Co-option and dissociation in larval origins and evolution: the sea urchin larval gut

SUMMARY The origin of marine invertebrate larvae has been an area of controversy in developmental evolution for over a century. Here, we address the question of whether a pelagic "larval" or benthic "adult" morphology originated first in metazoan lineages by testing the hypothesis that particular gene co-option patterns will be associated with the origin of feeding, indirect developing larval forms. Empirical evidence bearing on this hypothesis is derivable from gene expression studies of the sea urchin larval gut of two closely related but differently developing congenerics, Heliocidaris tuberculata (feeding indirect-developing larva) and H. erythrogramma (nonfeeding direct developer), given two subsidiary hypotheses. (1) If larval gut gene expression in H. tuberculata was co-opted from an ancestral adult expression pattern, then the gut expression pattern will remain in adult H. erythrogramma despite its direct development. (2) Genes expressed in the larval gut of H. tuberculata will not have a coordinated expression pattern in H. erythrogramma larvae due to loss of a functional gut. Five structural genes expressed in the invaginating archenteron of H. tuberculata during gastrulation exhibit substantially different expression patterns in H. erythrogramma with only one remaining endoderm specific. Expression of these genes in the adult of H. erythrogramma and larval gut of H. tuberculata , but not in H. erythrogramma larval endoderm, supports the hypothesis that they first played roles in the formation of adult structures and were subsequently recruited into larval ontogeny during the origin and evolution of feeding planktotrophic deuterostome larvae.     

Early starvation limits survival in amphidromous fishes

Newly hatched amphidromous larvae drift downstream to the sea. Since there is practically no food available for drifting larvae, an extended downstream migration may enhance the risk of starvation. We hypothesized that early survival of amphidromous fish varies among populations according to the length of the river, due to its effect on larval starvation. The hypothesis was tested with the common Japanese amphidromous goby, Rhinogobius brunneus . Based on morphological characteristics, larvae were categorized as being in an endogenous feeding state (EFS) or irrecoverable starved state (ISS). The frequency of ISS larvae in the population from a long river was nearly twice the frequency in the population from a short stream. More than half of larvae were judged to be dying during downstream migration in the comparatively long river, although this was possibly an underestimation. It is suggested that early starvation limits reproductive success far from the sea.     

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.     

Influence of watering and trenching ponderosa pine on a pine sawfly

Summary Neodiprion autumnalis (Smith) larvae were caged for two successive years on root-trenched, watered, and untreated ponderosa pine (Pinus ponderosa Doug. ex Laws.) to determine effects of host moisture stress on larval feeding. Levels of moisture stress (as measured by the Scholander pressure chamber) differed significantly among treatment levels during 1984 and 1985 larval feeding periods. Differences in larval feeding success were not detected in 1984. In 1985, however, larvae on trenched (stressed) trees clipped and rejected more foliage, consumed more needles, had lower pupal weights, lower survival, and a longer feeding period than larvae on watered or untreated trees. Frass production did not differ among treatment levels. The length of the feeding period was shorter for larvae on watered trees than for larvae on untreated trees, but other measures of feeding success did not significantly differ between watered and untreated trees.     

Aggregation facilitates larval growth in the neotropical nymphalid butterfly Chlosyne janais

1. Larvae of Chlosyne janais (Lepidoptera: Nymphalidae) feed gregariously as early instars on the shrub Odontonema callistachyum (Acanthaceae). During the fourth instar, aggregations break up and larvae feed as solitary individuals.
2. The hypothesis that aggregation increases growth rate was tested by raising larvae on intact plants in the field in different group sizes and measuring their daily growth.
3. There was a striking effect of group size on larval growth whereby larvae more than doubled their weight gain by feeding in large rather than small aggregations on intact plants in the field.
4. This group-feeding advantage was lost altogether if larvae were raised on excised leaves in the laboratory, suggesting that large aggregations may facilitate growth either by inducing a nutrient sink or by overwhelming an induced allelochemical response in the plant.
5. Although larval survival was higher in cages that excluded enemies than in exposed aggregations, there was no influence of group size (experimentally manipulated) on short-term survival in the field. However, there was a weak positive relationship between short-term survival and the size of naturally occurring larval aggregations in the field. These data provide mixed support for the notion that gregarious feeding promotes defence against natural enemies.
6. Although the group defence hypothesis warrants further investigation, feeding facilitation is clearly an important factor contributing to the aggregation behaviour of C. janais larvae.     

