The fine structure of ‘homology’

Abstract

There is long-standing conflict between genealogical and developmental accounts of homology. This paper provides a general framework that shows that these accounts are compatible and clarifies precisely how they are related. According to this framework, understanding homology requires both (a) an abstract genealogical account that unifies the application of the term to all types of characters used in phylogenetic systematics and (b) locally enriched accounts that apply only to specific types of characters. The genealogical account serves this unifying role by relying on abstract notions of ‘descent’ and ‘character’. As a result, it takes for granted the existence of such characters. This requires theoretical justification that is provided by enriched accounts, which incorporate the details by which characters are inherited. These enriched accounts apply to limited domains (e.g. genes and proteins, or body parts), providing the needed theoretical justification for recognizing characters within that domain. Though connected to the genealogical account of homology in this way, enriched accounts include phenomena (e.g. serial homology, paralogy, and xenology) that fall outside the scope of the genealogical account. They therefore overlap, but are not nested within, the genealogical account. Developmental accounts of homology are to be understood as enriched accounts of body part homology. Once they are seen in this light, the conflict with the genealogical account vanishes. It is only by understanding the fine conceptual structure undergirding the many uses of the term ‘homology’ that we can understand how these uses hang together.

This is a preview of subscription content, log in to check access.

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Notes

  1. 1.

    I do not here consider phylogenetic networks (Huson et al. 2010) that take into account tokogenetic relationships (produced by e.g. hybridization and lateral gene transfer). This issue is discussed briefly below (“The enriched account of gene homology” section).

  2. 2.

    This argument resembles others in the literature on homology (Wagner 1989, p. 1158; Müller and Newman 1999, p. 65; Laublichler 2014, p. 73). These authors defend the need for a developmental account of homology, but do not draw the broader conclusion about the need for enriched accounts.

  3. 3.

    This distinction is controversial (Minelli 2016). The issue is treated below (“Wagner’s enriched account of body part homology” section).

  4. 4.

    Unlike paralogy, xenology is not a problem to be avoided in systematics, but a phenomenon to included. Where xenology is prevalent, systematists cannot simply assume that relationships between taxa can be captured by a strict tree, and must instead infer from the data to a phylogenetic network (Huson et al. 2010). However, whether one infers a tree or a network, one must still undertake a sequence alignment step that furnishes the relevant transformation series, and this is presupposed, but not tested, by the data-to-tree/network inference.

  5. 5.

    The discussion of development in this section primarily applies to animal development, and it focuses exclusively on the role of gene regulation in development, ignoring the role of non-genetic resources that shape development. I exclude such considerations because they do not feature in Wagner’s account of body part homology.

  6. 6.

    Müller (2003) offers a distinct enriched account of body part homology. Alessandro Minelli (2016) raises serious challenges to Wagner’s approach to homology. I defer discussion of these challenges to the end of this section.

  7. 7.

    In this discussion, I have simplified things for ease of exposition. In fact, the appropriate bearer of character states is not the entire organism (or part) over the entire course of its life, but a suitably thick time-slice of the organism (part), called a semaphoront. In an excellent paper, Havstad et al. (2015) show that ontogenetic identity (identity of a part across the different semaphoronts of a single individual) and phylogenetic identity (identity of a part across evolutionary transformations) can come apart. For example, in Drosophila melanogaster, female genitalia develop from the embryonic segment A8. In males, however, A8 develops into a tergite-like structure (Keisman et al. 2001). A8 in females is phylogenetically identical to A8 in males, and it is ontogenetically identical to the adult female genitalia. Likewise, A8 in males is ontogenetically identical to the tergite-like structure. Yet the female genitalia and the male tergite-like structure are not homologous. Over the course of development, a homologous precursor develops into non-homologous structures. One task of an enriched account is to explain why this is so. Wagner’s account would analyze such cases as involving initially homologous precursors that come to express non-homologous ChINs.

  8. 8.

    For reasons of space, I do not discuss serial homology and paralogy, but similar considerations apply.

  9. 9.

    For additional critique of this assumption, see Currie (2014).

References

  1. Amundson R (1994) Two concepts of constraint: adaptationism and the challenge from developmental biology. Philos Sci 61(4):556–578. https://doi.org/10.1086/289822

    Article  Google Scholar 

  2. Amundson R (2005) The changing role of the embryo in evolutionary thought: roots of evo-devo. Cambridge University Press, Cambridge

    Google Scholar 

  3. Assis LCS, Brigandt I (2009) Homology: homeostatic property cluster kinds in systematics and evolution. Evol Biol 36(2):248–255. https://doi.org/10.1007/s11692-009-9054-y

    Article  Google Scholar 

  4. Brigandt I (2002) Homology and the origin of correspondence. Biol Philos 17(3):389–407. https://doi.org/10.1023/A:1020196124917

