Remipedia and the Evolution of Hexapods


With more than a million species that have already been described, the hexapods (insects and allies) constitute the largest animal group. Still their origin and phylogenetic affinities are matter of intense debate. Although previous morphological work generally considered the millipedes as sister taxon of the hexapods, molecular phylogenetic analyses agree that hexapods are actually closely related to crustaceans. Recent studies have provided evidence that the Remipedia, enigmatic crustaceans that have been discovered only 30 years ago in anchialine cave systems, may be the closest living relatives of hexapods. Support for this hypothesis comes from similar brain architecture, presence of an insect‐type respiratory haemocyanin in remipedes and phylogenomic studies. Thus hexapods may have evolved from a Remipedia‐like marine crustacean. These data evokes doubt on the generally described hypotheses in textbooks that might present an outdated picture of arthropod phylogeny.

Key Concepts:

  • Hexapods are the most successful animal group, but their relationship to other arthropods and evolutionary origins are matter of debate for more than a century.

  • Molecular phylogenetic studies have demonstrated that crustaceans are the closest living relatives of hexapods.

  • Crustaceans are most likely paraphyletic in terms of hexapods, thus one crustacean taxon is more closely related to the hexapods than the other crustaceans.

  • Brain morphology, haemocyanin structure and evolution, and phylogenomic studies suggest that the crustacean class Remipedia are the closest living relatives of hexapods.

  • Remipedia live in anchialine caves, which connect the inland ground water body with the salt water from the ocean.

  • Remipedia harbour a mixture of ancestral and derived morphological characters.

  • First hexapods may have evolved from marine Remipedia.

  • Remipedia thus occupy a key position for understanding hexapod evolution.

Keywords: crustacea; hexapoda; insecta; pancrustacea; remipedia

Figure 1.

An anchialine cave system as typically found on the Yucatan, Mexico.

Figure 2.

Conflicting hypotheses of remiped and hexapod evolution.

Figure 3.

Speleonectes tulumensis pictured in a frontal‐ventral photography.



Aguinaldo AMA, Turbeville JM, Linford LS et al. (1997) Evidence for a clade of nematodes, arthropods and other moulting animals. Nature 387: 489–493.

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

Brusca RC and Brusca GJ (2003) Invertebrates. Sunderland, Ma: Sinauer Associates.

Cameron SL, Miller KB, D'haese C et al. (2004) Mitochondrial genome data alone are not enough to unambiguously resolve the relationships of Entognatha, Insecta and Crustacea sensu lato (Arthropoda). Cladistics 20: 534–557.

Carapelli A, Liò P, Nardi F et al. (2007) Phylogenetic analysis of mitochondrial protein coding genes confirms the reciprocal paraphyly of Hexapoda and Crustacea. BMC Evolutionary Biology 7: S8.

Carracedo J (2002) Classic Geology in Europe 4: Canary Islands. Hertfordshire, UK: Terra Publishing.

Dunn CW, Hejnol A, Matus DQ et al. (2008) Broad phylogenomic sampling improves resolution of the animal tree of life. Nature 452: 745–749.

Ertas B, von Reumont BM, Wägele JW et al. (2009) Hemocyanin suggests a close relationship of Remipedia and Hexapoda. Molecular Biology and Evolution 26: 2711–2718.

Fanenbruck M and Harzsch S (2005) A brain atlas of Godzilliognomus frondosus Yager, 1989 (Remipedia, Godzilliidae) and comparison with the brain of Speleonectes tulumensis Yager, 1987 (Remipedia, Speleonectidae): implications for arthropod relationships. Arthropod Structure & Development 34: 343–378.

Fanenbruck M, Harzsch S and Wägele JW (2004) The brain of the Remipedia (Crustacea) and an alternative hypothesis on their phylogenetic relationships. Proceedings of the National Academy of Science of the USA 101: 3868–3873.

