About

Scott Applebaum is an Associate Professor of Environmental Studies at USC Dornsife. His research focuses on physiological and biochemical adaptation in animals, with an emphasis on the developmental stages of marine vertebrates and invertebrates from temperate, sub-tropical, and polar oceans. He investigates how planktonic embryos and larvae meet environmental challenges while undergoing growth and development of anatomical structures and physiological functions. His work aims to understand the mechanistic bases of complex traits in animals, assess the impacts of environmental stressors such as ocean acidification, and contribute to predicting the effects of current and future environmental conditions on marine life. His research integrates levels of biological organization from genes to whole organisms and their environment, with a focus on direct, quantitative assessment of physiological and biochemical rates.

Research topics

• Biology
• Botany
• Chemistry
• Environmental science
• Biochemistry
• Evolutionary biology
• Geology
• Environmental chemistry
• Oceanography
• Genetics
• Demography
• Biophysics

Selected publications

• Molecular consequences of mitochondrial replacement may be masked from organismal traits in Tigriopus californicus

  PLoS ONE · 2025-10-24

  articleOpen accessCorresponding

  Mitochondrial replacement therapy (MRT) presents a promising preventative measure to combat mitochondrial diseases. However, the long-term consequences of disrupting mitonuclear coevolution at both the molecular and organismal levels remain understudied. Data on sex-specific effects are also lacking despite predictions that males may be especially vulnerable to mitochondrial replacement. To address this, we used backcrossed lines of the copepod Tigriopus californicus to produce offspring with nuclear genotype contributions from two populations and a mitochondrial genotype from a third, separate, population. When compared to hybrid controls with mitochondrial genotypes that matched the maternal nuclear genotype but not the paternal, these "three-parent offspring" did not significantly differ in lifespan or routine metabolic rate. While these organismal-level traits showed no effect, molecular metrics of mitochondrial health revealed consequences of mitochondrial replacement. Oxidative DNA damage, measured by 8-hydroxy-2'-deoxyguanosine content, was higher in three-parent offspring, and mitochondrial DNA content was lower than in hybrid controls. While differences between sexes were present in some traits, sex did not interact with mitochondrial replacement for any of these metrics. Although these results could be due either to donor mitochondrial DNA matching neither of the nuclear parents, or to deficits in the donor mitochondrial DNA itself, they highlight the importance of considering molecular level consequences of mitochondrial replacement that may be masked at the organismal level when evaluating the health impacts of this treatment.

  PublisherDOI

• Mitonuclear effects on sex ratio persist across generations in interpopulation hybrids

  Journal of Evolutionary Biology · 2024-09-26 · 2 citations

  articleOpen accessSenior author

  Eukaryotic energy production requires tight coordination between nuclear and mitochondrial gene products. Because males and females often have different energetic strategies, optimal mitonuclear coordination may be sex-specific. Previous work found evidence for sex-specific mitonuclear effects in the copepod Tigriopus californicus by comparing two parental lines and their reciprocal F1 crosses. However, an alternative hypothesis is that the patterns were driven by the parental source of nuclear alleles. Here, we test this alternative hypothesis by extending the same cross to F2 hybrids, which receive both maternal and paternal nuclear alleles from F1 hybrids. Results confirm mitonuclear effects on sex ratio, with distorted ratios persisting from the F1 to F2 generations, despite reduced fitness in F2 hybrids. No sex-by-cross interactions were found for other phenotypic traits measured. Mitochondrial DNA content was higher in females. Both routine metabolic rate and oxidative DNA damage were lower in F2 hybrids than in parentals. The persistence of sex-specific mitonuclear effects, even in the face of F2 hybrid breakdown, attests to the magnitude of these effects, which contribute to the maintenance of within-population mitochondrial DNA polymorphisms.

  PublisherOA PDFDOI

• Mitonuclear effects on sex ratio persist across generations in interpopulation hybrids

  bioRxiv (Cold Spring Harbor Laboratory) · 2023 · 2 citations

  Senior authorCorresponding
  • Biology
  • Genetics
  • Evolutionary biology

  Abstract Eukaryotic energy production requires tight coordination between gene products from both the nuclear and mitochondrial genomes. Because males and females often have different energetic strategies, this mitonuclear coordination can be expected to differentially impact the two sexes. Previous work found evidence for sex-specific mitonuclear effects in the copepod Tigriopus californicus by comparing two parental lines and their reciprocal F1 crosses. However, an alternative hypothesis is that the patterns could instead be driven by the parental source of nuclear alleles. Here we test this alternative hypothesis by extending the same cross to F2 hybrids, who receive both maternal and paternal nuclear alleles from F1 hybrids. Results confirm mitonuclear effects on sex ratio, with distorted ratios persisting from the F1 to F2 generations, despite reduced fitness in F2 hybrids. No sex by cross interactions were found for other phenotypic traits measured. Mitochondrial DNA content was shown to be higher in females, the more stress-tolerant sex. Both routine metabolic rate and oxidative DNA damage were found to be lower in F2 hybrids than in parentals. Confirmation of sex-biased mitonuclear effects in T. californicus is notable, given that the species lacks sex chromosomes, which can confound interpretations of sex-specific mitochondrial effects.

