No full-text available
To read the full-text of this research,
you can request a copy directly from the authors.
Egg Energetics for the Facultative Planktotroph Clypeaster rosaceus (Echinodermata: Echinoidea), Revisited
Abstract
The sand dollar Clypeaster rosaceus has an unusual reproductive strategy known as facultative planktotrophy. The egg energy previously reported by Emlet (1) for C. rosaceus is low, and because it is used to estimate values of an important parameter in marine invertebrate life-history models (s), we remeasured the egg energy content. Our measurement of egg energy content was approximately 2-fold greater than Emlet's (0.11 ± 0.014 SD joules (J) egg-1 vs. 0.047 ± 0.007 SD J egg-1) with no difference in egg diameter (274 ± 4.38 SD μm vs. 280 ± 7.67 SD μm). This result is unlikely to be due to temporal or spatial variation among populations of C. rosaceus. Given the improved technique used to measure egg energy content, an egg energy density (J ml-1) more consistent with other observations, and the improved fit of egg size vs. egg energy regressions for echinoderm planktotrophs, we conclude that our estimate is more accurate. In addition, we detected small annual variation (10%) in egg energy content between females sampled during 2000 and 2001.
... Eggs were then collected, washed once in clean ASW and fertilized by adding 1 ml of a dilute sperm solution. Egg diameters for unfertilized eggs of two of the females used were 273.5 F 0.09 Am and 265.7 F 0.35 Am (mean F S.E.), similar to reports from previous studies (Emlet, 1986;Miner et al., 2002). ...
... Our data provide an estimate of energy loss during development of a facultative planktotroph, as well as an estimate of the contribution of feeding to increasing energy content. Recent measures of organic content found that eggs of C. rosaceus contained 2.82 Ag C (Miner et al., 2002). Assuming this starting value, we found that organic content declined by 18.5% to 25.5% in juveniles that were fed or unfed as larvae, respectively. ...
... echinoid Heliocidaris erythrogramma showed no loss of organic content during development . Given some discrepancy in the literature concerning egg organic content measures (Miner et al., 2002;Emlet, 1986), however, measurements of egg and juvenile organic content within a single study will be needed to estimate absolute changes in organic content during the development of C. rosaceus. ...
In free-spawning marine invertebrates, larval development typically proceeds by one of two modes: planktotrophy (obligate larval feeding) from small eggs or lecithotrophy (obligate non-feeding) from relatively large eggs. In a rare third developmental mode, facultative planktotrophy, larvae can feed, but do not require particulate food to complete metamorphosis. Facultative planktotrophy is thought to be an intermediate condition that results from an evolutionary increase in energy content in the small eggs of a planktotrophic ancestor. We tested whether an experimental reduction in egg size is sufficient to restore obligate planktotrophy from facultative planktotrophy and whether the two sources of larval nutrition (feeding and energy in the egg) differentially influence larval survival and juvenile quality. We predicted, based on its large egg size, that a reduction in egg size in the echinoid echinoderm Clypeaster rosaceus would affect juvenile size but not time to metamorphosis. We reduced the effective size of whole (W) zygotes by separating blastomeres at the two- or four-cell stages to create half- (H) or quarter-size (Q) “zygotes” and reared larvae to metamorphosis, both with and without particulate food. Larvae metamorphosed at approximately the same time regardless of food or egg size treatment. In contrast, juveniles that developed from W zygotes were significantly larger, had higher organic content and had longer and more numerous spines than juveniles from H or Q zygotes. Larvae from W, H and Q zygotes were able to reach metamorphosis without feeding, suggesting that the evolution of facultative planktotrophy in C. rosaceus was accompanied by more than a simple increase in egg size. In addition, our results suggest that resources lost by halving egg size have a larger effect on larval survival and juvenile quality than those lost by withholding particulate food.
... To calculate energy content per egg, we used the dichromate oxidation method as described by Miner et al. (2002) with the following modifications: eggs were briefly rinsed in distilled H 2 O, and 3-5 replicates of a known number of eggs (20/replicate for C. rosaceus, 25/replicate for B. latifrons, and 100/replicate for C. subdepressus) per female were then frozen in a minimal volume of dH 2 O. Energy per egg was then measured as described, with glucose as a standard. ...
... Our measurements of egg size for Clypeaster rosaceus, C. subdepressus, and Brisaster latifrons and for protein content in B. latifrons are consistent with previously reported values (Table 1). Our estimate of egg energy for C. rosaceus falls between four previous estimates: we studied Panamanian individuals and estimated egg energy at 0.076 J/egg, Emlet (1986) estimated that Panamanian C. rosaceus contain 0.047 J/egg (cited in Miner et al., 2002), whereas Miner et al. (2002) and Heyland et al. (2006) estimated that Floridian C. rosaceus contain 0.106 J/egg and 0.065 J/egg, respectively. The value from Heyland et al. (2006) was converted from reported values of organic C using the conversion 1 g C ϭ 3.9 ϫ 10 Ϫ2 J (after McEdward and Carson, 1987). ...
