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Ancient Convergent Losses of Paraoxonase 1 Yield Potential Risks for Modern Marine Mammals

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Ancient Convergent Losses of Paraoxonase 1 Yield Potential Risks for Modern Marine Mammals

Wynn K Meyer et al. Science.

Abstract

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.

Conflict of interest statement

Competing interests: The authors declare no competing financial interests.

Figures

Fig. 1.
Fig. 1.. PON1 functions and evolutionary history.
Illustration of PON1’s proposed roles in (A) preventing oxidative damage to low- and high-density lipoproteins (14, 15) and (B) detoxifying the oxon byproduct/metabolite of a common organophosphorus pesticide, chlorpyrifos (25). (C) Evolutionary rate of PON1 coding sequence across the phylogeny of 62 eutherian mammals. Branch lengths represent dN, and colors represent dN/dS (see color legend). dN/dS values greater than 1.2 were set to 1.2. Blue: marine species. ψ: genetic lesion(s) present.
Fig. 2.
Fig. 2.. Blood plasma enzymatic activity against two organophosphate-derived substrates.
Points represent rates of hydrolysis of chlorpyrifos oxon (left) or diazoxon (right) in μmol/min/mL for plasma from marine and semi-aquatic species (in blue) and terrestrial outgroups. Values for sheep, goat, and rat are from Furlong et al. (33), who performed assays under the same experimental conditions as in this study. Control assays of alkaline phosphatase activity show samples were not degraded (Fig. S3).
Fig. 3.
Fig. 3.. Manatee and adjacency of its habitat to agricultural land use.
Left: Florida manatee (photo by Robert K. Bonde, 2006). Center: Manatee protection zones and agricultural land in Florida. Right: Manatee protection zones, waterways, and agricultural land in Brevard County.

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