Review Article
The geological record and phylogeny of the Myriapoda

https://doi.org/10.1016/j.asd.2009.11.002Get rights and content

Abstract

We review issues of myriapod phylogeny, from the position of the Myriapoda amongst arthropods to the relationships of the orders of the classes Chilopoda and Diplopoda. The fossil record of each myriapod class is reviewed, with an emphasis on developments since 1997. We accept as working hypotheses that Myriapoda is monophyletic and belongs in Mandibulata, that the classes of Myriapoda are monophyletic, and that they are related as (Chilopoda (Symphyla (Diplopoda + Pauropoda))). The most pressing challenges to these hypotheses are some molecular and developmental evidence for an alliance between myriapods and chelicerates, and the attraction of symphylans to pauropods in some molecular analyses. While the phylogeny of the orders of Chilopoda appears settled, the relationships within Diplopoda remain unclear at several levels. Chilopoda and Diplopoda have a relatively sparse representation as fossils, and Symphyla and Pauropoda fossils are known only from Tertiary ambers. Fossils are difficult to place in trees based on living forms because many morphological characters are not very likely to be preserved in the fossils; as a consequence, most diplopod fossils have been placed in extinct higher taxa. Nevertheless, important information from diplopod fossils includes the first documented occurrence of air-breathing, and the first evidence for the use of a chemical defense. Stem-group myriapods are unknown, but evidence suggests the group must have arisen in the Early Cambrian, with a major period of cladogenesis in the Late Ordovician and early Silurian. Large terrestrial myriapods were on land at least by mid-Silurian.

Introduction

The fossil record and evolution of the Myriapoda were last reviewed in depth by Shear, in 1997. Since that time, new discoveries and new descriptions of important fossils, as well as recent broad-scale analyses of arthropod phylogeny and ingroup relationships of the extant myriapod taxa, have made desirable an updated overview of the field. In this article we first assess developments in our understanding of myriapod phylogeny, as a framework for a discussion of the fossils. We discuss fossil chilopods in a taxonomic framework, since there are only 5 extant orders and all known fossils except for the Devonian Devonobius can be confidently included in extant orders. Diplopod fossils are taken up chronologically, since no Palaeozoic representatives can be assigned with confidence to any of the 16 extant orders.

In the larger context of the Euarthropoda, myriapods have been difficult to place. Traditionally they have been regarded as closely allied to the Hexapoda, either as the hexapod sister group (i.e., Bäcker et al., 2008, Bitsch and Bitsch, 2004), or with the hexapods nested within a paraphyletic Myriapoda (i.e., Kraus, 2001, Willmann, 2003). But recent work utilizing both morphological and molecular characters (see Edgecombe and Giribet, 2002) has presented strong evidence that Myriapoda is not to be included in a clade with Hexapoda, now regarded as more closely related to Crustacea (Dohle, 2001). So do some myriapods belong near the base of the arthropod tree (Strausfeld et al., 2006), are they a part of the Mandibulata along with Tetraconata or Pancrustacea (Crustacea + Hexapoda; Harzsch et al., 2005), or do they form a taxon Paradoxopoda/Myriochelata with the Chelicerata (Negrisolo et al., 2004, Mayer and Whitington, 2009)? Is Myriapoda monophyletic, paraphyletic, or polyphyletic? Are the myriapod classes themselves monophyletic? And within those classes, how are the included orders related? The evidence available to be brought to bear on these questions is variable. Much morphological and diverse molecular data have been gathered for the Chilopoda (Edgecombe and Giribet, 2004, Giribet and Edgecombe, 2006), for example, and the internal phylogeny of the class now seems stable, while in the case of the Diplopoda, morphological analyses rely on relatively few characters, and only one kind of molecular marker (three nuclear coding genes) has been surveyed for a fairly restricted number of species, such that the analyses are sensitive to sampling breadth (Sierwald et al., 2001) as well as to parameters of analysis (Regier and Shultz, 2001, Regier et al., 2005, Sierwald and Bond, 2007). Exemplars of the Pauropoda and Symphyla have been included in few analyses, but in general data for these two classes are sparse, and nothing has been done regarding their internal phylogenies.