... Our measurements of egg size for Clypeaster rosaceus, C. subdepressus, and Brisaster latifrons and for protein content in B. latifrons are consistent with previously reported values (Table 1). Our estimate of egg energy for C. rosaceus falls between four previous estimates: we studied Panamanian individuals and estimated egg energy at 0.076 J/egg, Emlet (1986) estimated that Panamanian C. rosaceus contain 0.047 J/egg (cited in Miner et al., 2002), whereas Miner et al. (2002) and Heyland et al. (2006) estimated that Floridian C. rosaceus contain 0.106 J/egg and 0.065 J/egg, respectively. The value from Heyland et al. (2006) was converted from reported values of organic C using the conversion 1 g C ϭ 3.9 ϫ 10 Ϫ2 J (after McEdward and Carson, 1987). ...
Larvae of marine invertebrates either arise from small eggs and feed during their development or arise from large eggs that proceed to metamorphosis sustained only from maternal provisioning. Only a few species are known to possess facultatively feeding larvae. Of about 250 echinoid species with known mode of development, only two, Brisaster latifrons and Clypeaster rosaceus, are known to develop through facultatively planktotrophic larvae. To obtain more information on this form of development and its consequences, we determined egg size and egg energetic and protein content of these two species. We found that eggs of B. latifrons resemble those of species with nonfeeding larvae in these characteristics more than those of C. rosaceus. We also compared DNA sequences of the cytochrome oxidase (COI) gene from the Caribbean C. rosaceus to those of the sympatric planktotrophic developer C. subdepressus and also to those of the eastern Pacific species C. europacificus to estimate the degree of divergence between species with different developmental modes. Comparison of COI sequences of C. rosaceus from Panama and Florida revealed that there is no geographic differentiation in this species. Cross-fertilization experiments between C. rosaceus and C. subdepressus indicated that bidirectional gametic incompatibility has evolved between the two species.
... By contrast, larvae from the sea biscuit Clypeaster rosaceous (family Clypeasteridae; egg size 260-280µm) are functionally lecithotrophic in that larvae complete metamorphosis when starved. Since these larvae (unlike obligatorily lecithotrophic larvae) have the ability to feed, they are called facultative planktotrophic larvae (Emlet 1986;Miner et al. 2002, see Fig. 3-1). (Note that the egg size and juvenile size ranges mentioned here are data we collected over the past years from females we spawned in the laboratory. ...
... (Note that the egg size and juvenile size ranges mentioned here are data we collected over the past years from females we spawned in the laboratory. This variability in egg size however has also been previously mentioned (see Hadfield and Strathmann 1996;Miner et al. 2002). From an evolutionary point of view, facultative feeding has been hypothesized as an intermediate life history strategy between planktotrophy and lecithotrophy (Emlet 1986;Hart 1996). ...
... Another method that has been employed by many authors (e.g., McEdward et al., 1988;McEdward and Chia, 1991;Moreno and Hoegh-Guldberg, 1999;Miner et al., 2002;Zigler et al., 2008) is the potassium dichromate wet oxidation method (PDWO) described in Parsons et al., (1984). PDWO is a colorimetric method used to estimate total energetic content. ...
Egg size is one of the most important aspects of the life history of free-spawning marine organisms, and it is correlated with larval developmental mode and many other life-history characters. Egg size is simple to measure and data are available for a wide range of taxa, but we have a limited understanding of how large and small eggs differ in composition; size is not always the best measure of the characters under selection. Large eggs are generally considered to reflect increased maternal investment, but egg size alone can be a poor predictor of energetic content within and among taxa. We review techniques that have been used to measure the energetic content and biochemical makeup of invertebrate eggs and point out the strengths and difficulties associated with each. We also suggest a number of comparative and descriptive approaches to biochemical constituent analysis that would strengthen our understanding of how natural selection shapes oogenic strategies. Finally, we highlight recent empirical research on the intrinsic factors that drive intraspecific variation in egg size. We also highlight the relative paucity of these data in the literature and provide some suggestions for future research directions.
... A study by Adams et al. (2011) suggests that this type of manipulation or modification is feasible (see later). With respect to the second strategy, larger egg size typically reflects an increase in maternally provisioned energetic materials, which are used to build larger larvae and to fuel more rapid larval development (McAlister and Moran, 2012;see Marshall et al., 2008, and Moran and McAliste r, planktotroph Clypeaster rosaceus, egg volume 10.77 nl, egg energy 110 mJ; Miner et al., 2002). ...
