogenetic approach deny that serial homologues are homologous (Wake 1999; Ghiselin 2005). This seems to be an impasse. However, some developmental biologists believe that serial homologues owe their origins to the duplication of developmental mechanisms deep in the phylogeny of a character (Shubin et al. 1997; Müller and Newman 1999; Striedter 1999). If instances of a serial homologue trace back to a common ancestor, then what we call ‘serial homology’ is historical homology. For example, Striedter (1999: 40) suggests that the evolutionary mechanism producing fly bristles has a single origin. That mechanism was subsequently duplicated and expressed in different places on the body of an organism. Whether each serial homologue has a single phylogenetic ancestry has not been conclusively shown. Nevertheless, the evidence to date indicates that the phylogenetic and developmental approaches are not necessarily at odds concerning serial homology.
Though I distinguish types of historical explanations by calling some ‘strong historical explanations’ and others ‘weak historical explanations,’ I do not mean to imply that strong historical explanations are in any way more significant. Strong historical explanations are more historical in that they cite multiple factors that occur at different times in the history preceding an event. Not only are those factors spread over time, even the temporal order of those factors may be significant. Weak historical explanations merely cite the initial conditions of a later event. The distinction between weak and strong historical explanations is nicely captured by Desjardins (2011) distinction between initial condition dependent and path dependent explanations.
A referee for this journal asked about the relation between proximate and distal explanations and weak and strong historical explanations. The type of homology explanation highlighted in this paper concerns the use of homology in the distal sense. Such explanations refer to the evolutionary history of a homologue and, as we have seen, come in both historically strong and weak forms. Proximate explanations concerning homology cite the developmental factors that cause the ontogeny of a homologue. Such proximate explanations of homology are historical as well: the ontogeny of a homologue occurs over time, through a sequence of developmental events. For example, the imaginal disks of insect larvae develop into legs and wings through a sequence of gene and cellular interactions (Winther 2006: 493). Though the time scale of ontogenetic explanations is much shorter than the time scale of evolutionary explanations, they are historical explanations. Winther (ibid.) calls those ontogenetic explanations “temporal narratives.” Such ontogenetic explanations come in both historically strong and weak forms.
In some cases we can tease apart homology and analogy explanations. However, there are many cases where it is not clear whether a character is a homologue and whether a homology explanation is appropriate. For example, it is not clear whether atavisms and vestiges are homologues. This paper does not weight in on such cases. In a series of papers, Hall (2003, 2007a, b) discusses them. He suggests that the distinction between homologues and analogues should be viewed as a continuum. Nevertheless, Hall (2003, 409; 2007a, 442) concludes that the only clear case of analogy is convergence.
A referee for this journal asked what role phylogenetic inference plays in the historical explanations of homology thinking. Prum and Brush’s work on feathers can help answer this. In their explanation of character diversity, Prum and Brush pursue two lines of research. One line develops and tests hypotheses concerning the ontogenetic mechanisms that cause feather character states (e.g., undifferentiated epidermal rings cause Stage I feathers, differentiated epidermal rings cause Stage II feathers, and so on). The second line of research develops and tests a phylogenetic tree tracing the character states of feathers. The culmination of Prum and Brush’s research is establishing congruence between the developmental model and the phylogenetic hypothesis. Prum and Brush use this congruence to offer historical explanations of feather diversity. For example, to explain the differences between Stage II and Stage V feathers, they cite the phylogeny of those character states and the sequence of changes in their developmental mechanisms. Those changes, in that order, and their stable transmission explains the differences between Stage II and V feathers. Phylogenetic inference itself is not a part of this explanation. Nevertheless, phylogenetic inference makes an important contribution: it provides the phylogenetic hypothesis that allows us to trace the relevant changes in the developmental module of feathers. Stepping back from this example, Prum and Brush’s two avenues of research—one involving the developmental module of a homologue, the other investigating a character’s phylogeny, and whether those two lines of research are congruent—is just the pattern of research Wagner suggests in his (1999) paper “A research programme for testing the biological homology concept.”
A crucial element of Rosenberg’s reductionism is the reduction of selection processes at the macro-level to selection processes at the micro-level (2006, 199). However, it is not obvious that all cases of hierarchical disconnect (multiple realizability) are the result of selection. In the grasshopper song example, Striedter and Northcutt (1991) make no mention of selection for a second physical substructure for the homologous song. The change in physical substructures underlying the song could be selectively neutral. Consider a different type of case. Given what we know about gene substitution, it is plausible to suppose that some substitutions in the gene regulatory mechanisms of homologues are selectively neutral. Thus, some cases of hierarchical disconnect due to gene substitution may be the result of non-selective processes.
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Acknowledgments
I thank the referee for this journal as well as Eric Desjardins, Alan Love, Mohan Matthen, Olivier Rieppel, Alex Rosenberg, Elliott Sober, Rasmus Winther, and Gunter Wagner for their helpful comments on earlier versions of this paper. Financial support was provided by the Social Sciences and Humanities Research Council of Canada.
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Ereshefsky, M. Homology thinking. Biol Philos 27, 381–400 (2012). https://doi.org/10.1007/s10539-012-9313-7
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DOI: https://doi.org/10.1007/s10539-012-9313-7