EVOLUTIONARY LOSS OF LARVAL FEEDING: DEVELOPMENT,FORM AND FUNCTION IN A FACULTATIVELY FEEDING LARVA,BRISASTER LATIFRONS

Species with large eggs and nonfeeding larvae have evolved many times from ancestors with smaller eggs and feeding larvae in numerous groups of aquatic invertebrates and amphibians. This change in reproductive allocation and larval form is often accompanied by dramatic changes in development. Little is known of this transformation because the intermediate form (a facultatively feeding larva) is rare. Knowledge of facultatively feeding larvae may help explain the conditions under which nonfeeding larvae evolve. Two hypotheses concerning the evolutionary loss of larval feeding are as follows: (1) large eggs evolve before modifications in larval development, and (2) the intermediate form (facultatively feeding larva) is evolutionarily short-lived. I show that larvae of a heart urchin, Brisaster latifrons, are capable of feeding but do not require food to complete larval development. Food for larvae appears to have little effect on larval growth and development. The development, form, and suspension feeding mechanism of these larvae are similar to those of obligate-feeding larvae of other echinoids. Feeding rates of Brisaster larvae are similar to cooccurring, obligate-feeding echinoid larvae but are low relative to the large size of Brisaster larvae. The comparison shows that in Brisaster large egg size, independence from larval food, and relatively low feeding rate have evolved before the heterochronies and modified developmental mechanisms common in nonfeeding echinoid larvae. If it is general, the result suggests that hypotheses concerning the origin of nonfeeding larval development should be based on ecological factors that affect natural selection for large eggs, rather than on the evolution of heterochronies and developmental novelties in particular clades. I also discuss alternative hypotheses concerning the evolutionary persistence of facultative larval feeding as a reproductive strategy. These hypotheses could be tested against a phylogenetic hypothesis.     

Heterochronic developmental shift caused by thyroid hormone in larval sand dollars and its implications for phenotypic plasticity and the evolution of nonfeeding development

Recent work on a diverse array of echinoderm species has demonstrated, as is true in amphibians, that thyroid hormone (TH) accelerates development to metamorphosis. Interestingly, the feeding larvae of several species of sea urchins seem to obtain TH through their diet of planktonic algae (exogenous source), whereas nonfeeding larvae of the sand dollar Peronella japonica produce TH themselves (endogenous source). Here we examine the effects of TH (thyroxine) and a TH synthesis inhibitor (thiourea) on the development of Dendraster excentricus, a sand dollar with a feeding larva. We report reduced larval skeleton lengths and more rapid development of the juvenile rudiment in the exogenous TH treatments when compared to controls. Also, larvae treated with exogenous TH reached metamorphic competence faster at a significantly reduced juvenile size, representing the greatest reduction in juvenile size ever reported for an echinoid species with feeding larvae. These effects of TH on D. excentricus larval development are strikingly similar to the phenotypically plastic response of D. excentricus larvae reared under high food conditions. We hypothesize that exogenous (algae-derived) TH is the plasticity cue in echinoid larvae, and that the larvae use ingested TH levels as an indicator for larval nutrition, ultimately signaling the attainment of metamorphic competence. Furthermore, our experiments with the TH synthesis inhibitor thiourea indicate that D. excentricus larvae can produce some TH endogenously. Endogenous TH production might, therefore, be a shared feature among sand dollars, facilitating the evolution of nonfeeding larval development in that group. Mounting evidence on the effects of thyroid hormones in echinoderm development suggests life-history models need to incorporate metamorphic hormone effects and the evolution of metamorphic hormone production.     

