Surviving in an Acidifying Ocean: Acid-Base Physiology and Energetics of the Sea Urchin Larva.

The sea urchin larva has been used by biologists for more than a century to study the development and evolution of animals. Surprisingly, very little information has been generated regarding the physiology of this small planktonic organism. However, in the context of anthropogenic CO2-driven ocean acidification (OA), the membrane transport physiology and energetics of this marine model organism have received considerable attention in the past decade. This has led to the discovery of new, exciting physiological systems, including a highly alkaline digestive tract and the calcifying primary mesenchyme cells that generate the larval skeleton. These physiological systems directly relate to the energetics of the organisms when challenged by OA. Here we review the latest membrane transport physiology and energetics in the sea urchin larva, we identify emerging questions, and we point to important future directions in the field of marine physiology in times of rapid climate change.

An early global role for Axin is required for correct patterning of the anterior-posterior axis in the sea urchin embryo.

Activation of Wnt/ß-catenin (cWnt) signaling at the future posterior end of early bilaterian embryos is a highly conserved mechanism for establishing the anterior-posterior (AP) axis. Moreover, inhibition of cWnt at the anterior end is required for development of anterior structures in many deuterostome taxa. This phenomenon, which occurs around the time of gastrulation, has been fairly well characterized, but the significance of intracellular inhibition of cWnt signaling in cleavage-stage deuterostome embryos for normal AP patterning is less well understood. To investigate this process in an invertebrate deuterostome, we defined Axin function in early sea urchin embryos. Axin is ubiquitously expressed at relatively high levels in early embryos and functional analysis revealed that Axin suppresses posterior cell fates in anterior blastomeres by blocking ectopic cWnt activation in these cells. Structure-function analysis of sea urchin Axin demonstrated that only its GSK-3ß-binding domain is required for cWnt inhibition. These observations and results in other deuterostomes suggest that Axin plays a crucial conserved role in embryonic AP patterning by preventing cWnt activation in multipotent early blastomeres, thus protecting them from assuming ectopic cell fates.

An otopetrin family proton channel promotes cellular acid efflux critical for biomineralization in a marine calcifier.

Otopetrins comprise a family of proton-selective channels that are critically important for the mineralization of otoliths and statoconia in vertebrates but whose underlying cellular mechanisms remain largely unknown. Here, we demonstrate that otopetrins are critically involved in the calcification process by providing an exit route for protons liberated by the formation of CaCO3 Using the sea urchin larva, we examined the otopetrin ortholog otop2l, which is exclusively expressed in the calcifying primary mesenchymal cells (PMCs) that generate the calcitic larval skeleton. otop2l expression is stimulated during skeletogenesis, and knockdown of otop2l impairs spicule formation. Intracellular pH measurements demonstrated Zn2+-sensitive H+ fluxes in PMCs that regulate intracellular pH in a Na+/HCO3--independent manner, while Otop2l knockdown reduced membrane proton permeability. Furthermore, Otop2l displays unique features, including strong activation by high extracellular pH (>8.0) and check-valve-like outwardly rectifying H+ flux properties, making it into a cellular proton extrusion machine adapted to oceanic living conditions. Our results provide evidence that otopetrin family proton channels are a central component of the cellular pH regulatory machinery in biomineralizing cells. Their ubiquitous occurrence in calcifying systems across the animal kingdom suggest a conserved physiological function by mediating pH at the site of mineralization. This important role of otopetrin family proton channels has strong implications for our view on the cellular mechanisms of biomineralization and their response to changes in oceanic pH.

Has the concept of polyspermy prevention been invented in the laboratory?

