Life Cycle Evolution in Asteroids: What is a Larva?

14 Pages·1993·6.1 MB·English

by  L R Mcedward

Reference: Biol. Bull 184: 255-268. (June, 1993)
Life Cycle Evolution in Asteroids: What is a Larva?
LARRY R. McEDWARD AND DANIEL A. JANIES
University ofFlorida, Department ofZoology, 223 Bartram Hall. Gainesville. Florida 32611-2009
Abstract. The diversity of larval forms and develop- to asteroids. In general, four different patterns (Table I)
mental patterns in asteroid echinoderms has become in- havebeen identified: ( 1)planktotrophy, (2) pelagic lecith-
creasingly apparent over the past 10-15 years. However, otrophy, (3)demersal development, and(4)brooding(in-
theclassification ofdevelopmental patterns hasbeen am- cluding viviparity) (Thorson, 1950: Mileikovsky, 1971,
biguous because the patterns have not been defined as 1974;Chia, 1974;Jablonskiand Lutz, 1983;Grahmeand
unique sets of ecological and developmental character Branch, 1985). These patterns are distinguished largely
states. In addition, character stateshave not been defined on the basis ofecological characteristics, such as habitat
consistently. Thus attempts to understand the evolution- orsource ofnutrition. The followingdescriptionsofthese
ary changes in development (e.g.. heterochrony and het- major patterns ofdevelopment outline the features that
erotopy in morphogenesis) that underlie larval diversity apply specifically to asteroids.
have been hampered. We propose a multifactor classifi- In the planktotrophic pattern, development involves a
cation of asteroid developmental patterns that uses an pelagic larva that feeds on suspended particles from the
explicitsetofcharactersthatprovideinformation on hab- watercolumn (e.g.. Asterias rubens, Gemmill, 1914; Por-
itat (e.g.. pelagic or benthic) and mode ofnutrition (e.g.. ania pnlvillus. Gemmill, 1915; Astropecten aranciacns.
feeding or nonfeeding) ofthe developing young, as well Horstadius. 1939; Astropecten scoparim. Oguro el al.
=
asthetypeofmorphological development(indirect lar- 1976; Patiriella regidaris. Byrne and Barker, 1991; see
val: direct = nonlarval). We conclude that direct devel- Emlet et al.. 1987, for an extensive list ofasteroid species
opment is exceptionally rare. All asteroids whose devel- and patterns ofdevelopment). Feeding larvae often have
opment hasbeen studied, except Pterastertesselatus. have complex morphology and behavior associated with par-
the indirect type ofdevelopment. We also propose defi- ticlecapture (Strathmann, 1974, 1987). A universal char-
nitions ofsome important terms that have been used in- acteristic ofspecies with planktotrophic development is
consistently in the literature (e.g.. larva, metamorphosis, the production ofsmall eggs( 100-250^m)thatcontain
indirect development, and direct development). Ourdef- insufficient nutritional reserves to support larval devel-
initions take into account the continuous nature of de- opment to metamorphosis. Correlated with the very low
velopment and the evolutionary diversification ofonto- levels ofparental investment per offspring are extraordi-
genetic sequences. These definitions are intended to pro- narily high fecundities(rangingupto hundredsofmillions
vide a clear conceptual basis for analyzing asteroid life of eggs per female per year). Because successful larval
cycle evolution. We argue that the ancestral asteroid life feeding is obligatory in species with the planktotrophic
cpyicnlneariinavnolavnedd pberlaacghiicollaarrivaalndsetavgeels.opWmeentthweinthprbeostehntbia- pisatotfetrennoqfuidteevelloonpgm(ewnete,ksthteodmuornatthison),ofprtohveildairnvgalcpoenrsiiodd-
series of hypotheses for six types ofevolutionary transi- erable potential for larval dispersal.
tions in development that can account for the diversity Pelagic lecithotrophy involves development via a pe-
oflarval forms and developmental patterns in starfish. lagic nonfeeding larva (e.g., Solaster endeca, Gemmill,
1912; Crossasterpapposus, Gemmill, 1920; Pterastertes-
Patterns of Development in Asteroids
selatus. Chia, 1966;McEdward, 1992;Mediasteraequalis.
