Homology in Character Evolution

Joseph L Staton, University of South Carolina, Beaufort, South Carolina, USA

Published online: December 2011

DOI: 10.1002/9780470015902.a0001776.pub2

Homology forms the basis of organisation for comparative biology. Richard Owen's simple definition of homology as the ‘same organ in different animals under every variety of form and function’ takes on new meaning in light of Darwin's concept of descent with modification. The modern study of comparative biology and phylogenetics is grounded in the notion that organisms share a greater proportion of homologous (i.e. ‘derived’) characteristics the more recently they share a common ancestor. Instead of solely being the purview of anatomical study, homology of these characteristics can be applied at the level of molecular evolution, genomic organisation and modern evolutionary developmental biology (‘evo/devo’). Aspects of homology help us formulate hypotheses about the meaning of changes in homologous structures in the inference of evolution of organisms at all levels of biological organisation.

Key Concepts:

  • Homology was originally a measure of correspondence between anatomical structures.
  • Descent with modification explains homology as a result of shared ancestry that reflects modifications in characteristics within related lineages.
  • Comparative methods use changes in homologous characteristics to infer evolution within groups (phylogenetics).
  • Recent advances in molecular biology allow for the comparison of homologous characteristics at more diverse levels, including DNA sequences, genomic arrangements and developmental pathways.
  • Recent work highlights homologous characteristics at a fundamental or ancient level, termed ‘deep homology’.

Keywords: archetype; evolution; correspondence; gene; morphology; genome; phylogeny; development; deep homology

