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04 Hoeg Proof Final Version Web.Indd ZOBODAT - www.zobodat.at Zoologisch-Botanische Datenbank/Zoological-Botanical Database Digitale Literatur/Digital Literature Zeitschrift/Journal: Arthropod Systematics and Phylogeny Jahr/Year: 2009 Band/Volume: 67 Autor(en)/Author(s): Hoeg J.T., Pérez- Losada Marcos, Glenner Henrik, Kolbasov Gregory A., Crandall Keith A. Artikel/Article: Evolution of Morphology, Ontogeny and Life Cycles within the Crustacea Thecostraca 199-217 Arthropod Systematics & Phylogeny 199 67 (2) 199 – 217 © Museum für Tierkunde Dresden, eISSN 1864-8312, 25.8.2009 Evolution of Morphology, Ontogeny and Life Cycles within the Crustacea Thecostraca JENS T. HØEG 1 *, MARCOS PÉREZ-LOSADA 2, HENRIK GLENNER 3, GREGORY A. KOLBASOV 4 & KEITH A. CRANDALL 5 1 Comparative Zoology, Department of Biology, University of Copenhagen, Universitetsparken 15, 2100 Copenhagen, Denmark [[email protected]] 2 CIBIO, Centro de Investigação em Biodiversidade e Recursos Genéticos, Universidade do Porto, Campus Agrário de Vairão, 4485-661 Vairão, Portugal 3 Marine Organismal Biology, Department of Biology, University of Bergen, Box 7803, 5020 Bergen, Norway 4 Department of Invertebrate Zoology, White Sea Biological Station, Biological Faculty, Moscow State University, Moscow 119899, Russia 5 Department of Biology & Monte L. Bean Life Science Museum, Brigham Young University, Provo, Utah, 84602-5181, USA * Corresponding author Received 16.iii.2009, accepted 8.vi.2009. Published online at www.arthropod-systematics.de on 25.viii.2009. > Abstract We use a previously published phylogenetic analysis of the Thecostraca to trace character evolution in the major lineages of the taxon. The phylogeny was based on both molecular (6,244 sites from 18S rna, 28S rna and H3 genes) and 41 larval morphological characters with broad taxon sampling across the Facetotecta (7 spp.), Ascothoracida (5 spp.), and Cirripedia (3 acrothoracican, 25 rhizocephalan and 39 thoracican spp.). Morphological apomorphies are identifi ed in larval morpho- logy for almost all major branches within the Thecostraca. Characters from the cypris larva provide a long suite of apomor- phies for the Cirripedia and reinforce the concept that this larva was a prerequisite to the tremendous success of that taxon. The evolution of parasitism, obligatory in three major taxa, is discussed. We conclude that the last common ancestor to the Cirripedia was most likely a suspension feeder, and the advanced metamorphosis and endoparasitism known from the Rhizocephala and strongly indicated for the Facetotecta are the result of convergent evolution. We also discuss reproductive systems, which range from separate sexes, over hermaphrodites combined with a separate male sex (androdioecy), to pure hermaphroditism. It is concluded, as envisaged by Darwin, that the Thecostraca provide excellent opportunities for studying the evolution of a wide range of complex life history traits which can now be better analyzed and understood in a robust phylogenetic framework. > Key words Phylogeny, parasitology, metamorphosis, sessility, larval biology, nauplius, cyprid. 1. Introduction The taxon Thecostraca (class or subclass) encompasses relationships to discuss morphological and life history three major groups: the Cirripedia, the Ascothoracida trends in the different lineages. and the Facetotecta (MARTIN & DAVIS 2001). Due to The modern concept of the Thecostraca was not evolving ideas of relationships and taxonomy within conceived until GRYGIER (1987a) but has nevertheless these groups, we do not use absolute rank in this pa- won almost universal acceptance and is reproduced in per; rather, we discuss relationships of these taxa only most text books (BRUSCA & BRUSCA 2002; RUPPERT et in terms of relationships of lineages. We then use these al. 2004). While the monophyly of the Thecostraca is 200 HØEG et al.: Evolution of Thecostraca rarely challenged, it has been particularly diffi cult to basic arthropod traits (GRYGIER 1996a; GRYGIER & analyze the intrinsic phylogeny of the taxon, because HØEG 2005). it is one of the most variable groups within all Crus- The Facetotecta were known until recently only as tacea. This variability, present both within and among pelagic nauplius and cypris larvae of type ‘y’ (GRYGIER the three major lineages, concerns ontogeny, adult 1996b). But GLENNER et al. (2008) managed to induce morphology, mode of life and especially the repro- metamorphosis of the y-cyprid stage and obtained ductive systems, and it renders the Thecostraca excel- results indicating that the adult is a highly modifi ed lently suited for studying and testing theories on the parasite with early endoparasitic stages that bear a re- evolution of a host of biological traits. markable resemblance to those found in the life cycle