Pumping Ions: Rapid Parallel Evolution of Ionic Regulation Following Habitat Invasions

Lee, Carol Eunmi; Kiergaard, Michael; Gelembiuk, Gregory William; Eads, Brian D.; Posavi, Marijan

doi:10.1111/j.1558-5646.2011.01308.x

Cited by 147 publications

(251 citation statements)

References 71 publications

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“…Little is known about the osmoregulation of copepods, and marine copepods are considered osmoconformers (Mauchline, 1998). However, the calanoid copepod Eurytemora affinis has the capability to osmoregulate via the ion‐transport enzymes V‐type H + ‐ATPase and Na + /K + ‐ ATPase, an ability that allowed it to colonize freshwater from marine environments (Lee, Kiergaard, Gelembiuk, Eads, & Posavi, 2011). Our findings with C. glacialis lend additional support to the osmoregulatory capacity of marine copepods, possibly via sodium:proton antiporters.…”

Section: Discussionmentioning

confidence: 99%

Regulation of gene expression is associated with tolerance of the Arctic copepod Calanus glacialis to CO₂‐acidified sea water

Bailey

Wit

Thor

et al. 2017

Ecology and Evolution

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Ocean acidification is the increase in seawater pCO 2 due to the uptake of atmospheric anthropogenic CO 2, with the largest changes predicted to occur in the Arctic seas. For some marine organisms, this change in pCO 2, and associated decrease in pH, represents a climate change‐related stressor. In this study, we investigated the gene expression patterns of nauplii of the Arctic copepod Calanus glacialis cultured at low pH levels. We have previously shown that organismal‐level performance (development, growth, respiration) of C. glacialis nauplii is unaffected by low pH. Here, we investigated the molecular‐level response to lowered pH in order to elucidate the physiological processes involved in this tolerance. Nauplii from wild‐caught C. glacialis were cultured at four pH levels (8.05, 7.9, 7.7, 7.5). At stage N6, mRNA was extracted and sequenced using RNA‐seq. The physiological functionality of the proteins identified was categorized using Gene Ontology and KEGG pathways. We found that the expression of 151 contigs varied significantly with pH on a continuous scale (93% downregulated with decreasing pH). Gene set enrichment analysis revealed that, of the processes downregulated, many were components of the universal cellular stress response, including DNA repair, redox regulation, protein folding, and proteolysis. Sodium:proton antiporters were among the processes significantly upregulated, indicating that these ion pumps were involved in maintaining cellular pH homeostasis. C. glacialis significantly alters its gene expression at low pH, although they maintain normal larval development. Understanding what confers tolerance to some species will support our ability to predict the effects of future ocean acidification on marine organisms.

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Section: Discussionmentioning

confidence: 99%

Regulation of gene expression is associated with tolerance of the Arctic copepod Calanus glacialis to CO₂‐acidified sea water

Bailey

Wit

Thor

et al. 2017

Ecology and Evolution

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“…For example, Lee et al (2011) found an expansion of plasticity after a marine to freshwater invasion by the copepod Eurytemora affinis. This habitat shift of E. affinis occurred only 150-300 generations ago, such that insufficient time may have accumulated for assimilation of plasticity.…”

Section: Research Articlementioning

confidence: 99%

Reciprocal osmotic challenges reveal mechanisms of divergence in phenotypic plasticity in the killifish Fundulus heteroclitus

