Energy is required to maintain physiological homeostasis in response to environmental change. Although responses to environmental stressors frequently are assumed to involve high metabolic costs, the biochemical bases of actual energy demands are rarely quantified. We studied the impact of a near-future scenario of ocean acidification [800 μatm partial pressure of CO 2 (pCO 2 )] during the development and growth of an important model organism in developmental and environmental biology, the sea urchin Strongylocentrotus purpuratus. Size, metabolic rate, biochemical content, and gene expression were not different in larvae growing under control and seawater acidification treatments. Measurements limited to those levels of biological analysis did not reveal the biochemical mechanisms of response to ocean acidification that occurred at the cellular level. In vivo rates of protein synthesis and ion transport increased ∼50% under acidification. Importantly, the in vivo physiological increases in ion transport were not predicted from total enzyme activity or gene expression. Under acidification, the increased rates of protein synthesis and ion transport that were sustained in growing larvae collectively accounted for the majority of available ATP (84%). In contrast, embryos and prefeeding and unfed larvae in control treatments allocated on average only 40% of ATP to these same two processes. Understanding the biochemical strategies for accommodating increases in metabolic energy demand and their biological limitations can serve as a quantitative basis for assessing sublethal effects of global change. Variation in the ability to allocate ATP differentially among essential functions may be a key basis of resilience to ocean acidification and other compounding environmental stressors.ocean acidification | sea urchin | energetics | metabolic allocation | development

Hydrothermal vents are ephemeral because of frequent volcanic and tectonic activities associated with crust formation. Although the larvae of hydrothermal vent fauna can rapidly colonize new vent sites separated by tens to hundreds of kilometres, the mechanisms by which these larvae disperse and recruit are not understood. Here we integrate physiological, developmental and hydrodynamic data to estimate the dispersal potential of larvae of the giant tubeworm Riftia pachyptila. At in situ temperatures and pressures (2 degrees C and 250 atm), we estimate that the metabolic lifespan for a larva of R. pachyptila averages 38 days. In the measured flow regime at a fast-spreading ridge axis (9 degrees 50' N; East Pacific Rise), this lifespan results in potential along-ridge dispersal distances that rarely exceed 100 km. This limited dispersal results not from the physiological performance of the embryos and larvae, but instead from transport limitations imposed by periodic reversals in along-ridge flows and sustained episodes of across-ridge flow. The lifespan presented for these larvae can now be used to predict dispersal under current regimes at other hydrothermal vent sites.

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Compared with understanding of biological shape and form, knowledge is sparse regarding what regulates growth and body size of a species. For example, the genetic and physiological causes of heterosis (hybrid vigor) have remained elusive for nearly a century. Here, we investigate gene-expression patterns underlying growth heterosis in the Pacific oyster (Crassostrea gigas) in two partially inbred (f ‫؍‬ 0.375) and two hybrid larval populations produced by a reciprocal cross between the two inbred families. We cloned cDNA and generated 4.5 M sequence tags with massively parallel signature sequencing. The sequences contain 23,274 distinct signatures that are expressed at statistically nonzero levels and show a highly positively skewed distribution with median and modal counts of 9.25 million and 3 transcripts per million, respectively. For nearly half of these signatures, expression level depends on genotype and is predominantly nonadditive (hybrids deviate from the inbred average). Statistical contrasts suggest Ϸ350 candidate genes for growth heterosis that exhibit concordant nonadditive expression in reciprocal hybrids; this represents only Ϸ1.5% of the >20,000 transcripts. Patterns of gene expression, which include dominance for low expression and even underdominance of expression, are more complex than predicted from classical dominant or overdominant explanations of heterosis. Preliminary identification of ribosomal proteins among candidate genes supports the suggestion from previous studies that efficiency of protein metabolism plays a role in growth heterosis.MPSS ͉ nonadditive expression ͉ factorial cross of partially inbred lines ͉ potence ͉ protein metabolism W hole-genome sequencing has yielded rich insights into the number of genes required to make complex eukaryotic animals (1-4). Surprisingly few genes, however, can effect major changes in body design and shape. For example, elaboration and mutation of a fairly small number of developmentally important regulatory genes, such as the Hox gene cluster, appear to have driven the evolution of the major metazoan body plans (5). Profound changes in shape or morphology, underlying adaptive differences among closely related species, also can be caused by mutations in a very few genes (6-8).Compared with our growing understanding of the evolution of biological shape and form, our understanding of what regulates body size and the rates and efficiencies of physiological functions is much less developed. For example, the genetic and physiological causes of heterosis (hybrid vigor) and its converse, inbreeding depression, have remained elusive for nearly a century, despite the economic and scientific significance of these phenomena (9-12). Major genetic explanations for heterosis are overdominance, the superiority of heterozygotes at genes affecting fitness or economic traits, dominance, the masking, in hybrids, of deleterious recessive mutations by dominant alleles inherited from one or the other inbred parent, and epistasis, the interaction of alleles at differe...