The myriapod fossil record is uneven both in a chronological and taxonomic sense. A small number of Silurian and Devonian fossils are available and their mode of preservation, as impressions in fine-grained sediments, as organically preserved cuticle, or embedded in translucent chert often allows for detailed morphological observations (Almond, 1985, Shear and Bonamo, 1988, Shear et al., 1998, Anderson and Trewin, 2003, Wilson, 2005a, Wilson and Anderson, 2004, Wilson et al., 2005). The Carboniferous holds perhaps the richest trove of myriapod fossils, albeit taxonomically biased toward the Diplopoda, and sampled from only limited habitats (Hoffman, 1969, Hannibal, 1987, Shear, 1997). In contrast, only a few myriapod fossils are known from the Permian, and none of them have been described in detail (Hannibal, 2006, Wilson, 2006a). The entire Mesozoic is similarly bereft, with but a handful of fossil myriapods (Edgecombe et al., 2009, Cockerell, 1917; Wilson, 2001, Wilson, 2003). Cenozoic myriapod fossils are almost entirely limited to a few amber Lagerstätten and are assignable to extant taxa (i.e., Santiago-Blay and Poinar, 1992).

The taxonomic distribution of myriapod fossils is strongly biased toward the Diplopoda, likely due to their greater fossilization potential; except for one small group, their cuticle is reinforced with calcium carbonate and is quite robust. However, since the cuticle is almost always consumed by the animal after moulting (to recycle the calcium), cast cuticles, which potentially enable one animal to leave behind more than a single fossil remnant, are unlikely to be available for fossilization. Further, diplopods are ecologically bound to an environment where rapid decay of organic matter, including arthropod cuticles, is facilitated by abundant bacteria and fungi. So despite their strong, mineralized cuticles, millipedes are likely to become fossils only when carcasses are quickly washed into a basin of deposition. The preservation potential of chilopods is even less. Their cuticles are relatively thin and unmineralized and their habitats similarly inimical to the survival of undecayed bodies. Fossils of symphylans and pauropods, with cuticle like that of centipedes, a soil and litter habitat, and mostly minute size, are unknown except for a few examples from Tertiary ambers (Scheller and Wunderlich, 2001, Scheller and Wunderlich, 2004).

The usefulness of the fossil record in myriapod phylogenetics is further complicated by the fact that the characters used to construct trees of living myriapods are rarely available in the fossils, with the result that a number of extinct taxa simply cannot be placed, either systematically or phylogenetically. Nevertheless, we believe that significant information can be derived from them, especially as regards the timing of cladogenesis, and in some cases studies of fossils can provide additional evidence in support of phylogenetic trees. Study of fossil myriapods is also essential to our understanding of the process of terrestrialization in arthropods, since the earliest trace fossils as well as the earliest body fossils of such creatures are of myriapods. Fossil millipedes also provide the earliest evidence of air-breathing (the Silurian Pneumodesmus newmani Wilson and Anderson has spiracles; Wilson and Anderson, 2004) and of chemical defense against predators (Devonian xyloiulideans have ozopores; Wilson, 2006a).

Section snippets

Myriapod phylogeny

Here we briefly review a variety of competing hypotheses regarding myriapod phylogeny, as set out above. Our conclusions are that the data favour a position for Myriapoda within the more inclusive Mandibulata, myriapod monophyly, and monophyly of each of the myriapod classes. Although the traditional systematic arrangement with Chilopoda sister to Progoneata, and the division of Progoneata into Dignatha (Diplopoda + Pauropoda) and Symphyla has been challenged, we find no strong basis for

Interrelationships of Chilopoda

From the perspective of morphology, the relationships between the 5 extant orders of Chilopoda have widespread consensus. The relationships depicted in Fig. 1 conform to groupings recognized in early classifications (Pocock, 1902; Verhoeff, 1902–1925), were depicted in pre-Hennigian phylogenetic diagrams (Prunescu, 1965, Shinohara, 1970), were likewise retrieved when cladistic argumentation was applied to the problem (Dohle, 1985, Dohle, 1990, Shear and Bonamo, 1988, Borucki, 1996), and are

Interrelationships of Diplopoda

As indicated in Section 1, the phylogeny of millipedes is unsettled when compared to that of centipedes. Phylogenetic problems in the Diplopoda are inherently more complex, since 16 extant orders of millipedes (including 144 families; Shelley, 2003) are currently recognized, as opposed to only 5 orders in centipedes. Fewer morphological characters have been studied, and entire potentially valuable character systems, such as the mouthparts, female external genitalia, and legs have either not

