375
Preliminary Phylogeny of the Forcipulatacean Asteroidea1 CHRISTOPHERL. MAH2
Department of Invertebrate Zoology, California Academy of Sciences, Golden Gate Park, San Francisco, California 94118-4599
SYNOPSIS. The superorder Forcipulatacea (Asteroidea, Echinodermata) includes two orders, the Brisingida and the Forcipulatida. The Forcipulatida is diverse, including the Asteriidae, Coscinasteriinae, Pedicellasteridae, Labidiasteridae, Neo- morphasteridae, Pycnopodiinae (Asteriidae), Heliasteridae, and the Zoroasteridae, whereas the Brisingida is limited to the Brisingasteridae, Brisingidae, Freyellidae, Hymenodiscidae, and Odinellidae. A phylogenetic analysis of forcipulataceans us- ing morphological characters resulted in 12 most parsimonious trees at a tree length of 68 steps.
The Brisingida, recognized as basal in one early analysis and derived in another, is here considered to be derived. Two genera of pedicellasterids emerged as the sister group to the remaining Forcipulatida.
Bremer and bootstrap measures show strong support for the brisingidan and zoroasterid plus neomorphasterid clades. Certain other traditional taxonomic groupings, including the Pedicellasteridae, Labidiasteridae, Asteriidae, and Pyc- nopodiinae, are not supported as monophyletic. Support for the pedicellasterids as a sister group to the remainder of the Forcipulatida is not robust.
Morphological data suggest widespread homoplasy and therefore comprehensive generic or even species-level analyses are required to further evaluate questions of derivation and relationships among these taxa.
INTRODUCTION
The Forcipulatacea comprises one of three superorders within the post-Paleozoic Asteroidea (sensu Blake, 1987). Forcipula- taceans include approximately 90 genera, and they range from the Triassic Period (Blake, 1999) to the present. Forcipulata- ceans are important in many marine com- munities (e.g., Paine et al., 1985), from rocky intertidal zones [e.g., Pisaster ochra- ceus (Asteriidae)] abyssal plains [e.g., Fre- yella elegans (Freyellidae)]. Forcipulata- ceans are morphologically diverse, ranging from very delicate to very robust in skeletal development, and possessing from five to 50 rays (Clark and Downey, 1992). Most forcipulataceans inhabit cold to temperate waters. They are a minor component of
1From the Symposium Evolution of Starfishes: Mor- phology, Molecules, Development, and Paleobiology presented to the Annual Meeting of the Society for Integrative and Comparative Biology, 6–10 January 1999, at Denver, Colorado.
2Present address: Geology Department University of Illinois 245 NHB, 1301 W. Green St., Urbana, IL 61801; E-mail: [email protected]
tropical settings such as the Indo-West Pa- cific (Blake, 1990).
Blake (1987) recognized two orders, the Brisingida and the Forcipulatida, within the Forcipulatacea. Forcipulatidans (sensu Blake, 1987) included the Zoroasteridae, the Heliasteridae, and the Asteriidae. The Brisingida includes five families and 17 genera with nearly 70 species. Mah (1997, 1998) and Downey (1986) provided recent re-evaluations of the order. The Zoroaster- idae includes 7 genera and approximately 40 species. Downey (1970) proposed ordi- nal rank for the group. Phylogenetic anal- ysis of the Zoroasteridae has never been un- dertaken. The Heliasteridae contains about 10 species, all assigned to Heliaster (H. L.
Clark, 1907). It is known today exclusively from the tropical shallow-water shelf of Mexico and South America, although a Pli- ocene occurrence from Florida has been re- corded (Jones and Portell, 1988).
