Asterinid Sea Star Research Articles

Transcriptomic analysis of Nodal - and BMP- associated genes during development to the juvenile seastar in Parvulastra exigua (Asterinidae).

The molecular mechanisms underlying development of the pentameral body of adult echinoderms are poorly understood but are important to solve with respect to evolution of a unique body plan that contrasts with the bilateral body plan of other deuterostomes. As Nodal and BMP2/4 signalling is involved in axis formation in larvae and development of the echinoderm body plan, we used the developmental transcriptome generated for the asterinid seastar Parvulastra exigua to investigate the temporal expression patterns of Nodal and BMP2/4 genes from the embryo and across metamorphosis to the juvenile. For echinoderms, the Asteroidea represents the basal-type body architecture with a distinct (separated) ray structure. Parvulastra exigua has lecithotrophic development forming the juvenile soon after gastrulation providing ready access to the developing adult stage. We identified 39 genes associated with the Nodal and BMP2/4 network in the P. exigua developmental transcriptome. Clustering analysis of these genes resulted in 6 clusters with similar temporal expression patterns across development. A co-expression analysis revealed genes that have similar expression profiles as Nodal and BMP2/4. These results indicated genes that may have a regulatory relationship in patterning morphogenesis of the juvenile seastar. Developmental RNA-seq analyses of Parvulastra exigua show changes in Nodal and BMP2/4 signalling genes across the metamorphic transition. We provide the foundation for detailed analyses of this cascade in the evolution of the unusual pentameral echinoderm body and its deuterostome affinities.

Temporal pattern of offspring release and degree of parental investment in two viviparous asterinid sea stars with an overview of matrotrophy and offspring size variation in echinoderms that care for their offspring

ABSTRACT The temporal pattern of juvenile release by two species of viviparous asterinid sea stars that incubate their young in the gonads was documented. Parvulastra parvivipara released juveniles (400–3000 µm diameter) in 1–5 cohorts. Parents produced large juveniles (>1000-µm) irrespective of adult size. Released juveniles were larger than the retained juveniles. Most Cryptasterina hystera offspring were released in one large clutch of similarly sized juveniles (732-µm mean diameter). After this initial release, the presence of large juveniles (944-µm mean diameter) in the gonads of C. hystera indicates that they are supported by matrotrophy, potentially through sibling cannibalism. The degree of parental investment additional to the egg in both species was estimated by using a matrotrophy index (MI, the ratio of juvenile and egg dry mass). As the eggs of P. parvivipara and C. hystera could not be isolated, the eggs of their congeners (P. exigua and C. pentagona, respectively) were used as a proxy to estimate the MI, the first application of this index to a marine invertebrate. The MI ranged from 597 to 55082 in P. parvivipara and 1.7–6.2 in C. hystera for juveniles across the different size classes. Matrotrophy and size variation of offspring may be characteristics of echinoderms that incubate their young.

<p class="HeadingRunIn"><strong>Arrangement and size variation of intra-gonadal offspring in a viviparous asterinid sea star</strong></p>

Sibling competition and developmental asynchrony may greatly influence the arrangement and size of offspring of marine invertebrates that care for their young. In Parvulastra parvivipara, an asterinid sea star that incubates its young in the gonads, sibling cannibalism supports post-metamorphic development. Offspring size varies within (coefficient of variation, CV = 22.6 %) and among (CV = 17.7%) the gonads. Confocal microscopy was used to visualize early embryos and oocytes, and revealed the presence of several developmental stages within individual gonads. The eggs were a mean diameter of 84 μm. The observation of a gastrula at 86 µm smaller than the largest egg observed (134 µm) suggests that terminal egg size varies. The appearance of early embryos surrounded by somatic cells suggests that they may receive nutrients through histotrophy. Sibling competition intensifies once the digestive tract is functional in the tiny juveniles which then start to consume siblings. The arrangement of the offspring in the gonads was observed using micro-computed tomography. The juveniles were oriented with their oral surface facing each other, presumably as a defensive strategy to protect themselves from being eaten. Periodic release of offspring in single or several cohorts indicates continual reproduction. Released and retained juveniles varied in size. It is not known what initiates birth but it may be mediated by sibling competition. Larger adults had a greater allocation to female reproductive output than smaller adults.