Changes in the temporal pattern of antennal drumming behavior across the <Emphasis Type="Italic">Polistes fuscatus</Emphasis> colony cycle (Hymenoptera,Vespidae)

Social wasps in several genera exhibit a diverse array of conspicuous vibrational behavior patterns closely associated with larval feeding. Polistes, as the only genus in which these substrate-borne mechanical signals have been studied in some detail, is a useful system for understanding their functions. Most Polistes species examined perform antennal drumming (AD) in the context of feeding prey liquid to larvae. Two existing hypotheses on the function of AD propose that it is a behavioral releaser signal that regulates the release of larval saliva, but with opposite effects. One proposes that AD stimulates larvae to release their saliva for the drumming adult to imbibe, whereas the other proposes that AD inhibits saliva release. A recently proposed third hypothesis argues instead that AD has a modulatory effect on development: exposure to high levels of AD biases larvae toward a worker phenotype as adults. While the larval-saliva-release hypothesis for AD function has little support, predictions made by both the inhibition hypothesis and the mechanical switch hypothesis are yet to be tested within the broader ontogenetic framework of the Polistes colony cycle. We investigated the contexts, rates of performance, and actors associated with AD across 13 weeks of the P. fuscatus colony cycle. Mean colony-wide rates of AD were high during pre-emergence and early post-emergence stages, but dropped dramatically following the third week after the first workers emerged. This variation in the temporal pattern of AD was correlated neither with the rate at which larvae were fed liquid, the number of larvae on the nest, nor with the adult-to-larva ratio, but was solely a function of colony stage. In contrast, rates of feeding liquid to larvae varied only as a function of the number of larvae in the nest. Queens drummed and fed liquid to larvae at much higher rates than did workers. Queen AD and feed-liquid rates decreased after the third week of worker emergence. During the same period, total feed-liquid rates of workers became as high as levels of queens during pre-emergence. Colony-wide AD rates dropped dramatically because workers seldom drummed while feeding liquid to larvae. The mean duration of AD bursts for queens also decreased after the second week of worker emergence. These results fail to support the salivary inhibition hypothesis, but provide indirect support for the mechanical switch hypothesis on AD function.     

The effects of nurse eggs and sibling interactions on the larval development of the poecilogonous annelid Boccardia proboscidea (Spionidae)

In poecilogony, different types of larvae are produced within the same species. Previous studies have suggested maternal control of the production of larval types; however, it is not clear which factors or mechanisms generate contrasting developmental patterns among siblings. The spionid polychaete Boccardia proboscidea produces within the same capsule adelphophagic larvae that eat nurse eggs and siblings and complete all or most of their development inside the capsule (Type A larvae), and larvae with little growth until they hatch as planktotrophic larvae (Type B larvae). In this study, we manipulated capsule content to explore the factors determining larval type in B. proboscidea and the role of extra‐embryonic maternal nutrition and sib–sib interaction in the developmental fate of offspring. When early larval stages were grown individually in vitro, with nurse eggs as the only food source, some of them remained small, while others continue developing into larger pre‐competent larvae by feeding on nurse eggs. This suggests that larval types in B. proboscidea are determined very early in development and are not solely the product of sib–sib interaction inside the capsule. However, our data also suggest that hatching size variability within larval types of a clutch depends on nurse egg availability. Type B larvae grew normally to metamorphosis when phytoplankton was available, but suffered high rates of cannibalism by Type A larvae. These results are consistent with the hypothesis that individual larval fates are determined very early in development and that once their fate is determined, hatching size and intracapsular survival are affected by maternal food provisioning and sibling interaction.     