A number of familial and subfamilial taxon concepts have been used for the As- teriidae sensu latu, including the Asteriinae, Labidiasterinae, Neomorphasterinae, Pedi- cellasterinae, and Pycnopodiinae. The most
important taxonomic treatments of this group are those of Fisher (1923, 1928, 1930) and more recently Clark and Downey (1992), who elevated all but the Pycnopo- diinae (Asteriidae) from subfamilial to fa- milial rank. Rankings of Clark and Downey (1992) are used here. The Coscinasteriinae, synonymized with the Asteriinae (Spencer and Wright, 1966), is separated here based on the data of Mastsuoka et al. (1994).
MATERIALS AND METHODS
Twenty-five forcipulatacean taxa were selected to broadly sample the morphology of the group and to encompass all earlier taxon concepts at the subfamilial level and above (see Appendix 3). Twenty-five char- acters (summarized in Appendix 1) were in- cluded in the data matrix (Appendix 2). Ex- emplars are from all oceans and a broad range of depths. For each higher taxon, the name-bearing genus was utilized if possi- ble. Wet and dry specimens were examined.
Where necessary, specimens were par- tially denuded using a 5% solution of so- dium hypochlorite. Characters derived from endoskeletal morphology stress the ambu- lacral, adambulacral, abactinal, and actinal ossicular series. Soft-part characters are based on tube foot row number and papular and ampullar morphology. Aspects of over- all body morphology, such as arm length and general disk morphology, were also used. Multiple rays (.5) have arisen many times (Hotchkiss, 2000) and therefore ray number was omitted, although more com- prehensive research will certainly yield use- ful characters.
Henricia leviuscula (Echinasteridae, Spi- nulosida), a partial homeomorph of many asteriids, was chosen as the outgroup. Its usage does not imply direct sister group re- lationship.
RESULTS Cladistic analysis
A branch and bound search using PAUP 4.0* was run using unpolarized and un- weighted character options. Uninformative characters (e.g., autapomorphies) were omit- ted from the matrix. The search yielded 12 most parsimonious trees each of 68 steps with a consistency index of 0.53 and a re-
scaled consistency index of 0.39. Figure 1 shows the 50% majority rule consensus tree.
Relaxation from strict consensus permits the recognition of support for some signal in branch arrangement. Node 9 shows rel- atively strong support (83%) between labi- diasterids and brisingidans. Clades above node 12 show only modest support (50%).
Bremer-support values were calculated using methods outlined by Bremer(1988) and defined by Ka¨llersjo¨ et al. (1992) using the branch and bound search algorithm.
Support was also derived from 100 boot- strap replicates using the heuristic search option. Bremer and bootstrap support mea- sures are shown in Fig. 2. Bremer support shows overall collapse above node 1 after one step (Fig. 2b). However, the brisingidan and zoroasterid clades show Bremer sup- port values of at least 3 (Fig. 2b).
Bootstrap analysis (Fig. 2a) does not sup- port the tree topology summarized by the 50% consensus tree in Fig. 1. Nodes 1 and 2 are relatively well supported by the boot- strap analysis. Four clades, the Brisingida (99%), the Coscinasteriinae (65%), the Zo- roasteridae plus Neomorphasteridae (98%), and the Asteriidae (62%) are also relatively strong branches.
DISCUSSION Previous phylogenetic hypotheses
Blake (1987) separated post-Paleozoic as- teroids into two branches, the Forcipulatacea and the Spinulosacea plus Valvatacea; this in- terpretation was consistent with that of Fisher (1923, 1928). Gale (1987) in contrast, rec- ognized the Paxillosida as the sister group to the remaining living orders, the Forcipulatida, Valvatida and, Notomyotida, in his terminol- ogy. Gale’s positioning of the Paxillosida is in keeping with views of Mortensen (1922).
Both of these studies generalized approxi- mately at the familial level.
Based on combined morphological and molecular data, the reconstruction of Lafay et al. (1995) is in general agreement with the tree topology of Gale (1987), whereas the molecular phylogeny by Wada et al., (1996) places the forcipulataceans high in the asteroid tree as the sister group to the Asterinidae. Littlewood et al., (1997) pre-
FIG. 1. 50% Majority rule consensus tree showing distribution of characters mapped onto branches. Numbers in shadow represent nodes. Plesiomorphic state (50) represented by plain numbers on branches. Apomorphies and reversals are followed by dash and character state, for example 6–2 represents character six, state two.
