Poecilogony in the caenogastropod Calyptraea lichen (Mollusca: Gastropoda)

In marine invertebrates, polymorphism and polyphenism in mode of development are known as “poecilogony.” Understanding the environmental correlates of poecilogony and the developmental mechanisms that produce it could contribute to a better understanding of evolutionary transitions in mode of development. However, poecilogony is rare in marine invertebrates, with only ten recognized, well‐documented cases. Five examples occur in sacoglossan gastropods, and five occur in spionid polychaetes. Here, we document the eleventh case, and the first in a caenogastropod mollusc. Females of Calyptraea lichen collected in the field or reared in the laboratory often produce broods of planktotrophic larvae. They can also be collected with mixed broods, in which each capsule contains planktotrophic larvae, nurse embryos, and adelphophagic embryos. Adelphophages eat the nurse embryos and hatch as short‐lived lecithotrophic larvae, or even as juveniles. Mitochondrial COI and 16S DNA sequences for females with different types of broods differ by less than 0.5%, supporting conspecific status. Some females collected in the field with mixed broods subsequently produced planktotrophic broods, demonstrating that females can produce two different kinds of broods. Calyptraea lichen is therefore polyphenic in two ways: mode of development can vary among embryos within a capsule, and females can change the types of broods they produce.     

A new look at evolution in the Galápagos: evidence from the late Cenozoic marine molluscan fauna

Endemism is not as common in the marine invertebrate fauna of the Galápagos Islands region as in the adjacent terrestrial biota. Marine invertebrates in the Galápagos are largely cosmopolitan species from the Panamic, Indo-Pacific, Californian, or Peruvian faunal provinces. However, an endemic component is also present in the fauna. The observed pattern among marine invertebrate organisms can be accounted for by at least two processes: (1) genetic continuity between mainland and island populations mediated through planktonic larvae; and (2) lower rates of intrinsic evolutionary change. The evolutionary scenario standardly applied to terrestrial organisms in the Galápagos, namely, adaptive radiation and speciation in reproductive isolation from mainland source populations, does not apply to all marine invertebrates. Evidence in support of the alternative scenario for marine invertebrates comes from both published records of species occurring in the islands and recent studies of fossil-bearing deposits on several islands in the archipelago. Two misconceptions–considering the islands and sedimentary deposits to be older than now thought, and equating the rate of evolution of the terrestrial biota with the marine biota–can lead to an incorrect interpretation of evolution in the Galápagos Contrasts between marine invertebrate and terrestrial organisms serve to illustrate some fundamental differences which have important evolutionary implications. Some of these are: endemism; dispersal; taxonomic relationships; island definitions; rates of evolutionary change; and age of fossils. In terms of Darwin's evolutionary scenario, terrestrial organisms represent the paradigm and marine organisms represent the paradox.     

Inbreeding shapes the evolution of marine invertebrates

Inbreeding is a potent evolutionary force shaping the distribution of genetic variation within and among populations of plants and animals. Yet, our understanding of the forces shaping the expression and evolution of nonrandom mating in general, and inbreeding in particular, remains remarkably incomplete. Most research on plant mating systems focuses on self-fertilization and its consequences for automatic selection, inbreeding depression, purging, and reproductive assurance, whereas studies of animal mating systems have often assumed that inbreeding is rare, and that natural selection favors traits that promote outbreeding. Given that many sessile and sedentary marine invertebrates and marine macroalgae share key life history features with seed plants (e.g., low mobility, modular construction, and the release of gametes into the environment), their mating systems may be similar. Here, we show that published estimates of inbreeding coefficients (F_IS) for sessile and sedentary marine organisms are similar and at least as high as noted in terrestrial seed plants. We also found that variation in F_IS within invertebrates is related to the potential to self-fertilize, disperse, and choose mates. The similarity of F_IS for these organismal groups suggests that inbreeding could play a larger role in the evolution of sessile and sedentary marine organisms than is currently recognized. Specifically, associations between traits of marine invertebrates and F_IS suggest that inbreeding could drive evolutionary transitions between hermaphroditism and separate sexes, direct development and multiphasic life cycles, and external and internal fertilization.     

