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Hexapod-Crustacean Relationships and the Phylogeny of Crustacea**

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Hexapod-Crustacean Relationships and the Phylogeny of Crustacea** Org. Divers. Evol. 2, 217–237 (2002) © Urban & Fischer Verlag http://www.urbanfischer.de/journals/ode The Tetraconata concept: hexapod-crustacean relationships and the phylogeny of Crustacea** Stefan Richter* Institut für Biologie, Humboldt-Universität zu Berlin, Germany Received 3 March 2002 · Accepted 5 August 2002 Abstract A growing body of evidence indicates that Crustacea and Hexapoda are sister groups, rather than Hexapoda and Myriapoda. Some recent molecular data even suggest that Mandibulata is not monophyletic, with Myriapoda and Chelicerata instead being sister groups. Here, argu- ments for homology of the mandible throughout mandibulate arthropods and for a monophyletic Mandibulata will be presented, as well as ar- guments supporting the taxon Tetraconata (i.e. Crustacea + Hexapoda).The latter include molecular data (nuclear and mitochondrial ribosomal RNAs and protein coding genes), and morphological characters such as ommatidial structure, the presence of neuroblasts and a very similar ax- onogenesis of pioneer neurons. However, crustaceans are insufficiently sampled for the molecular data, and studies of neurogenesis are lacking for many crustacean taxa. Remipedia, Cephalocarida and Maxillopoda are particularly problematic.This is important for the entire problem, be- cause monophyly of the Crustacea has not yet been proven beyond doubt and several molecular analyses suggest a paraphyletic Crustacea. Here, arguments for the monophyly of the Crustacea are reviewed and two alternatives for the relationships between the five higher taxa Remi- pedia, Cephalocarida, Maxillopoda, Branchiopoda and Malacostraca are discussed: the Entomostraca concept sensu Walossek with Malacos- traca as sister group to Cephalocarida, Maxillopoda and Branchiopoda, and the Thoracopoda concept sensu Hessler with Cephalocarida, Bran- chiopoda and Malacostraca forming a monophylum. Key words: Pancrustacea, Distal-less, epipod, compound eye, optic neuropils, proventriculus Introduction Beginning in the early 1990s, an increasing number of studies using molecular data (Turbeville et al. 1991, For many decades it was generally accepted that Ballard et al. 1992, Adoutte & Philippe 1993, Friedrich Hexapoda and Myriapoda are sister groups forming the & Tautz 1995; for later references see below) have sug- monophylum Antennata or Atelocerata (e.g., Kraus & gested a sister group relationship between Crustacea and Kraus 1994, Kraus 1998, 2001, Kristensen 1998). Char- Hexapoda. This relationship also found support from acters such as the absence of appendages at the inter- different morphological character complexes (Averof & calary segment, the tentorial cephalic endoskeleton, the Akam 1995, Osorio et al. 1995, Whitington 1995). Quite ectodermal malpighian tubules and postantennular or- a few reviews have already been published, dealing with gans support this relationship (see, for example, Klass & different character complexes (Dohle 1997, 1998, 2001, Kristensen 2001 for a detailed review). Whether Myri- Klass & Kristensen 2001, Kraus 2001, Deutsch 2001, apoda is a monophyletic taxon (e.g., Ax 1999, Edge- Simpson 2001). A monophylum combining Crustacea combe & Giribet 2002), or whether it is paraphyletic and Hexapoda was introduced as Pancrustacea (Zrzav´y with the Progoneata as sister group to the Hexapoda & Stysˇ 1997) and has been renamed Tetraconata by (e.g., Dohle 1980, Kraus & Kraus 1994, Kraus 1998, Dohle (2001) based on the shared unique structure of 2001), is an open point in the context of the Antennata ommatidia in the compound eyes. Although some of concept. these analyses explicitly suggest different crustacean *Corresponding author: Stefan Richter, Vergleichende Zoologie, Institut für Biologie, Humboldt-Universität zu Berlin, Philippstr. 13, D-10115 Berlin, Germany; e-mail: [email protected] **Paper presented at the Phylogenetic Symposium held in Bielefeld, Germany, 24/25 November 2001 1439-6092/02/02/03-217 $ 15.00/0 Org. Divers. Evol. (2002) 2, 217–237 218 Richter taxa as sister group of the Hexapoda, implying a para- plays an important role in arthropod limb development phyletic Crustacea, the phylogenetic relationships of the and is expressed in distal parts of arthropod appendages – Crustacea and within them were not the focus of most of support homology of the mandibles (e.g., Panganiban et the studies and recent reviews dealing with the Pancrus- al. 1995, Popadic et al. 1996, 1998, Scholtz et al. 1998, tacea/Tetraconata concept (but see Schram & Jenner reviewed by Scholtz 2001). 