Evolution of Maternal Provisioning and Development in the Ophiuroidea: Egg Size, Larval Form and Parental Care.

The Ophiuroidea is the most speciose class of echinoderms and has the greatest diversity of larval forms, but we know less about the evolution of development (evo-devo) in this group than for the other echinoderm classes. As is typical of echinoderms, evo-devo in the Ophiuroidea resulted in the switch from production of small eggs and feeding (planktotrophic) larvae to large eggs and non-feeding (lecithotrophic) larvae. Parental care (ovoviviparity or viviparity/matrotrophy) is the most derived life history. Analysis of egg data for 140 species (excluding viviparity and facultative planktotrophy) indicated a bimodal distribution in egg volume corresponding to planktotrophy and lecithotrophy + ovoviviparity, with three significant egg size groups due to the very large eggs of the ovoviviparous species. The marked reduction in fecundity in species with extremely large eggs is exemplified by the ovoviviparous species. Egg size in the two species with facultative planktotrophy were intermediate with respect to the two modes. Identifying the ancestral larval life history pattern and the pathways in the switch from feeding to non-feeding larvae is complicated by the two patterns of metamorphosis seen in species with planktotrophic development: Type I (ophiopluteus only) and Type II (ophiopluteus + vitellaria larva). The variability in arm resorption at metamorphosis across ophiuroid families indicates that the Type I and II patterns may be two ends of a morphological continuum. This variability indicates ancestral morphological plasticity at metamorphosis followed by canalization in some taxa to the vitellaria as the metamorphic larva. Vestigial ophiopluteal traits in lecithotrophic ophioplutei and vitellaria indicate evolution from the ancestral (feeding larva) state. Parental care has evolved many times from an ancestor that had a planktonic ophiopluteus or vitellaria and is often associated with hermaphroditism and paedomorphosis. A secondary reduction in egg size occurred in the viviparous species.

Juvenile waiting stage crown-of-thorns sea stars are resilient in heatwave conditions that bleach and kill corals.

The juveniles of predatory sea stars can remain in their recruitment-nursery habitat for some time before their ontogenetic shift to the adult habitat and diet. These small juveniles are vulnerable to a range of factors with their sensitivity amplified by climate change-driven ocean warming. We investigate the thermal tolerance of the waiting stage herbivorous juveniles of the keystone coral predator, the crown-of-thorns sea star (COTS, Acanthaster sp.), in context with the degree heating weeks (DHW) model that predicts coral bleaching and mass mortality. In temperature treatments ranging from +1 to 3°C in prolonged heatwave acclimation conditions, the juveniles exhibited ~100% survival in DHW scenarios that trigger coral bleaching (4 DHW), resulting in mass mortality of corals (8 DHW) and extreme conditions well beyond those that kill corals (12 DHW). This indicates that herbivorous juvenile COTS are far more resistant to heatwave conditions than the coral prey of the adults. The juveniles exhibited higher activity (righting) and metabolic rate after weeks in increased temperature. In separate acute temperature experiments, the upper thermal limit of the juveniles was 34-36°C. In a warming world, juvenile COTS residing in their coral rubble nursery habitat will benefit from an increase in the extent of this habitat due to coral mortality. The juveniles have potential for long-term persistence as herbivores as they wait for live coral to recover before becoming coral predators, thereby serving as a proximate source of COTS outbreaks on reefs already in a tenuous state due to climate change.

Evo-Devo in Ophiuroids: The Switch from Planktotrophy to Lecithotrophy in Ophionereis.