Different schemes for classifying the patterns ofdevel- Birkeland et al., 1971; Astropecten gisselbrechti, Komatsu
opmentofmarine benthicinvertebrateshavebeen applied and Nojima, 1985). Lecithotrophic larvae are morpho-
logically simpler than related planktotrophic larvae, in
Received 24November 1992; accepted 23 March 1993. that they lack feeding structures, such as ciliated bands
255
256 L. R. McEDWARD AND D. A. JANIES
Table I
Traditionalclassification ofdevelopmentalpatternsinasteroids with characteristicsandexamples
Characters
Name ofpattern Development1 Habitat Nutrition2 Asteroidexamples'
Planktotrophy
ASTEROID LIFE CYCLE EVOLUTION 257
In the traditional classification, patterns are named and arms varies among species, the arms can be identified by
defined on the basis ofthe states ofone (or at most two) their anatomical location using the nomenclature desig-
characters. Forexample, demersal development isdefined nated by Mortensen (1898, pp: 6-7). The bipinnaria is a
solelyon thebasisofhabitatstate(benthic). Consequently, feeding larva and it occurs in the life cycle ofall asteroids
there are two major problems: ambiguity and inconsis- with planktotrophic larval development (e.g.. Asterias
tency. Ambiguity arises because only four patterns in the forbesi, A. vulgaris, Agassiz, 1877; Luidia sarsi, Wilson,
traditional classification attempt to encompass all ofthe 1978; Paliriella regularis, Byrne and Barker, 1991). A
possible combinations ofthe character states that describe brachiolarian larva (Fig. 1B) isdefined by the presence of
a developmental pattern. Therefore the four traditional specialized attachment structureson thepreoral lobe: the
patternsdonotdistinguish uniquesetsofcharacterstates. brachiolar arms and attachment disk. Brachiolar armsare
Demersal development (Table I) is an ambiguous defi- hollow, but contain extensions ofthe larval anterior coe-
nition ofadevelopmental pattern because itdoes notdis- lom, and are thereby distinguished from bipinnarian arms
tinguish between different nutritional (i.e., feeding or (Gemmill, 1914; Barker, 1978). Brachiolararmsare used
nonfeeding) or developmental states (direct or indirect by larvae to test the substratum and provide initial, tem-
development). porary adhesion during settlement. The adhesive disk se-
Thetraditional classification scheme isalso inconsistent cretes cement and provides more permanent attachment
because some patterns, such as planktotrophy. aredefined for metamorphosis. In asteroids with planktotrophic de-
and named on the basis of one character (nutrition), velopment, the brachiolarian stage only occurs after the
whereasothers, suchasbrooding, aredefined on thebasis bipinnaria (e.g.. Asterias rubens. Gemmill, 1914). Al-
of a different character (habitat). Inconsistency in the though these larvae are given different names, they are
classification ofdevelopmental patterns also arises from not independently evolved types oflarvae, but rather se-
the variable definition ofcharacter states (e.g., direct or quential developmental stages.
indirectdevelopment; seebelow)bydifferent authors. The Since thediscovery oftheseasteroid larvaeby Sarsand
result ofambiguity and inconsistency is that the patterns Mtiller, several other larval types have been discovered.
ofdevelopment described by the traditional classification Someasteroids(e.g.. Crossasterpapposits. Gemmill, 1920;
cannot be mutually exclusive, and theclassification must Echinaster echinophorus, Atwood, 1973) develop via a
fail to adequately distinguish the existing patterns. nonfeeding pelagic brachiolarian larva (Fig. 1C). Non-
We think that there is an additional difficulty with the feeding brachiolarian larvae are morphologically simpler
traditionalclassification. Thedefinitionsofdevelopmental than planktotrophicbrachiolarian larvaebecausetheylack
patternsemphasizeecological characteristics(habitat and theciliatedband feedingstructures, bipinnarian arms, and
nutrition)with little attention tothe morphological nature a functional gut. The most conspicuous larval structures
of development (direct or indirect). As pointed out by that characterize both feeding and nonfeeding brachio-
Bonar (1978, p. 179), ecological descriptions of devel- larian larvae are the attachment structures (brachiolar
opment have tended to mask the basic similarity ofmor- armsandattachmentdisk)and bilateral symmetry. Some
phogenesis in many taxa. Conversely, they have also asteroids develop via a benthic brachiolaria that has re-
hampered the recognition offundamental differences in ducedbrachiolarstructures. Forexample, inAsterinagib-
m1o99r2p;hoJganeineessainsd(Mec.gE..dwPatredr,asitnerrevtieesws)e.laTtuos,illMusctEradtweatrheds.e bosa, the brachiolar arms are reduced to nonfunctional
pmoeinnttas,l wchearwaicltlersiusrtivcesyitnheasltaerrvoailddeicvherisniotdyeramnsd.dWeveelwoipl-l abduhlebssiovendaisskirmepmlaeicnisli(aFtiegd. plrDe)o(rLaludlwoibge,,b1u8t82a; MfuanccBtriiodnea,l
