Reproductive strategies of marine benthic invertebrates revisited: facultative feeding by planktotrophic larvae

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.     

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.     

Induction of metamorphosis in the sand dollar Peronella japonica by thyroid hormones

The larva of the sand dollar Peronella japonica lacks a mouth and gut, and undergoes metamorphosis into a juvenile sand dollar without feeding. In the present study, it was found that thyroid hormones accelerate the metamorphosis of P. japonica larvae. The contents of thyroid hormones in larvae increased gradually during development. Thiourea and potassium perchlorate, inhibitors of thyroid hormone synthesis, delayed larval metamorphosis and simultaneously repressed an increase in the content of thyroxine in the larval body. These results suggest that the P. japonica larva has a system for synthesis of thyroid hormones that act as factors for inducing metamorphosis.     

Ultrastructure of the larval eye of the scorpionfly Panorpa dubia (mecoptera: Panorpidae) with implications for the evolutionary origin of holometabolous larvae

The evolutionary origin of holometabolous larvae is a long‐standing and controversial issue. The Mecoptera are unique in Holometabola for their larvae possessing a pair of compound eyes instead of stemmata. The ultrastructure of the larval eyes of the scorpionfly Panorpa dubia Chou and Wang, 1981 was investigated using transmission electron microscopy. Each ommatidium possesses a cornea, a tetrapartite eucone crystalline cone, eight retinula cells, two primary pigment cells, and an undetermined number of secondary pigment cells. The rhabdomeres of the eight retinula cells form a centrally‐fused, tiered rhabdom of four distal and four proximal retinula cells. The rhabdomeres of the four distal retinula cells extend distally into a funnel shape around the basal surface of the crystalline cone. Based on the similarity of the larval eyes of Panorpidae to the eyes of the hemimetabolous insects and the difference from the stemmata of the holometabolous larvae, the evolutionary origin of the holometabolous larvae is briefly discussed. Morphol., 2012. © 2012 Wiley Periodicals, Inc.     

The evolutionary ecology of detritus feeding in the larvae of freshwater Diptera

Detritus (dead organic matter), largely of terrestrial origin, is superabundant in inland waters but because of its indigestible nature, would appear to be a poor food source for animals. Yet this unpromising material is widely used as food and indeed can be viewed as a defining characteristic of the freshwater environment. We here explore the relationships among animals, detritus and its associated micro-organism decomposers, taking a functional approach. We pose questions about interrelationships and attempt to arrive at new insights by disentangling them from an adaptive point of view. To do this we have been careful in selecting the habitats for detailed consideration. Rain pools on rock surfaces in tropical Africa and pools on peat moorland in the UK were chosen. Both examples have a relatively simple community structure and hence offer the prospect of achieving our aim. As model organisms for study we focus principally on the aquatic stages of selected holometabolous insects; that is, selected genera of the universally common midges, Ceratopogonidae and Chironomidae. We approach these case studies from an evolutionary ecology perspective and see detritus as a simple template upon which a beautiful complex of adaptations can evolve.     

Comparison of the neuromuscular systems among actinotroch larvae: systematic and evolutionary implications

A comparative analysis of the larval and presumptive juvenile neuromuscular systems among actinotroch larvae was performed using confocal laser microscopy with probes for F-actin and serotonin. Currently, there are two main categories of larval nervous systems based on the origin of the nerve fibers that innervate the larval tentacles. Characteristics of the serotonergic cells of the larval apical ganglion and juvenile nervous system have remained relatively conserved, but the structure of the secondary (hood) sense organ and the juvenile tentacles has diversified among species. Differences in larval musculature are mainly associated with differences in hood morphology. The presumptive, juvenile neuromuscular system is either integrated or separated from that of the larva based on the origin of the juvenile tentacles. Among species, the juvenile tentacles are made by remodeling the larval tentacles, developed from a basal tentacular thickening, or developed as a completely separate set in the larva. Differentiation of the neuromuscular structures of the juvenile tentacles is more diverse than their outward morphological characteristics would suggest. Importance of these larval characters is discussed in terms of current problems that exist within phoronid systematics. Evolutionary implications of these morphological characters are discussed among the phoronids, brachiopods, and related bilaterians. Overall, the integration or separation of larval and juvenile neuromuscular characters may yield insights into the evolution of lophotrochozoan body plans.     

