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Character identity mechanisms: a conceptual model for comparative-mechanistic biology

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Abstract

There have been repeated attempts in the history of comparative biology to provide a mechanistic account of morphological homology. However, it is well-established that homologues can develop from diverse sets of developmental causes, appearing not to share any core causal architecture that underwrites character identity. We address this challenge with a new conceptual model of Character Identity Mechanisms (ChIMs). ChIMs are cohesive mechanisms with a recognizable causal profile that allows them to be traced through evolution as homologues despite having a diverse etiological organization. Our model hypothesizes that anatomical units at different levels of organization—cell types, tissues, and organs—have level-specific ChIMs with different conserved parts, activities, and organization. Relying on a methodology of conceptual engineering, we show how the ChIM concept advances our understanding of the developmental basis of morphological characters, while forging an important link between comparative and mechanistic biology.

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Fig. 1
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(from Hobert 2011)

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Re-drawn after a figure in Meizlish et al. in press with permission

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Notes

  1. The traceability of organisms through a life history in order to count them or lineages through a phylogeny as historical individuals have been analyzed extensively (e.g., Ghiselin 1987; Pepper and Herron 2008). However, the traceability of parts, characters, or mechanisms has been largely neglected (but see Love 2018a, b). Traceability and tracking practices are relevant for diverse sciences, from tracing alleles in a pedigree (transmission genetics) to tracking a comet through space and time (astronomy).

  2. Causal non-redundancy is different from causal specificity (Woodward 2010), which concerns the bijectivity of mapping between states of a pair of variables (X→Y) rather than the presence or absence of other causes (Z→Y, W→Y,…) with similar effects. The causal relations between ChIMs and phenotypic characters are often non-specific: given that activities of parts are often necessary for the operation of the ChIM as a cohesive unit, perturbing them will tend to “turn off” the effect completely.

  3. We refer to a consensus viewpoint on “mechanisms” (Craver and Tabery 2016), though this explicitly includes a dynamical perspective (DiFrisco and Jaeger 2019; McManus 2012) and therefore does not correspond to what has been termed “machine mechanisms” (Nicholson 2012). Further details are worked out below (see “Tracing ChIMs in evolution: outcomes, parts, activities, and organization”).

  4. Some units, like zooids, only apply to animals and plants that consist of the integration of multiple organisms (e.g., polyps in the case of siphonophores).

  5. Natural selection “sees” the character state but not the character. Stabilizing selection on a character state indirectly stabilizes—though does not determine—character identity.

  6. This case is more complicated, as duplicated genes are still traceable as paralogs and will likely retain the same cis-regulatory and protein–protein interaction domains. But a sufficiently high degree of sequence divergence can change these features and make the true gene phylogeny impossible to trace.

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Acknowledgements

ACL and GPW gratefully acknowledge the financial support of the John Templeton Foundation (Grant Number 61329). The opinions expressed in this paper are those of the authors and not those of the JTF. JD thanks the Research Foundation—Flanders (FWO) for financial support (Grant Number 41277) and for funding a research stay at Yale University in Spring 2020, where most of this paper was written.

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ACL and GPW are supported by a John Templeton Foundation Grant, Number 61329. JD is supported by the Research Foundation—Flanders (FWO), Grant Number 41277.

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DiFrisco, J., Love, A.C. & Wagner, G.P. Character identity mechanisms: a conceptual model for comparative-mechanistic biology. Biol Philos 35, 44 (2020). https://doi.org/10.1007/s10539-020-09762-2

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