touhtelninperoapomsuelteixfpalcitciotrdcelfaisnsiitfiiocnatsioonfismcphoermteanftortedremvselaonpd- d1e8v96e)l.opMeodraendtypfiucnacltlyi,onbarlobordaecdhiborlaacrhiaorlmasriaanrdetaaidnhewseilvle-
mental patterns. disks (e.g., Henricia sanguinolenta, Masterman, 1902;
Leptasteriashexactis, Osterud, 1918;Chia, 1968;Henricia
H
sp., Chia and Walker, 1991; [= variety F, leviuscula,
Asteroid Larval Types Fisher, 1911; p.282, according to Strathmann el ai,
Starfish have two characteristic larval types: the bipin- 1988]). Barrel-shaped larvae (Fig. IE) occurin some spe-
naria and the brachiolaria (see Fell, 1967, p.S68). A bi- ciesofpaxillosids(e.g.,Astropectenlatespinosus, Komatsu,
pinnarian larva (Fig. 1A) is characterized by the bilateral 1975;Komatsuetal., 1988,Ctenopleurafisheri, Komatsu,
arrangement ofthe pre- and post-oral ciliated swimming 1982; Astropecten gisselbrechti. Komatsu and Nojima,
and feeding bands that are borne on arms (MacBride, 1985). Barrel-shaped larvaearepelagic lecithotrophiclar-
1914, p.464; Kume and Dan, 1968, p.306). Bipinnarian vae with abbreviated development and simplified mor-
armsare hollowextensionsofthebodywall;theycontain phology. Pterastertesselatus has an unusual type ofnon-
blastocoelic space, but are not supported by calcareous brachiolarian pelagic lecithotrophic development (Chia,
skeletalrods. Althoughthenumberandsizeofbipinnarian 1966; McEdward, 1992). A similar type of nonbrachio-
L. R. McEDWARD AND D. A. JANIES
B C
/)
a.d.v
br.a.
br.a. a.d.
c.b.
bp.a.
bp.a.
D
br.a.
h.
G
br.a
a.d.
ASTEROID LIFE CYCLE EVOLUTION 259
larian development also occurs in a brooder (Fig. IF) Table II
(Pterastermilitaris, Kaufman, 1968). Relationships between typesolasteroidlarvaeandtraditionalpatterns
Appreciation of asteroid developmental diversity has ofdevelopment
increased over the past 10-15 years with the discovery of
new larval types (e.g., barrel-shaped larvae) and new de- Larval type Developmental pattern
velopmental patterns [e.g.. demersal development, Por-
Bipmnaria Planktotrophy
iinuisp., Bosch. 1989 (Fig. 1C); intragonadal ovovivipar- Demersal development
ity,Asterinapseudoexiguapacifica, Komatsu e/<//., 1990 Brachiolana Planktotrophy
(Fig. 1H); and viviparity, Pterastermilitaris. McClary and Pelagic lecithotrophy
Mladenov, 1990]. This diversity has been described and Demersal development
classified largely according to the patternsoutlined above Brooding
PaxiIIosid barrel-shaped larva Pelagic lecithotrophy
(e.g., planktotrophy. lecithotrophy, brooding, demersal Ptcrastcrid nonhrachiolaria Pelagic lecithotrophy
development). Theambiguityand inconsistency inherent Brooding
in the traditional classification scheme has hampered at-
tempts to understand the evolutionary changes in devel- Developmental pattern Larval type
opment that underlie larval diversity. For example, the Planktotrophs Bipmnaria
lack ofcorrespondence between larval type and the tra- Brachiolana
ditional classification ofdevelopmental patterns in starfish Pelagic Lecithotrophy Brachiolaria
isshown in Table II; thetraditional classification scheme, Paxillosid barrel-shaped larva
Pterastend nonbrachiolaria
cannot predict unambiguously the pattern of develop- Demersal development Bipmnaria
ment, given the type oflarva. Clearly the ecological and Brachiolaria
morphological charactersofdevelopmental patternshave Brooding Brachiolana
evolved independently (e.g., brachiolarattachment struc- Pterastend nonbrachiolaria
tures are often retained in brooded young).
in fact,theblastulaandgastrulastagesaredefiningfeatures
Life Cycle Terminology
of the Metazoa (Buss. 1987; Bonner, 1988; Margulis,
Manyapparentlysimpletermsareused todescribeand 1990). Hatching in asteroids occurs at various stages of
interpret the diversity ofdevelopment in asteroids. How- development (blastula, gastrula, orlater)andcan therefore
ever, a consensus for the definition these terms does not define neither the end ofthe embryonic period nor the
exist. The problem stems in large part from the different beginning ofthe larval period. In the course ofmorpho-
contexts (i.e.. ecological or morphological) inherent in genesis, structuresspecific to eachgroupoforganismsap-
considerations of the evolution of marine invertebrate pear and gradually produce a definitive form (larval or
larvae. The discussion ofterminology that follows is an juvenile). It is the seamless transition between the onset
attempt to provide a clearconceptual basis for analyzing ofmorphogenesisandtheachievementofadefinitiveform
evolutionary changes in asteroid life cycles. The appli- that makesthedistinction between lateembryoand early
cation ofthese terms to specific developmental patterns larva, or early juvenile, impossible to identify with pre-
and the resulting multifactor classification isdiscussed in cision. Forthisreason,theterm "embryo"isbestrestricted
the next sections. to the stages ofdevelopment that are ofuniversal occur-
rence (cleavage, blastula, and gastrula) and should not be
Embryo used to refer to the subsequent transitional period.