Assessing the energy costs of development in extreme environments is important for understanding how organisms can exist at the margins of the biosphere. Macromolecular turnover rates of RNA and protein were measured at -1.5 degrees C during early development of an Antarctic sea urchin. Contrary to expectations of low synthesis with low metabolism at low temperatures, protein and RNA synthesis rates exhibited temperature compensation and were equivalent to rates in temperate sea urchin embryos. High protein metabolism with a low metabolic rate is energetically possible in this Antarctic sea urchin because the energy cost of protein turnover, 0.45 joules per milligram of protein, is 1/25th the values reported for other animals.

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An understanding of the biochemical and physiological energetics of lecithotrophic development is useful for interpreting patterns of larval development, dispersal potential, and life-history evolution. This study investigated the metabolic rates and use of biochemical reserves in two species of abalone, Haliotis fulgens (the green abalone) and H. sorenseni (the white abalone). Larvae of H. fulgens utilized triacylglycerol as a primary source of endogenous energy reserves for development ( approximately 50% depletion from egg to metamorphic competence). Amounts of phospholipid remained constant, and protein dropped by about 30%. After embryogenesis, larvae of H. fulgens had oxygen consumption rates of 81.7 +/- 5.9 (SE) pmol larva(-1) h(-1) at 15 degrees C through subsequent development. The loss of biochemical reserves fully met the needs of metabolism, as measured by oxygen consumption. Larvae of H. sorenseni were examined during later larval development and were metabolically and biochemically similar to H. fulgens larvae at a comparable stage. Metabolic rates of both species were very similar to previous data for a congener, H. rufescens, suggesting that larval metabolism and energy utilization may be conserved among closely related species that also share similar developmental morphology and feeding modes.

The rates of oxygen consumption by embryos of antarctic echinoderms (Acodontaster hodgsoni, Odontaster validus, Psilaster charcoti, and Sterechinus neumayeri) were compared to the biomas (ash-free dry organic weight) of the egg of each species. These species could survive for months to years (range: 10 months to 5 years) by relying solely on the reserves present in the egg. However, certain species did not use any of the egg's reserves during early development. Embryonic stages of O. validus (a species with planktotrophic larvae) did not decrease in lipid, protein, or total biomass during the first 35 days of development. During the first 42 days of development, embryos of A. hodgsoni (a species with lecithotrophic development) used protein as an energy source. For both species lipid composed 40 to 50% of egg biomass, but was not used as an energy reserve. Larvae of O. validus have a high-affinity transport system for amino acids dissolved in seawater (K1 = 1.3 {mu}M for alanine). The rate of alanine transport from a low concentration (50 nM) could supply 32% of the larva's metabolic needs. This is a 10-fold higher input to metabolism than was determined (3% at 50 nM) for larvae of a temperate asteroid, Asterina miniata. Larvae of antarctic echinoderms live in an environment where the food supply is low for most of the year. Relative to their metabolic rates, antarctic larvae have larger energy stores and planktotrophic larvae have higher nutrient transport capacities when compared to larvae from temperate regions. These physiological differences allow antarctic larvae to survive for long periods without particulate food.