  PublisherOA PDFDOI

• Natural Analogues in pH Variability and Predictability across the Coastal Pacific Estuaries: Extrapolation of the Increased Oyster Dissolution under Increased pH Amplitude and Low Predictability Related to Ocean Acidification

  Environmental Science & Technology · 2022 · 33 citations

  • Oceanography
  • Environmental science
  • Environmental chemistry

  ) oysters under flow-through experimental conditions over a six-week period that simulate current and future conditions: static control and low pH (8.0 and 7.7); low pH with fluctuating (24-h) amplitude (7.7 ± 0.2 and 7.7 ± 0.5); and high-frequency (12-h) fluctuating (8.0 ± 0.2) treatment. The oysters showed physiological tolerance in vital processes, including calcification, respiration, clearance, and survival. However, shell dissolution significantly increased with larger amplitudes of pH variability compared to static pH conditions, attributable to the longer cumulative exposure to lower pH conditions, with the dissolution threshold of pH 7.7 with 0.2 amplitude. Moreover, the high-frequency treatment triggered significantly greater dissolution, likely because of the oyster's inability to respond to the unpredictable frequency of variations. The experimental findings were extrapolated to provide context for conditions existing in several Pacific coastal estuaries, with time series analyses demonstrating unique signatures of pH predictability and variability in these habitats, indicating potentially benefiting effects on fitness in these habitats. These implications are crucial for evaluating the suitability of coastal habitats for aquaculture, adaptation, and carbon dioxide removal strategies.

  PublisherOA PDFDOI

• Differing thermal sensitivities of physiological processes alter ATP allocation

  Journal of Experimental Biology · 2020 · 15 citations

  • Biophysics
  • Biology
  • Biochemistry

  Changes in environmental temperature impact rate processes at all levels of biological organization. Yet, the thermal sensitivity of specific physiological processes that impact allocation of the ATP pool within a species is less well understood. In this study of developmental stages of the Pacific oyster, Crassostrea gigas, thermal sensitivities were measured for growth, survivorship, protein synthesis, respiration, and transport of amino acids and ions. At warmer temperatures, larvae grew faster but suffered increased mortality. An analysis of temperature sensitivity (Q10 values) revealed that protein synthesis, the major ATP-consuming process in larvae of C. gigas, is more sensitive to temperature change (Q10 value of 2.9±0.18) than is metabolic rate (Q10 of 2.0±0.15). Ion transport by Na+/K+-ATPase measured in vivo has a Q10 value of 2.1±0.09. The corresponding value for glycine transport is 2.4±0.23. Differing thermal responses for protein synthesis and respiration result in a disproportional increase in the allocation of available ATP to protein synthesis with rising temperature. A bioenergetic model is presented illustrating how changes in growth and temperature impact allocation of the ATP pool. Over an environmentally relevant temperature range for this species, the proportion of the ATP pool allocated to protein synthesis increases from 35% to 65%. The greater energy demand to support protein synthesis with increasing temperature will compromise energy availability to support other essential physiological processes. Defining the tradeoffs of ATP demand will provide insights into understanding the adaptive capacity of organisms to respond to various scenarios of environmental change.

  PublisherOA PDFDOI

• Shifting Balance of Protein Synthesis and Degradation Sets a Threshold for Larval Growth Under Environmental Stress

  Biological Bulletin · 2018-02-01 · 33 citations

  articleCorresponding

  Exogenous environmental factors alter growth rates, yet information remains scant on the biochemical mechanisms and energy trade-offs that underlie variability in the growth of marine invertebrates. Here we study the biochemical bases for differential growth and energy utilization (as adenosine triphosphate [ATP] equivalents) during larval growth of the bivalve Crassostrea gigas exposed to increasing levels of experimental ocean acidification (control, middle, and high pCO2, corresponding to ∼400, ∼800, and ∼1100 µatm, respectively). Elevated pCO2 hindered larval ability to accrete both shell and whole-body protein content. This negative impact was not due to an inability to synthesize protein per se, because size-specific rates of protein synthesis were upregulated at both middle and high pCO2 treatments by as much as 45% relative to control pCO2. Rather, protein degradation rates increased with increasing pCO2. At control pCO2, 89% of cellular energy (ATP equivalents) utilization was accounted for by just 2 processes in larvae, with protein synthesis accounting for 66% and sodium-potassium transport accounting for 23%. The energetic demand necessitated by elevated protein synthesis rates could be accommodated either by reallocating available energy from within the existing ATP pool or by increasing the production of total ATP. The former strategy was observed at middle pCO2, while the latter strategy was observed at high pCO2. Increased pCO2 also altered sodium-potassium transport, but with minimal impact on rates of ATP utilization relative to the impact observed for protein synthesis. Quantifying the actual energy costs and trade-offs for maintaining physiological homeostasis in response to stress will help to reveal the mechanisms of resilience thresholds to environmental change.