In general, embryos can bedefined morphologically as Larva
cleavage stages, the blastula, and the gastrula. These are In spite ofnumerous attempts, no one has provided a
recognizable stages in the development ofall animals, and precise and generally accepted definition of the term
Figure 1. Diagramsofvariousasteroidlarvaltypes.A.Complexfeeding,pelagicbipinnaria(unidentified
luidiid,e.g..Luidiafaliolala;modifiedfromStrathmann, 1974.p.324);B.Complexfeeding,pelagicbrachiolaria
(unidentifiedastenid,e.g.. Pisaslerochraceus. modifiedfromStrathmann, 1974,p.324);C.Simplenonfeeding,
pelagicbrachiolaria(Solasterendeca. modified from Hyman, 1955. p.298): D. Simple nonfeeding, benthic
brachiolaria(Amerinagihhosa. modifiedfrom MacBnde, 1896,pi. 18);E. Nonfeeding,pelagicbarrel-shaped
larva (Ctenopleurafisheri, modified from Komatsu. 1982, p.202): F. Simple nonfeeding. benthic nonbra-
chiolarian stage(Pterastermilitaris. modified from Kaufman, 1968,p.508). G. Simplenonfeeding, benthic
brachiolaria (Porania sp., modified from Bosch, 1989, p.80); H. Simple nonfeeding, benthic brachiolaria
(Asterinapseudoexiguapacifica, modified from Komatsu ela/.. 1990,p.259). Abbreviations: a.d.,adhesive
disk; bp.a., bipinnarian arm; br.a., brachiolararm;c.b.,ciliated band;g.,gut; h., hydrocoel; p., podia.
260 L. R. McEDWARD AND D. A. JANIES
We
"larva." believe that such a definition is impossible to consider metamorphosis asthe transition from the lar-
fortworeasons: ( 1)thecontinuousnatureofdevelopment, val body plan to thejuvenile body plan, regardless ofthe
and (2) the evolutionary diversification ofdevelopment. rate or magnitude of the change. Metamorphosis then
First, "larva" refers to a stage (or series of stages) in a requires a definitive larval stage in the life cycle, and its
developmental sequence. In asteroids, development does occurrence thus defines the indirect pattern ofdevelop-
not progress as a sequence ofdiscrete instars but rather ment.
involves continuous changes in morphology. Stages can-
not be precisely defined, because they do not begin and Indirect development
end with unambiguously identifiable developmental
events. The larval form is produced by morphogenetic This refers to a pattern ofdevelopment in which the
processesthatgraduallytransform theembryo intoamore embryo is followed by intermediate stages with structural
complex shape. Larval stages transform into juvenile features that are not directly involved in the morphogen-
stages during metamorphosis, which can be rapid and esis ofthejuvenile (Fig. 2). These intermediate stages are
drastic orprolonged andgradual. Second, developmental larvaeand by virtue ofhavinga specialized structure and
sequences may have been greatly modified (accelerated, atransitory body plan must undergo a metamorphosis to
retarded, and condensed), and the stages within those se- the juvenile body plan. The construction oflarval mor-
quences may have undergone evolutionary modification. phology (e.g., specific organs or overall body symmetry)
Given the tremendous morphological, ecological, and defines the indirect nature ofa developmental sequence.
taxonomicdiversity ofmarine invertebrates, it is not sur- Larval structures might, but need not be functional during
prising that a single definition fails to be universally ap- development. A brooded larva that does not swim in the
plicable. water column or settle to the benthos may still possess
For evolutionary studies, we maintain that a larva the structures for swimming and settlement.
shouldbedefined asan intermediatestage in thelifecycle
that is produced by post-embryonic morphogenesis and Direct development
is eliminated by the metamorphic transition to the ju-
venile; in addition, this intermediate stage must possess This refers to a pattern of development wherein the
transitory structural features that are not developmentally embryonic stages are followed by the morphogenesis of
necessary for morphogenesis ofthe juvenile. Transitory the juvenile, without an intervening larval stage. The
larval features may be specialized for independent exis- idealized life cycles in Figure 2 illustrate the importance
tenceduringdevelopment, orbereduced inderived modes of the larval stage in distinguishing between direct and
ofdevelopment.