2001). Scholtz et al. (1998) studied the Dll expression of sev- The main issue of this review is to present the argu- eral arthropods including malacostracan crustaceans, ments for a sister group relationship between Hexapoda myriapods and hexapods. In the amphipod Gammarus and Crustacea with the phylogeny of the Crustacea as pulex, which develops a mandibular palp, Dll expression background. It will be shown that most characters sup- appears in the early limb bud but in more advanced porting the Tetraconata are only known for some of the stages it is restricted to the region of the outgrowth of the crustacean taxa. In the present paper I adopt as a work- mandibular palp. In those malacostracan crustaceans ing hypothesis that Myriapoda is monophyletic, based which do not possess a palp, such as the terrestrial iso- on the evidence presented by Edgecombe & Giribet pod Porcellio scaber or the amphipod Orchestia cavi- (2002), although this monophyly has been questioned mana, Dll expression starts early, but during develop- repeatedly in the context of the Atelocerata concept ment of the limb bud the expression is restricted to an (e.g., Dohle 1980, Kraus & Kraus 1994, Kraus 1998, area that can be interpreted as a vestigial anlage of the 2001). The Hexapoda is a well established monophylum palp. The same expression pattern can be found in the (e.g., Kristensen 1998). diplopod Glomeris marginata where also only a tempo- Not only are relationships within the Mandibulata rary expression of Dll in a lateral position is present. under debate, but Mandibulata itself has been chal- This expression can also be interpreted as the vestigial lenged several times. Old concepts such as the Schizo- anlage of a palp. This implies that also in adult Myriapo- ramia include Crustacea and Chelicerata but exclude da (at least Diplopoda) no distal parts of the mandible Myriapoda and Hexapoda (e.g., Cisne 1974, Bergström are present, and therefore a whole-limb mandible does 1980), and the Uniramia concept includes Onychophora, not exist. In the studied hexapods, Dll expression is to- Myriapoda and Hexapoda, but excludes Crustacea (e.g., tally absent, indicating the lack of even a vestige of a Manton 1973, 1977). Some recent molecular studies palp (e.g., Panganiban et al. 1995, Popadic et al. 1996, also favour the non-monophyly of the Mandibulata, and 1998, Scholtz et al. 1998). Therefore, the expression pat- a sister group relationship between Myriapoda and Che- tern of Dll strongly supports the hypothesis that myria- licerata is postulated (Friedrich & Tautz 1995, Cook et pod and hexapod mandibles are gnathobasic. This re- al. 2001, Hwang et al. 2001, Kusche & Burmester 2001, ceives some additional support from the expression of but see Kusche et al. 2002 supporting a monophyletic dachshund in the beetle Tribolium castaneum (see Prpic Mandibulata). Therefore, it seems justified to deal with a et al. 2001). Based on the similarity in size and expres- few aspects of mandibulate monophyly. sion of dachshund in all three gnathal appendages in em- bryos mutant for Tc’ Dll, the authors argued for a serial homology of the entire mandible with the coxal parts of Discussion maxilla and labium, and the coxae of the legs. Although we have convincing evidence for gnathoba- Monophyly of the Mandibulata sic mandibles in all mandibulate groups, we still have to At least four characters support the monophyly of the ask whether the gnathal part of the mandibles in Myri- Mandibulata (comprising Myriapoda, Crustacea, and apoda, Hexapoda and Crustacea is formed by a homolo- Hexapoda): the mandible, the 1st maxilla, ommatidia with gous part of the proximal portion. In Crustacea the crystalline cones (or precursors), and a moulting gland mandibular gnathal edge is formed by the coxa which is (e.g., Wägele 1993, Ax 1999). Here, I will focus only on obvious in examples where both parts of the protopod the character ‘mandible’. There is increasing evidence (coxa and basis) as well as endopod and exopod are pre- that not only crustacean mandibles are gnathobasic, but sent, such as in copepods (e.g., Gruner 1993). In cases also those of hexapods and myriapods (e.g., Lauterbach where no palp is present (even in early developmental 1972, Wägele 1993, Bitsch 2001b), rather than the latter stages), such as in myriapods and hexapods, no defini- being whole-limb mandibles (e.g., Manton 1964, Fryer tive decision can be made. According to Walossek 1996, Kraus & Kraus 1994). This means that the gnathal (1993, 1999), the coxa of certain crustacean legs has its edge is always formed by a process of the proximal part, origin in a so-called ‘proximal endite’, a lobate endite at and not by more distal parts of the mandible. As is the the inner proximal edge of the basipodite which is not case in several crustaceans, the mandibular palp would present in chelicerates. The proximal portion of the che- have been reduced in myriapods and hexapods. Recent licerate legs is therefore suggested as being homologous
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