    Article  Google Scholar 

  5. Brigandt I (2007) Typology now: homology and developmental constraints explain evolvability. Biol Philos 22(5):709–725. https://doi.org/10.1007/s10539-007-9089-3

    Article  Google Scholar 

  6. Brower AVZ, Schawaroch V (1996) Three steps of homology assesment. Cladistics 12(3):265–272. https://doi.org/10.1006/clad.1996.0020

    Google Scholar 

  7. Cracraft J (2005) Phylogeny and evo-devo: characters, homology, and the historical analysis of the evolution of development. Zoology 108(4):345–356. https://doi.org/10.1016/j.zool.2005.09.003

    Article  Google Scholar 

  8. Currie AM (2014) Venomous dinosaurs and rear-fanged snakes: homology and homoplasy characterized. Erkenn 79(3):701–727. https://doi.org/10.1007/s10670-013-9533-5

    Article  Google Scholar 

  9. Darwin C (1981) The descent of man, and selection in relation to sex. Princeton University Press, Princeton

    Google Scholar 

  10. Davidson EH, Erwin DH (2006) Gene regulatory networks and the evolution of animal body plans. Science 311(5762):796–800. https://doi.org/10.1126/science.1113832

    Article  Google Scholar 

  11. De Beer G (1971) Homology, an unsolved problem. Oxford University Press, Oxford

    Google Scholar 

  12. Eme L, Doolittle WF (2016) Microbial evolution: xenology (apparently) trumps paralogy. Curr Biol 26(22):R1181–R1183. https://doi.org/10.1016/j.cub.2016.09.049

    Article  Google Scholar 

  13. Fitch WM (1970) Distinguishing homologous from analogous proteins. Syst Biol 19(2):99–113. https://doi.org/10.2307/2412448

    Google Scholar 

  14. Fitch WM (2000) Homology a personal view on some of the problems. Trends Genet 16(5):227–231. https://doi.org/10.1016/S0168-9525(00)02005-9

    Article  Google Scholar 

  15. Goethe JWV (2009) The metamorphosis of plants. Miller GL (ed, trans) MIT Press, Cambridge

  16. Gray GS, Fitch WM (1983) Evolution of antibiotic resistance genes: the DNA sequence of a kanamycin resistance gene from Staphylococcus aureus. Mol Biol Evol 1(1):57–66. https://doi.org/10.1093/oxfordjournals.molbev.a040298

    Google Scholar 

  17. Griffiths PE (2007) The phenomena of homology. Biol Philos 22(5):643–658. https://doi.org/10.1007/s10539-007-9090-x

    Article  Google Scholar 

  18. Hall BK (ed) (1994) Homology: the hierarchical basis of comparative biology. Academic Press, San Diego

    Google Scholar 

  19. Havstad JC, Assis LCS, Rieppel O (2015) The semaphorontic view of homology. J Exp Zool (Mol Dev Evol) 324(7):578–587. https://doi.org/10.1002/jez.b.22634

    Article  Google Scholar 

  20. Hennig W (1966). In: Davis DD, Zangerl R (eds) Phylogenetic systematics. University of Illinois Press, Urbana

  21. Huson DH, Rupp R, Scornavacca C (2010) Phylogenetic networks: concepts, algorithms and applications. Cambridge University Press, Cambridge

    Google Scholar 

  22. Jamniczky HA (2005) Biological pluralism and homology. Philos Sci 72(5):687–698. https://doi.org/10.1086/50810841

    Article  Google Scholar 

  23. Keisman EL, Christiansen AE, Baker BS (2001) The sex determination dene doublesex regulates the A/P organizer to direct sex-specific patterns of growth in the Drosophila genital imaginal disc. Dev Cell 1(2):215–225. https://doi.org/10.1016/S1534-5807(01)00027-2

    Article  Google Scholar 

  24. Kendig C (2016) Homologizing as kinding. In: Kendig C (ed) Natural kinds and classification in scientific practice. Routledge, London, pp 106–125

    Google Scholar 

  25. Lankester ER (1870) On the use of the term homology in modern zoology, and the distinction between homogenetic and homoplastic agreements. Mag Nat Hist VI:34–43. https://doi.org/10.1080/00222937008696201

    Article  Google Scholar 

  26. Laublichler M (2014) Homology as a bridge between evolutionary morphology, developmental evolution, and phylogenetic systematics. In: Hamilton A (ed) The evolution of phylogenetic systematics. University of California Press, Berkeley, pp 63–85

    Google Scholar 

  27. Minelli A (2016) Tracing homologies in an ever-changing world. Riv Estetica 62:40–55

    Article  Google Scholar 

  28. Mohanraju P, Makarova KS, Zetsche B, Zhang F, Koonin EV, van der Oost J (2016) Diverse evolutionary roots and mechanistic variations of the CRISPR-Cas systems. Science 353(6299):aad5147. https://doi.org/10.1126/science.aad5147