Nearly three decades ago, biologists discovered that planktotrophic larvae of sea urchins can alter the size of their ciliated feeding structures in response to the concentration of food (i.e., unicellular algae). In the years since, this response has become one of the best-studied examples of phenotypic plasticity in marine organisms. Researchers have found that this form of plasticity occurs widely among different types of feeding larvae in several phyla, and involves energetic trade-offs with a suite of correlated life-history characters. Furthermore, investigators have recently started to unravel the genetic and molecular mechanisms underlying this plasticity. We review the literature on feeding-structure plasticity in marine invertebrate larvae highlighting the diversity of species and variety of experimental designs and statistical methodologies, and summarizing research findings to draw more general conclusions, and target promising directions for future research.
... The distilled water was then removed. Total energy was determined with the colorimetric acid dichromate oxidation method described by Miner et al. (2002) after the original method developed by Parsons et al. (1984). Ten zygotes, larvae, or juveniles were used per replicate. ...
Phylogenetic analyses have demonstrated that nonfeeding larvae have evolved from feeding larvae many times among marine invertebrates.
In light of this observation, it is surprising that an intermediate strategy, a larva that can feed but is provisioned with
enough energy to metamorphose without acquiring exogenous food (i.e., facultative planktotrophy), is rare. A hypothesis for
the lack of facultative planktotrophic species among marine invertebrates is that the transition from feeding to nonfeeding
is rapid due to this intermediate stage being evolutionarily unstable. Evidence that would support this hypothesis is if species
with facultative planktotrophy have reduced food assimilation when compared with obligate planktotrophs. We studied a species
with facultative planktotrophic larvae, Clypeaster rosaceus, that is very near the boundary between facultative and obligatory planktotrophy, to answer two questions: (1) does feeding
during the larval stage result in energy gains in larval or juvenile stages and (2) if not, are larvae capable of assimilating
exogenous food at all. Our measurements of energetics in larval and juvenile stages show that C. rosaceus larvae accumulate very little if any energy when fed, but stable isotope data indicate that larvae are able to assimilate
some food. Our results are consistent with similar studies on facultative planktotrophic larvae suggesting poor food assimilation
and rapid loss of larval feeding after a population evolves the ability to reach metamorphosis without feeding (lecithotrophy).
... Another method that has been employed by many authors (e.g., McEdward et al., 1988;McEdward and Chia, 1991;Moreno and Hoegh-Guldberg, 1999;Miner et al., 2002;Zigler et al., 2008) is the potassium dichromate wet oxidation method (PDWO) described in Parsons et al., (1984). PDWO is a colorimetric method used to estimate total energetic content. ...
Egg size is one of the most important aspects of the life history of free-spawning marine organisms, and it is correlated with larval developmental mode and many other life-history characters. Egg size is simple to measure and data are available for a wide range of taxa, but we have a limited understanding of how large and small eggs differ in composition; size is not always the best measure of the characters under selection. Large eggs are generally considered to reflect increased maternal investment, but egg size alone can be a poor predictor of energetic content within and among taxa. We review techniques that have been used to measure the energetic content and biochemical makeup of invertebrate eggs and point out the strengths and difficulties associated with each. We also suggest a number of comparative and descriptive approaches to biochemical constituent analysis that would strengthen our understanding of how natural selection shapes oogenic strategies. Finally, we highlight recent empirical research on the intrinsic factors that drive intraspecific variation in egg size. We also highlight the relative paucity of these data in the literature and provide some suggestions for future research directions.
... A question that needs further investigation is whether the phenotypically plastic response of larval and juvenile structures to endogenous hormone levels is a general characteristic of nonfeeding larvae, or whether it is only present in C. rosaceus with its specialized feeding mode (facultative planktotrophy). Because these sea biscuit larvae have the ability to feed, a certain amount of plasticity is retained because it could give larvae an adaptive advantage: Miner et al. (2002) observed previously that egg size and egg energy in C. rosaceus can vary significantly between females. This natural variation could lead to a situation where insufficient maternal reserves are compensated for during the larval period, making feeding obligatory in order to reach metamorphosis . ...
