Journal Article

Ancient convergent losses of Paraoxonase 1 yield potential risks for modern marine mammals

Marsillach, Judit, Crocker, Daniel E., Chikina, Maria, Richter, Rebecca, Furlong, Clement E., Partha, Raghavendran, Meyer, Wynn K., Jamison, Jerrica, Woods, Stacy E., Kronk, Charles, Clark, Nathan L., Kowalczyk, Amanda, Bonde, Robert K., Gaspard, Joseph, Lanyon, Janet M.

2018

Overview

Mammals evolved in terrestrial environments. Those that now live in the marine environment have had to adapt to the particular selective pressures that this environment imposes. Meyer et al. surveyed the genomes of several marine mammal species to identify regions of convergent change. Multiple losses of the Paraoxonase 1 gene are evident in marine mammals, likely resulting from remodeling of lipid metabolism or antioxidant networks. The multiple occurrences of this loss of function across taxa indicate an evolutionary benefit. However, Paraoxonase 1 is the primary mammalian defense against organophosphorus toxicity. Marine mammals may be at a great disadvantage in the Anthropocene if run-off of this agricultural product into the marine environment continues. Science , this issue p. 591 Convergent loss of Paraoxonase 1 may leave marine mammals unable to metabolize organophosphates. Mammals diversified by colonizing drastically different environments, with each transition yielding numerous molecular changes, including losses of protein function. Though not initially deleterious, these losses could subsequently carry deleterious pleiotropic consequences. We have used phylogenetic methods to identify convergent functional losses across independent marine mammal lineages. In one extreme case, Paraoxonase 1 ( PON1 ) accrued lesions in all marine lineages, while remaining intact in all terrestrial mammals. These lesions coincide with PON1 enzymatic activity loss in marine species’ blood plasma. This convergent loss is likely explained by parallel shifts in marine ancestors’ lipid metabolism and/or bloodstream oxidative environment affecting PON1’s role in fatty acid oxidation. PON1 loss also eliminates marine mammals’ main defense against neurotoxicity from specific man-made organophosphorus compounds, implying potential risks in modern environments.

• Publisher: The American Association for the Advancement of Science
• Subject: Adaptation, Biological / Agricultural management / Animals / Anthropocene / Antioxidants / Aryldialkylphosphatase - blood / Aryldialkylphosphatase - genetics / Blood plasma / Cetacea - blood / Cetacea - classification / Cetacea - genetics / Convergence / Ecological risk assessment / Environment / Environmental Exposure / Enzymatic activity / Evolution, Molecular / Genetic Fitness / Genomes / Identification methods / Lesions / Lipid Metabolism / Lipoproteins, HDL - metabolism / Lipoproteins, LDL - metabolism / Marine Biology / Marine environment / Marine mammals / Metabolic Detoxication, Phase I / Metabolism / Neurotoxicity / Organophosphorus compounds / Organophosphorus Compounds - metabolism / Organophosphorus Compounds - toxicity / Oxidation / Oxidation-Reduction / Oxidative metabolism / Paraoxonase / Paraoxonase 1 / Phylogeny / Proteins / Risk / Runoff / Selection, Genetic / Terrestrial environments / Toxicity