AbstractUnderstanding the evolution of development (evo-devo) in the Ophiuroidea and the pathways in the switch from a feeding to a nonfeeding larva is complicated by the variability in the phenotype of the metamorphic larva, being a reduced yolky ophiopluteus in some species (type I development) and a vitellaria larva in others (type II development). We investigated evo-devo in the family Ophionereididae, a group dominated by lecithotrophic development through a vitellaria larva. We reared the planktotrophic larvae of Ophionereis fasciata to settlement to determine the metamorphic phenotype. Counter to expectations, O. fasciata did not exhibit type II metamorphosis through a vitellaria, although it did exhibit transient vitellaria-like features. Resorption of the larval arms in the same interradial positions where the ciliary bands form in vitellariae gave them a fleeting vitellaria-like appearance. Development of O. fasciata exhibits heterochronic features in early formation of the skeletal primordium of the third pair (postoral) of larval arms and in the presettlement juvenile early appearance of the juvenile terminal arm plates on external view in parallel with larval arm resorption. Development of the fourth pair (posterodorsal) of larval arms, the last pair to be formed, is plastic, with 44% of larvae exhibiting partial arm growth. Heterochronic traits in development, as seen in O. fasciata, may have facilitated evolution of a lecithotrophic mode of development in Ophionereis. Comparison of the ophiopluteus of O. fasciata and the vestigial pluteus of O. schayeri provided insights into the simplification of larval form from the ancestral (feeding larva) state in Ophionereis. The diverse metamorphic phenotypes in ophiuroids indicate that type I and type II development may not be completely divergent lines of evo-devo and point to selective pressure in the pelagic-benthic transition in the evolution of ophiuroid development.

Evolutionary modification of gastrulation in Parvulastra exigua, an asterinid seastar with holobenthic lecithotrophic development.

Gastrulation is a fundamental morphogenetic process in development. In echinoderms with ancestral-type development through feeding larvae, gastrulation involves radially symmetrical invagination of cells around the blastopore. Gastrulation in the seastar Parvulastra exigua, a species with non-feeding larvae deviates from this pattern. Microinjection of cells with fluorescent lineage tracer dye revealed that early blastomeres contribute unequally to ectoderm and endoderm. In embryos injected at the two-cell stage, asymmetry was evident in the fluorescence at the top of the archenteron and animal pole ectoderm. Archenteron elongation is driven by asymmetrical involution of cells with more cells crossing the blastopore on one side. Lineages of cells injected at the four-cell stage also differed in allocation to endoderm and ectoderm. In embryos injected at the eight-cell stage ectodermal and endodermal fates were evident reflecting the animal and vegetal fates determined by third cleavage as typical of echinoderms. Modification of gastrulation associated with evolution of development in P. exigua shows that this foundational morphogenetic process can be altered despite its importance for subsequent development. However, observations of slight asymmetry in the lineage fates of blastomeres in asterinids with planktotrophic development indicates that gastrulation by asymmetrical involution in P. exigua may be a hypertrophic elaboration of a pre-existing state in ancestral-type development. As for echinoids with lecithotrophic development, involution as a mechanism to contribute to archenteron elongation may be associated with the impact of extensive maternal nutritive reserves on the mechanics of cell movement and a novel innovation to facilitate early development of the adult rudiment.

Unshelled abalone and corrupted urchins: development of marine calcifiers in a changing ocean.

The most fragile skeletons produced by benthic marine calcifiers are those that larvae and juveniles make to support their bodies. Ocean warming, acidification, decreased carbonate saturation and their interactive effects are likely to impair skeletogenesis. Failure to produce skeleton in a changing ocean has negative implications for a diversity of marine species. We examined the interactive effects of warming and acidification on an abalone (Haliotis coccoradiata) and a sea urchin (Heliocidaris erythrogramma) reared from fertilization in temperature and pH/pCO(2) treatments in a climatically and regionally relevant setting. Exposure of ectodermal (abalone) and mesodermal (echinoid) calcifying systems to warming (+2°C to 4°C) and acidification (pH 7.6-7.8) resulted in unshelled larvae and abnormal juveniles. Haliotis development was most sensitive with no interaction between stressors. For Heliocidaris, the percentage of normal juveniles decreased in response to both stressors, although a +2°C warming diminished the negative effect of low pH. The number of spines produced decreased with increasing acidification/pCO(2), and the interactive effect between stressors indicated that a +2°C warming reduced the negative effects of low pH. At +4°C, the developmental thermal tolerance was breached. Our results show that projected near-future climate change will have deleterious effects on development with differences in vulnerability in the two species.

Sea urchin fertilization in a warm, acidified and high pCO2 ocean across a range of sperm densities.

