Download Experimental Manipulation of Parental

AMER. ZOOL., 36:169-179 (1996)
Experimental Manipulation of Parental Investment in
Echinoid Echinoderms1
LARRY R. MCEDWARD
Department of Zoology, University of Florida, Gainesville, Florida 32611
In free spawning species, maternal investment is limited to
the contents of the egg. Striking correlations between egg size and larval
characteristics, such as development rate, larval size, body form, feeding
capability, nutritional requirements, and size at metamorphosis, have been
observed in many taxa of marine invertebrates, in spite of tremendous
morphological and ecological diversity. Analysis of these relationships
has historically been based on comparative observations or quantitative
modeling. Advances in our understanding of life history ecology in marine organisms require combining evolutionary theory with functional
analyses of larvae as pelagic organisms. I believe that development will
prove to be an important integrative link between these fields. In taxa
with regulative development {e.g., echinoid echinoderms), it is possible
to experimentally manipulate the amount of material that is available for
larval morphogenesis. This provides a powerful tool for elucidating the
developmental consequences of changes in maternal investment. Here, I
will examine the rationale and methodology underlying this experimental
approach and review the conclusions and some outstanding questions concerning the influence of maternal investment on the morphology, function,
growth, and development of larvae. The four main effects of an experimental reduction of egg size (blastomere isolation) are: 1) smaller larval
size, 2) simpler larval form, and 3) slower development in the early-stage
larvae, but 4) regulation of size, shape, and development rate in late-stage
larvae.
SYNOPSIS.
INTRODUCTION
This review addresses the following general question: Does egg size, or more properly the level of parental investment represented by the material contained in the egg,
influence the morphology, growth, or development of marine invertebrate larvae?
This question is important because it tests
a central assumption in life history studies
of marine invertebrates (Strathmann, 1988).
The level of parental investment per offspring is assumed to be an important determinant of the fitness of the offspring by influencing larval traits that affect performance and survival during the pelagic pe-
riod (McEdward, 1988) and possibly into
post-larval benthic stages,
the
BackRround
E
size
occupies a prominent position
y o f a n i m a l l i f e histories (see
Roff
> 1 9 9 2 ; Stearns, 1992; Bernardo, 1996).
™ s i s particularly true for marine invertebrates (e.g., Emlet et al, 1987; Kohn and
Perron
> 1994> w h e r e m a n y s P e c i e s a r e f r e e
spawners. Adults release gametes directly
into the
seawater; fertilization and larval
development take place in the plankton,
without parental care. This pattern of reproduction means that parents cannot provide
nutrition or protection to their offspring
during development. Therefore, the con1
From the symposium Maternal Effects on Early t e n t s o f t h e e g g represent the entire nutri-
^XI^^Z^M^ZZ
88
i n t h e stud
tional
contribution the offspring receive
American Society of Zoologists, 27-30 December from their parents.
1993, at Los Angeles, California.
Several quantitative, theoretical models
169
170
LARRY R. MCEDWARD
have attempted to explain the evolution of
life history patterns in marine invertebrates
(e.g., Vance, 1973a, b; Christiansen and
Fenchel, 1979; Strathmann, 1985; Havenhand, 1993, 1995; Levitan, 1993). An important assumption underlying many of
these models is that parental investment per
offspring directly determines offspring fitness. As parents allocate more resources to
each individual offspring, fewer offspring
are produced. The optimal egg size reflects
a balance between the quality and quantity
of offspring. The general prediction for animals with feeding larval development is
that strong directional selection favors production of very small eggs containing the
minimal material required to produce a
feeding larva. Empirical observations support the prediction: nearly all pelagic, feeding larvae of marine invertebrates develop
from small eggs (70-200 u,m diam) that
contain sufficient material to support development into a functional larva, but insufficient material to support complete development into a juvenile. For feeding larvae,
acquisition of food is necessary for successful completion of larval development,
metamorphosis into the juvenile, and settlement/recruitment into benthic populations.