Adult exposure influences offspring response to ocean acidification in oysters

It is essential to predict the impact of elevated Pco₂ on marine organisms and habitats to anticipate the severity and consequences of future ocean chemistry change. Despite the importance of carry‐over effects in the evolutionary history of marine organisms, few studies have considered links between life‐history stages when determining how marine organisms will respond to elevated Pco₂, and none have considered the link between adults and their offspring. Herein, we exposed adults of wild and selectively bred Sydney rock oysters, Saccostrea glomerata to elevated Pco₂ during reproductive conditioning and measured the development, growth and survival response of their larvae. We found that elevated Pco₂ had a negative impact on larvae of S. glomerata causing a reduction in growth, rate of development and survival. Exposing adults to elevated Pco₂ during reproductive conditioning, however, had positive carry‐over effects on larvae. Larvae spawned from adults exposed to elevated Pco₂ were larger and developed faster, but displayed similar survival compared with larvae spawned from adults exposed to ambient Pco₂. Furthermore, selectively bred larvae of S. glomerata were more resilient to elevated Pco₂ than wild larvae. Measurement of the standard metabolic rate (SMR) of adult S. glomerata showed that at ambient Pco₂, SMR is increased in selectively bred compared with wild oysters and is further increased during exposure to elevated Pco₂. This study suggests that sensitive marine organisms may have the capacity to acclimate or adapt to elevated Pco₂ over the next century and a change in energy turnover indicated by SMR may be a key process involved.     

Developmental and Evolutionary History Affect Survival in Stressful Environments

The world is increasingly impacted by a variety of stressors that have the potential to differentially influence life history stages of organisms. Organisms have evolved to cope with some stressors, while with others they have little capacity. It is thus important to understand the effects of both developmental and evolutionary history on survival in stressful environments. We present evidence of the effects of both developmental and evolutionary history on survival of a freshwater vertebrate, the rough-skinned newt (Taricha granulosa) in an osmotically stressful environment. We compared the survival of larvae in either NaCl or MgCl₂ that were exposed to salinity either as larvae only or as embryos as well. Embryonic exposure to salinity led to greater mortality of newt larvae than larval exposure alone, and this reduced survival probability was strongly linked to the carry-over effect of stunted embryonic growth in salts. Larval survival was also dependent on the type of salt (NaCl or MgCl₂) the larvae were exposed to, and was lowest in MgCl₂, a widely-used chemical deicer that, unlike NaCl, amphibian larvae do not have an evolutionary history of regulating at high levels. Both developmental and evolutionary history are critical factors in determining survival in this stressful environment, a pattern that may have widespread implications for the survival of animals increasingly impacted by substances with which they have little evolutionary history.     

Primary cell culture from the nose of a marine organism, the banded houndshark, Triakis scyllium

Animal cells have been widely and continuously studied due to their usefulness in biological researches and production of pharmacological agents as well as food additives. Nevertheless, there are several problems such as the existence of viruses which introduce the possibility of mammalian-infection. In this reason, recently, animal cells derived from marine organisms have emerged to overcome these problems by many researches. However, marine animal-derived cells have not yet been well developed. The banded hound shark occupies an important position in an evolutionary perspective and currently a few biological substances have been used for medicines or food additives such as shark squalene and cartilage extract. In this study, primary cells were cultivated from a banded hound shark nose containing many extracellular matrix (ECM) materials. After successful isolation of one type of primary nasal cell, we optimized culture conditions including coating materials, media composition, serum concentrations and pH. Additionally, these cells demonstrated proliferation ability in vitro, generating secretions of collagen and sulfated polysaccharides. The cultivated primary cells are useful in the study of cellular biology and may be used to create a variety of ECM-originated bioactive substances.     

Recruitment of marine invertebrates: the role of active larval choices and early mortality

Summary Spatial variation in the recruitment of sessile marine invertebrates with planktonic larvae may be derived from a number of sources: events within the plankton, choices made by larvae at the time of settlement, and mortality of juvenile organisms after settlement, but before a census by an observer. These sources usually are not distinguished.A study of the recruitment of four species of sessile invertebrates living on rock walls beneath a kelp canopy showed that both selection of microhabitats by settling larvae and predation by fish may be important. Two microhabitats were of interest; open, flat rock surfaces, and small pits and crevices that act as refuges from fish predators.The polychaete Spirorbis eximus and the cyclostome bryozoan Tubulipora spp. showed no preference for refuges, but settled apparently at random on the available substrata. Tubulipora was preyed upon heavily by fish, while Spirorbis was relatively unaffected. The bryozoans Celleporaria brunnea and Scrupocellaria bertholetti both recruited preferentially into refuges. Scrupocellaria were preyed upon, while Celleporaria juveniles seemed unaffected. Predation by fish modified the spatial distribution (Tubulipora), abundance (Tubulipora), or size distribution (Scrupocellaria) of the juvenile population, or had relatively little effect (Celleporaria, Spirorbis).All of the above events occur within three weeks of settlement. Since inferences about the effect of larval events on the population dynamics of adult organisms are often based on observations of the patterns of recruitment after one or two months, they are therefore likely to be misleading.     