The organisation of larval feeding in bumblebees (Hymenoptera,Apidae) and its significance to caste differentiation

Summary. In pollen-storing bumblebees, the rate at which workers nourish larvae has been proposed to be the main factor influencing caste differentiation since workers feed prospective queens more frequently and longer than worker larvae during the last instars. In order to determine how the frequency of feedings is established small groups of Bombus terrestris larvae were either subjected to starvation or nourished regularly by workers. Experimentally starved larvae were fed significantly earlier and more often than control larvae. Behavioural observations provide evidence for the existence of a stimulus of larval origin that releases feeding behaviour in workers. Intentional inspections in the sense of a recognisable and functional behaviour intended to organise the feeding process were never observed. We argue that worker inspections are not required for the adequate maintenance of larvae and that a simple stimulus-response chain appears to be sufficient to regulate feeding behaviour at the individual and the colony level in bumblebees. Furthermore, hand-rearing experiments with female larvae indicate that queen rearing is not dependent on a high frequency of feedings in itself, nor is worker development induced by larval deprivation. This makes it unlikely that workers impose a caste-specific frequency of feedings on larvae in order to actively control or manipulate caste development. Since caste fate seems to be predetermined early in larval life, we propose that early caste-specific differences in development are reflected in the physiology of the larvae and the associated nutritional needs to which workers respond accordingly. Consequently, caste-specific differences in feeding frequencies are a result, but not the cause of differences in development.     

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.     

When to press on or turn back: dispersal strategies for reef fish larvae

Events that occur during the pelagic larval stage are thought to be important determinants of reef fish population dynamics. Recent research contradicts the early paradigm of larvae being advected as passive propagules and indicates that many late stage larvae have well-developed sensory and locomotory capabilities. Whether and how larvae use these capabilities to influence their dispersal is unknown. We compare alternative hypotheses regarding larval behavior. Contrary to the trend in dispersal modeling, we focus on larval biology rather than physical oceanographic considerations. Specifically, we present two streams of models: one that describes a return-based strategy and one in which dispersal is a central component. The models depend on different sets of behavioral assumptions for a pomacentrid species and for acanthurids, two groups with contrasting early life histories. Whether dispersal or return-based strategies are favored depends on the efficiency and sustainability of larval swimming methods and the environmental conditions experienced during dispersal. We argue that dispersal models should consider a variety of behavioral hypotheses and that the sensitivity of results to the behavioral assumptions made should be quantified.     

Effect of group size on parasitism in a natural population of the Baltimore checkerspot Euphydryas phaeton

Summary The effect of group size of early instars on parasitism of Euphydryas phaeton (Nymphalidae) was examined. Different numbers of larvae were stocked per web to determine the effect of group size on parasitism. Larval aggregations of moderate size (the size occurring naturally) had the least parasitism. Larger larval groups had a disproportionately high rate of parasitism. The major larval parasitoids located vulnerable larvae within webs, instead of attacking larvae available on the outside of webs. Parasitism rates were similar for larvae of damaged and undamaged webs, a consequence of the behavior and location of larvae in the webs. Lower limit to group size was a function of facilitation of larval numbers in reaching the first feeding site, the top of the host plant. Feeding facilitation by larval aggregations was not a factor in larval survival or growth.     

From embryos to juveniles: morphogenesis in the spionid Boccardia proboscidea (Polychaeta)

Abstract. The polychaete Boccardia proboscidea has poecilogonous development that includes the production of both planktotrophic and adelphophagic young. In this study, we use scanning electron microscopy to analyse external morphogenesis of planktotrophic offspring with emphasis on early embryos, morphogenesis during metamorphosis, and the dynamic nature of larval structures during early ontogeny. Larval growth involves addition of terminal chaetigers and formation of segment-specific structures such as cilia and chaetae. Our observations reveal that most ciliary bands are reduced or incomplete relative to those found in larvae of other polychaete families. We describe a small metatroch (consisting of only a few trochoblasts) in early embryos, which has not previously been reported in the Spionidae. The presence of the metatroch does not imply a function in opposed-band feeding, as a food groove intermediate between the prototroch and metatroch is lacking. A neurotroch, inconsistently reported in the Spionidae, is also present and terminates in a ciliated pit. Many larval structures (e.g., presumptive sensory organs) are short-lived, implying a shift towards early functionality of adult traits in larvae. Metamorphosis is gradual and occurs over the latter half of the larval life. The reduction of larval structures, and early development of adult traits, suggests an overall shift in morphology facilitating settlement and juvenile development.     