Friedrich M and Tautz D (1995) Ribosomal DNA phylogeny of the major extant arthropod classes and the evolution of myriapods. Nature 376: 165–167.

Garcia‐Machado E, Pempera M, Dennebouy N et al. (1999) Mitochondrial genes collectively suggest the paraphyly of Crustacea with respect to Insecta. Journal of Molecular Evolution 49: 142–149.

Grimaldi D and Engel MS (2005) Evolution of the Insects. New York: Cambridge University Press.

Haas F, Waloszek D and Hartenberger R (2003) Devonohexapodus bocksbergensis, a new marine hexapod from the Lower Devonian Hunsrück Slates, and the origin of Atelocerata and Hexapoda. Organisms Diversity & Evolution 3: 39–54.

van der Ham JL and Felgenhauer BE (2008) Ultrastructure and functional morphology of glandular setae and distal claws of cephalic appendages of Speleonectes tanumekes (Crustacea: Remipedia). Arthropod Structure & Development 37: 235–247.

Hassanin A (2006) Phylogeny of Arthropoda inferred from mitochondrial sequences: strategies for limiting the misleading effects of multiple changes in pattern and rates of substitution. Molecular Phylogenetics and Evolution 38: 100–116.

Humphreys WF (1993) Stygofauna in semi‐arid tropical Western Australia: a Thetyan connection? Mémoire de Biospéleologie 20: 111–116.

Hwang UW, Friedrich M, Tautz D et al. (2001) Mitochondrial protein phylogeny joins myriapods with chelicerates. Nature 413: 154–157.

Iliffe T, Wilkens H, Parzefal J et al. (1984) Marine lava cave fauna: composition, iogeography and origins. Science 225: 309–311.

Ito T (1989) Origin of the basis in copepod limbs, with reference to remipedian and cephalocarid limbs. Journal of Crustacean Biology 9: 85–103.

Kadner D and Stollewerk A (2004) Neurogenesis in the chilopod Lithobius forficatus suggests more similarities to chelicerates than to insects. Development Genes and Evolution 214: 367–379.

Koenemann S, Jenner RA, Hoenemann M et al. (2010) Arthropod phylogeny revisited, with a focus on crustacean relationships. Arthropod Structure & Development 39: 88–110.

Koenemann S, Olesen J, Alwes F et al. (2009) The post‐embryonic development of Remipedia (Crustacea) – additional results and new insights. Development Genes and Evolution 219: 131–145.

Koenemann S, Schram FR, Iliffe TM et al. (2007) The behavior of Remipedia (Crustacea), with supporting field observations. Journal of Crustacean Biology 27: 534–542.

Kühl G and Rust J (2009) Devonohexapodus bocksbergensis is a synonym of Wingertshellicus backesi (Euarthropoda) – no evidence for marine hexapods living in the Devonian Hunsrück Sea. Organisms Diversity & Evolution 9: 215–231.

Kukalová‐Peck J (1998) Arthropod phylogeny and ‘basal’ morphological structures. In: Fortey RA and Thomas RH (eds) Arthropod Relationships, pp. 249–269. London: Chapman and Hall.

Lankester ER (1904) The structure and classification of the Arthropoda. Microscopical Society (London), Quarterly Journal 47: 523–582.

Lavrov DV, Brown WM and Boore JL (2004) Phylogenetic position of the Pentastomida and (pan)crustacean relationships. Proceedings of the Royal Society of London. Series B: Biological Sciences 271: 537–544.

Mallatt J and Giribet G (2006) Further use of nearly complete, 28S and 18S rRNA genes to classify Ecdysozoa: 37 more arthropods and a kinorhynch. Molecular Phylogenetics and Evolution 40: 772–794.

Markl J and Decker H (1992) Molecular structure of the arthropod hemocyanins. Advances in Comparative Physiology and Biochemistry 13: 325–376.

Nardi F, Spinsanti G, Boore JL et al. (2003) Hexapod origins: monophyletic or paraphyletic? Science 299: 1887–1889.