Intertidal population genetic dynamics at a microgeographic seascape scale

The intertidal community is among the most physically harsh niches on earth, with highly heterogeneous environmental and biological factors that impose strong habitat selection on population abundance, genetic connectivity and ecological adaptation of organisms in nature. However, most genetic studies to date have concentrated on the influence of basin-wide or regional marine environments (e.g. habitat discontinuities, oceanic currents and fronts, and geographic barriers) on spatiotemporal distribution and composition of intertidal invertebrates having planktonic stages or long-distance dispersal capability. Little is known about sessile marine organisms (e.g. seaweeds) in the context of topographic tidal gradients and reproductive traits at the microgeographic scale. In this issue of Molecular Ecology, Krueger-Hadfield et al. ( 2013a ) implemented an elaborate sampling strategy with red seaweed (Chondrus crispus) from a 90-m transect stand near Roscoff and comprehensively detected genome-scale genetic differentiation and biases in ploidy level. This study not only revealed that tidal height resulted in genetic differentiation between high- and low-shore stands and restricted the genetic exchange within the high-shore habitat, but also demonstrated that intergametophytic nonrandom fertilization in C. crispus can cause significant deviation from Hardy–Weinberg equilibrium. Such new genetic insights highlight the importance of microgeographic genetic dynamics and life history characteristics for better understanding the evolutionary processes of speciation and diversification of intertidal marine organisms.     

A new approach for testing contaminated marine sediments: fertilization success of lugworms following parental exposure

A sediment bioassay is being developed using several marine benthic invertebrates to assess the effects of parental transfer of contaminants to the gametes. In this preliminary study, the emphasis was placed on developing methods for the in vitro fertilization of lugworm, Arenicola marina, oocytes.Lugworms exposed to contaminated sediments in outdoor mesocosms were brought to the laboratory, just before the beginning of the spawning period. The reliability of an in vitro fertilization procedure was tested by varying several parts of the method. Main results are that eggs and embryos may be physically damaged by cleaning over a sieve. However, as no negative effects were observed when leaving eggs and sperm together for 24 h, the sperm need not be washed off until the embryos are preserved for further examination later on.A first, incomplete screening of the effects of contaminated harbour dredged sediments indicated some effect on the reproductive success.     

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.     

Metamorphosis of <Emphasis Type="Italic">Hydractinia echinata</Emphasis>—natural versus artificial induction and developmental plasticity

Many marine invertebrates reproduce through a larval stage. The settlement and metamorphosis of most of the species are synchronised and induced by environmental organisms, mainly bacteria. The hydrozoan Hydractinia echinata has become a model organism for metamorphosis of marine invertebrates. In this species, bacteria, e.g. Pseudoalteromonas espejiana, are the natural inducers of metamorphosis. Like in other species of marine invertebrates, metamorphosis can be induced artificially by monovalent cations, e.g. Cs⁺. In this study, we present systematic data that metamorphosis—with both inducing compounds, the natural one from bacteria and the artificial one Cs⁺—are indeed similar with respect to (a) the morphological progression, (b) the localisation of the primary induction signal in the larva, (c) the pattern of apoptotic cells occurring during the initial 10 h of metamorphosis and (d) the disappearance of RFamide-dependent immunocytochemical signals in sensory neurons during this process. However, a difference occurs during the development of the anterior end, insofar as apoptotic cells and settlement appear earlier in planulae induced with bacteria. Thus, basically, Cs⁺ may be used as an artificial inducer, mimicking the natural process. However, differences in the appearance of apoptotic cells and in settlement raise the question of how enormous developmental plasticity in hydrozoans actually can be, and how this is related to the absence of malignant devolution in hydrozoans.     