Molecular phylogenetic and embryological evidence that feeding larvae have been reacquired in a marine gastropod

Evolutionary transitions between different modes of development in marine invertebrates are thought to be biased toward the loss of feeding larvae. Because the morphology of feeding larvae is complex and nonfeeding larvae or encapsulated embryos with benthic development often have simplified morphologies, it is presumed to be easier to lose a larval stage than to reacquire it. Some authors have gone so far as to suggest that feeding larvae, morphologically similar to the ancestral feeding larvae, cannot be reacquired. However, the larval structures of some groups, most notably gastropods, are often retained in the encapsulated embryos of species that hatch as benthic juveniles. Therefore the re-evolution of feeding larvae using the same structures may be possible in these groups. Here we present the first well-substantiated case for the recent re-evolution of feeding larvae within a clade of direct-developers. DNA sequence data show that Crepipatella fecunda, a species of calyptraeid gastropod with planktotrophic development, is nested within a clade of species with direct development, and that Crepipatella dilatata, a species with direct development, appears to be paraphyletic with respect to C. fecunda. Observation of the embryos of C. dilatata shows that the features necessary for larval feeding and swimming are retained in the encapsulated veligers, suggesting that heterochronic shifts in hatching time and changes in nurse-egg allotment could have resulted in the re-evolution of feeding larvae in this species.     

Endogenous thyroid hormone synthesis in facultative planktotrophic larvae of the sand dollar Clypeaster rosaceus: implications for the evolutionary loss of larval feeding

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.     

Opposed bands of cilia in the nonfeeding larvae of the serpulid annelid Salmacina tribranchiata

The nonfeeding planktonic larvae of marine invertebrates typically lack larval feeding structures. One puzzling exception to this generalization is the annelid clade Sabellidae, in which nonfeeding larvae possess ciliary bands (specifically, food groove and metatroch) that, to the best of our knowledge, have no function other than in feeding. Nishi and Yamasu (1992b, Bulletin of the College of Sciences, University of the Ryukyus, 54 , 107–121) published a scanning electron micrograph showing that nonfeeding larvae of the serpulid annelid Salmacina dysteri also possess food groove and metatrochal cilia. Here I demonstrate that nonfeeding larvae of Salmacina tribranchiata also bear ciliary bands identifiable as food groove and metatroch by position. High‐speed video of ciliary beat patterns shows that, together with the prototrochal cilia, these bands function in an opposed band system. The presence of feeding structures in nonfeeding annelid larvae is thus more widely distributed than previously recognized. The presence of feeding structures may make evolutionary transitions to planktotrophy more likely, and may underlie an inferred origin of larval feeding in the common ancestor of one of the two major clades of serpulid annelids, Serpulinae.     

Evolutionary changes in the timing of gut morphogenesis in larvae of the marine annelid Streblospio benedicti

The planktonic larvae of marine invertebrates are diverse in their nutritional modes, suggesting that evolutionary transitions in larval nutritional mode have been frequent. One approach to identifying the developmental changes that play important roles in such transitions is to compare "intermediate" larval forms to closely related larvae representative of their common ancestor. Here we make such a comparison between obligately planktotrophic and facultatively feeding larvae of the poecilogonous polychaete annelid Streblospio benedicti. We used feeding experiments to show that the derived, facultatively feeding larvae of this species develop the ability to feed at a later developmental stage (five muscle bands) than planktotrophic larvae (two to three muscle bands). This delay in the onset of feeding ability does not appear to be caused by delay in the formation of particle capture structures, but instead by delay in the development of a continuous, functional gut. These observations are consistent with the hypothesis that evolutionary increases in egg size in annelids lead predictably to heterochronic delays in gut development, and hence to transitions in larval nutritional mode.     

Egg size and the evolution of phenotypic plasticity in larvae of the echinoid genus Strongylocentrotus

