Divergent Proteomic Responses to Lead Exposure in House Sparrows (Passer domesticus)

Abstract

Chronic exposure to environmental contaminants can drive population decline but also exert selective pressure favouring adaptive molecular responses that mitigate toxicity. Australian lead (Pb) mining and smelting towns provide a natural experiment to study such contemporary adaptation in the house sparrow (Passer domesticus), an invasive commensal species that has persisted in heavily contaminated environments for over a century. The Broken Hill population is of particular interest as it has remained geographically isolated with limited gene flow, whereas the Port Pirie population is connected to surrounding regions. Here, we used data-independent acquisition mass spectrometry to compare the blood and liver proteomes of wild-caught sparrows from both towns and identify divergent molecular responses to lead. Lead exposure altered the mitochondrial proteome and disrupted RNA splicing in both populations, but the two towns diverged sharply in haem biosynthesis and protein quality control. We identified a mechanistic cascade in which lead inhibits ALAD, depleting intracellular haem, stabilising the transcriptional repressor BACH1, and suppressing globin expression. Broken Hill birds maintained ALAD abundance, upregulated proteasomal subunits (PSMC) and HSP70 family chaperones, and preserved significantly higher haemoglobin concentrations despite equivalent blood lead levels. Port Pirie birds exhibited ALAD collapse, BACH1 accumulation, and reliance on autophagy rather than active protein quality control. Liver proteomics confirmed tissue-level convergence of the haem pathway disruption. Together, these findings reveal that over a century of isolation under sustained lead exposure has shaped population-specific molecular strategies in Broken Hill sparrows, with enhanced proteostasis and preserved haem biosynthesis representing signatures of local adaptation.

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