Intragonadal incubation of progeny in three viviparous asterinid sea stars that differ in offspring provisioning, lecithotrophy vs matrotrophy

In marine invertebrates that care for their young, the number of offspring is often correlated with adult size. The number, size, and mass of progeny relative to parent size were investigated in three asterinid sea star species that incubate their young in the gonads. Cryptasterina hystera has intragonadal planktonic-type lecithotrophic larvae with development supported by large eggs (440-µm diameter) and the juveniles are similar in size (655-µm diameter; coefficient of variation, CV = 6.89%). By contrast, Parvulastra vivipara and P. parvivipara have small vestigial larvae and small eggs (135–150-µm diameter) with offspring development supported by sibling cannibalism (matrotrophy). The juveniles in the gonads vary in size (500–5000-µm diameter, CV = 63.87 and 53.27%, respectively). All three species show a positive relationship between parent size and the number and size of juveniles. The allometry of brooding hypothesis that the number of progeny that can be cared for is (paradoxically) constrained in large adults due to space limitation was tested. In all species, the number of progeny increased with adult size, indicating that there are no allometric constraints on offspring incubation. To compare parental investment across the two modes of provisioning, the juvenile weight of C. hystera was used as a pro rata progeny unit. The matrotrophs had a higher reproductive output than similarly sized C. hystera. Of the hypotheses proposed to explain the evolution of parental care in marine invertebrates, none are broadly applicable to the viviparous asterinids because of the marked differences in their reproductive strategies.

Forever fissiparous: asexual propagation and stable demography in a tropical and geographically isolated asterinid sea star

Sea stars of the family Asterinidae are well known for their diverse life history strategies encompassing sexual reproduction through various larval forms, while others, all multi-armed species, through clonal asexual reproduction. For at least 25 years, a geographically isolated population of the minute (radius < 7 mm) tropical Pacific fissiparous asterinid, Ailsastra heteractis, has been locally abundant in a shallow water coral rubble habitat at One Tree Island, southern Great Barrier Reef. The population biology of this sea star was investigated over 14 years to characterise its asexual reproduction through fission (splitting in half) and to determine whether a size threshold is reached for an expected switch to sexual reproduction. Fission followed by regeneration was the dominant propagation mechanism generating individuals that varied in arm number (2–7) and length (0.5–6.9 mm). Recently split individuals were present year round with regenerating individuals being the most prevalent body form. Growth rates and fission activity, as measured by mean arm length, varied among months but with no overall pattern. Analyses of arm length data based on season indicated that fission activity was lowest in autumn. There was a positive correlation between the incidence of fission and air and water temperature with a decrease in the proportion of recently split individuals in winter and an increase in summer. Fission was present in all size classes with no evidence of a switch to a larger sexual morphotype with growth. Juvenile recruitment from sexual reproduction was not evident. Extensive searches did not reveal the presence of other populations of A. heteractis. The absence of recruitment and reproductive organs coupled with a stable population demography indicates that propagation by fission is the only reproductive mechanism for the A. heteractis population.

The Derwent River seastar: re-evaluation of a critically endangered marine invertebrate

The Derwent River seastar, ‘Marginaster’ littoralis (Echinodermata: Asteroidea), has been assessed as critically endangered owing to its highly restricted range within one estuary in Tasmania, Australia. However, there have been concerns about the validity and status of the species. Here, we use non-invasive X-ray computed tomography to review the morphology of the holotype. This reveals the presence of internal ossicles to strengthen the disc margin, a character that requires the taxonomic transfer of this species to the family Asterinidae, genus Patiriella. The presence of relatively long marginal spinelets (0.7–0.9 mm) reliably distinguishes this species from the invasive congeneric Patiriella regularis (0.2–0.35 mm). These findings remove doubt about the validity of the species; the recorded habitat and restricted range of Patiriella littoralis are not exceptional for an asterinid seastar. The weight of evidence suggests that it is an endemic species, rather than a transient exotic introduced to Tasmania via shipping or food importation. Its known habitat has been severely impacted by urbanization, poor water quality and invasive species. Targeted surveys in 1993 and 2010 failed to find this species, and it is highly probable that the Derwent River seastar is now extinct; one of the few documented recent marine invertebrate extinctions.

