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Role of mitochondria in mediating evolutionary rescue by anthropogenic pollutants in an invasive crab

Periodic Reporting for period 1 - MitoRescue (Role of mitochondria in mediating evolutionary rescue by anthropogenic pollutants in an invasive crab)

Okres sprawozdawczy: 2023-05-01 do 2025-06-30

Invasive alien species (IAS) are the cause of enormous socio-economic and biodiversity loss across the world. In the context of climate change and increased pollution, IAS are often more adaptive than native species, capable of adjusting their phenology in accordance with climatic changes, facilitating their invasion. It has been recently suggested that “rapid evolution” (allowing quickly adaption and avoiding extinction due to maladaptation), is the cause of the increased invasive capacity of IAS. MitoRescue takes this concept one step further, hypothesizing that mitochondria, being exquisitely sensitive to environmental stress and with a highly mutagenic DNA, are key organelles involved in rapid evolution resulting in “evolutionary rescue”. The project studies the combined impact of pollutants and increased temperature on an ancestral and an invasive (recently established) population of the European Green Crab, an extremely prolific invader. The study involves both field and laboratory approaches, from the organelle to the whole-organism. It merges the fields of toxicology, physiology, evolutionary and molecular biology to provide a highly multidisciplinary and integrative perspective. The final objective of this research subject is to predict future invasion scenarios, identify novel targets to control IAS proliferation and improve management and risk assessments of IAS in Europe and worldwide. In the long-term, this research will promote “restoring Europe’s biodiversity”, which is one of the four current key strategic orientations for EU’s R&I. It will contribute as well to the European Green Deal Initiatives and the EU Biodiversity Strategy for 2030 by addressing IAS socio-economical management in a thermally changing world.
During the first two years of the project, the MitoRescue project progressed in line with its core objectives, completing WP1 and WP2 and initiating WP3. WP1 examined bioenergetic capacity, osmoregulation, and redox homeostasis of native (European) and invasive (Australian) Carcinus maenas populations under different pollution and temperature regimes. Sampling was conducted across multiple pristine and polluted sites, integrating physiological, biochemical, histological, and genetic analyses. Results revealed higher respiration rates in cold-adapted crabs, but similar osmotic and redox profiles across native populations. Invasive Australian crabs exhibited lower metabolism yet elevated antioxidant defences, with principal component analysis showing distinct physiological profiles. Genetic analyses linked these differences to high genetic variability, providing a first mechanistic link between genetic diversity and redox adaptation in invasive populations.

WP2 assessed mitochondrial tolerance to cadmium and copper, both well-known mitotoxicants. Results showed that historically cadmium-exposed crabs displayed pro-adaptive mitochondrial traits (elevated OXPHOS, ETS capacity, complex II activity, antioxidant defences), whereas naïve crabs exhibited acute shifts in complex activity likely aimed at reducing the production of reactive oxygen species, deleterious for cellular components and responsible for the induction of oxidative stress. These findings suggest long-term metal exposure fosters mitochondrial adaptations enhancing invasion success in polluted environments.

Methodological innovations included developing a permeabilized gill tissue protocol for marine invertebrates, improving in vivo relevance of mitochondrial assays. The project integrated whole-animal, tissue, and molecular approaches, incorporating sex as a biological variable and revealing sex-specific biochemical responses. WP3 sample collection was completed ahead of schedule, with imaging and gene expression analyses underway. The work has generated multiple conference presentations, one peer-reviewed publication, and several manuscripts in preparation, advancing evolutionary toxicology by establishing mitochondrial plasticity as a key factor in invasive species resilience to pollution and climate stress.
MitoRescue breaks new ground by revealing mitochondrial plasticity—not just genetic mutations—as a rapid evolution driver enabling invasive species to thrive under pollution and climate stress. It delivers the first mechanistic link between genetic diversity and redox adaptation in an invasive invertebrate, supported by a novel permeabilized gill tissue protocol for in vivo-representative mitochondrial assays. By integrating whole-animal, tissue, and molecular data—and uniquely considering sex-specific responses—the project advances evolutionary toxicology beyond current models focused on vertebrates. The resulting bioenergetic and mitochondrial biomarkers will potentially offer predictive tools for assessing invasiveness and resilience, guiding cost-effective management of harmful species and reducing economic losses in aquaculture, fisheries, and coastal tourism. These outcomes directly support EU biodiversity, zero pollution, and climate resilience objectives, aligning with the European Green Deal.
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