Empirical studies have correlated egg
size with important features of feeding larvae, such as larval size and rate of development, in several taxa (e.g., Hadfield and
Switzer-Dunlap, 1984; Emlet et al., 1987;
Kohn and Perron, 1994), but in all cases
there is a substantial range of egg sizes
among species with planktotrophic larvae.
For example, in echinoids with feeding larvae, the range in egg size (volume) is approximately 60-fold and the egg content
(joules) range is approx. 20-fold (Emlet et
al., 1987). Clearly not all species are producing the smallest eggs that will support
development to the onset of larval feeding.
To improve the theoretical models, information is needed on the relationship between the level of parental investment and
the larval characteristics that influence survival. There are two reasons why existing
information, based on species comparisons,
is inadequate. First, comparative studies can
only describe correlations among traits, but
they cannot identify causal relationships.
Second, existing studies correlate egg size
with larval traits. Egg volume and energy
content are highly variable, both within and
among species (Turner and Lawrence,
1979; McEdward and Carson, 1987; McEdward and Coulter, 1987). The level of parental investment cannot be inferred with
confidence from measurements of egg dimensions among echinoderm species with
planktotrophic larval development (McEdward, 1991). The important practical implication of this result is that we lack a reliable, nondestructive index of egg energy
content. Consequently, it is difficult to explore the relationship between parental investment and offspring success. Because
egg volume is not a reliable predictor of
energy content, it is not possible to separate
a spawn into individuals with greater and
lesser parental investment on the basis of
egg size, and study the consequences for
larval traits likely to influence offspring
survival. This places limits on our ability to
explain the ecological diversity of marine
invertebrate life history patterns.
The experimental approach
What is needed is a method for experimentally manipulating the level of parental
investment within a species (Bernardo,
1991). There are at least six possible approaches: 1) manipulation of adult diet to
influence oogenesis, 2) hormonal alteration
of vitellogenesis, 3) genetic engineering to
increase or decrease investment during vitellogenesis, 4) addition or removal of egg
cytoplasm by microinjection, 5) fragmentation of eggs by ligation, cutting, or centrifugation, 6) removal or addition of blastomeres from early stage (2-4 cell) embryos. I am not aware of published attempts to
apply methods 2-5 to the manipulation of
egg size for life history studies on marine
invertebrates. Egg size or energy content
has been successfully altered by manipulating adult diet (Thompson, 1983) and in
some cases effects of egg characteristics on
larval development have been demonstrated
(George et al., 1991). The advantage of this
method is that it could, in principle, be applied to many taxa. However, its usefulness
is limited by the difficulty of controlling the
magnitude of change in egg size or content.
171
MANIPULATION OF ECHINOID EGG SIZE
Naturally occurring variation in egg content, combined with the lack of a nondestructive measure of egg content, results in
an imprecise analysis of the relationship between parental investment and larval characteristics. Furthermore, manipulations of
adult diet affect many features of the parent
besides investment in eggs (Bernardo,
1996).
In some cases, blastomeres can be removed from or added to early embryos to
change the amount of material available for
development to the initial feeding larval
stage, mimicking an evolved change in the
level of parental investment. The advantage
of this method is that embryonic volume
can be altered precisely (i.e., removal of 1
blastomere from a 4-cell embryo produces
a 25% reduction in the amount of material
available for development). A major limitation of the method is that it is applicable
only in taxa that have regulative development (e.g., echinoderms, hemichordates,
and phoronids). Furthermore, it is only
practical in those taxa for which there are
reliable methods for obtaining gametes and
culturing larvae through metamorphosis
(echinoid and asteroid echinoderms).
Echinoids (i.e., sea urchins and sand dollars) compensate for blastomere alterations
by means of regulative embryonic processes and produce qualitatively normal larvae
(see Horstadius, 1973) capable of development to metamorphosis. This provides an
opportunity to experimentally investigate
the following questions: What are the effects of an experimental change in parental
investment per offspring (egg size) on larval development rate, body size, body
shape, and juvenile size in echinoids? Does
the larval form that results from a change
in parental investment affect feeding capability? Are the form-function consequences
of a change in parental investment likely to
constrain the adaptive evolution of echinoid
life histories? Answers to these questions
are needed to evaluate and further develop
predictive models of life history evolution
in marine invertebrates with pelagic suspension feeding larvae.