Planktotrophic larvae grow by utilizing energy obtained from food gathered in the plankton. Morphological plasticity of feeding structures has been demonstrated in multiple phyla, in which food-limited larvae increase feeding structure size to increase feeding rates. However, before larvae can feed exogenously they depend largely on material contained within the egg to build larval structures and to fuel larval metabolism. Thus, the capacity for plasticity of feeding structures early in development may depend on egg size. Using the congeneric sea urchins Strongylocentrotus franciscanus and S. purpuratus, which differ in egg volume by 5-fold, I tested whether the degree of expression of feeding structure (larval arm length) plasticity is correlated with differences in the size of the egg. I experimentally manipulated egg size of S. franciscanus (the larger-egged species) by separating blastomeres at the 2-cell stage to produce half-sized larvae. I reared half-size and normal-size larvae under high and low food treatments for 20 days. I measured arm and body lengths at multiple ages during development and calculated the degree of plasticity expressed by larvae from all treatments. Control and unmanipulated S. franciscanus larvae (from ∼ 1.0 nl eggs) had significantly longer arms relative to body size and a significantly greater degree of plasticity than half-sized S. franciscanus larvae (from < 0.18 nl eggs), which in turn expressed a significantly greater degree of plasticity than S. purpuratus larvae (from ∼ 0.3 nl eggs). These results indicate that egg size affects larval arm length plasticity in the genus Strongylocentrotus; larger eggs produce more-plastic larvae both in an experimental and a comparative context. However, changes in egg size alone are not sufficient to account for evolved differences in the pattern of plasticity expressed by each species over time and may not be sufficient for the evolutionary transition from feeding to non-feeding.     

Evolutionary and experimental change in egg volume, heterochrony of larval body and juvenile rudiment, and evolutionary reversibility in pluteus form

SUMMARY Heterochronic developmental plasticity of the juvenile rudiment and larval body of sea urchin larvae occurs in response to supply of food. Evolutionary increase in egg size can also be associated with earlier development of the juvenile rudiment. We examined effects of egg volume of feeding larvae on this heterochrony and other changes in larval form. (1) Evolutionary and experimental enlargements of egg volume did not accelerate formation of the rudiment relative to the larval body. Development of the larval body and juvenile rudiment was compared for the echinoids Strongylocentrotus purpuratus (with an egg of 78–82 μm) and Strongylocentrotus droebachiensis (with an egg of 150–160 μm diameter). Development of both larval body and rudiment were accelerated in S. droebachiensis relative to S. purpuratus but with greater acceleration of the larval body, so that the rudiment of S. droebachiensi s was initiated at a later larval stage even though at an earlier age. Also, experimentally doubling the egg volume of S. purpuratus did not accelerate development of the juvenile rudiment relative to the larval body. (2) Both species exhibited similar plasticity in timing of rudiment development in response to food supplies. (3) Doubling egg volume of S. purpuratus produced a larval form more similar to that of S. droebachiensis . This result mirrors previous experiments in which larvae from half embryos of S. droebachiensis were more similar to larvae of S. purpuratus . Many of the effects of egg volume on larval form are similar against either species' genetic background and are thus evolutionarily reversible effects on larval form.     

Thyroid hormones determine developmental mode in sand dollars (Echinodermata: Echinoidea)

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.     

Larval development of Phoronis pallida (Phoronida): implications for morphological convergence and divergence among larval body plans

Morphological variation among larval body plans must be placed into a phylogenetic and ecological context to assess whether similar morphologies are the result of phylogenetic constraints or convergent selective pressures. Investigations are needed of the diverse larval forms within the Lophotrochozoa, especially the larvae of phoronids and brachiopods. The actinotroch larva of Phoronis pallida (Phoronida) was reared in the laboratory to metamorphic competence. Larval development and growth were followed with video microscopy, SEM, and confocal microscopy. Early developmental features were similar to other phoronid species. Gastrulation was accomplished by embolic invagination of the vegetal hemisphere. Mesenchymal cells were found in the remaining blastocoelic space after invagination began. Mesenchymal cells formed the body wall musculature during the differentiation of larval features. Body wall musculature served as the framework from which all other larval muscles proliferated. Larval growth correlated best with developmental stage rather than age. Consistent with other phoronid species, differentiation of juvenile tissues occurred most rapidly at the latest stages of larval development. The minimum precompetency period of P. pallida was estimated to be approximately 4-6 weeks. Previously published studies have documented that the planktonic embryos of P. pallida develop faster than the brooded embryos of P. vancouverensis. However, these data showed that the difference in developmental rate between the two species decreased in succeeding larval stages. There may be convergent selective pressures that result in similar timing to metamorphic competence among phoronid and brachiopod planktotrophic larval types. Morphological differences between these larval types result from heterochronic developmental shifts in the differentiation of juvenile tissue. Similarities in the larval morphology of phoronids and basal deuterostomes are likely the result of functional and developmental constraints rather than a shared (recent) evolutionary origin. These constraints are imposed by the functional design of embryological stages, feeding structures, and swimming structures.     