Critical roles of hormones in metamorphic life history transitions are well documented in amphibians, lampreys, insects, and many plant species. Recent evidence suggests that thyroid hormones (TH) or TH-like compounds can regulate development to metamorphosis in echinoids (sea urchins, sand dollars, and their relatives). Moreover, previous research has provided evidence for endogenous hormone synthesis in both feeding and nonfeeding echinoderm larvae. However, the mechanisms for endogenous synthesis remain largely unknown. Here, we show that facultatively planktotrophic larvae (larvae that reach metamorphosis in the absence of food but have the ability to feed) from the subtropical sea biscuit Clypeaster rosaceus can synthesize thyroxine endogenously from incorporated iodine (I(125)). When treated with the goitrogen thiourea (a peroxidase inhibitor), iodine incorporation, thyroxine synthesis, and metamorphosis are all blocked in a dose-dependent manner. The inhibitory effect on metamorphosis can be rescued by administration of exogenous thyroxine. Finally, we demonstrate that thiourea induces morphological changes in feeding structures comparable to the phenotypic plastic response of larval structures to low food conditions, further supporting a signaling role of thyroxine in regulating larval morphogenesis and phenotypic plasticity. We conclude that upregulation of endogenous hormone synthesis might have been associated with the evolution of nonfeeding development, subsequently leading to morphological changes characteristic of nonfeeding development.
Marine organisms exhibit substantial life-history diversity, of which egg size is one fundamental parameter. The size of an egg is generally assumed to reflect the amount of energy it contains and the amount of per-offspring maternal investment. Egg size and energy are thought to scale isometrically. We investigated this relationship by updating published datasets for echinoderms, increasing the number of species over those in previous studies by 62%. When we plotted egg energy versus egg size in the updated dataset we found that planktotrophs have a scaling factor significantly lower than 1, demonstrating an overall trend toward lower energy density in larger planktotrophic eggs. By looking within three genera, Echinometra, Strongylocentrotus, and Arbacia, we also found that the scaling exponent differed among taxa, and that in Echinometra, energy density was significantly lower in species with larger eggs. Theoretical models generally assume a strong tradeoff between egg size and fecundity that limits energetic investment and constrains life-history evolution. These data suggest that the evolution of egg size and egg energy content can be decoupled, possibly facilitating response to selective factors such as sperm limitation which could act on volume alone.
Per-offspring maternal investment is an integral part of life-history theory. To understand the evolution of per-offspring maternal investment in marine invertebrates, a number of mathematical models have been developed. These models examine how selection affects the proportion of maternally derived egg energy used to produce a newly metamorphosed juvenile (s) and make predictions about the distribution of s in nature. However, there are very few published values of s and therefore it is difficult to evaluate how well these models match nature. We present several equations to empirically estimate values of s for any group of marine invertebrate, and use data from echinoderms to compare the different equations. The calculations that directly estimate s require information on the amount of egg energy, juvenile energy, and energy metabolized during development. Currently, there are few data available for directly estimating s, and thus generating distributions of s derived from direct estimates is not possible. Furthermore, the direct estimations of s are informative for planktotrophy but not for lecithotrophy. We have developed an equation that can be used to directly estimate s for lecithotrophs. The calculations to indirectly estimate s only require egg energy or egg size for the species in question and the value of s and egg energy or size for a reference species. This reference species replaces the need to measure juvenile energy and energy metabolized during larval development. Because egg energy or size is currently available for many species, the indirect estimates will be useful for generating distributions of s, and will allow comparisons with models. Although these indirect methods are good for generating distributions of s, they do not provide reliable estimates of s for any particular species. Estimating values of s to compare models is a critical gap in our current evaluations of marine invertebrate life-history models.
Dichromate oxidation is a simple technique that is often used to estimate the energy content of eggs in studies of marine invertebrate life histories (1). We used this method to measure the energy contents of the eggs of 12 species of marine annelids. In combination with measures of egg ash-free dry weight (AFDW), these data yielded estimates of AFDW-specific energy density that were mostly lower than the average weight-specific energy density of carbohydrates. This seemed unlikely to be correct, as invertebrate eggs typically contain little carbohydrate and instead are composed primarily of energy-dense protein and lipid (1, 2). After validating our methods (by using them to estimate energy content and AFDW of the eggs of a previously studied echinoderm) and reexamining published data on the energy contents of echinoderm eggs, we conclude that dichromate oxidation often underestimates the energy contents of small eggs of marine invertebrates. This systematic error, which is likely related to the tendency of the assay to incompletely oxidize proteins, can only be corrected with substantial independent data on egg biochemical composition. We thus suggest that dichromate oxidation should not be used for routine measurement of the total energy content of marine invertebrate eggs.
