The hierarchical basis of serial homology and evolutionary novelty

• Published in: Journal of morphology (1931) 2023-01, Vol.284 (1), p.e21531-n/a
• Main Authors: DiFrisco, James, Love, Alan C., Wagner, Günter P.
• Format: Article
• Language: English
• Subjects: Animals; Biological Evolution; homology; insect wing evolution; Insecta - genetics; levels of organization; paired appendages; Phylogeny; serial homologs; Wings, Animal - anatomy & histology
• ISSN: 0362-2525; 1097-4687
• DOI: 10.1002/jmor.21531

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. Serial homologs form hierarchical, phylogenetic relationships like gene paralogues. Our novel classificatory scheme for serial homology provides an improved theoretical framework for comparative biology.