Regulation of feeding mode by the sand dollar Dendraster excentricus in a shallow estuarine habitat

The sand dollar Dendraster excentricus is a facultative suspension feeder, which is relatively rare within the Order Clypeasteroida. Field studies of regulation of its feeding mode have been mostly conducted in exposed coastal habitats, where they are typically observed in an inclined position and oriented parallel to each other during suspension feeding. Physical (current speed and direction, reduction of drag and lift) and biological factors (increased efficiency of capture of particulates, and density) have been associated with regulation of its feeding mode in exposed coastal systems. We simultaneously measured the role of physical and biological factors in regulating the selection mode for feeding under varying tidal conditions in a shallow estuary in Baja California, Mexico. We used photographic records and direct sampling in fixed plots to determine the relationship between feeding behavior and environmental conditions. Current direction and speed, tidal level, density and content of organic matter in the water column and sediments were measured with respect to feeding mode (prone or inclined) and orientation relative to prevailing currents during spring and neap tides. Multiple regression analysis indicated that the percentage of inclined sand dollars was strongly and positively correlated only with tidal level at the densities found in the estuary (mean < 180 individuals m^− 2); there was no relationship with current velocity, density, and organic matter content of the water. The prone position, indicative of deposit feeding, was largely limited to low tidal levels. We used circular statistics to determine whether the orientation of inclined sand dollars was correlated with current direction and speed. Sand dollars were only oriented parallel to the prevailing currents during the strongest currents of spring tides (> 20 cm s^− 1). We did not observe the predominant oral:aboral configuration found in exposed coastal systems, which may be attributed to the relatively low densities of sand dollars in the exposed coastal environment (30-180 individuals m^− 2), compared to protected coastal habitats (up to 1000 individuals m^− 2). Our results suggest that regulation of the feeding mode of sand dollars in shallow and hydrodynamically complex estuarine systems differs from the feeding mode found in exposed coastal environments.     

The relationship between egg size and the duration of the facultative feeding period in marine invertebrate larvae

Feeding larvae of marine invertebrates fuel development from both endogenous egg energy and exogenous energy obtained from the planktonic environment. Although both sources of energy likely influence certain larval stages, only the effects of exogenous food have been well studied. Despite the lack of research on the effects of egg size on larval stages, investigators have hypothesized that egg size influences the duration of the facultative feeding stage—the stage in which larvae can feed but do not have to because development is still being fueled by egg energy. To test this hypothesis, we investigated six species of sand dollars with different sized eggs and quantified the duration of the larval facultative feeding period of each species by comparing when fed and starved larvae diverged in size. Regardless of whether phylogeny was taken into account, the duration of the facultative feeding period was positively correlated with egg size. We further determined that our conclusions were not sensitive to either our estimation of the duration of the facultative feeding period, or the branch lengths of the phylogeny we used. This relationship is likely a result of larger eggs being provisioned with more energy, and may affect how well larvae can cope with natural variability in food concentrations. Furthermore, our results support an assumption of a theoretical model developed to understand the evolution of different life-history strategies in marine invertebrate larvae, which suggests that this relationship has important evolutionary consequences.     

The contribution of the facultative feeding period to echinoid larval development and size at metamorphosis: a comparative approach

Planktotrophic invertebrate larvae have two dissociable stages during development, a facultative feeding period, whose length is determined by the amount of maternal provisioning in the egg, and an obligate feeding period, whose length is determined by the quantity of exogenous energy needed to reach metamorphic competence. Here we set out to experimentally test the impact of feeding during the facultative feeding period at two food concentrations (limiting and nonlimiting) on larval development time and juvenile quality. We used two closely related subtropical sand dollar species that differ in the quantity of maternal investment for these comparisons: Leodia sexiesperforata (large egg, long facultative feeding period) and Mellita tenuis (small egg, short facultative feeding period). We found that feeding during the facultative period accelerates development to metamorphosis only in M. tenuis and only at the high food ration. Feeding during the facultative feeding period had no effect on development time for M. tenuis at a food limiting concentration and for L. sexiesperforata at either food concentration. Furthermore, we found feeding during the facultative period to significantly increase quantity of carbohydrates and lipids at metamorphosis only for M. tenuis in nonlimiting food concentration. Thus, our data reveal a two-fold benefit of the facultative feeding period for a poorly provisioned species under high food conditions but little effect on a well-provisioned species. We discuss our results in reference to McEdward's [McEdward, L.R., 1997. Reproductive strategies of marine benthic invertebrates revisited: facultative feeding by planktotrophic larvae. Am. Nat. 150, 48-72] facultative feeding model.     