There is no evidence, nor need, for a fast block to polyspermy in animal oocytes. The idea that oocytes have evolved a mechanism to allow the entry of one spermatozoon and repel all others has, however, gained consensus over the last century. The main culprit is the sea urchin, which has been used for over a century in in vitro studies of the fertilization process. Images of sea urchin oocytes with thousands of sperm attached to the surface are commonplace in textbooks and appeal to the nature of the reader implying an intriguing surface mechanism of sperm selection despite these oocytes being fixed for photography (Figure ). The abundance of gametes in this marine invertebrate and the ease of experimentation have given us the possibility to elucidate many aspects of the mechanism of fertilization, but has also led to ongoing controversies in reproductive biology, one being polyspermy prevention. Kinetic experiments by Rothschild and colleagues in the 1950s led to the hypothesis of a fast partial block to polyspermy in sea urchin oocytes that reduced the probability of a second spermatozoon from entering the oocyte by 1/20th. In the 1970s, Jaffe and colleagues suggested, with circumstantial evidence, that this partial block was due to the sperm-induced depolarization of the oocyte plasma membrane. However, the fate of supernumerary spermatozoa is determined well before the plasma membrane of the oocyte depolarizes. Transmembrane voltage does not serve to regulate sperm entry. Scholastic texts have inadvertently promulgated this concept across the animal kingdom with no logical correlation or experimentation and, as of today, a molecular mechanism to regulate sperm entry in oocytes has not been identified.

Sunflower sea star predation on urchins can facilitate kelp forest recovery.

The recent collapse of predatory sunflower sea stars (Pycnopodia helianthoides) owing to sea star wasting disease (SSWD) is hypothesized to have contributed to proliferation of sea urchin barrens and losses of kelp forests on the North American west coast. We used experiments and a model to test whether restored Pycnopodia populations may help recover kelp forests through their consumption of nutritionally poor purple sea urchins (Strongylocentrotus purpuratus) typical of barrens. Pycnopodia consumed 0.68 S. purpuratus d-1, and our model and sensitivity analysis shows that the magnitude of recent Pycnopodia declines is consistent with urchin proliferation after modest sea urchin recruitment, and even small Pycnopodia recoveries could generally lead to lower densities of sea urchins that are consistent with kelp-urchin coexistence. Pycnopodia seem unable to chemically distinguish starved from fed urchins and indeed have higher predation rates on starved urchins owing to shorter handling times. These results highlight the importance of Pycnopodia in regulating purple sea urchin populations and maintaining healthy kelp forests through top-down control. The recovery of this important predator to densities commonly found prior to SSWD, whether through natural means or human-assisted reintroductions, may therefore be a key step in kelp forest restoration at ecologically significant scales.

Alternations in the foraging behaviour of a primary consumer drive patch transition dynamics in a temperate rocky reef ecosystem.

Understanding the role of animal behaviour in linking individuals to ecosystems is central to advancing knowledge surrounding community structure, stability and transition dynamics. Using 22 years of long-term subtidal monitoring, we show that an abrupt outbreak of purple sea urchins (Strongylocentrotus purpuratus), which occurred in 2014 in southern Monterey Bay, California, USA, was primarily driven by a behavioural shift, not by a demographic response (i.e. survival or recruitment). We then tracked the foraging behaviour of sea urchins for 3 years following the 2014 outbreak and found that behaviour is strongly associated with patch state (forest or barren) transition dynamics. Finally, in 2019, we observed a remarkable recovery of kelp forests at a deep rocky reef. We show that this recovery was associated with sea urchin movement from the deep reef to shallow water. These results demonstrate how changes in grazer behaviour can facilitate patch dynamics and dramatically restructure communities and ecosystems.

Staying in place and moving in space: Contrasting larval thermal sensitivity explains distributional changes of sympatric sea urchin species to habitat warming.