Juvenile Sexually
mature adult
The term "juvenile" has been used in a very broad
sense. Atoneextreme, itreferstothe"post-larval" stages, Gametes
either immediately followingabrupt metamorphosis from
adefinitive larval stage, orat some ill-defined point during Fertilization
a prolonged, gradual metamorphosis. At the other ex-
treme,juveniles are "pre-adults" that have the definitive Juvenile
adult morphology, but are small or at least not sexually
Zygote
mature. For the present discussion, it is more important
tWoeesstuabglgiesshtctrhiatetriaajfuovredneiflienihnagsthaetteaairnleiedsttjhueveandiulletsbtoagdey. :..Diffe"rP"e/'ni-Ji.aJiieo"no""&,"-""*.. rr//GCatsotvmal.ilgaeuo&n
plan (symmetry, general body shape), and the majorsys- Embryo
tems are functional (especially locomotion and feeding, Metamorphosis
but not reproduction). This definition intentionally ex-
cludes the transitional period during metamorphosis. Differentiation&
Morphogenesis
Metamorphosis Figure2. DiagramofanidealizedMetazoanlifecycle.Smalltypeface
identitiesthemajorlifecycleprocesses(e.g.. Differentiation& Morpho-
This literally means a change in morphology. But as genesis);medium-sized typefaceidentifiesthemajorlifecyclestages(e.g..
was stated above, the entire developmental process pro- Juvenile);largetypefaceindicatesthetwoalternativetypesofdevelopment
ducescontinuouschangesin form. "Metamorphosis" has in the life cycle (e.g.. Direct Development). See the text sections Life
CycleTerminology, DirectandIndirectDevelopmentinAsteroids,and
often been restricted to cases where there is a drastic and What isa Larva, and What is Not? fordefinitions and explanationsof
rapid change in morphology. However, it is more useful lifecycle featuresin asteroids.
ASTEROID LIFE CYCLE EVOLUTION 261
indirect development. Direct modes ofdevelopment can lable HI
involve short, simple ontogenetic sequences or long, I'aryingapplieation ofthetermsthree!andindirect development in
complex ones. All that isrequired fordirect development asteroids
is that larval stages be absent from the life cycle. Iflarval
stagesareabsent, then metamorphosisdoes not occurbe- Reference
cause there is not a definitive morphological stage to be
transformed into thejuvenile. Thus, direct development,
as defined here, is equivalent to "ametamorphic" devel-
opment (Bonar, 1978). In contrast to indirect develop-
ment, thejuvenile develops progressively (directly) from
the embryo, through a seriesofintermediate stages, all of
which are transitional towards the juvenile and without
morphogenesis ofany larval structures. Since there is not
a generally accepted term to apply to these intermediate
ontogenetic stages and the term "larva" only refers to a
specialized stage in the indirect pattern ofdevelopment,
it seems useful to introduce the term "mesogen" ( =mid-
dle stage) to refer to the developmental stages that occur
between theembryoand thejuvenile in thedirect pattern
ofdevelopment. This recognizes thateven with direct de-
velopment there can be a prolonged period ofdevelop-
ment before the definitivejuvenile stage is reached. This
term is especially useful where stages ofdirect develop-
ment are free-living (e.g., Pterastertesselatus, McEdward,
1992).
Direct and Indirect Development in Asteroids
The distinction between direct and indirect develop-
ment has been widely used to characterize asteroid de-
velopmental patterns. This is potentially useful for the
study ofevolutionary changes in development because it
involves only morphological criteria, rather than ecolog-
icalones. However, inconsistentapplication oftheseterms
(Table III) has led to considerable confusion.
Originally, development via a larval stage was termed
indirect and development without a larval stage was de-
scribed as direct. Habitat and nutrition were not consid-
ered relevant to thedistinction. Masterman describedthe
broodeddevelopment ofHenriciasanguinolentaas". . .
enabling development to proceed independently of the
capture or acquirement offood. But although this is the
case, there istobediscerned no essential difference in the
courseofdevelopmentwhichwouldjustifytheapplication
ofa term like 'direct' development, . . . The presence of
lecithal nutrition, like that ofhaemal nutrition in vivip-
arous forms, no doubt accounts for certain marked ad-
aptationsnot unlikethosecharacteristicsofparasites, such
as loss of alimentation, sensory and motor organs, but
therecan belittlequestion thatthelarval 'entity' isevident
both in space and time in these demersal forms equally
with the pelagic" (Masterman, 1902, p.384). Henricia
sanguinolenta has a brachiolarian stage that remains
within a brood protected by the parent during develop-
ment. However, because it possesses purely larval struc-
262 L. R. McEDWARD AND D. A. JANIES
within the egg-spawn until hatching into a fully formed may or may not be endowed with special larval organs
juvenile bottom form. Therefore, larval development of and which always differs sensibly from the adult" (p.9).