Pauropoda and Symphyla

No reliable internal phylogenies for these orders have been proposed, and they are taxonomically understudied, despite the herculean efforts of Ulf Scheller, virtually the only active specialist apart from pauropod taxonomist Yasunori Hagino. Although symphylans and pauropods are known as fossils only from the Baltic (Scheller and Wunderlich, 2001, Scheller and Wunderlich, 2004) and Dominican ambers (Poinar and Edwards 1995), specimens which can be placed in extant families and genera, the

Kampecarida

Kampecarids are enigmatic but relatively common myriapod-like fossils from Late Silurian and Early Devonian deposits in Britain. They were examined in an unpublished thesis by J.E. Almond (with an overview in Almond, 1985), upon which Shear (1997) based some tentative conclusions and a reconstruction. The kampecarid head may have been diplopod-like, with antennae and mandibles, and may either have been covered by two separate plates or followed by a legless collum. At least some of the trunk

Fossil stem-group myriapods?

The problem of identifying a fossil stem-group myriapod was addressed by Edgecombe (2004). While conceding that the presence of stem-group myriapods in the Cambrian is phylogenetically sound, and is indeed strengthened by the discovery of apparent crown group representatives of its sister group, Tetraconata, in the early Cambrian (Harvey and Butterfield, 2008), Edgecombe (2004) found that a variety of candidate fossils from the Lower and Upper Cambrian had in common with Myriapoda only a series

Acknowledgements

Günther Bechly kindly provided the photographs of chilopods from the Cretaceous of Brazil. Markus Koch prepared and photographed the Craterostigmus maxillipedes in Fig. 2C. Joe Hannibal provided photographs of Paleozoic diplopods. Work on this article by WAS was supported by a grant from the National Science Foundation of the United States (DEB05-29715) to WAS, Petra Sierwald and Jason Bond, and by the Faculty Professional Development Committee of Hampden-Sydney College.

References (138)

  • L. Podsiadlowski et al.

    The complete mitochondrial genome of Scutigerella causeyae (Myriapoda: Symphyla) and the phylogenetic position of the Symphyla

    Molecular Phylogenetics and Evolution

    (2007)
  • J.C. Regier et al.

    A phylogenetic analysis of Myriapoda (Arthropoda) using two nuclear protein-encoding genes

    Zoological Journal of the Linnean Society

    (2001)
  • J.C. Regier et al.

    Phylogenetic analysis of Myriapoda using three nuclear protein-coding genes

    Molecular Phylogenetics and Evolution

    (2005)
  • J.E. Almond

    The Silurian-Devonian fossil record of the Myriapoda

    Philosophical Transactions of the Royal Society of London B

    (1985)
  • D.T. Anderson

    Embryology and Phylogeny in Annelids and Arthropods

    (1973)
  • L.I. Anderson et al.

    An Early Devonian arthropod fauna from the Windyfield Cherts, Aberdeenshire, Scotland

    Palaeontology

    (2003)
  • P. Ax

    Das System der Metazoa II. Ein Lehrbuch der phylogenetischen Systematik

    (1999)
  • A.F. Bachofen von Echt

    Über die Myriapoden des Bernsteins

    Palaeobiologica

    (1942)
  • C. Bitsch et al.

    Phylogenetic relationships of basal hexapods among the mandibulate arthropods: a cladistic analysis based on comparative morphological characters

    Zoologica Scripta

    (2004)
  • H. Borucki

    Evolution und Phylogenetisches System der Chilopoda (Mandibulata, Tracheata)

    Verhandlungen des naturwissenschaftlichen Vereins in Hamburg

    (1996)
  • H.-W. Brölemann

    Myriapodes Chilopodes. Faune de France 25

    (1930)
  • D.E.G. Briggs et al.

    A giant myriapod trail from the Namurian of Arran, Scotland

    Palaeontology

    (1979)
  • D.E.G. Briggs et al.