For marine ectotherms, larval success, planktonic larval duration and dispersal trajectories are strongly influenced by temperature, and therefore, ocean warming and heatwaves have profound impacts on these sensitive stages. Warming, through increased poleward flow in regions with western boundary currents, such as the East Australia Current (EAC), provides opportunities for range extension as propagules track preferred conditions. Two sea urchin species, Centrostephanus rodgersii and Heliocidaris tuberculata, sympatric in the EAC warming hotspot, exhibit contrasting responses to warming. Over half a century, C. rodgersii has undergone marked poleward range extension, but the range of H. tuberculata has not changed. We constructed thermal performance curves (TPC) to determine if contrasting developmental thermal tolerance can explain this difference. The temperatures tested encompassed present-day distribution and forecast ocean warming/heatwave conditions. The broad and narrow thermal optimum (Topt) ranges for C. rodgersii and H. tuberculata larvae (7.2 and 4.7°C range, respectively) matched their realized (adult distribution) thermal niches. The cool and warm temperatures for 50% development to the feeding larva approximated temperatures at adult poleward range limits. Larval cool tolerances with respect to mean local temperature differed, 6.0 and 3.8°C respectively. Larval warm tolerances were similar for both species as are the adult warm range edges. The larvae of both species would be sensitive to heatwaves. Centrostephanus rodgersii has stayed in place and shifted in space, likely due to its broad cold-warm larval thermal tolerance and large thermal safety margins. Phenotypic plasticity of the planktonic stage of C. rodgersii facilitated its range extension. In contrast, larval cold intolerance of H. tuberculata explains its restricted range and will delay poleward extension as the region warms. In a warming ocean, we show that intrinsic thermal biology traits of the pelagic stage provide an integrative tool to explain species-specific variation in range shift patterns.

Plasticity in fluctuating hydrodynamic conditions: tube foot regeneration in sea urchins.

Regenerating structures critical for survival provide excellent model systems for the study of phenotypic plasticity. These body components must regenerate their morphology and functionality quickly while subjected to different environmental stressors. Sea urchins live in high-energy environments where hydrodynamic conditions pose significant challenges. Adhesive tube feet provide secure attachment to the substratum but can be amputated by predation and hydrodynamic forces. Tube feet display functional and morphological plasticity in response to environmental conditions, but regeneration to their pre-amputation status has not been achieved under quiescent laboratory settings. In this study, we assessed the effect of turbulent water movement, periodic emersion and quiescent conditions on the regeneration process of tube foot morphology (length, disc area) and functionality (maximum disc tenacity, stem breaking force). Disc area showed significant plasticity in response to the treatments; when exposed to emersion and turbulent water movement, disc area was larger than that of tube feet regenerated in quiescent conditions. However, no treatment stimulated regeneration to pre-amputation sizes. Tube foot length was unaffected by treatments and remained shorter than non-amputated tube feet. Stem breaking force for amputated and non-amputated treatments increased in all cases when compared with pre-amputation values. Maximum tenacity (force per unit area) was similar among tube feet subjected to simulated field conditions and amputation treatments. Our results suggest a role of active plasticity of tube foot functional morphology in response to field-like conditions and demonstrate the plastic response of invertebrates to laboratory conditions.

Ocean acidification impacts sperm swimming performance and pHi in the New Zealand sea urchin Evechinus chloroticus.

In sea urchins, spermatozoa are stored in the gonads in hypercapnic conditions (pH<7.0). During spawning, sperm are diluted in seawater of pH>8.0, and there is an alkalinization of the sperm's internal pH (pHi) through the release of CO2 and H+. Previous research has shown that when pHi is above 7.2-7.3, the dynein ATPase flagellar motors are activated, and the sperm become motile. It has been hypothesized that ocean acidification (OA), which decreases the pH of seawater, may have a narcotic effect on sea urchin sperm by impairing the ability to regulate pHi, resulting in decreased motility and swimming speed. Here, we used data collected from the same individuals to test the relationship between pHi and sperm motility/performance in the New Zealand sea urchin Evechinus chloroticus under near-future (2100) and far-future (2150) atmospheric PCO2 conditions (RCP 8.5: pH 7.77, 7.51). Decreasing seawater pH significantly negatively impacted the proportion of motile sperm, and four of the six computer-assisted sperm analysis (CASA) sperm performance measures. In control conditions, sperm had an activated pHi of 7.52. Evechinus chloroticus sperm could not defend pHi in future OA conditions; there was a stepped decrease in the pHi at pH 7.77, with no significant difference in mean pHi between pH 7.77 and 7.51. Paired measurements in the same males showed a positive relationship between pHi and sperm motility, but with a significant difference in the response between males. Differences in motility and sperm performance in OA conditions may impact fertilization success in a future ocean.