the species is completely under the protection ofthe egg- The rationale for this broad definition ofthe term larva
envelopes and the spawn-substances. (Pelagic larval phase was a practical one: the preparation ofa comprehensive
is omitted)." Mileikovsky (1974. p.172). In these exam- catalogue ofmarine larvae (i.e.. pelagic dispersive prop-
ples, different and inconsistent sets ofcriteria were used agules). At the time that it was proposed, the broad, eco-
to define these patterns, thus effectively removing any logical definition ofa larva was recognized as "a point of
meaningful morphological interpretation ofdirect devel- dispute" (Vannucci, 1959, p.7). Chia( 1974) improved on
opment. Vannucci's definition by making the language less am-
Indirect development is usually restricted to cases of biguous. He maintained the ecological sense ofa larva by
feeding larval development (e.g.. Wray and Raff, 1991, making morphology, nutrition, and habitat alternative
p.45). This is particularly true for asteroids (Komatsu, criteria by which to define a larva. The advantage ofthis
1975; Oguro et a!.. 1976, 1988). "Development having broaderdefinition isthat it recognizes the important eco-
brachiolaria only, irrespective ofwhether it is pelagic or logical roles played by many "larvae" (i.e.. feeding and
benthic, is called the direct type. Development which dispersal). This was consistent with the current emphasis
passes through both the bipinnaria and the brachiolaria on larval ecology and the adaptive significance ofdevel-
is called the indirect type." (Oguro et a/.. 1976, p.571 ). opmental patterns in marine benthic invertebrates.
Differing criteria for direct and indirect development The disadvantage ofsuch an expanded definition ofa
create a problem because these patterns ofdevelopment larva is that by allowing three alternative characters to
are intimately tied to the definition ofa larva. Does this define a larva (morphology or nutrition or habitat) the
mean that nonfeedingorbenthic larvaeare not really lar- definition becomes ambiguous. Under this broad defini-
vae after all? Chia argued that ". . . it is indirect devel- tion, nutritional type or habitat could suffice to define a
opment when there is a larval stage and it is direct de- larva (indirect development), without regard to the nature
velopment when a larval stage is lacking. This definition of morphological development. In addition, numerous
seems clear and simple but in practice there has been applications ofthe ecological characterization ofa larva
much confusion. The main problem, as I see it, lies in have involved logical errors, in that negation ofonly one
differencesofdefiningwhat isa larva and much confusion ofthecriteria(morphology ornutrition orhabitat), rather
would be reduced if the term 'larva' is clarified" (Chia, than all of the criteria (morphology and nutrition anil
1974, p.121). habitat), have been used to designate development as
nonlarval (i.e.. direct).
What is a Larva, and What is Not? The problem is seen clearly with regard to brooded de-
velopment in which young stages can be larval by mor-
Chia(1974)proposed adefinition forthe term "larva." phological and developmental criteria (indirect develop-
"Larva is a developmental stage, occupying the period ment) but do not live in the plankton and thus do not
from post embryonic stage to metamorphosis, and it dif- provide larval dispersal (e.g., Leptasterias hexactis. Chia.
fers from the adult in morphology, nutrition, or habitat. 1968; Asterina pseudoexigua pacifica, Komatsu et a/..
In thisdefinition, postembryonic designatesthetime after 1990; Henridasp., Chiaand Walker, 1991). On theother
emerging (hatching) from the primary egg membrane; hand, there are pelagic propagules that undergo direct
prior to that it is considered as embryonic stage" (Chia, development and thus qualify as larvae only in the sense
1974, p.122). Chiaexplicitly rejected the idea that a larva thattheyaredispersed bywatermovements(e.g., Pteraster
had to possess purely "larval" structures. This was nec- tesselatus, McEdward, 1992).
essary to encompass the ecological sense ofa larva as a Of the four ecological patterns of development de-
dispersive propagule. In this regard. Chia was following scribed above (Table I), which necessarily have ordo not
Vannucci (1959), who had reviewed the various defini- have larval stages and which can potentially have larvae?
tionsofthe term larva that had been used previously and Planktotrophic development must include a larval stage
had rejected the common definition ofa larva as a de- inordertopossessthestructuresnecessaryforfoodparticle
velopmental stage that had transitory or larval organs. capture. In the other four patterns, indirect or direct de-
Vannucci's intention was"to use theword larva in avery velopment areevolutionary options. Pelagic lecithotrophy
broad sense, and will thus include many organisms that generally involves larval stageswith specialized swimming
would not be considered a larva by authors giving to this or settlement structures, but direct development could
word a restricted meaning" (Vannucci, 1959, p.7). He occur in the plankton via a pelagic mesogen. Demersal
cited as examples of organisms that had larvae only by development could involve feedingor nonfeeding larvae,
theecological criterion, the planula, actinula, and ephyrae as well as direct-developing mesogens. Benthic brooding
of cnidarians. Vannucci (1959) defined larva as "a de- often involveswell-developedlarval stages, somebrooded
velopmental stage, as a rule sexually immature, which younghave simplified larval features, but brooding rarely
ASTEROID LIFE CYCLE EVOLUTION 263
proceeds by strictly direct development. In numerous must be used to unambiguously describe or classify a de-
cases, brooding involves stages with larval structures velopmental pattern.