Ancestral variation and the potential for genetic accommodation in larval amphibians: implications for the evolution of novel feeding strategies

SUMMARY Few studies provide empirical evidence for phenotypic plasticity's role in the evolution of novel traits. One way to do so is to test whether latent plasticity is present in an ancestor that can be refined, enhanced, or diminished by selection in derived taxa (through "genetic accommodation"), thereby producing novel traits. Here, we evaluated whether gut plasticity preceded and promoted the evolution of a novel feeding strategy in spadefoot toad tadpoles. We studied Scaphiopus couchii , whose tadpoles develop an elongate gut and consume only detritus, and two derived species, Spea multiplicata and Sp. bombifrons , whose tadpoles also express a novel, short-gut phenotype in response to a novel resource (anostracan shrimp). Consistent with the expectations of plasticity-mediated trait evolution, we found that shrimp induced a range of phenotypes in Scaphiopus that were not produced with detritus. This plasticity was either suppressed or exaggerated in Spea depending on whether the induced phenotypes were adaptive. Moreover, in contrast to its effects on morphology, shrimp induced little or no functional plasticity, as assessed by gut cell proliferation, in Scaphiopus . Shrimp did, however, induce substantial proliferation in Sp. bombifrons , the species that consumes the most shrimp and that produces the short-gut phenotype the most frequently. Thus, if Spea had ancestral morphological plasticity in response to a novel diet, their shrimp-induced short-gut morphology may have undergone subsequent genetic accommodation that improved its functionality. Hence, diet-induced phenotypic plasticity may have preceded and even promoted the evolution of a novel phenotype.     

The physiological function of the coelom in starfish larvae and its evolutionary implications

The coelom in the bipinnaria larva of Asterias acts as a buoyancy tank. The concentrations of magnesium and sulphate in the coelomic fluid are lower than in seawater, reducing the density. The coelomic epithelium is a secretory epithelium, probably secreting sodium or chloride ions that then draw in the counter ion and water. The rate of urine production is very high for an isotonic marine animal, compensating for the large surface/volume ratio of the coelom. This function would account for the precocious development of the coelom and its association with an excretory duct. It is proposed that the coeloms of other pelagic larvae such as the actinotroch of Phoronis and of echiuran larvae have a similar function and that this may have been an original function of the coelom, although in many phyla this function has been modified or lost.     

Growth hormone and thyroid stimulating hormone concentrations in captive male orangutans: implications for understanding developmental arrest

There are two morphs of reproductive male in orangutans. Both morphs span the age range from adolescent to adult, but "subadult" males are smaller in size and lack secondary sexual features. In this study, urine samples were collected over a 2 year period from 23 captive male orangutans in order to define the endocrinology of this apparent arrest of secondary sexual development. Three males were juveniles, 3 to 5 years of age; seven males showed no secondary sexual trait development and were over 7 years of age; six males were in the process of developing secondary sexual features, with the youngest male being 6 years of age; and seven males were fully mature adults. Morning samples were analyzed by radioimmunoassay for levels of growth hormone (GH) and thyroid-stimulating hormone (TSH) and group hormone profiles were compared by analysis of variance. GH is the primary hormone of growth and development and its increase in teenage boys is associated with the adolescent growth spurt. TSH stimulates the thyroid to produce and secrete hormones that have metabolic effects and required for normal growth and development. Results show that arrested adolescent male orangutans have a GH level about 1/3 that of developing adolescents (P = .0006). TSH levels do not differ significantly between arrested and developing adolescents. These data complement other endocrine data showing significantly lower levels of sex steroids and luteinizing hormone (LH) in arrested males than developing males [Maggioncalda, 1995a,b; Maggioncalda et al., 1999]. Together with documented behavioral differences between reproductive males with and without secondary sexual features, these endocrine data support the hypothesis that in male orangutans there are alternative developmental pathways and corresponding alternative reproductive strategies.     