METHODS
Echinoids can be induced to release eggs
in the laboratory and the eggs can be arti-
ficially fertilized. Upon fertilization, a vitelline membrane elevates from the egg surface. The membrane can be removed by a
variety of methods (Hinegardner 1975a;
Strathmann, 1987), leaving a denuded egg.
During cleavage and prior to the formation
of distinct cell-cell junctions at the blastula
stage, the blastomeres are bound together
by hyaline, which can be dissolved in calcium-free-seawater (CFSW) to allow separation and isolation of the cells (Horstadius,
1975; McClay, 1986; Maruyama et al,
1986). Upon return to normal seawater the
hyaline reforms and the blastomeres from
subsequent divisions remain together. Isolation of a blastomere from the 2-cell stage
yields an egg of Vi normal size. Blastomeres
from the 4-cell stage are V* the size of normal eggs. Eggs that are treated with CFSW
but removed before 1st cleavage serve as
full sized controls. Blastomeres can be considered "eggs" of reduced size because
they are undifferentiated, totipotent cells capable of development through metamorphosis. Embryos can be raised to the pluteus
larval stage and on through metamorphosis
(Okazaki and Dan, 1954; Hinegardner,
19756; Marcus, 1979; Sinervo and McEdward, 1988; Hart, 1995; McWeeney and
McEdward, unpublished; Herrera and
McEdward, unpublished; McWeeney and
Herrera, unpublished).
AN EXAMPLE
(SINERVO AND MCEDWARD,
1988)
We have used blastomere manipulations
to change the level of parental investment
in two species of sea urchins, Strongylocentrotus droebachiensis and S. purpuratus.
We demonstrated that a reduction in the
level of parental investment caused a reduction in initial larval size, a simplification
of early larval body shape, and a reduction
in development rate. This study was the
first definitive demonstration of a causal relationship between the level of parental investment and important larval traits, such
as larval size and development rate, in any
marine invertebrate.
An essential aspect of the experimental
design involved the use of two species. This
allowed comparison of the experimental results with the correlates of an evolved
172
LARRY R. MCEDWARD
SD 1/1
0.8
e
•H
*
0-6
0.4
3D
1/2
SP
1/2
20
Age
30
50
(d)
FIG. 1. A simplified graph of relative, overall larval size plotted against larval age. SD, Strongylocentrotus
droebachiensis; SP, 5. purpuratus; '/„ full size "eggs"; Vi, half-size "eggs"; Vt quarter-size "eggs". Larval size
was obtained as the scale factor in the shape fitting statistical analysis. Larvae in the SD V* and SP V2 treatments
did not complete development to metamorphosis during the experiments.
change in parental investment. 5. droebachiensis and S. purpuratus are closely related, co-occurring species of sea urchins.
Egg diameters are 82 u,m for 5. purpuratus
and 152 jxm for S. droebachiensis, corresponding to a 6-fold difference in volume
(0.3 v*. 1.84 nl) and a 5-fold difference in
energy content (Strathmann and Vedder,
1977). These species differ in early larval
size and rate of development, but have very
similar later larval stages (McEdward
1986a, b). We predicted that if the differences in the early life histories of these two
species are due to differences in egg size,
then experimental reduction of the size of
S. droebachiensis eggs should yield a larval
form and rate of development similar to S.
purpuratus. We generated full-, half-, and
quarter-size embryos by means of blastomere separations, which produced a range
of egg sizes that spanned an order of magnitude.
It is not a trivial problem to objectively
compare larval body form among organisms that are known to differ in size and
shape and that change size and shape continuously but at different rates. Valid comparisons among experimental treatments
depend on identifying equivalent stages of
development. We used morphometric techniques (McEdward, 1984, 1985) and statistical shape fitting analyses to solve that
problem (Siegel, 1982; Siegel and Benson,
1982; see also: Rohlf, 1990; Chapman,
1990). These techniques provided information on similarity of shape (independent
of size) via goodness of fit statistics and
plots of residual vectors, as well as information on overall size differences via a
scale factor.