(sometimes reduced but often functional). This makes the Eight different developmental patterns can potentially
classification ofdevelopmental stages as larvae or meso- be described when three characters exist, each with two
gensdifficult; howeverit is important to realizethat there alternative states. Ofthese eight potential patterns, only
cannot bean absolutedistinction between larvaeand me- six are known to occur in asteroids (Table IV). Indirect
sogens, because the evolution from indirect to direct de- development via pelagic feeding larvae is common in as-
velopment usually involves the successive reduction and teroids, and it can involve either bipinnarian and bra-
eliminationoflarval structures. Theclosestapproximation chiolarian stages (e.g.. Asterias rubens, Gemmill, 1914)
totrulydirect development in theasteroids isin the highly or only bipinnarian stages (e.g., Astropecten scoparins,
derived pterasterids which lack all larval structures, as Oguro et uL, 1976). Indirect development via pelagic
well as bilateral symmetry, and are thus fundamentally nonfeeding larvae can involve a simplified brachiolaria
different from all other starfish (McEdward, 1992; Mc- or the barrel-shaped larva. Indirect development on the
Edward, in prep.; Janies and McEdward, in review). benthos with a feeding larva possibly occurs in the Ant-
To answer the question raised in the heading to this arctic asteroid Odontaster validus, but this is uncertain
section, only a larva (in the strictest morphological and (Pearse and Bosch, 1986). Indirect development via a
developmental sense) is a larva, and everything else in- benthic nonfeeding larva iscommon amongbroodingas-
cluding a mesogen is not. teroids (e.g., Ctenodiscus australis, Lieberkind. 1926:
Hfimcia sanguinolenta, Masterman, 1902; Leptasterias
Classification of Developmental Patterns of Asteroids lic.\tictis. Chia, 1968). Strict direct development is ex-
tremely rare in asteroids. Pelagic nonfeeding direct de-
We propose a multifactor classification scheme for as- velopment occursonly in Pterastertesselatus(McEdward,
teroiddevelopmental patterns(Table IV). Therearethree 1992). Benthic nonfeeding direct development has not
completely independent characters by which develop- been reported, butweinferit forthebroodingpterasterid,
mental patterns are classified. First, the morphological Pteraster militaris (Kaufman, 1968; McClary and Mlad-
nature of development can be described using the dis- enov, 1990), based on similarities with P. tesselatus
tinction between indirect and direct development, in the (McEdward, in prep.). Construction oftheproposed mul-
strict sense outlined above. In our scheme, all indirect tifactorclassification scheme was stimulated, in large part,
types have larvae and all direct types do not, regardless by the need to clarify the developmental differences be-
ofhabitat or mode ofnutrition duringdevelopment. Sec- tween pterasterids and other asteroids with nonfeeding
ond,developmental patternscan bedistinguished by hab- patterns ofdevelopment. Direct development involving
itat, using the pelagic or benthic distinction. Third, the feeding has not been reported for asteroids. Given the
distinction between feedingand nonfeedingdevelopment predatory nature ofmostjuvenile and adult asteroids, it
provides information about nutrition. All three characters is unlikely that transitional developmental stages (meso-
Table IV
Mullifactorclassification ofasteroiddevelopmentpatterns
Developmental pattern
Characters
Type
264 L. R. McEDWARD AND D. A. JANIES
gens) could acquire paniculate food without the use of lifecycleand resulted inapelagic, nonfeedingbrachiolaria.
specialized (i.e.. larval) feeding structures. Direct devel- Associated with the loss oflarval feeding structures, such
opment, with feedingseems to bean unlikelyevolutionary asciliated bands, bipinnarian arms, and a functional gut.
option for starfish. the morphology ofthe brachiolaria wasgreatly simplified
(Fig. 1C). However, the larva retained bilateral symmetry,
brachiolar arms, and many features ofinternal develop-
Evolution of Developmental Patterns in Asteroids
ment (e.g.. coelom formation) characteristic ofthe more
Although indirect development with a complex, feed- complex bipinnarian and brachiolarian forms. This has
ing, pelagic larvaisconsidered theancestral condition for occurred at least 6-9 times in the asteroids (Strathmann.