Percentage values represent.50% support. Asterisk (*) represents 58% support. Plus (1) represents 50% sup- port. Values represent support from consensus tree values.
sented two most parsimonious total-evi- dence trees. The first tree, including SSU rRNA data, showed a paxillosidan (Astro- pecten) as the sister to a branch containing a forcipulatacean(Asterias) and a valvatidan (Porania). The second tree included LSU rRNA data, and it showed a forcipulatacean (Asterias) as the sister taxon to a valvatidan
(Asterina) (sensu Blake, 1987) and a vela- tidan (Crossaster).
Matsuoka et al., (1994) examined genetic distance among five species of Japanese for- cipulataceans. They generated a distance tree showing Asterias amurensis (Asteriidae) and Plazaster borealis(Labidiasteridae) on one branch and Aphelasterias japonica (Cosci-
FIG. 2. Strict consensus trees expressing support val- ues. In a, only bootstrap values .50% are shown.
Numbers in shadow represent corresponding nodes from Figure 1.
nasteriinae) and Distolasterias nipon (Cos- cinasteriinae) on its sister branch. Coscinas- terias acutispina (Coscinasteriinae) was most distant from all four species. Wada et al., (1996) showed a coscinasterine (Cosci- nasterias) as the sister branch to a branch including an asteriid (Asterias) and a cosci- nasterine (Distolasterias).
The molecular phylogeny of Knott and Wray (2000) includes exemplars from the As- teriidae, Brisingida, Coscinasteriinae, Helias- teridae, Labidiasteridae, Pycnopodiinae, and Zoroasteridae. Their preliminary reconstruc- tion supports the Forcipulatacea as monophy- letic but suggests that many subfamilial and familial groupings are paraphyletic.
The inconsistencies probably reflect both incomplete taxon sampling and morpholog-
ical homoplasy derived from separate line- ages adapting to broadly similar habitats over long periods of geologic time.
Higher versus intermediate level taxon sampling
Results obtained from generic level sam- pling differ in important ways from earlier morphological treatments of Blake (1987) and Gale (1987). Brisingidans, rooted at or near the base of the tree in both Blake (1987) and Gale (1987), are here nested high in the tree, above node 10, and they are therefore considered derived. For com- parative purposes, the Brisingida were placed at the base of the tree using Mac- Clade, which added 7 steps and changed the tree topology from 69 to 76 steps. Brisin- gidans resemble labidiasterids, and the two were placed together by Perrier (1885). Ten of 12 most parsimonious trees show the la- bidiasterid clade (Fig. 1: node 11) as sister group to the Brisingida (Fig. 1: node 10), but support for this arrangement from Bre- mer and bootstrap measures was absent.
Figure 1 shows the pedicellasterid genera Ampheraster and Pedicellaster as the sister branches to the other extant forcipulata- ceans. Figure 2 does not show much sup- port from either Bremer or bootstrap mea- sures for Ampheraster or Pedicellaster as the sister clade to the Forcipulatida. How- ever, pedicellasterids were not included in earlier more broadly sampled studies (e.g., Blake, 1987; Gale, 1987), and it is impor- tant to note their inclusion in a tree topol- ogy that significantly differs from those of Blake (1987) or Gale (1987).
Paraphyly within the forcipulatacea The Forcipulatacea is monophyletic (Fig.
1), a conclusion consistent with perspec- tives extending back to Fisher (1923, 1928, 1930). Many of the historical subgroupings (e.g., the Pedicellasteridae, the Asteriidae) within the Forcipulatacea show varying de- grees of paraphyly. However, the present study, although more detailed in generic sampling than those of earlier cladistic mor- phological studies, only reaffirms rather than resolves the perplexing picture of re- lationships among the Forcipulatida.