Development and evolution of caste dimorphism in honeybees – a modeling approach

The difference in phenotypes of queens and workers is a hallmark of the highly eusocial insects. The caste dimorphism is often described as a switch‐controlled polyphenism, in which environmental conditions decide an individual's caste. Using theoretical modeling and empirical data from honeybees, we show that there is no discrete larval developmental switch. Instead, a combination of larval developmental plasticity and nurse worker feeding behavior make up a colony‐level social and physiological system that regulates development and produces the caste dimorphism. Discrete queen and worker phenotypes are the result of discrete feeding regimes imposed by nurses, whereas a range of experimental feeding regimes produces a continuous range of phenotypes. Worker ovariole numbers are reduced through feeding‐regime‐mediated reduction in juvenile hormone titers, involving reduced sugar in the larval food. Based on the mechanisms identified in our analysis, we propose a scenario of the evolutionary history of honeybee development and feeding regimes.     

EFFECTS OF EGG SIZE ON POSTLARVAL PERFORMANCE: EXPERIMENTAL EVIDENCE FROM A SEA URCHIN

Many life-history and developmental studies of marine invertebrates assume that eggs of species with nonfeeding larvae are large because they provide materials for rapid development. Using the sea urchin Heliocidaris erythrogramma which has 400 μm eggs and nonfeeding larvae, we removed an acellular, lipid-rich component from the blastula equivalent to ca. 40% of the egg volume and ca. 50% of the organic mass. Experimentally manipulated, reduced-lipid larvae survived well, developed in the usual time (3.5 d), and high percentages of the original numbers metamorphosed into anatomically normal juveniles. Control juveniles were larger at metamorphosis, grew more, and survived longer than siblings that lacked this lipid-rich material. Moderate increases in egg size in species with nonfeeding larvae may enhance postlarval performance significantly and therefore may reflect selection on early juvenile traits. The contrasts of our results and comparable experiments with feeding larvae suggests that egg size may play fundamentally different roles in species with feeding and nonfeeding larvae. The accommodation of materials reserved for the juvenile stage should be considered among hypotheses on evolutionary modification of developmental patterns.     

Gene expression and larval evolution: changing roles of distal-less and orthodenticle in echinoderm larvae

We describe the expression of the homeobox genes orthodenticle (Otx) and distal-less (Dlx) during the larval development of seven species representing three classes of echinoderms: Holothuroidea, Asteroidea, and Echinoidea. Several expression domains are conserved between species within a single class, including Dlx expression within the brachiolar arms of asteroid larvae and Otx expression within the ciliated bands of holothuroid larvae. Some expression domains are apparently conserved between classes, such as the expression of Dlx within the hydrocoel (left mesocoel) in all three classes. However, several substantial differences in expression domains among taxa were also evident for both genes. Some autapomorphic (unique derived) features of gene expression are phylogenetically associated with autapomorphic structures, such as Dlx expression within the invaginating rudiment of euechinoids. Other autapomorphic gene expression domains are associated with evolutionary shifts in life history from feeding to nonfeeding larval development, such as Otx expression within the ciliated bands of a nonfeeding holothuroid larva. Similar associations between evolutionary changes in morphology and life history mode with changes in regulatory gene expression have also been observed in arthropods, urochordates, and chordates. We predict that recruitment of regulatory genes to a new developmental role is commonly associated with evolutionary changes in morphology and may be particularly common in clades with complex life cycles and diversity of life history modes. Caution should be used when making generalizations about gene expression and function based on a single species, which may not accurately reflect developmental processes and life histories of the phyla to which it belongs.     

Relationships among development, ecology, and morphology in the evolution of Echinoderm larvae and life cycles

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.     