New asterinid seastars from the western Pacific Ocean (Echinodermata: Asteroidea)

New asterinid seastars from the western Pacific Ocean (Echinodermata: Asteroidea)

New asterinid seastars from northwest Australia, with a revised key to Aquilonastra species (Echinodermata: Asteroidea)

New asterinid seastars from northwest Australia, with a revised key to Aquilonastra species (Echinodermata: Asteroidea)

Highly expressed genes in gonads of the bat star Patiria miniata: gene ontology, expression differences, and gamete recognition loci

AbstractEvolutionary analysis of mating systems in broadcast‐spawning marine animals and plants has focused on sperm‐ and egg‐surface proteins and glycopeptides that mediate reproductive interactions at different stages of gamete recognition. Improved understanding of the ecology and evolution of such interactions depends on extending our knowledge to multiple genes expressed in both sperm and eggs of diverse taxonomic groups with different modes of fertilization. Here, we use readily accessible next‐generation sequencing methods and desktop bioinformatics to characterize the repertoire of highly expressed genes in testes and ovaries of the asterinid sea star Patiria miniata, including gene ontology annotations for male‐ and female‐expressed molecules, and descriptions of two genes that encode egg‐surface molecules involved in fertilization that have not previously been studied in sea stars. The results are used to contrast expression differences between the testis and ovary, and to develop hypotheses of gamete‐specific expression. We also explore differences in ovary gene expression among multiple females from northern and southern populations that show nucleotide differentiation at many non‐expressed loci and at a gamete recognition locus.

Very fine-scale population genetic structure of sympatric asterinid sea stars with benthic and pelagic larvae: influence of mating system and dispersal potential

The present study investigated the fine-scale population genetic structure of sympatric asterinid sea stars with contrasting modes of larval development (benthic versus pelagic). Parvulastra exigua lacks a dispersive life phase yet is one of the worlds most widely distributed and abundant sea stars, whereas Meridiastra calcar, a sea star with a dispersive larva, has a more limited regional scale distribution. Populations of P. exigua sampled from tide pools on three adjacent headlands showed significant genetic substructure (mitochodrial DNA control region) at fine spatial scales (tide pools < 300 m apart: FST = 0.249, P < 0.01; headlands 5–15 km apart: FST = 0.125, P = 0.04). As expected, M. calcar populations sampled from the same headlands did not exhibit significant genetic structuring (FST = 0.029, P = 0.14). The life-history traits of P. exigua, a mixed mating system (selfing + outcrossing), pseudocopulation among closely-related conspecifics, and an entirely benthic life cycle with a philopatric larva, undoubtedly influence its strong genetic structure across fine spatial scales. Localized genetic structure, especially at the very fine-scale of tide pools, would not be detected in the more typical regional scale approaches adopted by most studies of marine invertebrate populations. Biological Journal of the Linnean Society, 2013, ●●, ●●–●●.

Respiratory response of the intertidal seastar Parvulastra exigua to contemporary and near-future pulses of warming and hypercapnia

As typical of intertidal invertebrates the asterinid seastar Parvulastra exigua experiences marked variation in environmental temperature and pH/pCO2 due to tidal exchange and diurnal patterns of photosynthesis and respiration. We characterized the temperature and pH/pCO2 conditions in the mid-intertidal, rocky-shore habitat of this species and used these data along with projections for the ocean over coming decades to define treatments in oxygen consumption experiments. The metabolic response of P. exigua to warming and acidification was dominated by temperature as the most significant factor influencing oxygen consumption. When P. exigua were exposed to intermediate pH/pCO2 (7.8 /≈750ppm) levels combined with pulses of warming occasionally experienced in nature (6°C above sea surface temperature), the effect of temperature on metabolism was diminished. Our results show that the metabolic response of P. exigua is resilient to current levels of stress, but may be vulnerable in the future to the interactive effects of ocean warming and acidification at levels expected under near-future climate change.

Selfing in Parvulastra exigua: an asterinid sea star with benthic development

Parvulastra exigua, a species that lacks a dispersive larva, is paradoxically one of the most widely distributed and abundant sea stars in Australia. The potential that self-fertilization and successful development of self-generated progeny might contribute to population maintenance in this species was investigated through induction of spawning in isolated individuals collected from five populations near Sydney, New South Wales (34°S, 151°E), during the spawning period (August–October 2010, 2011). Evidence of selfing differed significantly among the five populations but the level of selfing within individual egg masses did not. Overall, there was a mean of 8.9% fertilization in egg masses with embryos. Some clutches developed to the juvenile stage while others arrested development before hatching. The presence of miniscule testis tissue in gonads that appeared to be ovaries indicated that hermaphroditism may be more common in some populations than indicated by anatomy. Mixed mating (selfing + outcrossing), pseudocopulation during egg laying and developmental success of self-fertilized embryos may contribute to the ecological success of P. exigua. These might influence population genetic structure and would facilitate establishment of founder populations by a small number of migrants.