Convergent Antifouling Activities of Structurally Distinct Bioactive Compounds Synthesized Within Two Sympatric Haliclona Demosponges

A wide range of sessile and sedentary marine invertebrates synthesize secondary metabolites that have potential as industrial antifoulants. These antifoulants tend to differ in structure, even between closely related species. Here, we determine if structurally divergent secondary metabolites produced within two sympatric haliclonid demosponges have similar effects on the larvae of a wide range of benthic competitors and potential fouling metazoans (ascidians, molluscs, bryozoans, polychaetes, and sponges). The sponges Haliclona sp. 628 and sp. 1031 synthesize the tetracyclic alkaloid, haliclonacyclamine A (HA), and the long chain alkyl amino alcohol, halaminol A (LA), respectively. Despite structural differences, HA and LA have identical effects on phylogenetically disparate ascidian larvae, inducing rapid larval settlement but preventing subsequent metamorphosis at precisely the same stage. HA and LA also have similar effects on sponge, polychaete, gastropod and bryozoan larvae, inhibiting both settlement and metamorphosis. Despite having identical roles in preventing fouling and colonisation, HA and LA differentially affect the physiology of cultured HeLa human cells, indicating they have different molecular targets. From these data, we infer that the secondary metabolites within marine sponges may emerge by varying evolutionary and biosynthetic trajectories that converge on specific ecological roles.     

Effects of ocean acidification on the early life history processes of the breadcrumb sponge Halichondria panicea

Ocean acidification (OA) is predicted to result in reduced survival, growth, reproduction, and overall biodiversity of marine invertebrates, and yet we lack information about the response to OA of some major groups of marine organisms. In particular, we know relatively little about how OA will impact temperate sponges, which will experience more extreme low pH conditions than tropical species. In this study, we quantified OA-induced changes in early life history patterns (larval mortality and condition, settlement rate, recruit survival, and size) in the non-calcifying breadcrumb sponge Halichondria panicea collected from a temperate intertidal site in the California Current Large Marine Ecosystem. Sponge larvae were exposed to OA conditions for 15 days, and early life history patterns were observed. Compared with baseline (“present”) conditions, larval mortality and settlement rates increased in the acidified treatment (“future”). This effect was restricted to larval stages; treatment had no effect on the growth and survival of recruits. This study is significant in that it shows that H. panicea may be particularly vulnerable to changes in ocean pH during the larval stage, which could ultimately reduce total sponge abundance by diminishing the number of larvae that survive to settlement.     

Fast accumulation of few polyhedra mutants during passage of a Spodoptera frugiperda multicapsid nucleopolyhedrovirus (Baculoviridae) in Sf9 cell cultures

Baculoviruses are a group of viruses that infect invertebrates and that have been used worldwide as a biopesticide against several insect pests of the Order Lepidoptera. In Brazil, the baculovirus Spodoptera frugiperda multicapsid nucleopolyhedrovirus (SfMNPV; Baculoviridae) has been used experimentally to control S. frugiperda (Lepidoptera: Noctuidae), an important insect pest of corn (maize) fields and other crops. Baculoviruses can be produced either in insect larvae or in cell culture bioreactors. A major limitation to the in vitro production of baculoviruses is the rapid generation of mutants when the virus undergoes passages in cell culture. In order to evaluate the potential of in vitro methods of producing SfMNPV on a large-scale, we have multiplied a Brazilian isolate of this virus in cell culture. Extensive formation of few polyhedra mutants was observed after only two passages in Sf9 cells.     

The synergism between hydrocarbon pollutants and UV radiation: a potential link between coastal pollution and larval mortality

Coastal, benthic invertebrates with complex life history strategies are exposed to stage- and habitat-specific selective forces. In the coastal environment, benthic adults are exposed to polycyclic aromatic hydrocarbon pollutants (PAHs) due to their proximity to human activities (shipping, urbanization, and industrialization). Benthic invertebrates produce lipid-rich eggs or larvae that absorb PAHs from polluted estuaries and coastal waters. The larvae of many coastal invertebrates move offshore following release from benthic adults. During development in offshore waters, larvae of some species are exposed to relatively high levels of ultraviolet (UV) radiation. Marine organisms vary in their tolerance to PAHs and UV radiation. The purpose of this study was to examine the effects of the sequential exposure of the larvae of marine crabs to PAHs and UV radiation.Using laboratory experiments, the larvae of four crab species were exposed to PAHs and UV radiation. There was a significant synergistic effect of exposure to PAH (fluoranthene or pyrene) and UV radiation on larvae of the spider crab (Libinia dubia), the stone crab (Menippe adina) and the mud crab (Panopeus herbstii). Larvae of blue crabs (Callinectes sapidus) were exposed to PAHs and UV radiation in both laboratory and solar UV experiments. Significantly higher mortality occurred for C. sapidus larvae using either type of UV-artificial or solar.Larvae of coastal invertebrates with complex life history strategies are susceptible to the combined effects of PAHs and UV radiation. In this study, the exposure of crab larvae to PAHs and UV radiation resulted in mortality to crab larvae using laboratory and solar UV experiments. There were no effects on larval crab mortality due to PAH or UV radiation independently but mortality was as high as 100% when both factors were present.     