Evolution of feeding structure plasticity in marine invertebrate larvae: a possible trade-off between arm length and stomach size

The ability of an organism to alter its morphology in response to environmental conditions (phenotypic plasticity) occurs in several species of marine invertebrates. Examples are sea urchin and sand dollar larvae (plutei). When food is scarce, plutei produce longer food-gathering structures (larval arms and a ciliary band) and smaller stomachs than when food is abundant. However, it is unclear whether stomach size is actually induced through changes in morphogenesis or simply by food distending the stomach. Distinguishing between these two hypotheses is possible because plutei morphologically respond to food concentrations and change the length of their food-gathering structures before they are capable of feeding. More importantly, these two hypotheses provide insights to whether a trade-off exists between the response in food-gathering structures and the response in stomach size—a possible explanation for the evolution of feeding-structure plasticity in marine invertebrate larvae. In this study, I investigated whether sea urchin larvae (Strongylocentrotus purpuratus and S. franciscanus) reared in different amounts of food produced stomachs of different sizes before they were capable of feeding. Prior to having the ability to ingest food, larvae produced larger stomachs and shorter arms when food was abundant than when food was scarce, consistent with the hypothesis that food induced changes in morphogenesis. In addition, there was a strong negative correlation between the magnitude of plasticity in larval arm length and the magnitude of plasticity in stomach size. These results are consistent with the idea that a trade-off exists between the response in arm length and the response in stomach size, and at least in part, explains the evolution of feeding structure plasticity in plutei. This may also explain why feeding-structure plasticity has evolved in larvae of other taxa (e.g. other echinoderms and gastropods).     

The nonfeeding auricularia of Holothuria mexicana (Echinodermata,Holothuroidea)

Among echinoderms, nonfeeding larvae usually are simplified in body shape, have uniform ciliation, and have lost the larval gut. A few species have nonfeeding larvae that express some remnant features of feeding larvae like ciliated bands and larval skeleton or larval arms, but typically their larval mouth never opens and their gut does not function. Still other species have retained the feeding larval form, a functional gut, and can feed, but they do not require food to metamorphose. The present note describes the development of a tropical holothurian, Holothuria mexicana, which hatches as a gastrula that is already generating coelomic structures. A translucent auricularia forms with a mouth that opens but becomes reduced soon thereafter. In form and ciliation this auricularia resembles a feeding larva, but it does not respond to food. A doliolaria forms on day 4 and the pentactula on day 6 post‐fertilization. Further study of this larva and that of its closely related congener, Holothuria floridana, is warranted.     

Body Form and Patterns of Ciliation in Nonfeeding Larvae of Echinoderms: Functional Solutions to Swimming in the Plankton?

SYNOPSIS. Nonfeeding larval forms of echinoderms are believedto have evolved repeatedly from feeding larval forms, and thesetransformations usually result in major shifts in morphogenesis.Current hypotheses on form change invoke relaxation of stabilizingselection on traits that functionin feeding, coupled with selectionfor rapid development of juvenile traits. However, comparativeevidence from 51 species of nonfeeding larvae, representing19 independent origins, suggests that body form, patterns ofciliation, and possibly buoyancy reflect functional requirementsfor maintenance of swimming performance. Nonfeeding larvae withbody lengths less than 600 µm usually have several transverseciliated bands, while those with body lengths greater than 800µm usually have uniform ciliation. A preliminary modelwhich compares estimated drag and buoyancy forces with ciliarypropulsive forces predicts that bands of simple cilia do notproduce sufficient propulsive forces to permit swimming in largerlarvae. For larger larvae, increases in areal coverage of ciliamay be required to produce propulsive forces sufficient to opposedrag and buoyancy forces and permit movement. For these largerlarvae, estimates of water velocities at the tips of uniformarrays of cilia are well below the upper limits of water movementsby cilia of echinoderms. Functional constraints on nonfeedinglarval forms should be considered, along with (above mentioned)current hypotheses, in explanations of morphogenetic changesassociated with transition from feeding to nonfeeding larvaldevelopment.     

