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The Pattern of Distal-Less Expression Inthe Mouthparts Ofcrusta- Ceans, Myriapods and Insects: New Evidence for a Gnathobasic Ma

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The Pattern of Distal-Less Expression Inthe Mouthparts Ofcrusta- Ceans, Myriapods and Insects: New Evidence for a Gnathobasic Ma Int..I. De.. BioI. ~2: 801-810 (1998) Original A rtiele The pattern of Distal-less expression in the mouthparts of crusta- ceans, myriapods and insects: new evidence for a gnathobasic mandible and the common origin of Mandibulata GERHARD SCHOLTZ,.3" BEATE MITTMANN'.3 and MATTHIAS GERBERDING3 'Australian Institute of Marine Science, Townsville Mail Centre, Queensland, Australia, 2Albert-Ludwigs-Universitat Freiburg, Institur fur Biologie I (Zo%gie), Freiburg, and 3Humboldt-Universitat zu Berlin, Institut fur 8i%gie, Vergleichende Zo%gie, Berlin, Germany ABSTRACT We examined embryos of representatives of crustaceans, myriapods and insects with respect to 011 expression in the mouthparts. In order to examine the relationships between mandibular Dllexpression and the occurrence of a mandibular palp we compared amphipod, isopod and decapod crustacean species. In species with mandibular palps, 011expression is maintained throughout development and is restricted to the palps. The species lacking a palp as an adult show only transient 011 expression in early embryonic stages. Furthermore, we studied mandibular 011 expression in the myriapod Glomer;s marg;nata that lacks like all myriapods mandibular palps as an adult. The expression pattern is similar to that in crustaceans lacking a palp as an adult. We examined entognathous and ectognathous insects. No sign of mandibular expression could be detected. It is shown that the distal parts of the mandibular appendage were reduced in several steps and lineages independently up to a total loss. Furthermore, we studied 011expression in the first and second maxillae. Except for Glomer;s and the collembolans, the first maxillae of all species show a similar pattern of three lobes expressing 011:the outer expression marks the maxillary palp and the inner two mark the outgrowing endites Igalea and lacinia of insects}. In the first maxillae of collembolans only two expression areas could be detected. In pal pless adult first maxillae of isopod crustaceans a transitory embryonic palp occurs which is also 011positive. In the second maxillae of insects, isopod and amphipod crustaceans only two OIl-positive lobes occur. Our data suggest a gnathobasic character of the mandibles of crustaceans, my ria pods and insects support- ing the monophyly of Mandibulata sensu Snodgrass. The interpretation of 011expression patterns and its limits are critically evaluated. KEY WORDS: mandibles, maxillae, arthropods, limb development, evolution Introduction These views are based on the claim of homology for these particular appendage Iypes. In the case of Ihe mandibles Ihe The nature, evolutionary origin and homology of arthropod specific similarities are seen in the segmental position in the head appendages have always been a matter of controversy. Some long and in the overall morphology (molar, incisivus). Furthermore, standing questions concern the relationship of annelid parapodia mandibles are interpreted as being enlarged proximal parts and arthropod legs, the question of the ground-patternof the (coxopodite) with the distal parts (telopodite) being eilher reduced arthropod leg, or the origin of the labrum and other non leg-like to a palp (some crustaceans) or completely absenl (some crusta- appendages from segmental arthropodia (Lauterbach, 1978; ceans, all myriapods and insects). According to this view, biting is Walossek, 1993; Scholtz, 1995,1997; Fryer, 1997; Kukalova- generally done with the inner margin of the enlarged coxopodite Peck, 1997). In some cases the specific characteristics of append- (gnathobasic mandible) (Snodgrass, 1938; Lauterbach, 1972; ages have been used to establish monophyletic groups, for exam- Boudreaux, 1987; Wagele, 1993). However, authors such as ple the chelicera forthe Chelicerata (Xiphosura, Pantopoda, Arach- nida) (Heymons, 1901) or the mandible and maxillae for the Mandibulata (crustaceans, insects, myriapods) (Snodgrass, 1938). AbbreuiatiuTUllSl'd in this paper: 011 . Distal-less. -Address for reprints: Humboldt-Universitat zu Berlin, Institut fUr Biologie, Vergleichende Zoologie, Philippstr. 13, D-10115 Berlin. Germany. FAX: 49-30-2093- 6002. e-mail: gerhard:[email protected] 0214-6282/98/$10.00 <!)UBC Pre" Printed in Spain -- 802 G. Scholtz et al. Fig. 1. Dllexpression in the nauplius larvae of the decapod crustacean Penaeus monodon. (A) First nauplius with Off expression in the distal parts of first and second antennae (aI, a2) and in the branches afrhe biramous mandi- bles (mdJ, In addition 011expression is seen in the brain anlage (b), in the forming labrum (lb), and rhe telson (t). 