Skip to main content

Developmental Genetics and the Diversity of Animal Form: Hox Genes in Arthropods

  • Chapter
The Biology of Biodiversity

Abstract

The wonderful diversity of animal forms is built upon a largely conserved set of genes and developmental mechanisms. The Hox genes provide one of the best studied examples of how such a conserved mechanism underlies a diversity of forms.

The Hox genes encode proteins that serve as molecular labels for the position of cells along the major body axis. The differential expression of these genes causes cells that would otherwise be equivalent to adopt different developmental fates in different regions of the body. This leads to the differentiation of segments in arthropods, and of regions along the axial skeleton of vertebrates. An analogous role is probably conserved in most other triploblastic bilaterian phyla. The family of Hox genes diversified at an early stage in the radiation of the metazoa. The set of Hox genes present in each phylum provides phylogenetic characters that are useful for establishing the relationships between phyla. Characteristics of the 5′ (Abd-B related) genes support the grouping of the metazoa into the same major lineages as the recent rRNA-based phylogeny proposed by Aguinaldo and colleagues.

The patterns of expression of the Hox genes provide markers to relate the body plans of distantly related animals. A good example is the comparison of head segmentation in chelicerate and mandibulate arthropods. Patterns of Hox gene expression refute a model of segment loss in chelicerates, and suggest that these very different arthropods retain a common set of uniquely defined head segments de-rived from their last common ancestor. No one gene can be taken to define “homology”, but in cases such as this where comparisons of several genes provide a consistent pattern, they may provide powerful discrimination between alternative hypotheses.

Comparisons of Hox gene expression in the arthropod trunk suggest a more flexible relationship between the processes of segment formation and Hox gene regulation. Changes in this relationship have led to changes in the pattern of tagmosis, which underlie the functional specialisation and evolutionary radiation of the arthropods.

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

Access this chapter

Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 119.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 159.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  • Abouheif E, Akam M, Dickinson WJ, Holland PWH, Meyer A, Patel NH, Raff RA, Roth VL, Wray GA (1997) Homology and developmental genes. Trends Genet 13:432–433

    Article  PubMed  CAS  Google Scholar 

  • Affolter M, Schier A, Gehring WJ (1990) Homeodomain proteins and the regulation of gene expression. Current Opinion Cell Biol 2:485–495

    Article  PubMed  CAS  Google Scholar 

  • Aguinaldo AMA, Turbeville JM, Linford LS, Rivera MC, Garey JR, Raff RA, Lake JA (1997) Evidence for a clade of nematodes arthropods and other moulting animals. Nature 387:489–493

    Article  PubMed  CAS  Google Scholar 

  • Akam M (1987) The molecular basis for metameric pattern in the Drosophila embryo. Development 101:1–22

    PubMed  CAS  Google Scholar 

  • Akam M (1989) Hox and HOM: Homologous gene clusters in insects and vertebrates. Cell 57:347–349

    Article  PubMed  CAS  Google Scholar 

  • Arenas-Mena C, Martinez C, Cameron RA, Davidson EH (1998) Expression of the Hox gene complex in the indirect development of a sea urchin. Proc Natl Acad Sci USA 95:13062–13067

    Article  PubMed  CAS  Google Scholar 

  • Averof M, Akam M (1995a) Hox genes and the diversification of insect and crustacean body plans. Nature 376:420–423

    Article  PubMed  CAS  Google Scholar 

  • Averof M, Akam M (1995b) Insect-crustacean relationships: insights from comparative developmental and molecular studies. Phil Trans Roy Soc 347:293–303

    Article  Google Scholar 

  • Averof M, Patel NH (1997) Crustacean appendage evolution associated with changes in Hox gene expression. Nature 388:682–686

    Article  PubMed  CAS  Google Scholar 

  • Bateson W (1894) Materials for the study of variation. MacMillan & Co, London

    Google Scholar 

  • Beeman RW, Stuart JJ, Brown SJ, Denell RE (1993) Structure and function of the homeotic gene complex (HOM-C) in the beetle Trilobium castaneum. Bio Essays 15:439–444

