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Adaptive plasticity as a key for invasion success in disturbed ecosystems

Periodic Reporting for period 2 - INVASOMICS (Adaptive plasticity as a key for invasion success in disturbed ecosystems)

Periodo di rendicontazione: 2023-10-01 al 2024-09-30

Invasive species are a major constituent of global change, threaten local biodiversity and cause serious economic damage. The science of biological invasions has tried to discern what factors determine the success of invasive populations, be it the species-specific intrinsic features or environmental factors, e.g. eutrophication. However, the outcomes are highly context-dependent. Moreover, the process of invasion often induces an initial reduction in population size associated with a reduction in genetic variation due to genetic drift. This reduction seems to not affect the invasive success of some established introduced populations, constituting a genetic paradox of biological invasions.

Three key questions related to evolutionary biology stand out in the study of biological invasions: i) Is the variable, environmentally-induced expression of life-history traits a key to invasion success? ii) How do genetics and biology of invasive species differ in their native vs. introduced areas? iii) Is environmental tolerance greater in invasive species and populations? In this project the invasive eastern mosquitofish (Gambusia holbrooki), whose invasion history is well known, is used as experimental model to characterize its tolerance to nitrogen pollution and identify mechanistic differences in its response between the native and invasive populations. Early warning molecular tools such as transcriptomics, but also whole organism responses like respiratory rates and life history traits are used to denote the health status of the experimentally exposed individuals to nitrogen pollution. This approach is then applied in three sympatric amphipod species in the Main river catchment. The overall objective is to understand the adaptive mechanisms that promote invasion success in a widespread invasive freshwater species.
Experimental sublethal exposures to nitrite and nitrate were conducted on adult G. holbrooki from six native populations in Florida and North Carolina (USA) and three introduced in Extremadura, Spain. All nine populations were selected based on the historic baseline of nitrogen pollution. Hemoglobin, respiratory rates, life history traits, and gene expression of exposed fish have been analyzed. The results revealed distinct patterns based on the biological complexity of the endpoints. Early-response endpoints, such as the gene expression in the gills, was primarily influenced by historic nitrogen pollution and by laboratory nitrite exposures. In contrast, endpoints of higher organizational complexity, such as respiratory rates and life history traits, were more strongly affected by the region of origin and nitrite exposure, with interactions observed in respiratory rates. These findings highlight the impact of nitrogen pollution on fish health and reveal that physiological responses to nitrite vary between populations of the same species.
This suggests that contemporary evolution has enabled native and introduced populations to better adapt to eutrophic conditions. However, regional characteristics appear to be conserved in life history traits in closely related populations, such as the invasive populations in Spain and their source population in NC. Both produce smaller embryos, which may explain the superior colonization abilities of fish from the expanding ranges of the species' distribution.

During the return phase we investigated the impact of nitrite pollution on three species of amphipods (Gammarus fossarum, G. pulex and G. roeselii) that play key roles in the rivers of the Main catchment area and have distinct colonization histories. Initially, lethal concentration values (LC50) were determined, serving as a basis for selecting sublethal nitrite concentration ranges. These ranges were then used to assess sublethal effects on gene expression, leaf litter consumption, and behavioral activity during 10-day experimental trials. The results revealed significant interspecies differences in responses to nitrite exposure. Notably, the native species, particularly G. fossarum, displayed much higher sensitivity compared to the more resilient G. roeselii. This heightened sensitivity among native species offers insights into ongoing shifts in species composition due to nitrogen pollution. These findings suggest that increasing nitrite pollution in aquatic ecosystems could drive further expansion of G. roeselii in headwaters. This has profound ecological implications, as the decline of sensitive native species may disrupt ecosystem functions and reduce biodiversity.

These results have been disseminated so far in two conferences (43th North American SETAC Meeting in Pittsburgh PA and the Southeast SETAC Meeting in Auburn AL), two internal seminars at the Goethe Universität Frankfurt, one at the University of Florida, one for professional management stakeholders (UF/IFAS CISMA series) and one as outreach dissemination in Mataró (Spain). The researcher has also been invited in November 2024 to give a lecture related to this project for the students of BSc Biology at the Universitat de Barcelona, and two online seminars the Universidad Nacional de Colombia. The data are presently in the final stages of analysis, and manuscripts for publication in ISI-indexed journals are being prepared.
This project is highly innovative in integrating the disciplines of ecotoxicology, evolutionary biology, and invasion science. The initial hypothesis to be tested was the newly proposed ‘anthropogenically induced adaptation to invade’ paradigm and especially the groundbreaking ‘selection model’ during transport. This newly proposed model calls for a clear demonstration by validating whether introduced populations exhibit increased adaptive tolerance to a stressor associated with the introduction, contributing to their invasive success. This proposal is purposely designed to answer this important question and it has been one of the firsts to investigate it.

The output of this project is fundamental research on mechanisms of invasiveness. Despite this theoretical approach, it does have an applied impact on society as well. There is a growing call for integrating evolutionary concepts in conservation policies, such as designing prevention or eradication plans for invasive species that integrate evolutionary aspects to better counteract the risks of biological introductions and that do not underestimate the shifted tolerance to pollution. The outputs of this project might also concern legislation on aquaculture or ornamental fish industry. Transport of ornamental aquatic fauna is regulated in the EU by the Council Regulation (EC) No 1/2005 and internationally by the Aquatic Animal Health Code of the World Organisation for Animal Health and the CITES guidelines for the non-air transport of live wild animals and plants. However, these regulations are oriented towards animal welfare, but they do not take into account conservation issues such as the presumed prior adaptations to invade facilitated by transport. Based on this results, the origin of the source population of a same species is a primordial factor on determining the fate of the species in the recipient environment. Therefore, the output in this project may reach EU and national environmental policymakers (e.g. European Environment Agency) to work the results into policies and adjust better to the UN Sustainable Development Goals and the Horizon Europe Global Challenges.
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