Evolutionary transitions in larval nutritional mode have occurred on numerous occasions independently in many marine invertebrate phyla. Although the evolutionary transition from feeding to nonfeeding development has received considerable attention through both experimental and theoretical studies, mechanisms underlying the change in life history remain poorly understood. Facultative feeding larvae (larvae that can feed but will complete metamorphosis without food) presumably represent an intermediate developmental mode between obligate feeding and nonfeeding. Here we show that an obligatorily feeding larva can be transformed into a facultative feeding larva when exposed to the thyroid hormone thyroxine. We report that larvae of the subtropical sand dollar Leodia sexiesperforata (Echinodermata: Echinoidea) completed metamorphosis without exogenous food when treated with thyroxine, whereas the starved controls (no thyroxine added) did not. Leodia sexiesperforata juveniles from the thyroxine treatment were viable after metamorphosis but were significantly smaller and contained less energy than sibling juveniles reared with exogenous food. In a second starvation experiment, using an L. sexiesperforata female whose eggs were substantially larger than in the first experiment (202+/-5 vs. 187+/-5 microm), a small percentage of starved L. sexiesperforata larvae completed metamorphosis in the absence of food. Still, thyroxine-treated larvae in this experiment completed metamorphosis faster and in much higher numbers than in the starved controls. Furthermore, starved larvae of the sand dollar Mellita tenuis, which developed from much smaller eggs (100+/-2 microm), did not complete metamorphosis either with or without excess thyroxine. Based on these data, and from recent experiments with other echinoids, we hypothesize that thyroxine plays a major role in echinoderm metamorphosis and the evolution of life history transitions in this group. We discuss our results in the context of current life history models for marine invertebrates, emphasizing the role of egg size, juvenile size, and endogenous hormone production for the evolution of nonfeeding larval development.
Observations of a sea urchin larvae show that most species adopt one of two life history strategies. One strategy is to make numerous small eggs, which develop into a larva with a required feeding period in the water column before metamorphosis. In contrast, the second strategy is to make fewer large eggs with a larva that does not feed, which reduces the time to metamorphosis and thus the time spent in the water column. The larvae associated with each strategy have distinct morphologies and developmental processes that reflect their feeding requirements, so that those that feed exhibit indirect development with a complex larva, and those that do not feed form a morphologically simplified larva and exhibit direct development. Phylogenetic studies show that, in sea urchins, a feeding larva, the pluteus, is the ancestral form and the morphologically simplified direct-developing larva is derived. The current hypothesis for evolution of the direct-developing larval form in sea urchins suggests that major developmental changes occur by neutral loss of larval features after the crucial transition to a nonfeeding life history strategy. We present evidence from Clypeaster rosaceus, a sea urchin with a life history intermediate to the two strategies, which indicates that major developmental changes for accelerated development have been selected for in a larva that can still feed and maintains an outward, pluteus morphology. We suggest that transformation of larval form has resulted from strong selection on early initiation and acceleration of adult development.
The protein and lipid content of the eggs, fed and starved larvae of Encope michelini were examined in the laboratory and results compared with those of other obligate planktotrophs. The protein and lipid content of the eggs of E. michelini were higher, and the lipid:protein ratios were five to nine times higher than in most other obligate planktotrophs. Increase in larval size and development to the 8-arm stage was accompanied by a decrease in protein and lipid content for starved larvae but an increase for fed larvae. The main advantage of producing planktotrophic eggs with a high protein and lipid content is that it reduces the amount of endogenous food that must be obtained by feeding to construct the complete set of larval arms. This reduces the total time spent in the plankton and thus the risk fiom being eaten. In addition, after a period of food scarcity, a filly developed 8-arm E. michelini larvae would be more efficient at capturing particles than a 4-arm larva fiom smaller eggs with a low protein and lipid content.
SYNOPSIS. The degree to which a female partitions resources between fecundity and per offspring investment is a central question in life-history theory. Maternal effects may influence the nature of this tradeoff through their effect on per offspring investment and subsequent offspring fitness. The purpose of this study was to determine the effect of female age and size on brood size (number of offspring), per offspring investment, and fitness in the polychaete Streblospio benedicti . Early stage embryos were collected from brooding females of known age and size over a period of 100 days; these embryos were counted and analyzed for their C and N content. Female size had a positive effect on brood size; larger females produced larger broods. However, brood size decreased with female age (females did not increase in size after reaching sexual maturity). Brood size declined 20–46% between 60 and 160 days of age. During this same age period per offspring investment, measured in terms of C and N, increased by 25%. Offspring survivorship and size at two weeks post-release from the female were used as measures of offspring fitness. Offspring survivorship increased 28% between 60 and 160 days of age. Increased growth in offspring from older females resulted in a 23% increase in offspring size at two weeks. Including the maternal age effect in two population models for S. benedicti increased population growth rate (λ). Population growth was increased to a greater degree when the maternal effect was modeled by enhancing offspring survival compared to when fecundity was increased by the same proportional amount. This suggests that the maternal effect may be adaptive, particularly when conditions for offspring survival and growth are poor.