    CAS  Google Scholar 

  • Bridges CB, Morgan TH (1923) Bithorax In The third chromosome group of mutant characters of Drosophila melanogaster. Carnegie Inst Wash Publ, pp 137–146

    Google Scholar 

  • Brooke NM, Garcia-Fernandez J, Holland PWH (1998) The Para Hox gene cluster is an evolutionary sister of the Hox gene cluster. Nature 392:920–922

    Article  PubMed  CAS  Google Scholar 

  • Brusca RC, Brusca GJ (1990) Invertebrates. Sinauer, Massachusetts

    Google Scholar 

  • Burglin TR (1995) The evolution of homeobox genes In: Arai R, Kato M, Doi Y (Eds) Biodiversity and evolution. The National Science Museum Foundation, Tokyo, pp 289–334

    Google Scholar 

  • Burke AC, Nelson CE, Morgan BA, Tabin C (1995) Hox genes and the evolution of vertebrate axial morphology. Development 121:333–346

    PubMed  CAS  Google Scholar 

  • Castelli-Gair J, Akam M (1995) How the Hox gene Ultrabithorax specifies two different segments: the significance of spatial and temporal regulation within metameres. Development 121:2973–2982

    PubMed  CAS  Google Scholar 

  • Cohn MJ, Patel K, Krumlauf R, Wilkinson DG, Clarke JDW, Tickle C (1997) Hox9 genes and vertebrate limb specification. Nature 387:97–101

    Article  PubMed  CAS  Google Scholar 

  • Damen WGM, Hausdorf M, Seyfarth EA, Tautz D (1998) A conserved mode of head segmentation in arthropods revealed by the expression pattern of Hox genes in a spider. Proc Natl Acad Sci USA 95:10665–10670

    Article  PubMed  CAS  Google Scholar 

  • Denell RE, Brown SJ, Beeman RW (1996) Evolution of the organization and function of insect homeotic complexes. Seminars in Cell & Developmental Biology 7:527–538

    Article  Google Scholar 

  • De Rosa R, Grenier J, Andreeva T, Cook C, Adoutte A, Akam M, Carroll S, Balavoine G (1999) Hox genes in brachiopoods and priapulids and protostome evolution. Nature 399:772–775

    Article  PubMed  CAS  Google Scholar 

  • Digregorio AD, Spagnuolo A, Ristoratore F, Pischetola M, Aniello F, Brauno M, Cariello L, Di Lauro R (1995) Cloning of ascidian homeobox genes provides evidence for a primordial chordate cluster. Gene 156:253–257

    Article  CAS  Google Scholar 

  • Freidrich M, Tautz D (1995) rDNA phylogeny of the major extant arthropod classes and the evolution of myriapods. Nature 376:165–167

    Article  Google Scholar 

  • Fromental-Ramain C, Warot X, Iakkaraju S, Favier B, Haack H, Birling C, Dierich A, Dolle P, Chambon P (1996) Specific and redundant functions of the paralogous Hoxa9 and Hoxd9 genes in forelimb and axial skeleton patterning. Development 122:461–472

    PubMed  CAS  Google Scholar 

  • Gehring WJ (1987) Homeo boxes in the study of development. Science 236:1245–52

    Article  PubMed  CAS  Google Scholar 

  • Grenier JK, Garber TL, Warren R, Whitington PM, Carroll S (1997) Evolution of the entire arthropod Hox gene set predated the origin and radiation of the onychophoran/arthropod clade. Curr Biol 7:547–553

    Article  PubMed  CAS  Google Scholar 

  • Haider G, Callaerts P, Gehring WJ (1995) New perspectives on eye evolution. Current Opinion Genes Dev 5:602–609

    Article  Google Scholar 

  • Kelsh R, Weinzierl ROJ, White RAH, Akam M (1994) Homeotic gene expression in the Locust Schistocerca: an antibody that detects conserved epitopes in Ultrabithorax and abdominal-A proteins. Develop Genet 15:19–31

    Article  CAS  Google Scholar 

  • Kmita-Cunisse M, Loosli F, Bierne J, Gehring WJ (1998) Homeobox genes of the ribbonworm Linens sanguineus: Evolutionary implications. Proc Natl Acad Sci USA 95:3030–3035

