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With rising ocean temperatures, extreme weather events such as marine heatwaves (MHWs) are increasing in frequency and duration, pushing marine life beyond their physiological limits. The potential to respond to extreme conditions through physiological acclimatization, and pass on resistance to the next generation, fundamentally depends on the capacity of an organism to cope within their thermal tolerance limits. To elucidate whether heat conditioning of parents could benefit offspring development, we exposed adult sea urchins (Heliocidaris erythrogramma) to ambient summer (23°C), moderate (25°C) or strong (26°C) MHW conditions for 10 days. Offspring were then reared at constant temperature along a thermal gradient (22-28°C) and development was tracked to the 14-day juvenile stage. Progeny from the MHW-conditioned adults developed through to metamorphosis faster than those of ambient conditioned parents, with most individuals from the moderate and strong heatwaves developing to the larval stage across all temperatures. In contrast, the majority of offspring from the control summer temperature died before metamorphosis at temperatures above 25°C (moderate MHW). Juveniles produced from the strong MHW-conditioned adults were also larger across all temperatures, with the largest juveniles in the 26°C treatment. In contrast, the smallest juveniles were from control (current-day summer) parents (and reared at 22 and 25°C). Surprisingly, initial survival was higher in the progeny of MHW exposed parents, even at temperatures hotter than predicted MHWs (28°C). Importantly, however, there was substantial mortality of juveniles from the strong MHW parents by day 14. Therefore, while carryover effects of parental conditioning to MHWs resulted in faster growing, larger progeny, this benefit will only persist beyond the more sensitive juvenile stage and enhance survival if conditions return promptly to normal seasonal temperatures within current thermal tolerance limits.

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Kelps are ecosystem engineers, which collectively form forests that provide a variety of important ecosystem services for humans and other organisms. Kelp forests are threatened by multiple local and global stressors, one of the most notable is herbivory. Overabundant sea; urchins can consume kelp, leading to a phase shift from productive forests to unproductive; rocky barrens. Reducing sea urchin densities by directly removing them can reverse this; phase shift. However, maintaining low densities of sea urchins, is logistically and financially; challenging. Following a review of herbivore exclusion methods to date, we tested the efficacy of three different methods for excluding sea urchins from kelp in the laboratory: flexible fences; electricity; and copper anti-fouling paint. The results from the laboratory; experiment showed that flexible fencing was the most successful method for excluding sea urchins. To test the efficacy of this method in the field, sea urchins were removed from 1m2 patches in barrens and intact kelp beds, and the effectiveness of flexible fences of two different heights (30 cm and 60 cm) at excluding sea urchins were tested. The results from the field study demonstrated that flexible fences of both heights were effective at maintaining low sea urchin densities in barrens but not in intact kelp beds, relative to unmanipulated; rocky barrens. These findings suggest that flexible fencing could be an important tool in restoring kelp in barrens, however the costs of fencing are likely to place limits on the scale at which this management strategy can be implemented.

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Microinjection is a common embryological technique used for many types of experiments, including lineage tracing, manipulating gene expression, or genome editing. Injectable reagents include mRNA overexpression, mis-expression, or dominant-negative experiments to examine a gene of interest, a morpholino antisense oligo to prevent translation of an mRNA or spliceoform of interest and CRISPR-Cas9 reagents. Thus, the technique is broadly useful for basic embryological studies, constructing gene regulatory networks, and directly testing hypotheses about cis-regulatory and coding sequence changes underlying the evolution of development. However, the methods for microinjection in typical planktotrophic marine invertebrates may not work well in the highly modified eggs and embryos of lecithotrophic species. This protocol is optimized for the lecithotrophic sea urchin Heliocidaris erythrogramma.

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Aquaculture of higher trophic level species is increasingly dependent on the use of terrestrial oil products. The input of terrestrially derived n-6 polyunsaturated fatty acids (PUFA) into marine environments has subsequently increased, with unknown consequences for recipient species. We exposed a sea urchin, Heliocidaris erythrogramma to three experimental diets for 78 days: a high n-3 PUFA marine imitation treatment, a high n-6 PUFA "future aquafeed" treatment and an intermediate "current aquafeed" treatment. Female urchins fed the high n-6 PUFA diet produced larvae with lower survival rates than all other treatments. Males fed the high n-6 PUFA diet produced no viable sperm. Fatty acid composition in reproductive material revealed comprehensive biosynthetic and dietary sparing capabilities in H. erythrogramma. Despite this, the ratio of n-6 PUFA to n-3 PUFA in reproductive tissue increased significantly with diet. We suggest alterations to this ratio is the likely mechanism of negative impact on larval development.

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Body size and temperature are the major factors explaining metabolic rate, and the additional factor of pH is a major driver at the biochemical level. These three factors have frequently been found to interact, complicating the formulation of broad models predicting metabolic rates and hence ecological functioning. In this first study of the effects of warming and ocean acidification, and their potential interaction, on metabolic rate across a broad range in body size (two to three orders of magnitude difference in body mass), we addressed the impact of climate change on the sea urchin ITALIC! Heliocidaris erythrogrammain context with climate projections for southeast Australia, an ocean warming hotspot. Urchins were gradually introduced to two temperatures (18 and 23°C) and two pH levels (7.5 and 8.0), at which they were maintained for 2 months. Identical experimental trials separated by several weeks validated the fact that a new physiological steady state had been reached, otherwise known as acclimation. The relationship between body size, temperature and acidification on the metabolic rate of ITALIC! H. erythrogrammawas strikingly stable. Both stressors caused increases in metabolic rate: 20% for temperature and 19% for pH. Combined effects were additive: a 44% increase in metabolism. Body size had a highly stable relationship with metabolic rate regardless of temperature or pH. None of these diverse drivers of metabolism interacted or modulated the effects of the others, highlighting the partitioned nature of how each influences metabolic rate, and the importance of achieving a full acclimation state. Despite these increases in energetic demand there was very limited capacity for compensatory modulating of feeding rate; food consumption increased only in the very smallest specimens, and only in response to temperature, and not pH. Our data show that warming, acidification and body size all substantially affect metabolism and are highly consistent and partitioned in their effects, and for ITALIC! H. erythrogramma, near-future climate change will incur a substantial energetic cost.