181 Same preparation as in A. counterstained to show the morphol. ogy. No structures for feeding are formed in the mandibles. ICI Last metanaupliusstage. Theproximalparts of the mandibles are enlarged forming the prospective gnathal elements. The first and second maxillae (mx1, mx2) express DfJin the distal parts as well as in the inner lobes_ ID) Same prepara- tion as in C, counterstamed to show the morphology. Manton (1964.1973) and Fryer (1996) doubt mandible homology. Recently, the expression patterns of the gene Distal-less (011) They agree that crustaceans mandibles are gnathobasic but they have provoked a new discussion of the long standing questions of claim that the mandibles of myriapods and insects represent whole arthropod limb homologies. The expression pattern of Ollhas been limbs and biting is done with the tips (whole-limb mandible). In used to analyze leg formation and evolution in representatives of conclusion, these authors do not accept Mandibulata as a valid crustaceans, insects, myriapods. and chelicerates (Panganiban et taxon but suggest an independent origin of myriapods and insects al., 1994,1995; Popadic et al., 1996; Williams and Nagy, 1996; (Uniramia) on the one hand, and crustaceans on the other hand. Niwa et al., 1997; Rogers and Kaufman, 1997; Scholtz and More recently. similar ideas have been stressed by Brusca and Gerberding, 1997; Williams, 1998). From experiments with Dro- Brusca (1990) and Kraus and Kraus (1994). These authors claim sophila embryos and larvae it has been shown that Oltplays a key that the whole-limb mandible is a synapomorphy of myriapods and role in the differentiation of appendages (Cohen and JOrgens, insects but they do not deny the monophyly of the Mandibulata, 1989a,b). Moreover, it has been suggested that 011expression including the Crustacea. Kraus (1997) modified this view suggest- marks the telopodite of arthropod legs (Gonzalez-Crespo and ing that insect and myriapod mandibles are not composed of the Morata, 1996; Niwa et at. 1997). If this assumption is correct one whole limb but of three basal limb segments with the most distal would expect that in a gnathobasic mandible no 01/ expression one forming the biting and chewing parts (telognathic mandible). occurs whereas the tip of a whole-limb mandible should express The question of homology between crustacean, insect and myriapod 011.A striking result of many of these investigations is that there is mandibles has also been raised by arthropod phylogenies based no 01/ expression in the mandibles of any insect examined. From on molecular characters or paleontological data because in some this absence of mandibular 01/ expression it was concluded that cases the mandibulates are not monophyletic (e.g., Friedrich and insects possess a gnathobasic mandible (Panganiban et al., Tautz, 1995; Wills et a/., 1995). 1994,1995; Popadic et al. 1996; Niwa et al., 1997; Rogers and DIl expression in crustaceans, myriapods and insects 803 Kaufman, 1997). Popadic el a/. (1996) went so far as to suggest us with a model for a putative loss of distal structures (palps?) in that the absence of mandibular 011expression they found in an myriapod and insect mandibles? Do all insects, even entognathans, isopod crustacean is indicative of a close crustacean.insect rela- share the total absence of mandibular Ollexpression? In addition we tionship. However, there are some inconsistencies with either analyze the 011expression pattern in the first and second maxillae of classical model (Snodgrass or Manton). Some crustacean larvae the species investigated. In the discussion we draw conclusions and embryos show mandibular 011expression while others do not concerning mandibulate monophyly and evolution. Furthermore, we (Panganiban el al., 1995; Popadic el al., 1996). Furthermore, 011 discuss a putative twofold function of the 011gene. expression is seen in the mandibles of myriapods (Popadic et aI., 1996; Grenier el al., 1997). Also 011expression is not restricted to Results distal leg structures in all cases. Dllexpression was found in clearly proximal elements such as the endites (galea, lacinia) of insect Crustaceans maxillae (Williams and Nagy, 1996; Niwa el al., 1997; Rogers and The development of the decapod crustacean Penaeus monodon Kaufman, 1997) and in the basal parts of the phyllopodous legs of is characterized by several larval stages (Fig. 1). During late crustaceans (panganiban el al., 1995; Williams, 1998). Therefore, embryonic development 011is expressed in the buds of the two conclusions concerning phylogenetic relationships among pairs of antennae and the mandibles. The earliest post-embryonic mandibulates orthe interpretation of the occurrence of gnathobasic stage is the naupfius larva comprising the three anteriormost or whole limb mandibles based on the available data of 011 segments and their appendages, the first antennal segment, the expression seem to be precocious. second
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