Loss and gain of the juvenile rudiment and metamorphic competence during starvation and feeding of bryozoan larvae

SUMMARY In many animals, larval structures and juvenile rudiments develop independently. One advantage of this independence is that juvenile rudiments can be expended as a nutrient reserve or for energy conservation. When bryozoan cyphonautes larvae were starved, structures required for settlement and metamorphosis shrank. When the larvae were again fed, these structures grew back. Starvation reduced the size of both the internal sac, a rudiment of postlarval juvenile structures, and the pyriform organ, which functions in sensing and crawling on the substratum at settlement. In contrast, starvation affected neither the size of the larval shell nor the lengths of the ciliary bands used in swimming and feeding. Starved larvae that had reduced the pyriform organ and internal sac did not metamorphose in response to stimuli from a laminarian alga. The laminarian alga did stimulate metamorphosis of the same larvae after renewed feeding, when the larvae had regrown these structures. Thus starved larvae expended body parts needed for settlement and metamorphosis when food was scarce while retaining structures for feeding, swimming, and defense. Starved larvae thereby retained the capacity to regrow structures needed for settlement and metamorphosis when they again encountered food. Advantages from expendable juvenile rudiments may enhance selection for their being developmentally distinct from structures for larval swimming and feeding.     

Developmental plasticity in larval development in the echinometrid sea urchin Evechinus chloroticus with varying food ration

Developmental plasticity in the morphology of planktotrophic echinoid larvae has been studied primarily in temperate sea urchins from the Northern Hemisphere. These studies have shown that echinoplutei with reduced food ration generally respond by increasing the length of the larval arms, and thus the length of the ciliated band, and delaying formation of the rudiment. Using the endemic New Zealand sea urchin Evechinus chloroticus we tested for the presence of developmental plasticity in larvae fed a high or low algal food ration (6000 or 600 Dunaliella cells/ml), or with no algal food. Our results show that developmental plasticity in larval form is seen in a Southern Hemisphere representative of the Family Echinometridae, but the general pattern of longer arms with low food ration was only seen in the earliest part of development. Larvae in the High food treatment were largest in all dimensions and formed rudiments within 23 days of fertilization. Larvae fed a low algal ration or no algal food stalled at the four-arm echinopluteus stage, and were significantly smaller in size, and differed in shape, when compared in a multivariate analysis to the High food treatment. We suggest that the response of echinoplutei to low levels of particulate food is a species-specific trait, depending in part on the level of dependence of the larvae on exogenous food. Previous studies in Lytechinus variegatus, and the present study with E. chloroticus, suggest that in species where development stalls at the four-arm stage, the pattern of longer larval arms with low food ration will only be seen during the initial early period of larval growth. Additionally our results show that there can be significant variation in larval morphology between replicate jars in the same feeding treatment, suggesting that future research on developmental plasticity should also consider differences in larval morphology between culture containers.     

Divergence and ontogenetic coupling of larval behaviour and thermal reaction norms in three closely related butterflies

Genetic trade-offs such as between generalist–specialist strategies can be masked by changes in compensatory processes involving energy allocation and acquisition which regulation depends on the state of the individual and its ecological surroundings. Failure to account for such state dependence may thus lead to misconceptions about the trade-off structure and nature of constraints governing reaction norm evolution. Using three closely related butterflies, we first show that foraging behaviours differ between species and change remarkably throughout ontogeny causing corresponding differences in the thermal niches experienced by the foraging larvae. We further predicted that thermal reaction norms for larval growth rate would show state-dependent variation throughout development as a result of selection for optimizing feeding strategies in the respective foraging niches of young and old larvae. We found substantial developmental plasticity in reaction norms that was species-specific and reflected the different ontogenetic niche shifts. Any conclusions regarding constraints on performance curves or species-differentiation in thermal physiology depend on when reaction norms were measured. This demonstrates that standardized estimates at single points in development, or in general, allow variation in only one ecological dimension, may sometimes provide incomplete information on reaction norm constraints.