Calcium-vesicles perform active diffusion in the sea urchin embryo during larval biomineralization.

Biomineralization is the process by which organisms use minerals to harden their tissues and provide them with physical support. Biomineralizing cells concentrate the mineral in vesicles that they secret into a dedicated compartment where crystallization occurs. The dynamics of vesicle motion and the molecular mechanisms that control it, are not well understood. Sea urchin larval skeletogenesis provides an excellent platform for investigating the kinetics of mineral-bearing vesicles. Here we used lattice light-sheet microscopy to study the three-dimensional (3D) dynamics of calcium-bearing vesicles in the cells of normal sea urchin embryos and of embryos where skeletogenesis is blocked through the inhibition of Vascular Endothelial Growth Factor Receptor (VEGFR). We developed computational tools for displaying 3D-volumetric movies and for automatically quantifying vesicle dynamics. Our findings imply that calcium vesicles perform an active diffusion motion in both, calcifying (skeletogenic) and non-calcifying (ectodermal) cells of the embryo. The diffusion coefficient and vesicle speed are larger in the mesenchymal skeletogenic cells compared to the epithelial ectodermal cells. These differences are possibly due to the distinct mechanical properties of the two tissues, demonstrated by the enhanced f-actin accumulation and myosinII activity in the ectodermal cells compared to the skeletogenic cells. Vesicle motion is not directed toward the biomineralization compartment, but the vesicles slow down when they approach it, and probably bind for mineral deposition. VEGFR inhibition leads to an increase of vesicle volume but hardly changes vesicle kinetics and doesn't affect f-actin accumulation and myosinII activity. Thus, calcium vesicles perform an active diffusion motion in the cells of the sea urchin embryo, with diffusion length and speed that inversely correlate with the strength of the actomyosin network. Overall, our studies provide an unprecedented view of calcium vesicle 3D-dynamics and point toward cytoskeleton remodeling as an important effector of the motion of mineral-bearing vesicles.

Conspecific cues, not starvation, mediate barren urchin response to predation risk.

Prey state and prey density mediate antipredator responses that can shift community structure and alter ecosystem processes. For example, well-nourished prey at low densities (i.e., prey with higher per capita predation risk) should respond strongly to predators. Although prey state and density often co-vary across habitats, it is unclear if prey responses to predator cues are habitat-specific. We used mesocosms to compare the habitat-specific responses of purple sea urchins (Strongylocentrotus purpuratus) to waterborne cues from predatory lobsters (Panulirus interruptus). We predicted that urchins from kelp forests (i.e., in well-nourished condition) tested at low densities typically observed in this habitat would respond more strongly to predation risk than barren urchins (i.e., in less nourished condition) tested at high densities typically observed in this habitat. Indeed, when tested at densities associated with respective habitats, urchins from forests, but not barrens, reduced kelp grazing by 69% when exposed to lobster risk cues. Barren urchins that were unresponsive to predator cues at natural, high densities suddenly responded strongly to lobster cues when conspecific densities were reduced. Strong responses of low densities of barren urchins persisted across feeding history (i.e. 0-64 days of starvation). This suggests that barren urchins can respond to predators but typically do not because of high conspecific densities. Because high densities of urchins in barrens should weaken the non-consumptive effects of lobsters, urchins in these habitats may continue to graze in the presence of predators thereby providing a feedback that maintains urchin barrens.

Reference Genome of the California Sheephead, Semicossyphus pulcher (Labridae, Perciformes), A Keystone Fish Predator in Kelp Forest Ecosystems.