Life-history models for marine invertebrate larvae generally predict a dichotomy in egg size in different species: eggs should be either minimal in size or large enough to support development fully without larval feeding. This prediction is contradicted, however, by the empirical observation of wide, continuous variation in egg size between these extremes. The prediction of dichotomy rests on the assumption of a negative linear relationship between egg size and development time. Here, I present a simple model in which development time is inversely proportional to egg size. Incorporating this relationship into an optimality model produces predictions of intermediate rather than extreme egg size. Modeled variations in mortality, food availability, fertilization rates, and temperature all produce continuous shifts in the value of the intermediate optimal size, in direct contrast to those produced by previous models, which predict shifts between two extreme optima. Empirical data on echinoid egg size and development time strongly support the model's assumption of an inverse proportional relationship between egg size and development time. A composite phylogeny is constructed of the 37 species for which egg size, development time, water temperature, and phylogenetic relatedness are known. Independent contrasts are made of the evolutionary changes in egg size and development time. This analysis indicates that evolutionary shifts in development time are correlated with the inversely proportional shifts in egg size assumed in the model. The assumption of a negative linear relationship used in previous models is rejected. This model provides a potential explanation for intraspecific variation in egg size along environmental gradients, sympatric differences in egg size among species, and biogeographic trends in egg size and development mode across taxa.
Per brood and per offspring C and N invest- ment were examined in four developmental morphs of the spionid polychaete Streblospio: S. shrubsolii (direct development, D), S. benedicti (lecithotrophic, L), S. bene- dicti (planktotrophic, P), and Streblospio n. sp. (plank- totrophic, P). Large differences were apparent among these morphs in fecundity and embryo size. S. shrubsolii (D) and S. benedicti (L) invested about 10 X more C and N in each offspring and 30% more C and N in each brood than did the morphs with planktotrophic development. C and N concentration (pg per unit volume) was signifi- cantly greater in S. benedicti (L) than in the other morphs, though no general relationship with embryo size was ev- ident. The C:N ratio of offspring did not differ among the four morphs. Comparisons of estimated lifetime repro- ductive investment made by the two developmental types of S. benedicti indicated that lecithotrophic development involved twice the C and N investment in reproduction. Positive, significant regressions were evident between em- bryo C and N content and embryo volume at the inter- morph level. Significant intra-morph regressions were ev- ident in all morphs but Strebfospio n. sp. (P). However, the large amount of variation unaccounted for by embryo volume calls into question the use of embryo size as a predictor of parental investment in offspring.
The evolution of life cycles involves transitions between discrete states in one or more of the characters that comprise a developmental pattern. In this paper, we examine three of the major life cycle characters and the states for these characters. Using examples from echinoderms, we discuss the evolutionary transitions that have occurred in the type of morphogenesis, developmental habitat, and mode of nutrition during development. We evaluate the functional requirements associated with these transitions to infer the likelihood (frequency or rapidity) of change in a given character and of biases in the polarity of character state transitions. Using comparisons of closely related species, we evaluate the change between states in one character for dependence on the state of, or correlated changes in, other characters. Based on our analysis of congeneric species that differ in developmental habitat, we conclude that the transition between pelagic and benthic development is an ecological change that is independent of changes in morphogenesis and should be reversible. In contrast, the transition from feeding to nonfeeding development has been considered to be irreversible because it involves marked changes in larval morphology. We re-examine the transition between different modes of larval nutrition in light of recent studies that show that there exists a continuum of nutritional strategies between planktotrophy and lecithotrophy. This continuum is largely determined by variation in maternal investment and does not involve alterations in larval morphology. We suggest that the boundary between planktotrophy and lecithotrophy is frequently crossed and that this transition is reversible. Ecological changes represent the crossing of a functional threshold. Only after crossing the threshold, do larvae experience qualitatively different selective pressures that can lead to subsequent changes in morphology and development. Two different changes have occurred in the type of morphogenesis: the simplification of larval morphology that is associated with obligate (nonfeeding) lecithotrophy and the loss of the larval body plan in the evolution from indirect to direct development. It is the modification of morphology independent of the ecological changes that requires alterations in developmental processes, constrains evolutionary options, imposes irreversibility, and establishes the discrete nature of larval patterns in marine invertebrates.
