Research & Publications

The Evolution of Stress Tolerance in Marine Invertebrates

Our approach is to investigate species that naturally occur at the edges of their physiological tolerance limits in order to understand the molecular mechanisms that allow some organisms to survive while others cannot. By understanding how organisms have naturally evolved to tolerate environmental variability, we can then begin to predict how populations may respond to the accelerated rates of global climate change.

Specifically our research focuses on the physiological responses of a population of back-reef corals in American Samoa that routinely survive temperatures thought to cause bleaching and mortality in most other areas. If we can understand how this particular group of corals is able to survive these extreme exposures, then we can start to identify other populations of corals that may be best adapted to survive future stresses caused by climate change.

We use molecular tools (genomic, proteomic) combined with experimental ecology and physiology to explore the evolutionary basis for phenotypic variability in stress tolerance limits of marine invertebrates.

Current Projects:

  • The Global Search for naturally resilient coral reefs (funded by Vulcan/Paul G. Allen Family Foundation: https://pgafamilyfoundation.org/News/2021/new-coral-grants.aspx)
  • EAGER: Bleaching phenotypes of acute vs. chronic coral bleaching susceptibility and resilience: towards a standardized coral resilience diagnostic (funded by the National Science Foundation)
  • Coral Thermal Adaptation in the Red Sea (funded by the US-Israeli Binational Science Foundation)
  • Mesophotic Coral Ecosystems of American Samoa (funded by NOAA)
  • Wild Genome Project (funded by Revive & Restore: https://reviverestore.org/projects/wild-genomes/)

Publications (updated August 2022):

Google Scholar: https://scholar.google.com.au/citations?user=fxHxwoEAAAAJ&hl=en&oi=ao