Keystone species are known to play a critical role in kelp forest health, including the well-known killer whales, sea otter, sea urchin, kelp trophic cascade in the Aleutian Islands, Alaska, USA. In California, a major player in the regulation of sea urchin abundance, and in turn, the health of kelp forests ecosystems, is a large wrasse, the California Sheephead, Semicossyphus pulcher. We present a reference genome for this ecologically important species that will serve as a key resource for future conservation research of California's inshore marine environment utilizing genomic tools to address changes in life-history traits, dispersal, range shifts, and ecological interactions among members of the kelp forest ecological assemblages. Our genome assembly of S. pulcher has a total length of 0.794 Gb, which is similar to many other marine fishes. The assembly is largely contiguous (N50 = 31.9 Mb) and nearly complete (BUSCO single-copy core gene content = 98.1%). Within the context of the California Conservation Genomics Project (CCGP), the genome of S. pulcher will be used as an important reference resource for ongoing whole genome resequencing efforts of the species.

Evolution of nitric oxide regulation of gut function.

Although morphologies are diverse, the common pattern in bilaterians is for passage of food in the gut to be controlled by nerves and endodermally derived neuron-like cells. In vertebrates, nitric oxide (NO) derived from enteric nerves controls relaxation of the pyloric sphincter. Here, we show that in the larvae of sea urchins, there are endoderm-derived neuronal nitric oxide synthase (nNOS)-positive cells expressing pan-neural marker, Synaptotagmin-B (SynB), in sphincters and that NO regulates the relaxation of the pyloric sphincter. Our results indicate that NO-dependent pylorus regulation is a shared feature within the deuterostomes, and we speculate that it was a characteristic of stem deuterostomes.

Trophic control of cryptic coralline algal diversity.

Understanding how trophic dynamics drive variation in biodiversity is essential for predicting the outcomes of trophic downgrading across the world's ecosystems. However, assessing the biodiversity of morphologically cryptic lineages can be problematic, yet may be crucial to understanding ecological patterns. Shifts in keystone predation that favor increases in herbivore abundance tend to have negative consequences for the biodiversity of primary producers. However, in nearshore ecosystems, coralline algal cover increases when herbivory is intense, suggesting that corallines may uniquely benefit from trophic downgrading. Because many coralline algal species are morphologically cryptic and their diversity has been globally underestimated, increasing the resolution at which we distinguish species could dramatically alter our conclusions about the consequences of trophic dynamics for this group. In this study, we used DNA barcoding to compare the diversity and composition of cryptic coralline algal assemblages at sites that differ in urchin biomass and keystone predation by sea otters. We show that while coralline cover is greater in urchin-dominated sites (or "barrens"), which are subject to intense grazing, coralline assemblages in these urchin barrens are significantly less diverse than in kelp forests and are dominated by only 1 or 2 species. These findings clarify how food web structure relates to coralline community composition and reconcile patterns of total coralline cover with the widely documented pattern that keystone predation promotes biodiversity. Shifts in coralline diversity and distribution associated with transitions from kelp forests to urchin barrens could have ecosystem-level effects that would be missed by ignoring cryptic species' identities.

Gross and microscopic pathology of West Indian sea eggs (Tripneustes ventricosus).

In this study, we performed comprehensive pathology examinations on 83 Tripneustes ventricosus from 11 locations on St. Kitts to build baseline data necessary for disease diagnosis in this species. Gross abnormalities were observed in 23/83 (28%) urchins and included spine loss, visceral hyperpigmentation, test discoloration, and test ulceration. Ciliates were the only protists identified in this study via examination of tissue wet mounts and histology, documented in 50/83 (60%) urchins. Microscopic observations associated with visibly abnormal status included muscle necrosis, test and appendage inflammation, appendage (tube feet, spines, and pedicellariae) degeneration, severe coelomocytosis, and generalized hypermelanosis. Enterocyte intranuclear inclusion bodies, microbial aggregates, nerve pigmentation, enteric pigmentation, integument-associated crustaceans, and encysted metazoan parasites were of uncertain pathological significance. The etiology for any lesion was not microscopically apparent, contrasting literature implicating common marine bacteria in urchin diseases. This study highlights the importance of histopathology in urchin disease investigations and facilitates the recognition of disease in T. ventricosus.