Figure 1. Concepts of homology. (a) Owen's homology was a concept of corresponding structures between organisms as similar or homologous based on their relationship to the archetype. (b) After Darwin, the similarity in structure is understood to arise from ancestor/descendant relationships.
Figure 2. Phylogenetic analysis of characteristics. (a) Hypothetical list of taxa and traits analysed (b and c). ‘0’ and ‘1’ designate alternative forms for a feature, for example a forelimb might be a leg or a wing. Trait 12 is an autapomorphy and trait 1 is a symplesiomorphy. (b) A nesting of taxa showing their relatedness based on the traits in A (a Venn diagram). (c) A phylogenetic tree of the relationships shown in (b). Synapomorphies (from (a)) can be clearly mapped onto the branches since they are congruent with one another. All taxa above a marked branch share the same derived features. Homoplasies (shadowed in (a)) are in conflict with phylogenetic patterns of the tree presented.
Figure 3. Homology in phylogenetic reconstruction. (a) An alignment of the first 30 bases of DNA for eight hypothetical taxa implies a hypothesis of positional homology among bases. Distribution of sequence change across taxa allows us to infer homology of a change at that position. Bases in blue boxes are inferred to be a homologous change for that base position, whereas bases in green boxes are inferred to be changes in conflict, or a result of homoplasy. (b) The distribution of these homologous changes are presented on a phylogenetic tree (* denotes homoplasy within a base/locus). (c) A gene tree of and genes for globins is presented (after Goodman et al., 1987). The duplication event for and globins precedes the diversification of vertebrates. This is supported by the independent phylogenies for each being congruent for each of the paralogous sequences. (d) Evidence of a homologous gene rearrangement in the mitochondrial DNA of eukaryotes (Boore, 1999). Hexapods and crustaceans share a similar arrangement of the leucine transfer ribonucleic acid (tRNA) (anticodon UUR) gene (L) occurring between the first and second subunits of cytochrome c oxidase. Chelicerates and other invertebrates do not share this arrangement. This supports the unity of mandibulate arthropods suggested earlier by some morphologists.
Figure 4. Inverted expression of homologous gene products in transverse and longitudinal sections of fly and frog embryos (after De Robertis and Sasai, 1996). The fly embryo ventralising factor short gastrulation (sog) and the frog embryo dorsalising factor chordin (chd) are homologous genes. De Robertis and Sasai (1996) argued that the inverse position of their expression in these two distantly related organisms resurrects Geoffroy Saint-Hilaire's notions of dorsal and ventral homology between vertebrates and arthropods.
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 References
    Abouheif E (1997) Developmental genetics and homology: a hierarchical approach. Trends in Ecology and Evolution 12: 405–408.
    Arendt D, Tessmar-Raible K, Snyman H, Dorresteijn AW and Wittbrodt J (2004) Ciliary photoreceptors with a vertebrate-type opsin in an invertebrate brain. Science 306: 869–871.
    Bajsa J, Singh K, Nanayakkara D et al. (2007) A survey of synthetic and natural phytotoxic compounds and phytoalexins as potential antimalarial compounds. Biological and Pharmaceutical Bulletin 30: 1740–1744.
    book vonBaer KE (1828) Über Entwickelungsgeschichte der Thiere: Beobachtung und Reflexion. Königberg: Bornträger.
    book Belon P (1555) L’Histoire de la Nature des Oyseaux. Paris: Guillaume Cavellat (figure reproduced in Panchen, 1994).
    Boore JL (1999) Animal mitochondrial genomes. Nucleic Acids Research 27: 1767–1780.
    book Darwin CR (1859) On the Origin of Species by Means of Natural Selection, or the Preservation of Favoured Races in the Struggle for Life. London: John Murray.
    book de Beer G (1971) Homology: An Unsolved Problem. Oxford Biology Readers. Oxford: Oxford University Press.
    De Robertis EM (2008) Evo-devo: variations on ancestral themes. Cell 132: 185–195.
    De Robertis EM and Sasai Y (1996) A common plan for dorsoventral patterning in Bilateria. Nature 380: 37–40.
    Duke SO (2010) Herbicide and pharmaceutical relationships. Weed Science 58: 334–339.
    Fan Y, Linardopoulou E, Friedman C, Williams E and Trask BJ (2002) Genomic structure and evolution of the ancestral chromosome fusion site in 2q13–2q14.1 and paralogous regions on other human chromosomes. Genome Research 12: 1651–1662.
    Fennell BJ, Naughton JA, Dempsey E and Bell A (2006) Cellular and molecular actions of dinitroaniline and phosphorothioamidate herbicides on Plasmodium falciparum: tubulin as a specific antimalarial target. Molecular and Biochemical Parasitology 145: 226–238.
    book Goodman M, Miyamoto MM and Czelusniak J (1987) "Pattern and process in vertebrate phylogeny revealed by coevolution of molecules and morphologies". In: Patterson C (ed.) Molecules and Morphology in Evolution: Conflict or Compromise? pp. 141–176. Cambridge: Cambridge University Press.
    Halder G, Callaerts P and Gehring WJ (1995) Induction of ectopic eyes by targeted expression of the eyeless gene in Drosophila. Science 267: 1788–1792.
    book Hennig W (1966) Phylogenetic Systematics. Urbana, IL: University of Illinois Press.
    Jacob F (1977) Evolution and tinkering. Science 196: 1161–1166.
    Jacobs DK (1990) Selector genes and the Cambrian radiation of Bilateria. Proceedings of the National Academy of Sciences of the USA 87: 4406–4410.
    Köhler S, Delwiche CF, Denny PW et al. (1997) A plastid of probable green algal origin in apicomplexan parasites. Science 275: 1485–1489.
    McFadden GI, Reith ME, Munholland J and Lang-Unnasch N (1996) Plastid in human parasites. Nature 381: 482.
    other Owen R (1843) Lectures on the Comparative Anatomy and Physiology of the Invertebrate Animals, Delivered at the Royal College of Surgeons, in 1843. London: Longman, Brown, Green, and Longmans.
    book Panchen AL (1994) "Richard Owen and the concept of homology". In: Hall BK (ed.) Homology: The Hierarchical Basis of Comparative Biology, pp. 21–62. San Diego: Academic Press.
    Panganiban G, Irvine SM, Lowe C et al. (1997) The origin and evolution of animal appendages. Proceedings of the National Academy of Sciences of the USA 94: 5162–5166.
    Passamaneck Yj, Furchheim N, Hejnol A, Martindale MQ and Lüter C (2011) Ciliary photoreceptors in the cerebral eyes of a protostome larva. EvoDevo 2: 6 doi:10.1186/2041-9139-2-6
    Rota-Stabelli O, Kayal E, Gleeson D et al. (2010) Ecdysozoan mitogenomics: evidence for a common origin of the legged invertebrates, the Panarthropoda. Genome Biology and Evolution 2: 425–440.
    Scotland RW (2010) Deep homology: a view from systematics. Bioessays 32: 438–449.
    Shubin N, Tabin C and Carroll S (1997) Fossils, genes and the evolution of animal limbs. Nature 388: 639–648.
    Shubin N, Tabin C and Carroll S (2009) Deep homology and the origins of evolutionary novelty. Nature 457: 818–823.
    Slack JMW, Holland PWH and Graham CF (1993) The zootype and the phylotypic stage. Nature 361: 490–492.
    Strickland HE (1846) On the structural relations of organized beings. Philosophical Magazine and Journal of Science 3(28): 354–364.
    Waller RF and McFadden GI (2005) The apicoplast: a review of the derived plastid of apicomplexan parasites. Current Issues in Molecular Biology 7: 57–80.
    Williamson DH, Gardner MJ, Preiser P et al. (1994) The evolutionary origin of the 35 kb circular DNA of Plasmodium falciparum: new evidence supports a possible rhodophyte ancestry. Molecular and General Genetics 243(2): 249–252.
    Yeh E and DeRisi JL (2011) Chemical rescue of malaria parasites lacking an apicoplast defines organelle function in blood-stage Plasmodium falciparum. PLoS Biology 9(8): e1001138. doi:10.1371/journal.pbio.1001138.
 Further Reading
    book de Beer G (1958) Embryos and Ancestors. Oxford: Clarendon Press.
    book Gilbert SF (2010) Developmental Biology. Sunderland, Massachusetts: Sinauer Associates.
    book Hall BK (ed.) (1994) Homology: The Hierarchical Basis of Comparative Biology. San Diego: Academic Press.

Related Sub-Topics:

Evolution and Development | Diversification of Plants and Animals | Reconstruction of Phylogeny | Evolution: Theories and Ideas | Evolutionary Processes
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Article Title: Homology in Character Evolution
 
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Staton, Joseph L(Dec 2011) Homology in Character Evolution. In: eLS. John Wiley & Sons Ltd, Chichester. http://www.els.net [doi: 10.1002/9780470015902.a0001776.pub2]