Settlement inhibition of fouling invertebrate larvae by metabolites of the marine bacterium halomonas marina within a polyurethane coating

The marine bacterium, Halomonas marina (ATCC 27129), was shown to inhibit settlement and development of the sessile invertebrates Balanus amphitrite and Bugula neritina. Different bacterial treatments were employed to investigate this interaction. Filmed bacteria and liquid suspensions of whole cells, lysed cells and culture filtrate all reduced settlement of B. amphitrite. Polyurethane coatings containing whole cells were partially inhibitory while lysed cells caused complete inhibition of B. amphitrite larval settlement. In contrast, culture filtrate in a polyurethane matrix stimulated settlement of B. amphitrite larvae. Whole cells, culture filtrate, and lysed cells embedded in a polyurethane coating also controlled B. neritina settlement and maturation.     

Immunocytochemical localization of serotonin in embryos, larvae and adults of the lancelet, Branchiostoma floridae

Serotonin (5-hydroxytryptamine) is a biogenic amine distributed throughout the metazoans and has an old evolutionary history. It is involved as a developmental signal in the early morphogenesis of both invertebrates and vertebrates, whereas in adults it acts mainly as a neurotransmitter and gastrointestinal hormone. In vertebrates, serotonin regulates the morphogenesis of the central nervous system and the specification of serotonergic as well as dopaminergic neurons. The present study uses, as an experimental model, an invertebrate chordate, the lancelet Branchiostoma floridae, characterized by its remarkable homologies with vertebrates that allows the 'bauplan' of the probable ancestor of vertebrates to be outlined. In particular, the involvement of serotonin as a developmental signal in embryos and larvae, as well as a neurotransmitter and gastrointestinal hormone in adult specimens of Branchiostoma floridae, gives further support to a common origin of cephalocordates and vertebrates.     

DEVELOPMENTAL CONSEQUENCES OF AN EVOLUTIONARY CHANGE IN EGG SIZE: AN EXPERIMENTAL TEST

Larvae of two species of sea urchins (Strongylocentrotus droebachiensis and S. purpuratus) differ in initial form and in the rate of development. To determine whether these differences are attributable to the large interspecific difference in egg size, we experimentally reduced egg size by isolating blastomeres from embryos. The rate of development of feeding larvae derived from isolated blastomeres was quantified using a novel morphometric method. If the differences early in the life histories of these two species are due strictly to differences in egg size, then experimental reduction of the size of S. droebachiensis eggs should yield an initial larval form and rate of development similar to that of S. purpuratus. Our experimental manipulations of egg size produced three clear results: 1) smaller eggs yielded larvae that were smaller and had simpler body forms, 2) smaller eggs resulted in slower development through the early feeding larval stages, and 3) effects of egg size were restricted to early larval stages. Larvae from experimentally reduced eggs of the larger species had rates of development similar to those of the smaller species. Thus, cytoplasmic volumes of the eggs, not genetic differences expressed during development, account for differences in larval form and the rate of form change. This is the first definitive demonstration of the causal relationship between egg size (parental investment per offspring) and life-history characteristics in marine benthic invertebrates. Because larval form influences feeding capability, the epigenetic effects of egg size on larval form are likely to have important functional consequences. Adaptive evolution of egg size may be constrained by the developmental relationships between egg size and larval form: evolutionary changes in egg size alone can result in concerted changes in larval form and function; likewise evolutionary changes in larval form and function can be achieved through changes in egg size. These findings may have broader implications for other taxa in which larval morphology and, consequently, performance may be influenced by changes in egg size.     

Temperature and embryonic development in polar marine invertebrates

The life-history tactics of many Antarctic marine invertebrates suggest that the commonly observed slow rates of growth are adaptations to the pattern of food availability, and not due to low temperature per se. This implies that marine invertebrates have been able, over the course of evolutionary time, to compensate their rates of embryonic development for the effect of temperature. Data from north Atlantic copepods indicate that this is so. It is therefore suggested that the slow rates of embryonic development in many Antarctic marine invertebrates are the result of large egg size, and not the low temperature. Large, slowly developing eggs are part of a suite of tactics, often called K-strategies, which characterise many marine invertebrates in Antarctica.