    Arthropleura trails from the Westphalian of eastern Canada

    Palaeontology

    (1984)
  • J.J. Burke

    Notes on the morphology of Acantherpestes (Myriapoda, Archipolypoda) with the description of a new species from the Pennsylvania of West Virginia

    Kirtlandia

    (1973)
  • J.J. Burke

    A new millipede genus, Myriacantherpestes, (Diplopoda, Archipolypoda) and a new species, Myriacantherpestes bradebirksi, from the English coal measures

    Kirtlandia

    (1979)
  • T.D.A. Cockerell

    Arthropods in Burmese amber

    Psyche

    (1917)
  • W. Dohle

    Sind die Myriapoden eine monophyletische Gruppe? Eine Diskussion der Verwandtschaftsbeziehungen der Antennaten

    Abhandlungen des Naturwissenschaftlichen Vereins in Hamburg

    (1980)
  • W. Dohle

    Phylogenetic pathways in the Chilopoda

    Bijdragen tot de Dierkunde

    (1985)
  • Dohle, W., 1990. Some observations on morphology and affinities of Craterostigmus tasmanianus (Chilopoda), in: Minelli,...
  • W. Dohle

    Myriapod-insect relationships as opposed to an insect-crustacean sister group relationship

  • Dohle, W., 2001. Are the insects terrestrial crustaceans? A discussion of some new facts and arguments and the proposal...
  • S.K. Donovan et al.

    Unusual preservation of late Quaternary millipedes from Jamaica

    Lethaia

    (1994)
  • H. Dove et al.

    Comparative analysis of neurogenesis in the myriapod Glomeris marginata (Diplopoda) suggests more similarities to chelicerates than to insects

    Development

    (2004)
  • I.J. Duncan et al.

    Three-dimensionally mineralized insects and millipedes from the Tertiary of Riversleigh, Queensland, Australia

    Palaeontology

    (1998)
  • J. Dzik

    Results of the Polish-Mongolian paleontological expeditions–Part VI. Spiroboloid millipedes from the Late Cretaceous of the Gobi Desert, Mongolia

    Paleontologica Polonica

    (1975)
  • J. Dzik

    An early Triassic millipede from Siberia and its evolutionary significance

    Neues Jahrbuch der Geologie und Paläontologie Monatshefte

    (1981)
  • G.D. Edgecombe

    Morphological data, extant Myriapoda, and the myriapod stem-group

    Contributions to Zoology

    (2004)
  • G.D. Edgecombe et al.

    Myriapod phylogeny and the relationships of Chilopoda

  • G.D. Edgecombe et al.

    Adding mitochondrial sequence data (16S rRNA and cytochrome c oxidase subunit I) to the phylogeny of centipedes (Myriapoda, Chilopoda): an analysis of morphology and four molecular loci

    Journal of Zoological Systematics and Evolutionary Research

    (2004)
  • Edgecombe, G.D., Giribet, G., Wheeler, W.C., 1999. Phylogeny of Chilopoda: Combining 18S and 28S rRNA sequences and...
  • G.D. Edgecombe et al.

    Phylogeny of Henicopidae (Chilopoda: Lithobiomorpha): a combined analysis of morphology and five molecular loci

    Systematic Entomology

    (2002)
  • G.D. Edgecombe et al.

    A geophilomorph centipede (Chilopoda) from La Buzinie amber (Late Cretaceous: Cenomanian), SW France

    Geodiversitas

    (2009)
  • H. Enghoff

    Phylogeny of millipedes: a cladistic analysis. Zeitcschrift für Zoologie

    Systematik und Evolutionsforschung

    (1984)
  • S.R. Fayers et al.

    A review of the palaeoenvironments and biota of the Windyfield chert. Transactions of the Royal Society of Edinburgh

    Earth Sciences

    (2003)
  • S.R. Fayers et al.

    A hexapod from the early Devonian Windyfield Chert, Rhynie, Scotland

    Palaeontology

    (2005)
  • Y.-H. Gai et al.

    Myriapod monophyly and relationships among myriapod classes based on nearly complete 28S and 18S rDNA sequences

    Zoological Science

    (2006)
  • Y. Gai et al.

    The complete mitochondrial genome of Symphylella sp. (Myriapoda: Symphyla): extensive gene order rearrangement and evidence in favour of Progoneata

    Molecular Phylogenetics and Evolution

    (2008)
  • G. Giribet et al.

    Conflict between data sets and phylogeny of centipedes: an analysis based on seven genes and morphology

    Proceedings of the Royal Society B

    (2006)
  • G. Giribet et al.

    Internal phylogeny of the Chilopoda (Myriapoda, Arthropoda) using complete 18S rDNA and partial 28S rDNA sequences

    Philosophical Transactions of the Royal Society of London

    (1999)
  • Giribet, G., Richter, S., Edgecombe, G.D., Wheeler, W.C., 2005. The position of crustaceans within Arthropoda –...
  • Cited by (0)

    View full text