Brennan

Gálvez

Whitehead

2015

Journal of Experimental Biology

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The killifish Fundulus heteroclitus is an estuarine species with broad physiological plasticity, enabling acclimation to diverse stressors. Previous work suggests that freshwater populations expanded their physiology to accommodate low salinity environments; however, it is unknown whether this compromises their tolerance to high salinity. We used a comparative approach to investigate the mechanisms of a derived freshwater phenotype and the fate of an ancestral euryhaline phenotype after invasion of a freshwater environment. We compared physiological and transcriptomic responses to high-and low-salinity stress in fresh and brackish water populations and found an enhanced plasticity to low salinity in the freshwater population coupled with a reduced ability to acclimate to high salinity. Transcriptomic data identified genes with a conserved common response, a conserved salinity-dependent response and responses associated with population divergence. Conserved common acclimation responses revealed stress responses and alterations in cell-cycle regulation as important mechanisms in the general osmotic response. Salinityspecific responses included the regulation of genes involved in ion transport, intracellular calcium, energetic processes and cellular remodeling. Genes diverged between populations were primarily those showing salinity-specific expression and included those regulating polyamine homeostasis and the cell cycle. Additionally, when populations were matched with their native salinity, expression patterns were consistent with the concept of 'transcriptomic resilience', suggesting local adaptation. These findings provide insight into the fate of a plastic phenotype after a shift in environmental salinity and help to reveal mechanisms allowing for euryhalinity.

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“…We found that executing laboratory selection in response to crude oil was comparatively more difficult relative to the ease to which laboratory populations of E. affinis could respond to selection in response to salinity or temperature stress (Ketzner & Bradley, 1982; Lee et al., 2007, 2011). The selection experiments in this study used similar approaches as prior studies, with similar starting population size (hundreds of copepods).…”

Section: Discussionmentioning

confidence: 99%

Evolutionary responses to crude oil from the Deepwater Horizon oil spill by the copepod Eurytemora affinis

Lee

Remfert

Opgenorth

et al. 2017

Evolutionary Applications

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The BP Deepwater Horizon Oil Disaster was the most catastrophic offshore oil spill in U.S. history, yet we still have a poor understanding of how organisms could evolve in response to the toxic effects of crude oil. This study offers a rare analysis of how fitness‐related traits could evolve rapidly in response to crude oil toxicity. We examined evolutionary responses of populations of the common copepod Eurytemora affinis residing in the Gulf of Mexico, by comparing crude oil tolerance of populations collected before versus after the Deepwater Horizon oil spill of 2010. In addition, we imposed laboratory selection for crude oil tolerance for ~8 generations, using an E. affinis population collected from before the oil spill. We found evolutionary increases in crude oil tolerance in the wild population following the oil spill, relative to the population collected before the oil spill. The post‐oil spill population showed increased survival and rapid development time in the presence of crude oil. In contrast, evolutionary responses following laboratory selection were less clear; though, development time from metamorphosis to adult in the presence of crude oil did become more rapid after selection. We did find that the wild population, used in both experiments, harbored significant genetic variation in crude oil tolerance, upon which selection could act. Thus, our study indicated that crude oil tolerance could evolve, but perhaps not on the relatively short time scale of the laboratory selection experiment. This study contributes novel insights into evolutionary responses to crude oil, in directly examining fitness‐related traits before and after an oil spill, and in observing evolutionary responses following laboratory selection.

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Pumping Ions: Rapid Parallel Evolution of Ionic Regulation Following Habitat Invasions

Cited by 147 publications

References 71 publications

Regulation of gene expression is associated with tolerance of the Arctic copepod Calanus glacialis to CO₂‐acidified sea water

Regulation of gene expression is associated with tolerance of the Arctic copepod Calanus glacialis to CO₂‐acidified sea water

Reciprocal osmotic challenges reveal mechanisms of divergence in phenotypic plasticity in the killifish Fundulus heteroclitus

Evolutionary responses to crude oil from the Deepwater Horizon oil spill by the copepod Eurytemora affinis

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Pumping Ions: Rapid Parallel Evolution of Ionic Regulation Following Habitat Invasions

Cited by 147 publications

References 71 publications

Regulation of gene expression is associated with tolerance of the Arctic copepod Calanus glacialis to CO2‐acidified sea water

Regulation of gene expression is associated with tolerance of the Arctic copepod Calanus glacialis to CO2‐acidified sea water

Reciprocal osmotic challenges reveal mechanisms of divergence in phenotypic plasticity in the killifish Fundulus heteroclitus

Evolutionary responses to crude oil from the Deepwater Horizon oil spill by the copepod Eurytemora affinis

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Regulation of gene expression is associated with tolerance of the Arctic copepod Calanus glacialis to CO₂‐acidified sea water

Regulation of gene expression is associated with tolerance of the Arctic copepod Calanus glacialis to CO₂‐acidified sea water