Pick C, Schneuer M and Burmester T (2009) The occurrence of hemocyanin in Hexapoda. FEBS Journal 276: 1930–1941.

Pisani D, Poling LL, Lyons‐Weiler M et al. (2004) The colonization of land by animals: molecular phylogeny and divergence times among arthropods. BMC Biology 2: 1.

Pocock RI (1893) On the classification of the tracheate Arthropoda. Zoologischer Anzeiger 16: 271–275.

Regier JC, Shultz JW, Ganley AR et al. (2008) Resolving arthropod phylogeny: exploring phylogenetic signal within 41 kb of protein‐coding nuclear gene sequence. Systematic Biology 57: 920–938.

Regier JC, Shultz JW and Kambic RE (2005) Pancrustacean phylogeny: hexapods are terrestrial crustaceans and maxillopods are not monophyletic. Proceedings of the Royal Society of London, Series B: Biological Sciences 272: 395–401.

Regier JC, Shultz JW, Zwick A et al. (2010) Arthropod relationships revealed by phylogenomic analysis of nuclear protein‐coding sequences. Nature 463: 1079–1083.

von Reumont BM, Meusemann K, Szucsich NU et al. (2009) Can comprehensive background knowledge be incorporated into substitution models to improve phylogenetic analyses? A case study on major arthropod relationships. BMC Evolutionary Biology 9: 119.

Richter S (2002) The Tetraconata concept: hexapod‐crustacean relationships and the phylogeny of Crustacea. Organisms Diversity & Evolution 2: 217–237.

Roeding F, Hagner‐Holler S, Ruhberg H et al. (2007) EST sequencing of Onychophora and phylogenomic analysis of Metazoa. Molecular Phylogenetics and Evolution 45: 942–951.

Rota‐Stabelli O and Telford MJ (2008) A multi criterion approach for the selection of optimal outgroups in phylogeny: recovering some support for Mandibulata over Myriochelata using mitogenomics. Molecular Phylogenetics and Evolution 48: 103–111.

Schram FR (1986) Crustacea. Oxford: Oxford University Press.

Schram FR and Lewis CA (1989) Functional morphology of feeding in Nectiopoda. In: Felgenhauer BE, Watling L and Thistle AB (eds) Crustacean Issues 6: Functional Morphology of Feeding and Grooming in Crustacea, pp. 115–122. Rotterdam: A. A. Balkema Press.

Spears T and Abele LG (1997) Crustacean phylogeny inferred from 18S rDNA. In: Fortey RA and Thomas RH (eds) Arthropod Relationships, pp. 169–187. London: Chapman and Hall.

Timmermans M, Roelofs D, Marien J et al. (2008) Revealing pancrustacean relationships: phylogenetic analysis of ribosomal protein genes places Collembola (springtails) in a monophyletic Hexapoda and reinforces the discrepancy between mitochondrial and nuclear DNA markers. BMC Evolutionary Biology 8: 83.

Wilson K, Cahill V, Ballment E et al. (2000) The complete sequence of the mitochondrial genome of the crustacean Penaeus monodon: are malacostracan crustaceans more closely related to insects than to branchiopods? Molecular Biology and Evolution 17: 863–874.

Yager J (1981) Remipedia, a new class of Crustacea from a marine cave in the Bahamas. Journal of Crustacean Biology 1: 328–333.

Zrzavý J and Štys P (1997) The basic body plan of arthropods: insights from evolutionary morphology and developmental biology. Journal of Evolutionary Biology 10: 353–367.

Contact Editor close
Submit a note to the editor about this article by filling in the form below.

* Required Field

How to Cite close
von Reumont, Björn M, and Burmester, Thorsten(Dec 2010) Remipedia and the Evolution of Hexapods. In: eLS. John Wiley & Sons Ltd, Chichester. [doi: 10.1002/9780470015902.a0022862]