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Larval Development of the Tropical Deep-Sea Echinoid Aspidodiademajacobyi: Phylogenetic Implications

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Larval Development of the Tropical Deep-Sea Echinoid Aspidodiademajacobyi: Phylogenetic Implications FAU Institutional Repository http://purl.fcla.edu/fau/fauir This paper was submitted by the faculty of FAU’s Harbor Branch Oceanographic Institute. Notice: ©2000 Marine Biological Laboratory. The final published version of this manuscript is available at http://www.biolbull.org/. This article may be cited as: Young, C. M., & George, S. B. (2000). Larval development of the tropical deep‐sea echinoid Aspidodiadema jacobyi: phylogenetic implications. The Biological Bulletin, 198(3), 387‐395. Reference: Biol. Bull. 198: 387-395. (June 2000) Larval Development of the Tropical Deep-Sea Echinoid Aspidodiademajacobyi: Phylogenetic Implications CRAIG M. YOUNG* AND SOPHIE B. GEORGEt Division of Marine Science, Harbor Branch Oceanographic Institution, 5600 U.S. Hwy. 1 N., Ft. Pierce, Florida 34946 Abstract. The complete larval development of an echi- Introduction noid in the family Aspidodiadematidaeis described for the first time from in vitro cultures of Aspidodiademajacobyi, Larval developmental mode has been inferredfrom egg a bathyal species from the Bahamian Slope. Over a period size for a large numberof echinodermspecies from the deep of 5 months, embryos grew from small (98-,um) eggs to sea, but only a few of these have been culturedinto the early very large (3071-pum)and complex planktotrophicechino- larval stages (Prouho, 1888; Mortensen, 1921; Young and pluteus larvae. The fully developed larva has five pairs of Cameron, 1989; Young et al., 1989), and no complete red-pigmented arms (preoral, anterolateral,postoral, pos- ontogenetic sequence of larval development has been pub- lished for invertebrate.One of the terodorsal,and posterolateral);fenestrated triangular plates any deep-sea species whose have been described et at the bases of fenestratedpostoral and posterodorsalarms; early stages (Young al., 1989) is a small-bodied sea urchin with a complex dorsal arch; posterodorsalvibratile lobes; a ring Aspidodiademajacobyi, flexible that lives at in the of cilia around the region of the preoral and anterolateral long spines bathyal depths eastern Atlantic 1). The of arms; and a long, unpaired posterior process containing a tropical (Fig. early development A. jacobyi is unusual in that its small (94-100 ,um) fenestrated rod. The presence of a posterior process and eggs contain sufficient yolk reserves to support a posterodorsalarms makes the larva of Aspidodiademaja- prefeeding developmentalperiod that extends well into the larval stage cobyi much more similarto larvaeof irregularurchins in the (Young et al., 1989), a feature that might permit larvae to order Spatangoideathan to other families of the order Dia- move long distances,either verticallyor horizontally,before dematoida, to which the family is normally assigned. This feeding becomes necessary. In this paper, we describe the unexpected larval form lends supportto a recommendation complete larval development of A. jacobyi, document un- that the Aspidodiadematidaeshould be either elevated to expected morphological traits in the late-stage larvae, and ordinalstatus as a sister group of the orderDiadematoida, or discuss how these unexpected traits could help justify a split off as a sister of the other families within the group realignment of the currently accepted ordinal-level taxon- order. In either if we the case, accept parsimonioushypoth- omy of the Euechinoidea. esis that the aboral and arms were process posterodorsal The echinoid family Aspidodiadematidaecontains only derived once in the of euechi- only evolutionary history two genera, Aspidodiademaand Plesiodiadema, all species noids, then the larval data that the suggest Aspidodiadema- of which are found at bathyal and abyssal depths (Hyman, tidae be near the node where may very the irregularand 1955), many on island slopes in tropical seas. On the basis regular euechinoids first diverged. of adult characters, notably aulodont teeth and hollow spines, Mortensen (1927) placed the family in the order Diadematoida,suborder Aulodonta, in the company of the Received 8 December 1999; accepted 1 February2000. * the and the Author for correspondence.E-mail: [email protected] Echinothuriidae, Pedinidae, Diadematidae.Re- t Present address: Biology Department,Georgia Southern University, cent authors (e.g., Smith, 1984) have elevated the echi- Statesboro, GA 30460. nothuriidsand pedinids to ordinal level, placing three fam- 387 388 C. M. YOUNG AND S. B. GEORGE the present paper, we confirm Emlet's prediction concern- ing the presence of posterodorsalarms in the Aspidodiade- matidaeand documentother larval characterssupporting the idea that this family of urchinsmay have originatednear the node