  • Blanco-Pimentel M, Evensen NR, Cortés-Useche C, Calle-Triviño J, Barshis DJ, Galvan V, Harms E, Morikawa MK (Accepted) All-inclusive coral reef restoration: how the tourism sector can boost restoration efforts in the Caribbean. Frontiers in Marine Science
  • Klepac CN, Barshis DJ (2022) High-resolution in situ thermal metrics coupled with acute heat stress experiments reveal differential coral bleaching susceptibility. Coral Reefs 41:1045–1057
  • Evensen NR, Voolstra CR, Fine M, Perna G, Cardenas A, Buitrago-Lopez C, Rowe K, Barshis DJ (2022) Empirically derived thermal thresholds of four coral species along the Red Sea using a portable and standardized experimental approach. Coral Reefs. 41:239–252
  • Banc-Prandi G, Evensen NR, Barshis DJ, Perna G, Omar YM, Fine M (2022) Assessment of temperature optimum signatures of corals at both latitudinal extremes of the Red Sea. Conservation Physiology 10(1):coac002
  • Naugle MS, Oliver TA, Barshis DJ, Gates RD and Logan CA (2021) Variation in Coral Thermotolerance Across a Pollution Gradient Erodes as Coral Symbionts Shift to More Heat-Tolerant Genera. Frontiers in Marine Science 8:760891
  • Voolstra CR, Suggett DJ, Peixoto RS, Parkinson JE, Quigley KM, Silveira CB, Sweet M, Muller EM, Barshis DJ, Bourne DG, Aranda M (2021) Extending the natural adaptive capacity of coral holobionts. Nature Reviews Earth & Environment 2(11):747–762
  • Voolstra CR, Valenzuela JJ, Turkarslan S, Ca ́rdenas A, Hume BCC, Perna G, Buitrago-Lo ́pez C, Rowe K, Orellana MV, Baliga NS, Paranjape S, Banc-Prandi G, Bellworthy J, Fine M, Frias-Torres S, Barshis DJ (2021a) Contrasting heat stress response patterns of coral holobionts across the Red Sea suggest distinct mech- anisms of thermal tolerance. Molecular Ecology 30:4466–4480
  • Savary R, Barshis DJ, Voolstra CR, Cárdenas A, Evensen NR, Banc-Prandi G, Fine M, Meibom A (2021) Fast and pervasive transcriptomic resilience and acclimation of extremely heat-tolerant coral holobionts from the northern Red Sea. Proceedings of the National Academy of Sciences 118(19):e2023298118
  • Evensen NR, Fine M, Perna G, Voolstra CR, Barshis DJ (2021) Remarkably high and consistent tolerance of a Red Sea coral to acute and chronic thermal stress exposures. Limnology and Oceanography 66(5):1718-29
  • Voolstra CR, Quigley KM, Davies SW, Parkinson JE, Peixoto RS, Aranda M, Baker AC, Barno AR, Barshis DJ, Benzoni F, Bonito V. Consensus guidelines for advancing coral holobiont genome and specimen voucher deposition. Frontiers in Marine Science 2021:1029.
  • Aichelman HE, Barshis DJ (2020) Adaptive divergence, neutral panmixia, and algal symbiont population structure in the temperate coral Astrangia poculata along the Mid-Atlantic United States. PeerJ 8:e10201
  • Klepac CN, Barshis DJ (2020) Reduced thermal tolerance of massive coral species in a highly variable environment. Proceedings of the Royal Society B. 287:20201379
  • Voolstra CR, Buitrago‐López C, Perna G, Cárdenas A, Hume BC, Rädecker N, Barshis DJ (2020) Standardized short‐term acute heat stress assays resolve historical differences in coral thermotolerance across microhabitat reef sites. Global Change Biology 26(8):4328-43
  • Kleinhaus K, Al-Sawalmih A, Barshis DJ, Genin A, Grace LN, Hoegh-Guldberg O, Loya Y, Meibom A, Osman EO, Ruch J-D, Shaked Y, Voolstra CR, Zvuloni A, Fine M (2020) Science, Diplomacy, and the Red Sea’s Unique Coral Reef: It’s Time for Action. Frontiers in Marine Science 7:90. doi: 10.3389/fmars.2020.00090
  • Martinez A, Crook ED, Barshis DJ, Potts DC, Rebolledo-Vieyra M, Hernandez L, Paytan A (2019) Species-specific calcification response of Caribbean corals after 2-year transplantation to a low aragonite saturation submarine spring. Proceedings of the Royal Society B. 2862019057220190572
  • Aichelman HE, Zimmerman RC, Barshis DJ (2019) Adaptive signatures in thermal performance of the temperate coral Astrangia poculata. Journal of Experimental Biology 222, jeb189225
  • Barshis, DJ, Birkeland, C, Toonen, RJ, Gates, RD, Stillman, JH (2018) High-frequency temperature variability mirrors fixed differences in thermal limits of the massive coral Porites lobata. Journal of Experimental Biology 221, jeb188581
  • Safaie, A., Silbiger, N.J., McClanahan, T.R. et al. (2018) High frequency temperature variability reduces the risk of coral bleaching. Nature Communications 9, 1671