For example, at node 11 (Fig. 1) Coron-
aster, Labidiaster, and Plazaster (Labidias- teridae) consistently group together whereas Rathbunaster (Labidiasteridae) emerges at node 12 on a branch with the Pycnopodiinae (Pycnopodia), Coscinasteriinae (Psalidaster), and Asteriidae (Lysasterias). The weakness of the groupings as tested using Bremer sup- port and bootstrap analysis suggest wide- spread homoplasy, a hypothesis not contra- dicted by the relatively low CI.
CONCLUSION
The Brisingida is a monophyletic, de- rived forcipulatacean branch. Subfamilial and familial grouping within the Forcipu- latida are paraphyletic. The apparent para- phyly of many groups within the Forcipu- latacea suggests widespread homoplasy.
Furthermore, our level of knowledge re- garding basic homologies in forcipulates is relatively poor, ontogenetic information is not well known, and an extensive, generic- level revision of the group has not been at- tempted since Fisher (1923). Results of this study suggest that many historical forcipu- latacean groupings are phylogenetically weak. Incomplete knowledge of the char- acters probably is significant.
The very differing tree topologies of this study compared to previous studies illus- trates the need for greater sampling at lower taxonomic levels. Development of a phy- logeny calls for enlarged taxon samples in both morphological and molecular work and further research on a poorly understood but significant fossil record.
ACKNOWLEDGMENTS
This paper benefited greatly from discus- sions with Daniel Blake and Rich Mooi.
My thanks to Fred Hotchkiss for allowing me to read an early draft of his manuscript.
The CAS In-House Research Funds and SICB are graciously thanked for supporting this research. My thanks to Alan Kohn, John Pearse and an anonymous reviewer for constructive comments. Stephen Downie also provided useful input. I am especially grateful to Daniel Janies and the organizing committee for inviting my contribution.
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APPENDIX1
MORPHOLOGICAL CHARACTERS
1. Pedicellarial Wreath. 0 5 wreath ab- sent; 1 5wreath absent; 2 5 sock-like sheath
2. Actinal Plates. 05absent; 15present 3. Adoral Carina. 05present; 15absent 4. Tube Foot Rows. 0 5 2 rows; 1 5 4
rows
5. Pillar on Odontophore. 0 5 absent; 1 5 present
6. Adambulacral Morphology. 0 5 co- lumnar; 1 5 compressed; 2 5 block shaped.
7. Pedicellariae Location. 0 5 associated with spines; 1 5 scattered over body surface
8. Marginal Plate Arrangement. 0 5 sin- gle; 15dimorphic; 25 identical; 35 reduced
9. Abactinal Spine Morphology. 05short spinelet; 15 short blunt; styliform 10. Pedicellariae on Adambulacral Spine. 0
5 absent; 1 5 present
11. Papulae on Actinal Surface. 0 5 pre- sent; 15 absent
12. Fleshy Body Wall. 05absent; 15ab- sent
13. Abactinal Radial Plates. 0 5 large and prominent; 1 5 indistinct; 2 5 absent
14. Ambulacral Ossicle Morphology. 0 5 squarish; 1 5 compressed; 2 5 extra compressed; 3 5 vertebrae-like 15. Crossed Pedicellariae. 05present; 15