where the regular and irregularurchins diverged. Materials and Methods Adult Aspidodiademajacobyi were collected by suction using Johnson-Sea-Link submersibles between depths of 500 and 750 m at various sites in the Northern Bahamas Figure 1. Adult Aspidodiademajacobyi from the Bahamian Slope, (Young, 1992). They were transportedto the surface in flexible L. F. showing long spines. (Photo by Braithwaite). closed acrylic containers of seawater and transferredto 14?C incubatorswithin minutes of arriving at the surface. ilies in the order Diadematoida: the Aspidodiadematidae, Although we collected this species duringthe springmonths the Diadematidae,and the Lissodiadematidae.Larvae of the of every year from 1985 through 1999, we were able to Lissodiadematidaeremain unknown (Emlet, 1988a; Pearse induce spawning only twice, once in 1987 (Young et al,, and Cameron, 1991). Emlet (1988a) has arguedon the basis 1989) and once on 11 April 1994. Spawning was inducedby of larval form that the Micropygidae,which have also been intracoelomicinjection of 0.55 M KC1.In the 1994 spawn- raised to ordinal status by Jensen (1981), should also be ing, we injected 28 individuals; of these, 13 males and 2 includedas a family in the Diadematoida.Although it seems females released gametes. Cultures were established by clear that the aspidodiadematidsare closely related to the mixing the eggs of a single female with active sperm from diadematoids,the relationships among orders and families 6 males in a small bowl of seawater. The other female was near the base of the euechinoid tree remain obscure. This not used because she released very few oocytes, many of portion of the tree remains inadequatelyresolved because a which appearedirregular. Zygotes were split among five 1-1 thorough cladistic analysis of extant species has not been jars of 0.45-,am filteredseawater, at an initial density of 800 undertaken(R. Mooi, CaliforniaAcademy of Sciences, San embryos per liter. After larvae had developed complete Francisco, pers. comm.), and also because fossil material guts, they were fed with a mixture of the algae Isochrysis from the relevant time periods contains too few meaningful galbana, Thalassiosira weissflogii, and Dunaliella terti- charactersfor construction of a robust tree (A. B. Smith, olecta. At the outset, we used an algal concentration of The NaturalHistory Museum, London, pers. comm.). Fossil 1000-2000 cells/ml, but this was increased graduallyas the aspidodiadematidsclosely resembling moder urchins in larvae grew, up to a maximum of 5000 cells/ml, 49 days the genus Plesiodiadema have been described from the after fertilizationand thereafter.These algal concentrations upper Jurassic clays of England and France (Smith, 1995), were chosen because similar concentrationspromote opti- indicating that the family differentiatedmore than 200 mil- mal larval growth in some shallow-waterechinoderm larvae lion years ago. (Fenaux et al., 1985; George, 1990; George et al., 1990). By analyzingthe crystallineaxes of echinoid apical plates Larvae were reared in dark incubatorsexcept during water (Raup, 1965), Emlet (1985, 1988a) was able to infer certain changes, when they were exposed briefly to the fluorescent details of larval form for a number of rare species with overhead lights. To simulate temperature changes that unknown larvae. On the basis of this indirect evidence, he bathyal larvae would encounter if they undertook ontoge- predicted that all members of the genera Aspidodiadema netic vertical migration(Young et al., 1996a), we increased and Plesiodiadema should have larvae with both preoraland the culture temperaturefrom 14?C to 16?C 14 days after posterodorsal arms (Emlet, 1988a). This prediction is in fertilization, reduced it to 14?C 66 days after fertilization, stark contrastto the 2-arm larvae with widely spread arms then finally to 13?C (the temperaturenear the bottom of the (the "Echinopluteus transversus" of Mortensen, 1921) adult depth range) 77 days after fertilization. Initially, sea- found in all members of the closely related families Diade- water was changed and the larvae were fed every 2 days. matidae and Micropygidae. By assuming that the 2-arm This interval was increased to 4 days beginning 28 days larval form with widely spread arms is synapomorphic, after fertilization. Emlet (1988a) argues parsimoniously that the Aspidodia- Each time water was changed, we examined the larvaefor demidae must be a sister group to the Diadematoida,having the appearance of any new arms or other structures and branchedoff the major clade of regulareuechinoids earlier measured the lengths of the postoral, somatic, posterodor- than the diadematids or micropygids. Indeed, he recom- sal, and posterolateralrods. Because there were 2-day or mends that the Aspidodiadematidae should be removed 4-day intervalsbetween observations,the times for reported from the Diadematoidsand
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