    Article  Google Scholar 

  29. Müller GB (2003) Homology: the evolution of morphological organization. In: Müller GB, Newman SA (eds) Origination of organismal form: beyond the gene in developmental and evolutionary biology. MIT Press, Cambridge, pp 51–69

    Google Scholar 

  30. Müller GB, Newman SA (1999) Generation, integration, autonomy: three steps in the evolution of homology. In: Bock GR, Cardew G (eds) homology. Wiley, Chichester, pp 65–79

    Google Scholar 

  31. Müller GB, Wagner GP (1991) Novelty in evolution: restructuring the concept. Annu Rev Ecol Syst 22(1):229–256. https://doi.org/10.1146/annurev.es.22.110191.001305

    Article  Google Scholar 

  32. Owen R (1843) Lectures on the comparative anatomy and physiology of the vertebrate animals, delivered at the Royal College of Surgeons, in 1843. Longman, Brown, Green and Longmans, London

    Google Scholar 

  33. Owen R (2007). In: Amundson R (ed) On the nature of limbs: a discourse. University of Chicago Press, Chicago

  34. Panchen AL (1999) Homology—history of a concept. In: Hall BK (ed) Homology. Wiley, Chichester, pp 5–23

    Google Scholar 

  35. Peter IS, Davidson EH (2015) Genomic control process: development and evolution. Academic Press, Saint Louis

    Google Scholar 

  36. Ramsey G, Peterson AS (2012) Sameness in biology. Philos Sci 79(2):255–275. https://doi.org/10.1086/664744

    Article  Google Scholar 

  37. Salazar-Ciudad I, Jernvall J (2013) The causality horizon and the developmental bases of morphological evolution. Biol Theory 8(3):286–292. https://doi.org/10.1007/s13752-013-0121-3

    Article  Google Scholar 

  38. Shubin N, Tabin C, Carroll S (2009) Deep homology and the origins of evolutionary novelty. Nature 457(7231):818–823. https://doi.org/10.1038/nature07891

    Article  Google Scholar 

  39. Spencer WP (1963) Gene homologies and the mutants of Drosophila hydei. In: Jepsen GL, Simpson GG, Mayr E (eds) Genetics, paleontology and evolution. Atheneum, New York, pp 23–44

    Google Scholar 

  40. Strimmer K, von Haeseler A, Salemi M (2009) Genetic distances and nucleotide substitution models. In: Lemey P, Salemi M, Vandamme AM (eds) The phylogenetic handbook: a practical approach to phylogenetic analysis and hypothesis testing, 2nd edn. Cambridge University Press, Cambridge, pp 111–141

    Google Scholar 

  41. Wagner GP (1989) The origin of morphological characters and the biological basis of homology. 42. Evolution 43(6):1157–1171

    Article  Google Scholar 

  42. Wagner GP (1994) Homology and the mechanisms of development. In: Hall BK (ed) Homology: the hierarchical basis of comparative biology. Academic Press, San Diego, pp 273–299

    Google Scholar 

  43. Wagner GP (1999) A research programme for testing the biological homology concept. In: Bock GR, Cardew G (eds) Homology. Wiley, Chichester, pp 125–134

    Google Scholar 

  44. Wagner GP (2014) Homology, genes, and evolutionary innovation. Princeton University Press, Princeton. https://doi.org/10.1017/CBO9781107415324.004

    Google Scholar 

  45. Wiley EO, Lieberman BS (2011) Phylogenetics: theory and practice of phylogenetic systematics, 2nd edn. Wiley, Hoboken

    Google Scholar 

  46. Wray GA, Abouheif E (1998) When is homology not homology? Curr Opin Genet Dev 8:675–680. https://doi.org/10.1016/S0959-437X(98)80036-1

    Article  Google Scholar 

Download references

Acknowledgements

The author thanks Günter Wagner, James Lennox, Sandra Mitchell, Mark Wilson, Mark Rebeiz, James Woodward, Nora Boyd, David Colaço, Adrian Currie, Karen Kovaka, Liam Kofi Bright, Catherine Kendig, Maureen O’Malley, and two anonymous reviewers for helpful comments and discussion.

Author information

Affiliations

Authors

Corresponding author

Correspondence to Aaron Novick.

Ethics declarations

Conflict of interest

The author declares he has no conflict of interest.

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Novick, A. The fine structure of ‘homology’. Biol Philos 33, 6 (2018). https://doi.org/10.1007/s10539-018-9617-3

Download citation

Keywords

  • Homology
  • Character identity
  • Phylogenetic systematics
  • Scientific concepts
  • Evo-devo
  • Gene regulatory networks