The hierarchical basis of serial homology and evolutionary novelty

Abstract

Given the pervasiveness of gene sharing in evolution and the extent of homology across the tree of life, why is everything not homologous with everything else? The continuity and overlapping genetic contributions to diverse traits across lineages seem to imply that no discrete determination of homology is possible. Although some argue that the widespread overlap in parts and processes should be acknowledged as “partial” homology, this threatens a broad base of presumed comparative morphological knowledge accepted by most biologists. Following a long scientific tradition, we advocate a strategy of “theoretical articulation” that introduces further distinctions to existing concepts to produce increased contrastive resolution among the labels used to represent biological phenomena. We pursue this strategy by drawing on successful patterns of reasoning from serial homology at the level of gene sequences to generate an enriched characterization of serial homology as a hierarchical, phylogenetic concept. Specifically, we propose that the concept of serial homology should be applied primarily to repeated but developmentally individualized body parts, such as cell types, differentiated body segments, or epidermal appendages. For these characters, a phylogenetic history can be reconstructed, similar to families of paralogous genes, endowing the notion of serial homology with a hierarchical, phylogenetic interpretation. On this basis, we propose a five‐fold theoretical classification that permits a more fine‐grained mapping of diverse trait‐types. This facilitates answering the question of why everything is not homologous with everything else, as well as how novelty is possible given that any new character possesses evolutionary precursors. We illustrate the fecundity of our account by reference to debates over insect wing serial homologs and vertebrate paired appendages.

Against unifying homology concepts: Redirecting the debate

“…New fossil finds and quantitative sequencing alike have taken us far from Lankester's picture of a rudimentary ancestral limb. However, they have confirmed his intuition that simple inheritance is not the full explanation of homology, and even his hunch that serial homology can be an important guide to understanding the rest (see also DiFrisco et al, 2023).…”

“…(Lankester, 1870, p. 36) A feature in two or more taxa is homologous when it is derived from the same (or a corresponding) feature of their common ancestor. (Mayr, 1982, p. 45) In Mayr's modern rendition, a trait in the descendant can be "derived from" a trait in the ancestor without being markedly similar to that trait (DiFrisco et al, 2023;Novick, 2018). Lankester's appeal (quoted above) to an ancestral "representative" in his famous paper seems to impose the same loose restriction, but this is not actually the case.…”

“…His new category of homoplasy takes a tentative step toward a mechanistic investigation of this process. Lankester motivates this step by the same appeal to serial homology that irked Haas and Simpson because of their agenda of enshrining common ancestry in the definition of homology (see also DiFrisco et al, 2023). Assuming again that limbs of the past were quite simple, how can we explain the matching complexity that we now see in animals' forelimbs and hindlimbs?…”

“…Moreover, his primary need—a framework for integrating mechanistic and historical reasoning—remains very much alive in contemporary homology research. Finally, he makes use of a conceptual variant (serial homology) that is currently receiving significant attention (e.g., DiFrisco et al, 2023; Fusco, 2022; Schmitt, 2017).…”

Can you tell me anything about homology? Any one thing that is new?

“…With the article “The Hierarchical Basis of Serial Homology and Evolutionary Novelty” by James DiFrisco, Alan C. Love, and Günter P. Wagner there is another approach to homology (DiFrisco et al., 2023). Drawing on examples from evo‐devo studies and from concepts in molecular evolution, these authors champion a method they call “theoretical articulation.” This system essentially proposes a refinement of the concept of homology, depending on the particular research question posed.…”