Entomopathogenic fungi disturbed the larval growth and feeding performance of Ocinara varians (Lepidoptera: Bombycidae) larvae

Abstract Feeding experiments using three strains of entomopathogenic fungi, Beauveria bassiana, Metarhizium anisopliae and Isaria fumosorosea were conducted with newly moulted 3rd–5th instar Ocinara varians Walker larvae in the laboratory. The mortality of larvae immersed individually in spore suspension (1 × 10⁷ spores/mL) of all the strains was ≥ 80% except 5th instar larvae treated with M. anisopliae which transformed into pupae, but did not result in adult emergence. The growth (total body mass), consumption, relative consumption rate and relative growth rate, were reduced at all three larval stages, while developmental time was extended in infected larvae with concurrent significant increase in approximate digestibility in infected larvae. Conversion of digested food (ECD) and ingested food (ECI) values declined in infected larvae as compared to the healthy larvae (control). The 5th instar larvae treated with M. anisopliae showed higher ECD and ECI values than control. Based on mortality and growth inhibition it can be suggested that all the studied fungal strains have a high potential for biocontrol and could be developed into biocontrol agents against O. varians.     

Differences in larval feeding behavior correlate with altered developmental strategies in two parasitic wasps: implications for the size-fitness hypothesis

Parasitoid wasps have long been favored organisms for fundamental studies on reproductive strategies and life-history evolution. Progeny allocation models designed with parasitoids in mind assume that offspring develop by consuming most or all of the resources available from a single host, and that size is the most important factor affecting offspring fitness. Many parasitoids exhibit host usage patterns consistent with these assumptions, but our recent observations suggested that endoparasitic wasps in the family Braconidae often do not. To investigate how differences in host usage patterns might affect developmental strategies, we compared two related braconids with contrasting host usage patterns. Apanteles carpatus consumed virtually all host tissues during immature development, whereas Microplitis demolitor fed exclusively on host hemolymph and consumed a relatively small proportion of available host resources. Development time of M. demolitor was unaffected by host size, whereas development time of A. carpatus was much longer in small hosts than in large hosts. On the other hand, offspring size in M. demolitor correlated strongly with host size, but it correlated only weakly with host size in A. carpatus . Our results collectively suggest that selection has favored rapid development at the potential cost of reduced size in M. demolitor , and increased size at the potential cost of increased development time in A. carpatus . Tissue feeding appears to be more prevalent among parasitoids overall, but hemolymph feeding is the predominant pattern of host usage in several subfamilies of endoparasitic braconids. We argue that the relative importance of offspring size and development time will be influenced by host ecology and the effects of selected traits on parasitoid survival.     

Chronic loss of melanin-concentrating hormone affects motivational aspects of feeding in the rat

Current epidemic obesity levels apply great medical and financial pressure to the strenuous economy of obesity-prone cultures, and neuropeptides involved in body weight regulation are regarded as attractive targets for a possible treatment of obesity in humans. The lateral hypothalamus and the nucleus accumbens shell (AcbSh) form a hypothalamic-limbic neuropeptide feeding circuit mediated by Melanin-Concentrating Hormone (MCH). MCH promotes feeding behavior via MCH receptor-1 (MCH1R) in the AcbSh, although this relationship has not been fully characterized. Given the AcbSh mediates reinforcing properties of food, we hypothesized that MCH modulates motivational aspects of feeding.Here we show that chronic loss of the rat MCH-precursor Pmch decreased food intake predominantly via a reduction in meal size during rat development and reduced high-fat food-reinforced operant responding in adult rats. Moreover, acute AcbSh administration of Neuropeptide-GE and Neuropeptide-EI (NEI), both additional neuropeptides derived from Pmch, or chronic intracerebroventricular infusion of NEI, did not affect feeding behavior in adult pmch(+/+) or pmch(-/-) rats. However, acute administration of MCH to the AcbSh of adult pmch(-/-) rats elevated feeding behavior towards wild type levels. Finally, adult pmch(-/-) rats showed increased ex vivo electrically evoked dopamine release and increased limbic dopamine transporter levels, indicating that chronic loss of Pmch in the rat affects the limbic dopamine system.Our findings support the MCH-MCH1R system as an amplifier of consummatory behavior, confirming this system as a possible target for the treatment of obesity. We propose that MCH-mediated signaling in the AcbSh positively mediates motivational aspects of feeding behavior. Thereby it provides a crucial signal by which hypothalamic neural circuits control energy balance and guide limbic brain areas to enhance motivational or incentive-related aspects of food consumption.     