Involvement of Huntingtin in Development and Ciliary Beating Regulation of Larvae of the Sea Urchin, Hemicentrotus pulcherrimus.

The multiple functions of the wild type Huntington's disease protein of the sea urchin Hemicentrotus pulcherrimus (Hp-Htt) have been examined using the anti-Hp-Htt antibody (Ab) raised against synthetic oligopeptides. According to immunoblotting, Hp-Htt was detected as a single band at around the 350 kDa region at the swimming blastula stage to the prism larva stage. From the 2-arm pluteus stage (2aPL), however, an additional smaller band at the 165 kDa region appeared. Immunohistochemically, Hp-Htt was detected in the nuclei and the nearby cytoplasm of the ectodermal cells from the swimming blastula stage, and the blastocoelar cells from the mid-gastrula stage. The Ab-positive signal was converged to the ciliary band-associated strand (CBAS). There, it was accompanied by several CBAS-marker proteins in the cytoplasm, such as glutamate decarboxylase. Application of Hp-Htt morpholino (Hp-Htt-MO) has resulted in shortened larval arms, accompanied by decreased 5-bromo-2-deoxyuridin (BrdU) incorporation by the ectodermal cells of the larval arms. Hp-Htt-MO also resulted in lowered ciliary beating activity, accompanied by a disordered swirling pattern formation around the body. These Hp-Htt-MO-induced deficiencies took place after the onset of CBAS system formation at the larval arms. Thus, Hp-Htt is involved in cell proliferation and the ciliary beating pattern regulation signaling system in pluteus larvae.

Cellular bicarbonate accumulation and vesicular proton transport promote calcification in the sea urchin larva.

The sea urchin embryo develops a calcitic endoskeleton through intracellular formation of amorphous calcium carbonate (ACC). Intracellular precipitation of ACC, requires [Formula: see text] concentrating as well as proton export mechanisms to promote calcification. These processes are of fundamental importance in biological mineralization, but remain largely unexplored. Here, we demonstrate that the calcifying primary mesenchyme cells (PMCs) use Na+/H+-exchange (NHE) mechanisms to control cellular pH homeostasis during maintenance of the skeleton. During skeleton re-calcification, pHi of PMCs is increased accompanied by substantial elevation in intracellular [Formula: see text] mediated by the [Formula: see text] cotransporter Sp_Slc4a10. However, PMCs lower their pHi regulatory capacities associated with a reduction in NHE activity. Live-cell imaging using green fluorescent protein reporter constructs in combination with intravesicular pH measurements demonstrated alkaline and acidic populations of vesicles in PMCs and extensive trafficking of large V-type H+-ATPase (VHA)-rich acidic vesicles in blastocoelar filopodial cells. Pharmacological and gene expression analyses underline a central role of the VHA isoforms Sp_ATP6V0a1, Sp_ATP6V01_1 and Sp_ATPa1-4 for the process of skeleton re-calcification. These results highlight novel pH regulatory strategies in calcifying cells of a marine species with important implications for our understanding of the mineralization process in times of rapid changes in oceanic pH.

Effect of acclimation on thermal limits and hsp70 gene expression of the New Zealand sea urchin Evechinus chloroticus.