absent
16. Papulae in Corners of Plates. 0 5 no;
1 5 yes
17. Gap Between First Ambulacrals. 0 5 present; 1 5 absent (seam only) 18. Four Tube Foot Pores on Disc. 05ab-
sent; 15 present
19. Cross Section of Arm. 05 round; 15 angular
20. Abactinal Plate Pattern. 0 5 densely packed; 15 open reticulate
21. Degree of Skeletal Calcification. 0 5 weak; 15 strong
22. Carinals, Marginals, and Dorsolaterals in Series. 05 present; 1 5 absent 23. Carinals and Marginals in Parallell Se-
ries. 0 5 absent; 1 5 present
24. Rate of Adoral Carina Development. 0 5 absent; 1 5 weak (1–8); 2 5 high (,10)
25. Morphology of First Two Ambulacrals.
0 5 L5 W; 1 5 L . W; 25 W . L APPENDIX2
DATA MATRIX Taxon
1 1 1 1 1 1 1 1 1 1 2 2 2 2 2 2 1 2 3 4 5 6 7 8 9 0 1 2 3 4 5 6 7 8 9 0 1 2 3 4 5
Brisinga Odinella Rathbunaster Coronaster Labidiaster Plazaster Psalidaster Coscinasterias Pycnopodia Lysastroma Zoroaster Pisaster Heliaster Neomorphaster Pedicellaster Sclerasterias Stylasterias Leptasterias Stephanasterias Ampheraster Cryptasterias Lysasterias Asterias Stichaster Cosmasterias OG: Henricia
2000000001?01300110101011 2000010001?01100110101011 1000010120?12100000101021 1000110120?01100000101011 1000110121?01100000101021 0000111100?01100000101021 1001110100?12100000101011 1101110120001100000111111 1001010101?12100000101021 1001010120?12100100101011 0101021201100011001010010 1101010210001200000011021 0001011210?01100000011122 01010?1200100001001010111 0110021200001000000001000 1101110120001100000011111 1101110120001100000011111 1101010211001100000011011 0001011100101100000011011 0110021100?01100000101001 1001010?00?01100000101011 1001010320?12100000101011 1101010210001200000011011 0101011110001100000011111 1101010211001100000011111 01100??200001010000001001
APPENDIX3
EXEMPLARS USED FOR ANALYSIS (Taxonomy follows Clark and Downey, 1992)
BRISINGIDA:
Brisinga synaptoma NMNHIZ E09296;
Novodinia antillensis NMNHIZ E12913;
Astrolirus panamensis CASIZ 108121;
Odinella nutrix CASIZ 103266.
FORCIPULATIDA: ASTERIIDAE:
Asterias forbesi CASIZ 108851; Cosmas- terias lurida CASIZ 102715; Cryptasterias sp. UCB no number; Leptasterias hexactis CASIZ 8612; Lysasterias sp. UCB RCI.3;
Pisaster brevispinus CASIZ no number; Pi- saster ochraceus CASIZ 112049; Stephan- asterias albula CASIZ 34622, 112417; Sti- chaster striatus CASIZ 111937.
ASTERIIDAE: COSCINASTERIINAE:
Coscinasterias acutispina CASIZ 108865;
Psalidaster mordax, holotype BMNH, Sclerasterias heteropaes, CASIZ 111722;
Stylasterias forreri CASIZ 111935.
HELIASTERIDAE: Heliaster kubiniji CASIZ 75598.
LABIDIASTERIDAE: Coronaster halice- pus CASIZ 108860; Labidiaster annulatus CASIZ 113228; Plazaster borealis CASIZ 113229; Rathbunaster californicus CASIZ 103200, 106655.
NEOMORPHASTERIDAE: Neomorphas- ter margaritaceus CASIZ 116534.
PEDICELLASTERIDAE: Ampheraster marianus CASIZ 112096; Pedicellaster magister CASIZ 111713.
PYCNOPODIINAE: Lysastroma sp. CAS- IZ no number; Pycnopodia helianthoides CASIZ 102818.
ZOROASTERIDAE: Zoroaster fulgens CASIZ 113326; Zoroaster evermanni CAS- IZ 769.
Bold represents specific taxon represented in phylogenetic analysis. Groupings shown are in alphabetical order. Abbreviations are as follow: CASIZ5California Academy of Sciences, NMNHIZ5Natural History Mu- seum, Smithsonian Institution, UCB5Uni- versity of California, Berkeley, and BMNH 5 British Museum of Natural History.