HETEROCHRONIC DEVELOPMENTAL PLASTICITY IN LARVAL SEA URCHINS AND ITS IMPLICATIONS FOR EVOLUTION OF NONFEEDING LARVAE

Preexisting developmental plasticity in feeding larvae may contribute to the evolutionary transition from development with a feeding larva to nonfeeding larval development. Differences in timing of development of larval and juvenile structures (heterochronic shifts) and differences in the size of the larval body (shifts in allocation) were produced in sea urchin larvae exposed to different amounts of food in the laboratory and in the field. The changes in larval form in response to food appear to be adaptive, with increased allocation of growth to the larval apparatus for catching food when food is scarce and earlier allocation to juvenile structures when food is abundant. This phenotypic plasticity among full siblings is similar in direction to the heterochronic evolutionary changes in species that have greater nutrient reserves within the ova and do not depend on particulate planktonic food. This similarity suggests that developmental plasticity that is adaptive for feeding larvae also contributes to correlated and adaptive evolutionary changes in the transition to nonfeeding larval development. If endogenous food supplies have the same effect on morphogenesis as exogenous food supplies, then changes in genes that act during oogenesis to affect nutrient stores may be sufficient to produce correlated adaptive changes in larval development.     

Gregariousness does not vary with geography,developmental stage,or group relatedness in feeding redheaded pine sawfly larvae

Aggregations are widespread across the animal kingdom, yet the underlying proximate and ultimate causes are still largely unknown. An ideal system to investigate this simple, social behavior is the pine sawfly genus Neodiprion, which is experimentally tractable and exhibits interspecific variation in larval gregariousness. To assess intraspecific variation in this trait, we characterized aggregative tendency within a single widespread species, the redheaded pine sawfly (N. lecontei). To do so, we developed a quantitative assay in which we measured interindividual distances over a 90‐min video. This assay revealed minimal behavioral differences: (1) between early‐feeding and late‐feeding larval instars, (2) among larvae derived from different latitudes, and (3) between groups composed of kin and those composed of nonkin. Together, these results suggest that, during the larval feeding period, the benefits individuals derive from aggregating outweigh the costs and that this cost‐to‐benefit ratio does not vary dramatically across space (geography) or ontogeny (developmental stage). In contrast to the feeding larvae, our assay revealed a striking reduction in gregariousness following the final larval molt in N. lecontei. We also found some intriguing interspecific variation: While N. lecontei and N. maurus feeding larvae exhibit significant aggregative tendencies, feeding N. compar larvae do not aggregate at all. These results set the stage for future work investigating the proximate and ultimate mechanisms underlying developmental and interspecific variation in larval gregariousness across Neodiprion.     

Origins of carbon sustaining the growth of whitefish Coregonus lavaretus early larval stages in Lake Annecy: insights from fatty-acid biomarkers

The hypothesis that diatom carbon (C) produced during the spring peak supported spring zooplankton production and, ultimately, the growth of Coregonus lavaretus early larval stages from March to May 2006 in Lake Annecy, France, was tested using gut content analyses and fatty acid biomarkers. Gut content results showed that C. lavaretus larvae from stages 1 to 4 preferentially fed on copepods with Daphnia sp. only a minor proportion of larval diet. The levels of diatom-marker fatty acids (C16:1n-7 and C20:5n-3) were high in Daphnia sp., but lower in both copepods and C. lavaretus larvae from stages 0 to 4. These results indicated that the spring diatom biomass was actually grazed by Daphnia sp., but, contrary to what was expected, the spring bloom was not the only C source supporting copepods secondary production and, consequently, the growth of C. lavaretus early larval stages. In contrast, levels of terrestrial fatty acid marker (C24:0) were low in Daphnia sp. but high in copepods and C. lavaretus larvae, indicating a significant contribution of terrestrial carbon to copepods and, ultimately, to the growth of C. lavaretus early larval stages.     