    Article  PubMed  CAS  Google Scholar 

  • Lawrence PA, Morata G (1994) Homeobox genes: their function in Drosophila segmentation and pattern formation. Cell 78:181–189

    Article  PubMed  CAS  Google Scholar 

  • Lewis EB (1963) Genes and developmental pathways. Am Zool 3:33–56

    Google Scholar 

  • Lewis EB (1978) A gene complex controlling segmentation in Drosophila. Nature 276:565–570

    Article  PubMed  CAS  Google Scholar 

  • Lewis EB (1995) The Bithorax complex: the first fifty years. Les prix Nobel 233–260

    Google Scholar 

  • Mahaffey JW, Kaufman TC (1987) The homeotic genes of the antennapedia complex and the bithorax complex of Drosophila In: Malacinski GM (Ed) Developmental genetics of higher organisms. MacMillan, New York, pp 329–359

    Google Scholar 

  • McGinnis W, Garber RL, Wirz J, Kuroiwa A, Gehring WJ (1984) A homologous protein-coding sequence in Drosophila homoeotic genes and its conservation in other meta-zoans. Cell 37:403–408

    Article  PubMed  CAS  Google Scholar 

  • McGinnis W, Krumlauf R (1992) Homeobox genes and axial patterning. Cell 68:283–302

    Article  PubMed  CAS  Google Scholar 

  • Minelli A, Bortoletto S (1988) Myriapod metamerism and arthropod segmentation. Biol J Linn Soc 33:323–343

    Article  Google Scholar 

  • Popadic A, Rusch D, Peterson M, Rogers BT, Kaufman TC (1996) Origin of arthropod mandible. Nature 380:395

    Article  CAS  Google Scholar 

  • Rogers BT, Kaufman TC (1997) Structure of the insect head in ontogeny and phylogeny: a view from Drosophila. Int Rev Cytol 174:1–84

    Article  PubMed  CAS  Google Scholar 

  • Schram F R (1986) Crustacea. University Press, Oxford

    Google Scholar 

  • Slack JMW, Holland PWH, Graham CF (1993) The zootype and the phylotypic stage. Nature 361:490–492

    Article  PubMed  CAS  Google Scholar 

  • Smith ML (1998) An analysis of Hox genes in myriapods. Ph D thesis. University of Cambridge

    Google Scholar 

  • Snodgrass RE (1931) Evolution of the insect head and the organs of feeding. In Smithsonian Report, pp 443–489

    Google Scholar 

  • Snow P, Buss LW (1994) HOM/Hox-Type Homeoboxes from Stylaria lacustris (Annelida: Oligochaeta). Mol Phyl E vol 3:360–364

    Article  CAS  Google Scholar 

  • Tazima Y (1964) The genetics of the silkworm. Logos Press, London

    Google Scholar 

  • Telford MJ, Thomas RH (1998) Expression of homeobox genes shows chelicerate arthropods retain their deutocerebral segment. Proc Natl Acad Sci USA 95:10671–10675

    Article  PubMed  CAS  Google Scholar 

  • Von Allmen G, Hogga I, Spierer A, Karch F, Bender W, Gyurkovics H, Lewis E (1996) Splits in fruitfly Hox gene complexes. Nature 380:116

    Article  Google Scholar 

  • Weygoldt P (1985) Ontogeny of the arachnid central nervous system. In: Barth FG (Ed) Neurobiology of arachnids. Springer-Verlag, Berlin, pp 20–37

    Chapter  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Editor information

Editors and Affiliations

Rights and permissions

Reprints and permissions

Copyright information

© 2000 Springer-Verlag Tokyo

About this chapter

Cite this chapter

Akam, M. (2000). Developmental Genetics and the Diversity of Animal Form: Hox Genes in Arthropods. In: Kato, M. (eds) The Biology of Biodiversity. Springer, Tokyo. https://doi.org/10.1007/978-4-431-65930-3_13

Download citation

  • DOI: https://doi.org/10.1007/978-4-431-65930-3_13

  • Publisher Name: Springer, Tokyo

  • Print ISBN: 978-4-431-65932-7

  • Online ISBN: 978-4-431-65930-3

  • eBook Packages: Springer Book Archive

Publish with us

Policies and ethics