In this paper, I review the four main effects of an experimental reduction of egg
size (blastomere isolation): 1) smaller larval
size, 2) simpler larval form, and 3) slower
development in early-stage larvae, but 4)
regulation of size, shape, and development
rate in late-stage larvae.
Larval size
Note that relative, overall larval size has
been plotted in Figure 1 to facilitate comparison among experimental treatments.
The larvae that developed from full-size
eggs of 5. droebachiensis (SD '/,) were used
as the standard for calculation of relative
larval size. Larvae that developed from
smaller eggs (SD Vi, SD YA, SP '/„ SP **)
were smaller during the early stages of development (compare the extreme left end of
all five lines; Fig. 1). The developmental
basis for the effects of a change in egg size
on larval size seems clear. Isolation of blastomeres from early embryonic stages does
not influence blastomere size, nor cleavage
schedules, but does reduce the total number
of cells in the early embryo and larva at
MANIPULATION OF ECHINOID EGG SIZE
173
any given stage (Takahashi and Okazaki,
1979). On the other hand, an evolved
change in egg size (e.g., SD '/, vs. SP '/,)
should not alter the number of cells at any
given stage but would result in smaller blastomeres, and hence a smaller larva. The
consequences of this difference are not
known.
Larval size increased substantially during
development in all treatments (Fig. 1), as is S. droebachiensis
S. purpuratus
typical for echinoids with planktotrophic
FIG. 2. Camera lucida tracings of early 4-arm larvae
larvae (e.g., McEdward, 1984, 19866). Dif- (dorsal
view, anterior end up) of S. droebachiensis and
ferences in larval size relative to the stan- S. purpuratus. Larvae developed from full-size, undard decreased throughout development manipulated eggs. The dark line encircling the larval
and were eventually eliminated. Size equiv- body and extending onto the arms is the ciliated band
alence occurred at the point where any an- feeding structure.
gled line (treatments) intersected the horizontal line of the standard (SD '/,). Size
equivalence was reached at different ages Larval shape
in the various treatments but occurred at the
The most surprising and interesting result
same stage of larval development: the 6obtained
in this study was that larvae that
armed larval stage. Sizes of later stage lardeveloped
from small eggs had different
vae and metamorphosed juveniles were independent of egg size. However, Hart body shapes (compared to larvae from larg(1995) recently detected differences in ju- er eggs) during the initial stages of develvenile size between SD ('/,) and SD (Vz) opment but not during later stages (after the
treatments. Size regulation has been docu- 6-armed pluteus stage). The main differmented in other species following experi- ence in shape was that larvae from small
mental reduction of egg size (e.g., Arbacia eggs had short arms relative to body size
punctulata, Harvey, 1949; Lytechinus pic- resulting in a simpler overall form (Fig. 2).
Why don't small larvae maintain body
tus, Hinegardner, 19756) and in cases where
closely related species differ substantially proportions and normal shape? My hypothin egg size (e.g., S. nudus and 5. interme- esis is that the larval skeleton causes
dius, Kawamura, 1970; Naidenko, 1983). changes in larval shape when egg size is
Furthermore, juvenile size at metamorpho- reduced. Our unpublished observations sugsis is remarkably uniform among echinoid gest that the scale and pattern of the skelspecies (Emlet et al., 1987). Some degree eton does not change with body size when
of size regulation is probably a general egg size is reduced. The posterior body
characteristic of echinoid larvae and occurs regions have larger than expected skeletal
via larval growth (increase in cell number structures and the arms have smaller than
and arrangement), rather than by adjust- expected skeletal rods. Morphogenesis of
ment of cell size during development. Sim- the larval skeleton might be species-specific
ilarity of juvenile size, in spite of differ- and relatively insensitive to changes in egg
ences in egg size and intitial larval size, size. If so, then reducing the volume of larvalidates an important assumption of the val tissue without proportional reduction of
theoretical models (at least for echinoids), skeletal features must yield altered body
namely that the only important trade-off is shape. Altered body shapes result in reegg size (and fecundity) against develop- duced functional capabilities. We are curment time. The optimum egg sizes should rently investigating the developmental basis
be strongly influenced by rates of mortality of this using experimental manipulations,
in the plankton (Strathmann, 1985; Emlet morphometric measurements, and computer
et al., 1987), which set the cost associated simulations of skeletal growth in several
with a given developmental duration.
species of sea urchins and sand dollars.