鲥鱼仔幼鱼食性与生长的初步研究

本文主要描述鲥鱼仔幼鱼阶段有关摄食、消化器官的发育、不同大小仔幼鱼食物组成特点、摄食量及其昼夜摄食节律。此外,还就仔幼鲥鱼人工饲养条件与天然状况下的生长作了比较。结果表明,只要供饵正常,孵化环道内生活的仔幼鲥生长速度可以略快于鄱阳湖同期天然生长个体的速度,为今后人工培育仔幼鲥进行放流和增殖提供资料。       

Ontogeny of feeding and respiration in larval Atlantic cod Gadus morhua (Teleostei,Gadiformes): I. Morphology

Cranial development in larval Atlantic cod Gadus morhua was studied throughout ontogeny using specimens treated by staining and clearing, scanning electron microscopy and histology. Newly hatched cod larvae have closed mouths, no operculii, five well-developed branchial arches, and transversii ventralis muscles. During the endogenous feeding (yolk-sac) stage, viscerocranial structures remain simple and nonarticulated. Six days after hatching at 5°C, articulation occurs between the quadrate/Meckel's cartilage and the hyomandibula/cranium. Integration of skeletal elements results in a functional jaw that facilitates the transition from endogenous to exogenous feeding. During later ontogenetic stages, the opercular apparatus and levator-operculi coupling develops, facilitating the transition of cutaneous to branchial respiration. Overall, feeding and respiratory needs are met by changes in form (including composition) and function during larval fish growth and are correlated with demands of energy acquisition essential to survival. © 1996 Wiley-Liss, Inc.     

Environmental variation and behaviour: resource availability during ontogeny and feeding performance in salamander larvae (Ambystoma texanum)

1. The effects of resource availability during ontogeny on subsequent feeding performance were investigated in larvae of the small-mouthed salamander ( Ambystoma texanum ).
2. Salamander larvae were reared individually in either high or low prey density treatments for 7 weeks prior to intermediate prey density foraging trials. Larvae from the low prey density treatment were on average 35% smaller in body size than individuals from the high prey density treatment.
3. Resource availability during development influenced larval feeding rates and altered the relationship between body size and three feeding performance measures (attack rates, capture success and feeding rates). Feeding rates in predation trials were also positively correlated with growth rate early in the larval period (until the end of week 5).
4. These results suggest that the environment to which developing organisms are exposed can have significant effects on subsequent behaviour, and that small-mouthed salamander larvae may show state-dependent changes in feeding behaviour in response to differences in long-term feeding history. Additionally, differences in feeding performance may influence the probability of survival to the adult stage for organisms that utilize ephemeral habitats.     

Visual acuity and feeding in larval Premnas biaculeatus

Ontogenetic change in the visual acuity of Premnas biaculeatus larvae was determined both behaviourally and anatomically. Visual acuity improved substantially between early feeding (day 3 post-hatch) and the pre-settlement (day 10 post-hatch) larvae but, at both ages, the anatomically-measured visual acuity was greater than that determined behaviourally. It appears that estimated anatomical visual acuity values substantially over-estimate the functional visual acuity realized under normal conditions. The distribution of the reactive angles indicated that most frequently prey within 0 to 9° of the longitudinal larval axis elicited a feeding response at both larval ages. This suggests that stereoscopic vision is used extensively during feeding in this species. The prey capture success with rotifers ranged from 96% at 3 days post-hatch to 100% at 10 days post-hatch. These values differ markedly from previous studies on temperate species and highlight the well developed abilities of larval P. biaculeatus at a given     

Environmental variation and behaviour: resource availability during ontogeny and feeding performance in salamander larvae (Ambystoma texanum)

1. The effects of resource availability during ontogeny on subsequent feeding performance were investigated in larvae of the small-mouthed salamander ( Ambystoma texanum ).
2. Salamander larvae were reared individually in either high or low prey density treatments for 7 weeks prior to intermediate prey density foraging trials. Larvae from the low prey density treatment were on average 35% smaller in body size than individuals from the high prey density treatment.
3. Resource availability during development influenced larval feeding rates and altered the relationship between body size and three feeding performance measures (attack rates, capture success and feeding rates). Feeding rates in predation trials were also positively correlated with growth rate early in the larval period (until the end of week 5).
4. These results suggest that the environment to which developing organisms are exposed can have significant effects on subsequent behaviour, and that small-mouthed salamander larvae may show state-dependent changes in feeding behaviour in response to differences in long-term feeding history. Additionally, differences in feeding performance may influence the probability of survival to the adult stage for organisms that utilize ephemeral habitats.