Microsatellite mutations in the germline: implications for evolutionary inference

Microsatellite DNA sequences mutate at rates several orders of magnitude higher than that of the bulk of DNA. Such high rates mean that spontaneous mutations that form new-length variants can realistically be seen in pedigree analysis. Data on observed mutation events from various organisms are now accumulating, allowing inferences on DNA sequence evolution to be made through an unusually direct approach. Here I discuss and integrate microsatellite mutation data in an evolutionary context. A striking feature of the mutation process is that it seems highly heterogeneous, with distinct differences between species, repeat types, loci and alleles. Age and sex also affect the mutation rate. Within genomes at equilibrium, the microsatellite-length distribution is a delicate balance between biased mutation processes and point mutations acting towards the decay of repetitive DNA. Indeed, simple repeats do not evolve simply.     

Flexible larval development and the timing of destructive feeding by a solitary endoparasitoid: an optimal foraging problem in evolutionary perspective

1. In studying the evolution of life-history strategies in parasitoids, considerable attention has been paid to the relationship between host quality and parasitoid fitness. Various workers have reported that host quality influences parasitoid size, development time, and survival. Because body size is frequently correlated with fecundity, longevity, and host-finding ability in parasitoids, this parameter is usually considered to be the main target of selection. 2. In koinobiont parasitoids that consume the entire host before pupation, adult parasitoid size and development time are often strongly correlated with host size at the time when it is developmentally arrested through destructive feeding by the parasitoid larva. 3. Here, a mathematical model is proposed to describe the larval feeding behaviour of the solitary koinobiont endoparasitoid Venturia canescens in four larval stadia of its host Plodia interpunctella. In particular, the model describes how adult size, represented by an exponential growth rate, and development time are traded off when the parasitoid develops in nutritionally suboptimal second stadium hosts. 4. Using a graphical model, the different conditions faced by V. canescens during development in various host species of greatly differing mass are illustrated. 5. It is argued that the relative importance of size and development time on parasitoid fitness is determined by ecological and biological characteristics of both host and parasitoid, and it is suggested that there may be correlations between life-history traits and host-utilisation strategies among koinobionts.     

Labyrinthulomycetes phylogeny and its implications for the evolutionary loss of chloroplasts and gain of ectoplasmic gliding

The labyrinthulomycetes, also known as the 'Labyrinthulomycota' are saprotrophic or less frequently parasitic stramenopilan protists, usually in marine ecosystems. Their distinguishing feature is an 'ectoplasmic net,' an external cytoplasmic network secreted by a specialized organelle that attaches the cell to its substrate and secretes digestive enzymes for absorptive nutrition. In this study, one of our aims was to infer the phylogenetic position of the labyrinthulomycetes relative to the non-photosynthetic bicoeceans and oomycetes and the photosynthetic ochrophytes and thereby evaluate patterns of change from photosynthesis to saprotrophism among the stramenopiles. For the labyrinthulomycetes, we determined sequences of the actin, beta-tubulin, and elongation factor 1-alpha gene fragments and where necessary, ribosomal small subunit (SSU) genes. Multilocus analysis using standard tree construction techniques not only strongly supported the oomycetes as the sister group to the phototrophic stramenopiles, but also, for the first time with moderate statistical support, showed that the labyrinthulomycetes and the bicoecean as sister groups. The paraphyly of the non-photosynthetic groups was consistent with independent loss of photosynthesis in labyrinthulomycetes and oomycetes. We also wished to develop a phylogenetically based hypothesis for the origin of the gliding cell bodies and the ectoplasmic net found in some labyrinthulomycetes. The cells of species in Labyrinthula and Aplanochytrium share a specialized form of motility involving gliding on ectoplasmic tracks. Before our study, only ribosomal DNA genes had been determined for these genera and their phylogenetic position in the labyrinthulomycetes was equivocal. Multilocus phylogenies applying our newly determined protein-coding sequences divided the labyrinthulomycetes between sister clades 'A' and 'B' and showed that the monophyletic group containing all of the gliding species was nested among non-gliding species in clade B. This phylogeny suggested that species that glide via an ectoplasm evolved from species that had used the ectoplasm mainly for anchorage and assimilation rather than motility.