A New Asterinid Sea Star, Disasterina akajimaensis (Echinodermata: Asteroidea) from the Ryukyu Islands, Japan, with Notes on the Genus Disasterina

A new asterinid, Disasterina akajimaensis sp. nov., is described from a specimen collected at Akajima Island, the Ryukyu Islands, Japan. It is clearly distinguishable from its five congeners by the following diagnostic characters: body relatively low and flat, uncalcified interradial areas conspicuous on ventral interradii, papulae numerous in center of disc, abactinal plates mostly lacking spinelets, inferomarginal plates with 2-4 spinelets, actinolateral plates with 1 spine, oral plates with 4-5 oral spines and no suboral spine, adambulacral plates with 1-3 furrows and 1 subambulacral spine. This is the first report of this genus from Japanese waters. Notes on the genus Disasterina and a tabular summary of the characters of the currently known species are also given.

The coeloms in a late brachiolaria larva of the asterinid sea star Parvulastra exigua: deriving an asteroid coelomic model

Morris, V.B., Selvakumaraswamy, P., Whan, R., and Byrne, M. 2011. The coeloms in a late brachiolaria larva of the asterinid sea star Parvulastra exigua: deriving an asteroid coelomic model. —Acta Zoologica (Stockholm) 92: 266–275. The coeloms and their interconnexions in a late pre-metamorphic brachiolaria larva of a sea star are described from the series of images in the frontal, transverse and sagittal planes obtained by confocal laser scanning microscopy. A larval, brachial coelom connects with the coeloms of the adult rudiment that lie posteriorly. The connexion is through the anterior coelom, which lies over the head of the archenteron, to the right anterior coelom and then to the left posterior coelom through the ventral horn of the left posterior coelom. The right posterior coelom is a separate coelom. The hydrocoele is on the larval left side separated from other coeloms except for a connexion to the anterior coelom. On the larval right side, the anterior coelom and right anterior coelom connect with the pore canal that opens to the exterior at the hydropore. From these coeloms, we derived an asteroid coelomic model comprising the larval left and right coeloms linked over the head of the archenteron by a common anterior coelom. The asymmetry of the hydrocoele and the left posterior coelom on the left side linked through the common anterior coelom to the right side, with the external opening, translates into the oral and aboral coeloms of the adult stage. The coelomic model has application in the search for morphological homology between the echinoderm classes and the deuterostome phyla.

Allelic inheritance in naturally occurring parthenogenetic offspring of the gonochoric sea star Patiria miniata

Abstract. In laboratory studies of fertilization using the gonochoric broadcast‐spawning asterinid sea star Patiria miniata, we found many cases in which some mature eggs spawned by females formed cleavage‐stage embryos and feeding bipinnaria larvae without fertilization by sperm. Segregation of maternal microsatellite alleles among the parthenogenetic offspring of known heterozygous females was consistent with several specific modes of asexual reproduction, including polar body suppression. Cryptic outcrossing by sperm contamination was ruled out by the failure to observe non‐maternal alleles. The potential for asexual reproduction by the normally outcrossing members of P. miniata may suggest a shared propensity for asexuality among asterinid species from several clades in which isolated adults can produce offspring without outcrossing.

Bindin from a sea star.

The genetic basis for the evolution of development includes genes that encode proteins expressed on the surfaces of sperm and eggs. Previous studies of the sperm acrosomal protein bindin have helped to characterize the adaptive evolution of gamete compatibility and speciation in sea urchins. The absence of evidence for bindin expression in taxa other than the Echinoidea has limited such studies to sea urchins, and led to the suggestion that bindin might be a sea urchin-specific molecule. Here we characterize the gene that encodes bindin in a broadcast-spawning asterinid sea star (Patiria miniata). We describe the sequence and domain structure of a full-length bindin cDNA and its single intron. In comparison with sea urchins, P. miniata bindin is larger but the two molecules share several general features of their domain structure and some sequence features of two domains. Our results extend the known evolutionary history of bindin from the Mesozoic (among the crown group sea urchins) into the early Paleozoic (and the common ancestor of eleutherozoans), and present new opportunities for understanding the role of bindin molecular evolution in sexual selection, life history evolution, and speciation among sea stars.