Seawater temperature is projected to increase globally due to climate change, affecting physiological responses, fitness and survival of marine organisms. Thermal tolerance studies are critical to determine the ability of animals to adapt to future environmental conditions. In this study, we aimed to determine if the thermal limits of the New Zealand Evechinus chloroticus would shift with animal's thermal history. We tested the effect of six thermal regimes on the righting ability, temperature of loss of righting (TLOR), median lethal temperature (LT50), lethal temperature (LT) and the gene expression of the heat shock protein 70 (hsp70) of the New Zealand sea urchin E. chloroticus when exposed to a thermal shock of 1 °C day-1 (duration of 7-16 days depending on the treatment). Treatments consisted of laboratory acclimation for one and four weeks to 18 °C and 24 °C (mean winter (15 °C) and summer temperature (21 °C) + 3 °C of warming, respectively), compared to non-acclimated sea urchins collected during winter (14.6 °C) and summer seasons (20.4 °C). Thermal history did not have a significant effect on the righting ability of E. chloroticus (TLOR ranged between 28 and 29 °C for all treatments) and LT50 (ranged between 29 and 30 °C for all treatments). However, LT of E. chloroticus collected during winter season was significantly lower than animals acclimated for one week at 18 °C. Maximum expression of hsp70 mRNA (Tmax) was observed at around 27-28 °C regardless of treatment; however, relative hsp70 mRNA levels were significantly higher in animals acclimated for four weeks at 24 °C. Despite proving to be a thermotolerant species with LTs around 30 °C, E. chloroticus was unable to increase thermal tolerance and Tmax when acclimated to high temperatures, suggesting that E. chloroticus may have a limited adaptive capacity to modify its phenotype; however, evolutionary adaptations may allow E. chloroticus to adapt to future ocean temperatures.

A comparative analysis of egg provisioning using mass spectrometry during rapid life history evolution in sea urchins.

A dramatic life history switch that has evolved numerous times in marine invertebrates is the transition from planktotrophic (feeding) to lecithotrophic (nonfeeding) larval development-an evolutionary tradeoff with many important developmental and ecological consequences. To attain a more comprehensive understanding of the molecular basis for this switch, we performed untargeted lipidomic and proteomic liquid chromatography-tandem mass spectrometry on eggs and larvae from three sea urchin species: the lecithotroph Heliocidaris erythrogramma, the closely related planktotroph Heliocidaris tuberculata, and the distantly related planktotroph Lytechinus variegatus. We identify numerous molecular-level changes possibly associated with the evolution of lecithotrophy in H. erythrogramma. We find the massive lipid stores of H. erythrogramma eggs are largely composed of low-density, diacylglycerol ether lipids that, contrary to expectations, appear to support postmetamorphic development and survivorship. Rapid premetamorphic development in this species may instead be powered by upregulated carbohydrate metabolism or triacylglycerol metabolism. We also find proteins involved in oxidative stress regulation are upregulated in H. erythrogramma eggs, and apoB-like lipid transfer proteins may be important for echinoid oogenic nutrient provisioning. These results demonstrate how mass spectrometry can enrich our understanding of life history evolution and organismal diversity by identifying specific molecules associated with distinct life history strategies and prompt new hypotheses about how and why these adaptations evolve.

Sea urchin reproductive performance in a changing ocean: poor males improve while good males worsen in response to ocean acidification.

Ocean acidification (OA) is predicted to be a major driver of ocean biodiversity change. At projected rates of change, sensitive marine taxa may not have time to adapt. Their persistence may depend on pre-existing inter-individual variability. We investigated individual male reproductive performance under present-day and OA conditions using two representative broadcast spawners, the sea urchins Lytechinus pictus and Heliocidaris erythrogramma. Under the non-competitive individual ejaculate scenario, we examined sperm functional parameters (e.g. swimming speed, motility) and their relationship with fertilization success under current and near-future OA conditions. Significant inter-individual differences in almost every parameter measured were identified. Importantly, we observed strong inverse relationships between individual fertilization success rate under current conditions and change in fertilization success under OA. Individuals with a high fertilization success under current conditions had reduced fertilization under OA, while individuals with a low fertilization success under current conditions improved. Change in fertilization success ranged from -67% to +114% across individuals. Our results demonstrate that while average population fertilization rates remain similar under OA and present-day conditions, the contribution by different males to the population significantly shifts, with implications for how selection will operate in a future ocean.