Gamete production, somatic growth and reproductive effort were measured in sea urchins maintained on a mixture of kelp and mussel flesh at three ration levels. Urchins on low ration were able to maintain an output of gametes half that of urchins fed ad libitum. This was achieved at the expense of somatic production, which was negative in the low ration groups. Despite the reduction in the output of gametes, reproductive effort was greater in the low ration urchins than in the well fed ones. The lipid content and the energy content were greater in eggs released by urchins fed ad libitum than in eggs produced by urchins at low ration.Several indices of reproductive effort were derived from the data and their advantages and disadvantages evaluated. All showed the same trend towards an increase in reproductive effort as the food supply was depleted. In order to obtain some of these indices, it was necessary to measure oxygen uptake, ammonia excretion, ingestion rate and absorption rate, but a direct partitioning of energy between growth and reproduction was found to be the most ecologically meaningful approach to the problem, and does not require measurement of physiological variates. In situations where growth cannot be measured, however, reproductive effort may be expressed as the production of gametes divided by the energy ingested or absorbed.A shift in the allocation of resources from growth to reproduction is seen as an appropriate response to a depletion of the food supply in an environment in which the duration of adverse conditions cannot be predicted. Under these circumstances, investment in growth may be unprofitable, yet the urchin may retain the capacity to restore the normal energy balance should conditions improve.
In 7 species of echinoderms, 2 species of polychaetes, and 1 species of oyster with feeding larvae, larger eggs were found to contain more organic matter. Although organic matter per egg increases with egg diameter or volume, it is not proportionate to egg volume, because small eggs have more concentrated organic matter than larger eggs. There appear to be differences among higher taxa in the minimum size of freely spawned eggs. These differences could result from different relationships between mortality and reduced egg size arising from differences between larval feeding mechanisms or differences in size at metamorphosis. An egg has more than five times the organic matter of a diatom of the same size and is thus a bigger meal for suspension feeders.
Mean egg energy content (J · egg−1) was significantly and positivelycorrelated with mean egg volume among seven species of holothuroid and asteroid echinoderms with pelagic lecithotrophic (non-feeding) larval development. However, there were not consistent intraspecific relationships between egg size and energy content. Mean egg energy concentration (J · μl−1) was variable but was not significantly correlated with egg volume, in contrast to the negative correlation reported for species with planktotrophic (feeding) larvae. Egg energy concentrations in species with pelagic lecithotrophic larvae are similar to those in species with benthic lecithotrophic development (brooding) and significantly greater than in species with pelagic planktotrophic larvae.
Larvae of the tropical sand dollar Encope michelini (Agassiz) have a novel feeding strategy in which they can develop all larval structures and survive in the absence of external food, but require external food (greater than 1 μm) to build the juvenile rudiment and undergo metamorphosis. E. michelini larvae are “enhanced” planktotrophs. They use maternal reserves to develop further than planktotrophs in the absence of external sources of nutrition. Yet they are different from lecithotrophs or facultative planktotrophs, because they cannot develop consistently to metamorphosis in the absence of external sources of nutrition. Three experiments were conducted to examine this novel feeding strategy. The first tested the effect of varying the quantity and quality of food. The second tested the effect of varying the timing of feeding, and the third tested the effect of culturing the larvae in sterile, autoclaved seawater. In the first experiment starved larvae survived as well as fed larvae for the first nine days of development and persisted for up to 48 days, which was five times the development time of fed larvae. Larvae that were cultured with enrichment [either 50 cells · μl−1 of Dunaliella tertiolecta (Butcher) or Isochrysis galbana (Tahitian) (Green)] had longer bodies, metamorphosed earlier, and resulted in larger postmetamorphic juveniles. Natural seawater was a better culture medium than filtered seawater, because a higher proportion of larvae cultured in natural seawater survived, had larger larval bodies, and metamorphosed. In the second experiment providing food during the early stage of development influenced the size of the larval body early in development and the proportion of larvae that metamorphosed. Providing food during later stages in development, when juvenile structures were being built, resulted in larvae with larger bodies, a higher proportion of metamorphosis, and larger postmetamorphic juveniles. A higher proportion of larvae that were cultured in sterile, autoclaved seawater survived compared to larvae cultured in only filtered seawater, presumably because deleterious bacteria and viruses were not present. Larvae cultured in sterile, autoclaved seawater tended to be smaller (in arm length and body length) than larvae cultured in filtered seawater.The ability of E. michelini larvae to grow to full size under starvation conditions is unique for a species with feeding development. If larvae can still become competent after starvation, then this is a mechanism by which this species of larvae can extend the larval period if food is not available. The feeding strategy employed by E. michelini larvae is a novel intermediate which most closely resembles planktotrophy. Such an intermediate is predicted by theoretical models to be evolutionarily unstable. Perhaps it is, but alternatively, the models may be incomplete because they only consider selection on gamete size and larval survival. Revision of the models to include selection on juvenile success may reveal different evolutionary patterns, because selection for large eggs, in planktotrophic species, may be based on juvenile success rather than on larval success. If this revised theory is correct, then this type of feeding strategy may occur in other marine invertebrate taxa.