Nervous System Development in Feeding and Nonfeeding Asteroid Larvae and the Early Juvenile

Larval and juvenile nervous systems (NS) of three asterinid sea stars with contrasting feeding and nonfeeding modes of development were characterized using the echinoderm-specific synaptotagmin antibody. In the feeding bipinnaria and brachiolaria larvae of Patiriella regularis, the species with ancestral-type development, an extensive NS was associated with the ciliary bands (CBs) and attachment complex. Lecithotrophic planktonic (Meridastra calcar) and benthic (Parvulastra exigua) brachiolariae lacked CBs and the associated NS, but had an extensive NS in the attachment complex. The similarity in the distribution and morphology of synaptotagmin immunoreactive neurons and the anatomy of the NS in the attachment complex of these closely related sea stars suggests conservation of neurogenesis in settlement-stage larvae regardless of larval feeding mode. Nerve cells were prominent on the brachia of all three species. In advanced brachiolariae the larval nervous system was localized to the adhesive disc as the larval body resorbed during metamorphosis. The structures and tissues that contained larval neurons degenerated during metamorphosis. There was no evidence that the larval NS persists through metamorphosis. In juvenile development, synaptotagmin IR was first evident in the NS of the tube feet. As the central nervous system developed, synaptotagmin IR reflected the histological organization of the adult NS. The juvenile NS formed de novo with a temporal lapse between histogenesis and synaptotagmin IR. We evaluated the ontogeny of NS organization in the change in body plan from the bilateral larva to the radial juvenile.

Emerging infectious disease in sea stars: castrating ciliate parasites in Patiria miniata

Orchitophrya stellarum is a holotrich ciliate that facultatively parasitizes and castrates male asteriid sea stars. We discovered a morphologically similar ciliate in testes of an asterinid sea star, the northeastern Pacific bat star Patiria miniata (Brandt, 1835). This parasite may represent a threat to Canadian populations of this iconic sea star. Confirmation that the parasite is O. stellarum would indicate a considerable host range expansion, and suggest that O. stellarum is a generalist sea star pathogen.

Something for nothing? Reconstruction of ancestral character states in asterinid sea star development

Traits from early development mapped onto phylogenetic trees can potentially offer insight into the evolutionary history of development by inferring the states of those characters among ancestors at nodes in the phylogeny. A key and often-overlooked aspect of such mapping is the underlying model of character evolution. Without a well-supported and realistic model ("nothing"), character mapping of ancestral traits onto phylogenetic trees might often return results ("something") that lack a sound basis. Here we reconsider a challenging case study in this area of evolutionary developmental biology: the inference of ancestral states for ecological and morphological characters in the reproduction and larval development of asterinid sea stars. We apply improved analytical methods to an expanded set of asterinid phylogenetic data and developmental character states. This analysis shows that the new methods might generally offer some independent insight into choice of a model of character evolution, but that in the specific case of asterinid sea stars the quantitative features of the model (especially the relative probabilities of different directions of change) have an important effect on the results. We suggest caution in applying ancestral state reconstructions in the absence of an independently corroborated model of character evolution, and highlight the need for such modeling in evolutionary developmental biology.

Fuels for development: evolution of maternal provisioning in asterinid sea stars

For marine invertebrates, larval developmental mode is inseparably linked to the nutritional content of the egg. Within the asterinid family of sea stars there have been multiple, independent, evolutionary transitions to lecithotrophic development from the ancestral, planktotrophic state. To investigate the evolution of maternal investment and development within the Asterinidae, we quantified individual lipid classes and total protein for eggs and larval stages of closely related species representing three developmental modes (planktotrophy, planktonic lecithotrophy and benthic lecithotrophy). Within species, maternal provisioning differed between females indicating that egg quality varied with parentage. Maternal investment was related to egg size but, after correcting for egg volume, we identified two major oogenic modifications associated with the evolution of lecithotrophic development: (1) a reduction in protein deposition that probably reflects the reduced structural requirements of nonfeeding larvae, (2) an increase in deposition of a single class of energetic lipid, triglyceride (TG). The exception was Parvulastra exigua, which has benthic, lecithotrophic development and lays eggs with a lipid to protein ratio close to that of planktotrophs. This oogenic strategy may provide P. exigua larvae with a protein “weight-belt” that assists in maintaining a benthic existence. Asterinids with planktotrophic development used a significant portion of egg TG to build a feeding bipinnaria larva. For Meridiastra mortenseni, female-specific differences in egg TG were still evident at the bipinnaria stage indicating that egg quality has flow-on effects for larval fitness. In lecithotrophic asterinids, TG reserves were not depleted in development to the larval stage whereas protein stores may help fuel early larval development. Available data indicate that there may be two evolutionarily stable egg lipid profiles for free-spawning, temperate echinoderms.