  • Torda G, Donelson JM, Aranda M, Barshis DJ, et al. (2017) Rapid adaptive responses to climate change in corals. Nature Climate Change. 7, 627-636. Selected for Journal Cover
  • McKeon S, Weber M, Alter SE, Seavy N, Crandall E, Barshis DJ, et al. (2016) Melting barriers to faunal exchange across ocean basins. Global Change Biology. 22, 465-471. Selected for journal cover and featured in the Washington Post
  • Egekwu N, Sonenshine DE, Garman H, Barshis DJ, Cox N, Bissinger BW, Roe RM (2016) Comparing synganglion neuropeptides, neuropeptide receptors and neurotransmitter recepters and their gene expression response to feeding in Ixodes scapularis (Ixodidae) versus Ornithodoros turicata (Argasidae). Insect Molecular Biology 25, 72-92
  • McKeon S, Tunberg BG, Johnston CA, Barshis DJ (2015) Ecological drivers and habitat associations of esturaine bivalves. PeerJ. 3:e1348
  • Palumbi SR, Barshis DJ, Traylor-Knowles N, Bay RA (2014) Mechanisms of reef coral resistance to future climate change. Science. 344, 895-898 (pdf)
  • Barshis DJ, Ladner JT, Oliver TA, Palumbi SR (2014) Lineage specific transcriptional profiles of Symbiodinium spp. unaltered by heat stress in a coral host. Molecular Biology and Evolution. 31, 1343-1352 (pdf)
  • Anderson EC, Skaug HJ, Barshis DJ (2014) Next-generation sequencing for molecular ecology: A caveat regarding pooled samples. Molecular Ecology. 23, 502-512
  • Barshis DJ, Oliver TA, Ladner JT, Seneca FO, Traylor-Knowles N, Palumbi SR (2013) Genomic basis for coral resilience to climate change. Proceedings of the National Academy of Sciences. 110, 1387-1392, Selected for journal cover and the subject of over 30 popular press articles (this one’s the best) (open access pdf)
  • Ladner JT, Barshis DJ, Palumbi SR (2012) Amino acid sequence evolution in four Symbiodinium clades: an exploration into the genetic basis of thermal tolerance in Symbiodinium clade D. BMC Evolutionary Biology 12:217 (open access pdf)
  • Amend A, Barshis DJ, Oliver TA (2012) Coral-associated marine fungi form novel lineages and heterogeneous assemblages. The ISME Journal. 6:1291-1301 (open access pdf)
  • DeWit P, Pespeni MH, Ladner JT, Barshis DJ et al. (2012) The simple fool’s guide to population genomics via RNA-Seq: an introduction to high-throughput sequencing data analysis. Molecular Ecology Resources. 12:1058-1067 (pdf)
  • Padilla-Gamino J, Bidigare RR, Barshis DJ, Alamaru A et al. (2012) Are all eggs created equal? A case study from the Hawaiian reef building coral Montipora capitata. Coral Reefs. 31, 137-152 (link)
  • Barshis DJ, Sotka EE, Kelly RP, Sivasundar A, Menge BA, Barth JA, Palumbi SR (2011) A link between coastal upwelling and temporal genetic variability in the Acorn Barnacle Balanus glandula. Marine Ecology Progress Series. 439:139-150 (link)
  • Barshis DJ, Stillman JH, Gates RD, Toonen RJ, Smith LW, Birkeland C (2010) Protein expression and genetic structure of the coral Porites lobata in an environmentally extreme Samoan back reef: does host genotype limit phenotypic plasticity? Molecular Ecology 19(8):1705-1720
  • Brown DP, Basch L, Barshis DJ, Forsman Z, Fenner D, Goldberg J (2009) American Samoa’s island of giants: Massive Porites colonies at Ta’u Island. Coral Reefs 28:735
  • Forsman Z, Barshis DJ, Hunter C, Toonen RJ (2009) Shape-shifting corals: Molecular markers show morphology is evolutionarily plastic in Porites. BMC Evolutionary Biology 9:45 (open access pdf)
  • Smith LW, Barshis DJ, Birkeland C (2007) Phenotypic plasticity for skeletal growth, density and calcification of Porites lobata in response to habitat type. Coral Reefs 26:559-567

Other Publications:

  • Barshis DJ (2015) Genomic potential for coral survival of climate change. In: Coral Reefs in the Anthropocene (C. Birkeland, editor), Springer, Netherlands. 133-146
  • Willette DA, Allendorf FW, Barber PH, Barshis DJ et al. (2014) So, you want to use next-generation sequencing in marine systems? Insight from the Pan-Pacific Advanced Studies Institute. Bulletin of Marine Science. 90(1), 79-122
  • Pinsky ML, Kroeker KJ, Logan CA, Barshis DJ (2013) Marine conservation and climate change. In: Encyclopedia of Biodiversity (S. Levin, editor), Academic Press, San Diego. 32-44
  • Spalding H, Gupta A, Barshis DJ, Knope M, Tice K, Dirzo R, Wilber C (2010) Broader impacts from the bottom-up: integrating K-12 education into your grant applications. Frontiers in Ecology and the Environment 8(4), 217-218