Larval development to metamorphosis and early juvenile growth and survivorship were examined in Clypeaster subdepressus (Gray) and C. rosaceus (Linnaeus). C. subdepressus has an obligatorily planktotrophic larva that metamorphoses after 16 to 28 days at 27°C. The larva of C. rosaceus can, but need not feed prior to metamorphosis, which occurs after 5 to 7 days at 27°C. Feeding by larvae of C. rosaceus does not change the time to metamorphosis but does increase size at metamorphosis, early juvenile growth and may increase juvenile survivorship relative to unfed larvae. Size at metamorphosis increases in larvae of C. rosaceus that feed for several days after they are competent to metamorphose, but there may be a limit to this increase because the condition of the rudiment degenerates after a period of time. The development of C. rosaceus may represent a transition between planktotrophy and lecithotrophy. This intermediate state has advantages for the juvenile stage that are not included in the trade of fecundity against risk to offspring usually considered in life history discussions of developmental mode of marine invertebrates.
Differences in egg quality within and between populations of Arbacia lixula were investigated in the laboratory. Individuals from Cap Ferrat, Mediterranean, France, produced eggs with a higher protein and lipid contt than individuals from Villefranche, Mediterranean, France. This led to faster growth and development and greater survival in larvae from individuals from Cap Ferrat. The low protein and lipid content of eggs from individuals from Villefranche compared to those from Cap Ferrat. may have bn due to differences in the abundance of different algal species in the two localities and consequently the diet of sea urchins.
Fecundity-time models of reproductive strategies in marine invertebrates all predict that reproductive success is maximized only at the extreme levels of investment. Selection should drive egg sizes toward small eggs and planktotrophy or large eggs and lecithotrophy. The existence of two distinct larval types, feeding and nonfeeding, has been taken as confirmation of this prediction and has established the current paradigm for larval ecology. However, comparative and experimental evidence does not support the prediction that egg size is minimized in species with planktotrophic larvae. Recent discoveries have documented the existence of planktotrophs that have intermediate egg sizes, differing degrees of dependence on exogenous food, and differing capacities for facultative feeding. A fecundity-time model is presented that includes facultative larval feeding by dissociating the onset of feeding capability from the need for exogenous food. The facultative feeding model shows that reproductive success can be maximized at intermediate levels of investment per offspring between the minimum for development and the threshold for lecithotrophy, depending on the amount of food available to larvae and the intensity of planktonic mortality. A continuum of larval strategies is predicted.
The larval patterns of marine invertebrates pose intriguing questions for both evolutionary and developmental biologists. However, combined investigations have been rare. Quantitative models analyze the selective factors that drive evolutionary change in larval nutrition and timing of metamorphosis. Developmental studies describe the morphogenesis characterizing ancestral and derived larval patterns. Rigorous evolutionary analysis of the transition to derived modes of development is lacking and detailed developmental and ecological data are needed to test and refine theoretical models. A major challenge facing studies of life cycle evolution is the elucidation of the genetic structure and covariance of important developmental and larval traits.
The relationship between the size of an egg and its energy content was analyzed using published data for 47 species of echinoderms. Scaling relationships were evaluated for all species, as well as for subsets of the species, based on mode of development. Regressions were calculated using linear, power function, full allometric, and second-order polynomial models. The full allometric model is preferred because it is relatively simple and the most general. Among these species of echinoderms, larger eggs contain more energy. Egg energy content scales isometrically across a wide range of egg sizes both among and within different modes of development. The only exception is among species with feeding larval development, where there does not seem to be a clear scaling relationship. In most cases, the regressions were statistically significant and explained a very large proportion of the variance in energy content. However, there were wide confidence intervals around the estimated regression parameters. In all cases, the predictive power of the regression was poor, requiring large differences in egg size to yield significantly different predictions of energy content. Consequently, egg size is of limited value for the quantitative prediction of egg energy content and should be used with caution in life-history studies.
Clypeasteroida: Echinoidea)
- Clypeaster Egg
CLYPEASTER ROSACEUS EGG ENERGETICS planktotrophy in Clypeaster subdepressus (Gray) (Clypeasteroida: Echinoidea). J. Exp. Mar. Biol. Ecol. 95: 183-202.
planktotrophy in Clypeaster subdepressus (Gray) (Clypeasteroida: Echinoidea)
- B G Miner
B. G. MINER ET AL.
planktotrophy in Clypeaster subdepressus (Gray) (Clypeasteroida:
Echinoidea). J. Exp. Mar. Biol. Ecol. 95: 183–202.