echinoderms (Jagersten, 1972; Strathmann, 1978), there 1978). Indirect development via a simple brachiolarian
has been considerable debate over the nature ofthe an- larva is known to occur in four orders: Forcipulatida,
cestral asteroid life cycle (Bather 192la. b, 1923; Mac- Valvatida, Spinulosida, and Velatida (Fig. 4). From this
Bride, 1921, 1923a, b; Mortensen, 1922, 1923). Until re- pelagic, nonfeeding pattern of development, a second
cently, it was widely accepted that indirect development evolutionary change (transition B, Fig. 3) eliminated the
viaa pelagic feeding bipinnaria with complex larval mor- pelagic phase ofdevelopment and resulted in benthicde-
phology, but without a brachiolaria stage, characterized velopment via brooding, or a free-living demersal larva.
theoriginaldevelopmental pattern ofasteroids(Fell, 1967. This resulted in an indirect pattern ofdevelopment with
p.S71; Oguro et ai. 1988). This argument was first de- a nonfeeding brachiolarian larva and is known from the
veloped by Mortensen (1921, p.219-220), and it was orders Forcipulatida, Valvatida. Spinulosida, and Velatida
largely based on the absence ofthe brachiolarian stage in (Fig. 4).
the paxillosids (esp. Luidiidae and Astropectinidae). Pax- Direct development, in the strict sense that we use the
illosids were considered to be the most primitive ofthe term, is known among asteroids only in the family Pter-
starfish orders, so the lack ofa brachiolarian larval stage asteridae. We postulate that direct development evolved
was interpreted as the original condition forthe asteroids in a lineage of brooders within the order Velatida (Fig.
(Oguroetai, 1988). Thebrachiolariawasthoughttohave 4). Brooding is rare in solasterids, but is presumed to be
evolved later, at about the same time as the appearance thepredominantmodeofdevelopment intheothervelatid
ofsuckered podia (Fell, 1967, p.S71). The importance of families: Korethrasteridae, Caymanostellidae, Myxaster-
thetaxonomicposition ofthepaxillosidsinthisargument idae, and Pterasteridae. Unfortunately, because these are
was clearly pointed out by Mortensen (1923, p.323): "I mostlydeep-seaorganisms, very littleisknown about their
have no direct interest in maintainingthe Brachiolaria to development (Clark and Downey, 1992). Larval attach-
beasecondarilyspecialized larval type. Ifconclusiveproof ment structures were likely lost in the pterasterids as the
is given that the Brachiolaria is the primitive, the Astro- lineage became specialized in the deep-sea and evolved
pectinid-larva the specialized form, I shall not hesitate to brooded young. Direct development wasprobably the re-
drop my present view. But I must maintain that this view sult ofselection forgeneral developmental efficiency(i.e..
is not unjustified by the facts so far known." In contrast, the discontinuance ofvestigial larval programs) during a
MacBride(1921, 1923b)argued that paxillosidswere spe- long history of brooding. Extreme simplification of de-
cialized, not primitive, and he explained the lack of a velopment(transitionC, Fig. 3),eliminatedallofthelarval
brachiolarian larva as an adaptation for life on soft sub- features (e.g.. brachiolar arms, bilateral symmetry) from
strata. This view was strengthened by the discovery that the lifecycleand produced an ontogenetic sequence lead-
some paxillosids have suckered podia for a short period ing directly from the embryo to thejuvenile (Fig. 2). In-
immediately after metamorphosis (Astropecten latespi- termediate developmental stages represent mesogens (Fig.
nosus, Komatsu, 1975, p.53',Astropectenscoparius, Oguro IF) that are brooded by the parent. The developmental
et ai, 1976, p.567). The recent analyses ofpaxillosid bi- pattern is benthic, nonfeeding, and direct (Table IV) and
ology by Blake (1987, 1988) have provided convincing it is known for only a single species, Pteraster militaris
support to the view that paxillosids are highly derived (Kaufman, 1968; McEdward, in prep.) (Fig. 4). A sub-
asteroids with body form, digestive, podial, as well asde- sequent modification ofthispattern ofdirectdevelopment
velopmental, specializations for life in sandy and muddy involved the re-evolution ofa pelagic period during de-
habitats. We accept this view and consider the original velopment(transition D, Fig. 3). Thisproducedtheunique
asteroid life cycle to have consisted ofpelagic feeding in- typeofpelagic, nonfeeding "larva" ofPterastertesselatus
direct development via a complex bipinnaria and a com- (McEdward, 1992). This pelagic developmental stage isa
plex brachiolaria (Fig. 1A, B, 3, 4). mesogen (not a larva) and the pattern ofdevelopment is
All ofthe other developmental patterns that occur in direct, pelagic, and nonfeeding (Table IV). The pelagic
asteroids (Table IV) can be derived by means ofsix dif- mesogen ofPterastertesselatusisfundamentallydifferent
ferent evolutionary transitions (Fig. 3). Loss of larval from the pelagic, nonfeeding brachiolarian larva ofother
feeding(transition A) eliminated the bipinnaria from the starfish. Important differences include: absence of bra-