All thecostracans are sessile as adults. The lar- of rhizocephalan cirripedes. This, and the general un- val development normally comprises a series of pe- certainty about thecostracan phylogeny, puts special lagic nauplii and is terminated by the cypridoid stage, emphasis on tracing the evolution of parasitism within which is specialized for attaching to a substratum and this taxon (PÉREZ-LOSADA et al. 2009). initiating the juvenile phase. Following HØEG et al. As a further complication, the Tantulocarida are (2004), the cypridoid stage is called ‘y-cyprid’ in the often mentioned as the most likely sister group to Facetotecta, ‘a-cyprid’ in the Ascothoracida and sim- the Thecostraca. The tantulocarids are also highly ply ‘cyprid’ in the Cirripedia (Electronic Supplement advanced parasites and, especially given the lack of video clip 1). knowledge about facetotectan adults, it cannot be ex- cluded that they are nested somewhere within the The- The Cirripedia (barnacles) comprises the Acro- costraca (BOXSHALL 2005a). thoracica (burrowing barnacles), the Rhizocephala (parasitic barnacles) and the Thoracica (pedunculated and sessile barnacles). Like all other thecostracans, cirripedes are sessile as adults (ANDERSON 1994). The 2. Variation within the Thecostraca acrothoracicans and thoracicans have become special- ized suspension feeders, using their six pairs of highly modifi ed thoracopods (cirri) as a highly specialized 2.1. Larval development basket for food capture. As a consequence, they con- tain modifi cations in the orientation of the body and Details of larval development vary both among and the entire morphology. The acrothoracicans burrow within the major taxa. The cypridoid stage is always into calcareous substrata, but most thoracicans are non-feeding. In the Thoracica, most species have freely exposed, and their body is more or less com- planktotrophic nauplii, but lecitotrophy is prevalent or pletely armed by a system of mineralized shell plates. obligatory in several families such as the Scalpellidae. Thoracicans therefore sport a highly modifi ed mode All Rhizocephala and Acrothoracica have lecitotroph- of moulting and growth, and Louis Agassiz is alleged ic nauplii. This is also the prevalent mode of devel- to have described them as “Nothing but a tiny little opment in the Ascothoracida and the Facetotecta, but shrimp-like animal, standing on its head in a lime both these taxa also have species with planktotrophic stone house and kicking food into its mouth” (RUPPERT nauplii. There is accordingly no obligatory link be- & BARNES 1994). The Rhizocephala are all parasitic, tween parasitism and naupliar mode of feeding in the their hosts being other Crustacea. The adult, devel- Thecostraca. Some ascothoracids and cirripedes have oping from an internal parasitic phase, is highly re- an abbreviated development. In the Thecostraca many duced and has lost almost all arthropod traits such as taxa have six naupliar instars just as in the Copepoda, segmentation and appendages. But within this highly so this could be the ground pattern, but some forms, modifi ed body morphology, adult rhizocephalans dis- such as the Rhizocephala, have only fi ve or four. There play a remarkable morphological variation includ- is no obligatory relation between numbers of instars or ing forms where multiple parasites are produced by feeding mode and the duration of the naupliar phase asexual budding from a common internal system of as shown by some cold water rhizocephalans that use rootlets, a situation unique in the Arthropoda. The only almost 30 days to reach the cyprid stage (WALOSSEK et morphological evidence that the Rhizocephala belong al. 1996). Pelagic nauplii are absent in many groups. to the Cirripedia comes from the development of the In the Cirripedia this seems always to involve larvae larvae (THOMPSON 1836; HØEG & MØLLER 2006). hatching as cyprids, but in the Ascothoracida some The Ascothoracida are also parasites, but the least species seem to brood the hatched nauplii in the mantle modifi ed members of the taxon have a morphology cavity and later release them as a-cyprids. As a further with few if any obvious adaptations to this mode of complication, some ascothoracids have two consecu- life. More advanced forms can be extensively modi- tive a-cyprid stages, with only the latter performing fi ed to parasitism although they always retain some settlement on the host (KOLBASOV et al. 2007). Finally, Arthropod Systematics & Phylogeny 67 (2) 201 A B Fig. 1. Metamorphosis in the Cirripedia Thoracica. Recently settled, but fully metamorphosed specimens. A: Lepas sp., presum- ably L. pectinata. Note the distinct similarity with a cypris larva although the appearance of annulated cirri and a true peduncle are clear post-metamorphic traits.
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