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Understanding the unusual radial body plan of echinoderms and its relationship to the bilateral plan of other deuterostomes remains a challenge. The molecular processes of embryonic and early larval development in sea urchins are well characterised, but those giving rise to the adult and its radial body remain poorly studied. We used the developmental transcriptome generated for Heliocidaris erythrogramma, a species that forms the juvenile soon after gastrulation, to investigate changes in gene expression underlying radial body development. As coelomogenesis is key to the development of pentamery and juvenile formation on the left side of the larva, we focussed on genes associated with the nodal and BMP2/4 network that pattern this asymmetry. We identified 46 genes associated with this Nodal and BMP2/4 signalling network, and determined their expression profiles from the gastrula, through to rudiment development, metamorphosis and the fully formed juvenile. Genes associated with Nodal signalling shared similar expression profiles, indicating that they may have a regulatory relationship in patterning morphogenesis of the juvenile sea urchin. Similarly, many genes associated with BMP2/4 signalling had similar expression profiles through juvenile development. Further examination of the roles of Nodal- and BMP2/4-associated genes is required to determine function and whether the gene expression profiles seen in H. erythrogramma are due to ongoing activity of gene networks established during early development, or to redeployment of regulatory cassettes to pattern the adult radial body plan.

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Polyandry (female multiple mating) has profound evolutionary and ecological implications. Despite considerable work devoted to understanding why females mate multiply, we currently lack convincing empirical evidence to explain the adaptive value of polyandry. Here, we provide a direct test of the controversial idea that bet-hedging functions as a risk-spreading strategy that yields multi-generational fitness benefits to polyandrous females. Unfortunately, testing this hypothesis is far from trivial, and the empirical comparison of the across-generations fitness payoffs of a polyandrous (bet hedger) versus a monandrous (non-bet hedger) strategy has never been accomplished because of numerous experimental constraints presented by most 'model' species. In this study, we take advantage of the extraordinary tractability and versatility of a marine broadcast spawning invertebrate to overcome these challenges. We are able to simulate multi-generational (geometric mean) fitness among individual females assigned simultaneously to a polyandrous and monandrous mating strategy. Our approaches, which separate and account for the effects of sexual selection and pure bet-hedging scenarios, reveal that bet-hedging, in addition to sexual selection, can enhance evolutionary fitness in multiply mated females. In addition to offering a tractable experimental approach for addressing bet-hedging theory, our study provides key insights into the evolutionary ecology of sexual interactions.

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We apply qPCR molecular techniques to detect in situ rates of consumption of sea urchins (Centrostephanus rodgersii and Heliocidaris erythrogramma) by rock lobsters (Jasus edwardsii). A non-lethal method was used to source faecal samples from trap-caught lobsters over 2 years within two no-take research reserves. There was high variability in the proportion of lobsters with faeces positive for sea urchin DNA across years and seasons dependent on lobster size. Independent estimates of lobster predation rate on sea urchins (determined from observed declines in urchin abundances in the reserves relative to control sites) suggest that rates of molecular prey detection generally overestimated predation rates. Also, small lobsters known to be incapable of directly predating emergent sea urchins showed relatively high rates of positive tests. These results indicate that some lobsters ingest non-predatory sources of sea urchin DNA, which may include (i) ingestion of C. rodgersii DNA from the benthos (urchin DNA is detectable in sediments and some lobsters yield urchin DNA in faeces when fed urchin faeces or sediment); (ii) scavenging; and/or predation by rock lobsters on small pre-emergent urchins that live cryptically within the reef matrix (although this possibility could not be assessed). While the DNA-based approach and direct monitoring of urchin populations both indicate high predation rates of large lobsters on emergent urchins, the study shows that in some cases absolute predation rates and inferences of predator-prey interactions cannot be reliably estimated from molecular signals obtained from the faeces of benthic predators. At a broad semi-quantitative level, the approach is useful to identify relative magnitudes of predation and temporal and spatial variability in predation.

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This study documents evolutionary modifications in mechanisms of gastrulation in Heliocidaris erythrogramma, an echinoid with lecithotrophic larvae. Radially symmetrical cell rearrangements and changes in cell shape drive elongation of the archenteron in the ancestral mode of echinoid gastrulation. Cell marking experiments indicate that in H. erythrogramma, however, prolonged movement of cells over the ventral lip of the blastopore accompanies extension of the archenteron. Evolutionary modifications to archenteron extension in H. erythrogramma thus include utilization of a different type of cellular movement as well as the imposition of dorsoventral asymmetry in cellular movements. The conservation of gastrulation mechanisms among phylogenetically divergent echinoids with planktotrophic development suggests that the plesiomorphic condition has persisted at least 250 million years and perhaps much longer. Yet H. erythrogramma diverged from an ancestor with planktotrophic development only about 10 mya, indicating that morphogenetic mechanisms of early development can undergo substantial evolutionary changes, even after long periods of stasis.