174
LARRY R. MCEDWARD
8D 1/1
elopment
Metamorphosis
S
/
ug)
<n
/
SD
SP 1/1
1/4
/
r
8-R
/
8-pl
0
o
t»
SD 1/2
6-pl
4-pl
2-pl
//
/
A
/
/
/
/
SP 1/2
^
10
20
30
40
60
Age (d)
FIG. 3. A simplified graph of the stage of larval development plotted against larval age. SD, Strongylocentrotus
droebachiensis; SP, S. purpuratus; '/„ full size "eggs"; Vi, half-size "eggs"; Vi quarter-size "eggs"; 2-pl, 2-arm
pluteus larva; 4-pl, 4-arm pluteus larva; 6-pl, 6-arm pluteus larva; 8-pl, 8-arm pluteus larva; 8-R, 8-arm pluteus
larva with a juvenile rudiment; Juv, post-metamorphic juvenile.
size and time to metamorphic competence.
Development rate
A plot of the stage of larval development The volume of water that can be cleared of
against the age of the larvae in days post- particles per unit time by an echinoid larva
fertilization illustrates that larvae from is set by the total length of the feeding
small eggs had slower rates of development structure, the ciliated band (Strathmann,
(as indicated by shallower slopes in Fig. 3). 1971, 1975; Strathmann et al., 1972; Hart,
The effects of reduced egg size were re- 1991). Shape changes during echinoid destricted to the early larval stages (below the velopment influence larval feeding rate and
dashed line). During development, the de- growth. Since most of the ciliated band is
velopment rates changed and thereafter located on the arms (McEdward, 1984,
(i.e., above the dashed line) became the 1986Z?), short arms result in a short ciliated
same among all treatments. This occured at band, low clearance capacity, and therefore
different ages in the various treatments but slower growth. Hart (1995) has recently
occured at the same stage in all cases: the shown that dwarf larvae of 5. droebachien6-armed larval stage. This is the same stage sis have reduced feeding structures (i.e.,
at which larval sizes became equivalent. shorter ciliated bands) and reduced feeding
The general result is that a reduction in egg capability (lower maximum clearance rate).
size causes a reduction in development rate, Larvae that develop from small eggs must
and it does not matter whether the reduction grow more to reach a size suitable for metais produced experimentally (compare SD ^, morphosis, but start smaller and are less
vs. SD Vi or SD %; compare SP V, vs. SPable to acquire the food to fuel growth and
Vi) or evolved naturally (compare SD V} vs.development.
Alterations of body form as a conseSP '/,)Reduced development rate is probably at- quence of changes in egg size could have a
tributable to the differences in larval size very important implication for life history
and shape (Fig. 2). We inferred that a sim- evolution. Selection for increased fecundity,
ple body form made a larva a less effective via reduced egg size, would normally be
suspension feeder and that it would grow balanced by increased mortality associated
more slowly as a consequence. It seems with the increased time necessary to grow
likely that reduced growth rate, rather than from a smaller initial larval size to the fixed
retardation of developmental processes per size required for metamorphosis (see
se, underlies the relationship between egg above). However, if the larvae that develop
MANIPULATION OF ECHINOID EGG SIZE
from small eggs also have different body
forms that confer reduced capacity to feed,
then there would be an additional increase
in developmental time and mortality. If
smaller larvae have to grow more, but are
less capable of acquiring the food to fuel
that growth, then the adaptive evolution of
egg size would be constrained by this formfunction consequence of skeletal growth
and would require the independent evolution of skeletal morphology. One reason
that I find this particularly interesting is that
this constraint should be taxon-specific, occurring only in those echinoderm larvae
that have a mineralized skeleton (e.g., echinoids and ophiuroids, but not asteroids and
holothuroids). Blastomere separation experiments can be conducted with asteroids to
test this hypothesis. I predict that a reduction in egg size in asteroids will result in
smaller larvae that can maintain normal
body proportions and size-specific feeding
capability.