  PublisherDOI

• Biochemical bases of growth variation during development: A study of protein turnover in pedigreed families of bivalve larvae (<i>Crassostrea gigas</i>)

  Journal of Experimental Biology · 2018-01-01 · 23 citations

  articleOpen access

  Animal size is a highly variable trait regulated by complex interactions between biological and environmental processes. Despite the importance of understanding the mechanistic bases of growth, the ability to predict size variation in early stages of development remains challenging. Pedigreed lines of the Pacific oyster (Crassostrea gigas) were crossed to produce contrasting growth phenotypes to analyze the metabolic bases of growth variation in larval stages. Under controlled environmental conditions substantial growth variation of up to 430% in shell length occurred among 12 larval families. Protein was the major biochemical constituent in larvae, with an average protein-to-lipid content ratio of 2.8. On average, rates of protein turnover were high at 86% and showed a regulatory shift in depositional efficiency that resulted in increased protein accretion during later larval growth. Variation in protein depositional efficiency among families did not explain the range in larval growth rates. Instead, changes in protein synthesis rates predicted 72% of growth variation. High rates of protein synthesis to support faster growth, in turn, necessitated greater allocation of the total ATP pool to protein synthesis. An ATP allocation model is presented for larvae of C. gigas that includes the major components (82%) of energy demand: protein synthesis (45%), ion pump activity (20%), shell formation (14%), and protein degradation (3%). The metabolic trade-offs between faster growth and the need for higher ATP allocation to protein synthesis could be a major determinant of fitness for larvae of different genotypes responding to the stress of environmental change.

  PublisherOA PDFDOI

• Metabolic Cost of Protein Synthesis in Larvae of the Pacific Oyster (<i>Crassostrea gigas</i>) Is Fixed Across Genotype, Phenotype, and Environmental Temperature

  Biological Bulletin · 2016-06-01 · 29 citations

  article

  The energy made available through catabolism of specific biochemical reserves is constant using standard thermodynamic conversion equivalents (e.g., 24.0 J mg protein(-1)). In contrast, measurements reported for the energy cost of synthesis of specific biochemical constituents are highly variable. In this study, we measured the metabolic cost of protein synthesis and determined whether this cost was influenced by genotype, phenotype, or environment. We focused on larval stages of the Pacific oyster Crassostrea gigas, a species that offers several experimental advantages: availability of genetically pedigreed lines, manipulation of ploidy, and tractability of larval forms for in vivo studies of physiological processes. The cost of protein synthesis was measured in larvae of C. gigas for 1) multiple genotypes, 2) phenotypes with different growth rates, and 3) different environmental temperatures. For all treatments, the cost of protein synthesis was within a narrow range--near the theoretical minimum--with a fixed cost (mean ± one standard error, n = 21) of 2.1 ± 0.2 J (mg protein synthesized)(-1) We conclude that there is no genetic variation in the metabolic cost of protein synthesis, thereby simplifying bioenergetic models. Protein synthesis is a major component of larval metabolism in C. gigas, accounting for more than half the metabolic rate in diploid (59%) and triploid larvae (54%). These results provide measurements of metabolic cost of protein synthesis in larvae of C. gigas, an indicator species for impacts of ocean change, and provide a quantitative basis for evaluating the cost of resilience.

  PublisherDOI

• Metabolic cost of calcification in bivalve larvae under experimental ocean acidification

  ICES Journal of Marine Science · 2016-11-03 · 103 citations

  article

  Abstract Physiological increases in energy expenditure frequently occur in response to environmental stress. Although energy limitation is often invoked as a basis for decreased calcification under ocean acidification, energy-relevant measurements related to this process are scant. In this study we focus on first-shell (prodissoconch I) formation in larvae of the Pacific oyster, Crassostrea gigas. The energy cost of calcification was empirically derived to be ≤ 1.1 µJ (ng CaCO3)−1. Regardless of the saturation state of aragonite (2.77 vs. 0.77), larvae utilize the same amount of total energy to complete first-shell formation. Even though there was a 56% reduction of shell mass and an increase in dissolution at aragonite undersaturation, first-shell formation is not energy limited because sufficient endogenous reserves are available to meet metabolic demand. Further studies were undertaken on larvae from genetic crosses of pedigreed lines to test for variance in response to aragonite undersaturation. Larval families show variation in response to ocean acidification, with loss of shell size ranging from no effect to 28%. These differences show that resilience to ocean acidification may exist among genotypes. Combined studies of bioenergetics and genetics are promising approaches for understanding climate change impacts on marine organisms that undergo calcification.

  PublisherDOI

• Bioenergetic Approaches to Define Resilience Potential to Compounding Environmental Stressors

  AGUOS · 2016-02-01

  article
  Publisher

Frequent coauthors

• Donal T. Manahan

  University of Southern California

  97 shared

• David W. Ginsburg

  University of Southern California

  85 shared

• John P. Adelman

  81 shared

• Roy M. Anderson

  London Centre for Neglected Tropical Disease Research

  81 shared

• Shigeru Kuratani

  Pioneer (Japan)

  81 shared

• Kirk Baldwin

  Princeton University

  81 shared

• Amy L. Angert

  University of British Columbia

  81 shared

• Sócrates B. Munoz

  Kansas State University

  81 shared