Marine invertebrate gametes are being spawned into an ocean simultaneously warming, acidifying and increasing in pCO(2). Decreased pH/increased pCO(2) narcotizes sperm indicating that acidification may impair fertilization, exacerbating problems of sperm limitation, with dire implications for marine life. In contrast, increased temperature may have a stimulatory effect, enhancing fertilization. We investigated effects of ocean change on sea urchin fertilization across a range of sperm densities. We address two predictions: (1) low pH/increased pCO(2) reduces fertilization at low sperm density and (2) increased temperature enhances fertilization, buffering negative effects of acidification and increased pCO(2). Neither prediction was supported. Fertilization was only affected by sperm density. Increased acidification and pCO(2) did not reduce fertilization even at low sperm density and increased temperature did not enhance fertilization. It is important to identify where vulnerabilities lie across life histories and our results indicate that sea urchin fertilization is robust to climate change stressors. However, developmental stages may be vulnerable to ocean change.

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.

Temperature, but not pH, compromises sea urchin fertilization and early development under near-future climate change scenarios.

Global warming is causing ocean warming and acidification. The distribution of Heliocidaris erythrogramma coincides with the eastern Australia climate change hot spot, where disproportionate warming makes marine biota particularly vulnerable to climate change. In keeping with near-future climate change scenarios, we determined the interactive effects of warming and acidification on fertilization and development of this echinoid. Experimental treatments (20-26 degrees C, pH 7.6-8.2) were tested in all combinations for the 'business-as-usual' scenario, with 20 degrees C/pH 8.2 being ambient. Percentage of fertilization was high (>89%) across all treatments. There was no difference in percentage of normal development in any pH treatment. In elevated temperature conditions, +4 degrees C reduced cleavage by 40 per cent and +6 degrees C by a further 20 per cent. Normal gastrulation fell below 4 per cent at +6 degrees C. At 26 degrees C, development was impaired. As the first study of interactive effects of temperature and pH on sea urchin development, we confirm the thermotolerance and pH resilience of fertilization and embryogenesis within predicted climate change scenarios, with negative effects at upper limits of ocean warming. Our findings place single stressor studies in context and emphasize the need for experiments that address ocean warming and acidification concurrently. Although ocean acidification research has focused on impaired calcification, embryos may not reach the skeletogenic stage in a warm ocean.

Development of the five primary podia from the coeloms of a sea star larva: homology with the echinoid echinoderms and other deuterostomes.

Confocal laser scanning microscopy of larvae of the asteroid Parvulastra exigua was used to investigate the development of the five primary podia from the coeloms in the echinoderm phylum in an approach to the problem of morphological homology in the deuterostome phyla. The development is shown from an early brachiolaria larval stage to a pre-settlement late brachiolaria larval stage. In the early brachiolaria larva, a single enterocoele connected to the archenteron has formed into two lateral coeloms and an anterior coelom. The primary podia form from the coelomic regions on the left side of the brachiolaria larva, while on the right the coelomic regions connect with the exterior through the pore canal and hydropore. The anterior coelom forms the coelom of the brachia. Homology between the primary podia of the asteroid and the echinoid classes of echinoderms is described and extended to coeloms of other deuterostome phyla.

Evolution of larval form in ophiuroids: insights from the metamorphic phenotype of Ophiothrix (Echinodermata: Ophiuroidea).

Comparison of development through metamorphosis in Ophiothrix species provided insights into the evolutionary relationships between Type I (ophiopluteus only) and Type II (ophiopluteus and vitellaria) patterns of development in the Ophiuroidea. As typical of Type I developers, the six inner larval arms in Ophiothrix spongicola were fully resorbed at metamorphosis and no remnants of ciliated epithelia were retained. The postero-lateral arms function as locomotory organs for the developing juvenile and were discarded at settlement. In contrast, in O. ciliaris the epithelia of the inner arms were transformed into ciliated ridges, similar to those seen in vitellariae and the postero-lateral arms were resorbed rather than being discarded. Larval arm resorption in O. ciliaris is similar to that in Type II developers. The metamorphic phenotype of O. ciliaris provides a link between Type I and II development. The presence of two types of metamorphosis in congeneric ophiuroids and the variable metamorphic phenotype of O. ciliaris was unexpected. It appears that closely related ophiuroids and individual species may have the capacity to metamorphose using either Type I or Type II pathways. Although the phylogenetic distribution of metamorphic phenotypes indicates that Type II development may be the ancestral state, comparative morphology suggests that a developmental dichotomy based on larval arm resorption may not be appropriate for the Ophiuroidea. Until metamorphosis is characterized for more taxa, the ancestral developmental mode for the Ophiuroidea will remain a matter of conjecture.