Summary of results from the blastomere
isolation experiment
The principle result of these studies is
that differences in the life histories of these
two species are attributable to differences
in egg size. Smaller eggs resulted in smaller
larvae and slower development. There is a
causal relationship between parental investment per offspring and important life history characteristics in these larvae. Egg size
effects were restricted to early larval stages,
before the 6-armed larval stage. Later
stages were equivalent in larval size, shape,
development rate, and size of the juvenile
at metamorphosis. One interesting implication of these findings is that species differences in larval morphology may be epigenetic consequences of quantitative differences in egg content and need not reflect
changes in the larval genome. This is very
different from the prevailing paradigm in
developmental biology, especially in studies of the evolution of ontogeny in which
the effects of changes in regulatory genes
that have cascading effects during development are emphasized. In this study, a
phenotypic character was manipulated
without changing the underlying genetic
make-up of the embryo or larva. This
175
caused a substantial change in larval form
that was similar to the difference between
these two species. These results implicate
egg size as a far more significant factor in
the evolution of marine invertebrate life
history patterns than previously thought.
SOME UNANSWERED QUESTIONS
Generality
We are currently conducting experiments
on several species of sea urchins and sand
dollars to evaluate the degree of generality
in the effects of altered egg size. To date, a
reduction in initial larval size and initial development rate has been documented in
Mellita quinquiesperforata (Herrera and
McWeeney, unpublished; McWeeney and
Herrera, unpublished), Dendraster excentricus (McWeeney and McEdward, unpublished), and Encope aberrans (Herrera and
McEdward, unpublished). Comparative experimental research will provide information on different families and subclasses of
echinoids with different levels of parental
investment and different larval morphology. Very few organisms have regulative
embryonic development and are amenable
to blastomere manipulation experiments of
this type (e.g., echinoderms, hemichordates,
phoronids). Of these, only echinoid and asteroid echinoderms have feeding larvae that
can be cultured to metamorphosis readily in
the laboratory. Minimally, we must demonstrate that the results are general (within
a variety of echinoids and asteroids) in order to apply these findings to a general theory of life histories of marine animals.
Food limitation and phenotypic plasticity
Are the results described above from the
study by Sinervo and McEdward (1988) an
artifact of the un-naturally high (unlimited)
food concentrations provided during the experiments? When larvae are food limited,
as is likely in nature, are the effects of egg
size reduction still limited to early stages
and fully eliminated by the 6-armed larval
stage or do they persist through metamorphosis? Work currently underway in my
laboratory by Herrera and McWeeney suggests that high food concentrations are necessary in order for larvae to overcome the
176
LARRY R. MCEDWARD
initial effects of reduced egg size and reach
"normal" size at metamorphic competence.
Larvae often alter body form in response
to different particle concentrations to adjust
the capacity for processing seawater and
capturing food particles (e.g., Boidron-Metairon, 1988; Fenaux et al, 1988; Strathmann et al, 1992). Does the level of parental investment set the scope for morphological, developmental, or physiological
plasticity by determining the nutritional reserves available for allocation to different
larval structures? Answers to these questions will place the relationship between
egg size and larval development within a
more realistic ecological context.
Parental investment and the type of larval
development
Marine organisms with types of larval
development intermediate between feeding
(obligate planktotrophy) and nonfeeding
(obligate lecithotrophy) have been considered rare (Emlet et al., 1987). Theory predicts that intermediates are rare because
natural selection favors only the extreme
levels of parental investment (e.g., Vance,
1973a, b\ Christiansen and Fenchel, 1979).
Almost nothing is known about how organisms evolve from one type of larval development to another. Can a change in the level of parental investment alone shift an organism between feeding and nonfeeding
types of larval development?
We have recently discovered a wide
range of energetic strategies among subtropical echinoids with feeding larvae (Eckert, 1995; Herrera et al, 1996). Many species produce larvae that possess functional
ciliated feeding structures and require particulate exogenous food for development to
metamorphosis. Although they are obligate
planktotrophs, they differ in the degree to
which larvae depend on exogenous food.
The degree of dependence on larval feeding
is related to egg size and energy content
(Herrera et al, 1996). The sand dollar Mellita quinquiesperforata can develop to the
advanced 6-armed larval stage without
feeding (McEdward and George, unpublished). However, dwarf larvae, produced
by blastomere separations can only develop
to the early 4-armed larval stage on endog-
enous reserves (Herrera and McWeeney,
unpublished). This indicates a direct link
between the level of parental investment
and the degree of dependence on exogenous
food.
Clypeaster rosaceus has an unusual type
of larval development known as facultative
planktotrophy. It produces typical feeding
larvae, but the larvae do not need to feed
to complete development to metamorphosis: they are functionally lecithotrophic.
This species produces large eggs (280 u,m
diameter) with a high energy content. Is
facultative planktotrophy the result of a
high level of parental investment? This
question is being addressed by experimentally reducing the level of parental investment and culturing the larvae under conditions of starvation and unlimited food. I
see two possible outcomes. 1) Reduction of
egg size could shift the type of development
to obligate planktotrophy. Larvae that develop from smaller eggs would not have
sufficient material available to complete development to metamorphosis without feeding. Smaller eggs would yield smaller larvae that, if fed, would develop slower, but
metamorphose at the normal size. This is
the result expected based on the observations of Sinervo and McEdward (1988) and
recent work by Herrera and McWeeney. 2)
Reduction of egg size could affect larval
size and development rate without a shift in
development type. Small eggs would produce small larvae that develop as facultative planktotrophs at the normal rate, but
metamorphose into smaller juveniles. This
is the result predicted from the observation
that feeding by larvae of Clypeaster rosaceus does not affect rate of development,
but does result in larger juveniles (Emlet,
1986).
These experiments can provide a definitive answer to the question, can a change in
egg size alone cause a shift in the type of
larval development between obligate and
facultative feeding (lecithotrophy). However, they do not address the question of
evolutionary shifts between complex larvae
that are capable of feeding and simple larvae that are incapable of feeding, which involve major changes in morphogenesis
MANIPULATION OF ECHINOID EGG SIZE
(Wray and Raff, 1991; McEdward and Janies, 1993; Herrera et al., 1996).
CONCLUSIONS
Advances in our understanding of the
ecology of reproduction and development
in marine organisms require combining life
history theory with functional analyses of
larvae as pelagic organisms (Strathmann,
1988). I believe that development will
prove to be an important integrative link between these fields. For that reason, we are
investigating two general questions. First,
what are the developmental effects of a
change in the level of parental investment
on the morphology of feeding larvae? Second, what are the functional consequences
of a given body form for larval growth and
development? These questions are important precisely because development is absent from life history theory as well as from
most studies of larval function. Because larvae change dramatically in form and functional capability throughout ontogeny, it is
insufficient to examine the performance of
larvae at a single stage of development to
infer the consequences for the growth of
subsequent larval stages. Furthermore, we
need to go beyond the correlations among
life history traits that can be obtained from
species comparisons. Experimental manipulations of parental investment, such as
blastomere isolations, combined with morphometric analyses, represent a powerful
approach to the study of larval form, function, and development. Such studies can
provide new information on the effects of
experimental changes in egg size on the larvae that develop from those eggs.
ACKNOWLEDGMENTS
Thanks go to J. Bernardo for his efforts
in organizing the Maternal Effects symposium. S. McWeeney critically reviewed the
manuscript. Discussions with R. Strathmann, M. Hart, I. Boidron-Metairon, J.
Herrera, G. Eckert, and S. McWeeney were
enjoyable and extremely helpful. Special
thanks go to J. Herrera for kindly presenting this paper at the symposium, in my absence. A. O. D. Willows, Director, provided
facilities at the Friday Harbor Laboratories.
Support was provided by NSF grant OCE
177
9115549 and an award from the Division of
Sponsored Research at the University of
Florida.
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