Academic literature on the topic 'Evolutionary ecotoxicology'

Abstract A fundamental objective within ecotoxicology lies in understanding and predicting effects of contaminants. This objective is made more challenging when global climate change is considered as an environmental stress that co-occurs with contaminant exposure. In this multi-stressor context, evolutionary processes are particularly important. In this paper, we consider several non-”omic” approaches wherein evolutionary responses to stress have been studied and discuss those amenable to a multiple stressor context. Specifically, we discuss common-garden designs, artificial and quasi-natural selection, and the estimation of adaptive potential using quantitative genetics as methods for studying evolutionary responses to contaminants and climate change in the absence of expensive molecular tools. While all approaches shed light on potential evolutionary impacts of stressor exposure, they also have limitations. These include logistical constraints, difficulty extrapolating to real systems, and responses tied strongly to specific taxa, populations, and/or testing conditions. The most effective way to lessen these inherent limitations is likely through inclusion of complementary physiological and molecular tools, when available. We believe that an evolutionary context to the study of contaminants and global climate change is a high priority in ecotoxicology and we outline methods that can be implemented by almost any researcher but will also provide valuable insights.

Although interest in Acanthocephala seems to have reached only a small community of researchers worldwide, we show in this opinion article that this group of parasites is composed of excellent model organisms for studying key questions in parasite molecular biology and cytogenetics, evolutionary ecology, and ecotoxicology. Their shared ancestry with free-living rotifers makes them an ideal group to explore the origins of the parasitic lifestyle and evolutionary drivers of host shifts and environmental transitions. They also provide useful features in the quest to decipher the proximate mechanisms of parasite-induced phenotypic alterations and better understand the evolution of behavioral manipulation. From an applied perspective, acanthocephalans’ ability to accumulate contaminants offers useful opportunities to monitor the impacts – and evaluate the possible mitigation – of anthropogenic pollutants on aquatic fauna and develop the environmental parasitology framework. However, exploring these exciting research avenues will require connecting fragmentary knowledge by enlarging the taxonomic coverage of molecular and phenotypic data. In this opinion paper, we highlight the needs and opportunities of research on Acanthocephala in three main directions: (i) integrative taxonomy (including non-molecular tools) and phylogeny-based comparative analysis; (ii) ecology and evolution of life cycles, transmission strategies and host ranges; and (iii) environmental issues related to global changes, including ecotoxicology. In each section, the most promising ideas and developments are presented based on selected case studies, with the goal that the present and future generations of parasitologists further explore and increase knowledge of Acanthocephala.

The presence of metals in the environment has been linked to the evolutionary processes of man and nature. Its influence on biochemical mechanisms in organisms has been proven by numerous studies in recent years. However, due to the influences of anthropogenic activities, the presence of important amounts of metals has been found mainly in the regions close to the metal manufacturing industries, causing a local geochemical alteration, aggravated by natural factors such as rainfall, contaminating all levels of the chain trophic region.

Les isothiazolinones sont des molécules organiques utilisées comme biocides à large spectre dans une grande variété d'applications industrielles et de consommation. Bien que leur présence dans les sols et les eaux douces ait été détectée, les rapports des fabricants ont jugé les quantités concernées inoffensives pour l'écosystème. Toutefois, compte tenu des quantités libérées dans l'environnement depuis des décennies, des inquiétudes ont été exprimées quant à leur impact sur les processus d'évolution des espèces non ciblées, qui ne sont pas examinés dans des conditions de tests de toxicité standard. Ce travail vise à étudier en particulier les effets de la plus inoffensive de ces molécules, la méthylisothiazolinone (MIT). Sa toxicité aiguë a été évaluée sur Daphnia pulex, un invertébré aquatique emblématique en écotoxicologie et en biologie évolutive.Ces tests à court terme ont révélé une grande variabilité intraspécifique dans la tolérance, ce qui a également été vérifié dans une expérience à long terme utilisant de faibles concentrations de MIT. En outre, l'exposition à la MIT a eu des effets létaux et sublétaux sur la fitness des daphnies, avec une évolution sur quatre générations dans le cas d'une exposition multigénérationnelle continue, mais pas dans le cas d'une exposition parentale ou grand-parentale. Ces effets ont été étudiés plus en détail par analyse d’expression différentielle à partir de données globales d'ARNseq. La variabilité intraspécifique et les changements dans les réponses au sein d'une espèce appellent à l'inclusion des processus évolutifs dans les évaluations des risques et au réexamen des interprétations des tests d'écotoxicité standards
Isothiazolinones are a family of organic molecules used as broad-spectrum biocides in a wide variety of consumer and industrial applications. Although their presence in the environment has been detected, especially in soils and freshwater, reports by the manufacturers deemed the quantities involved harmless for the ecosystem. However, given the daily amounts of it released in the environment over decades, concerns were raised about their impact on non-target species evolutionary processes, which cannot be examined under standard ecotoxicity test conditions. This work aims to provide some answers by studying the effects of the most innocuous of these molecules, methylisothiazolinone (MIT). MIT acute toxicity was assessed on Daphnia pulex, an iconic ecotoxicology and evolutionary model species of aquatic invertebrates.These short-term tests revealed a great intraspecific variability in the tolerance to MIT contamination, which was also verified in a longterm experiment using low concentration. Moreover, MIT exposure caused lethal and sublethal effects on daphnia fitness, with developments over four generations in the case of a continuous multigenerational exposure, but not in the case of parental or grandparental exposure. These effects were further investigated with differential expression analysis from global RNAseq data. Both intraspecific variability and multigenerational change in the responses within one species call for the inclusion of evolutionary processes in risk assessments and the reconsideration of standard ecotoxicity tests interpretations

Comme ils conduisent à des modifications de sensibilité toxicologique et de traits d'histoire de vie au sein des populations naturelles exposées, les phénomènes d'adaptation à la contamination questionnent la pertinence de l'évaluation du risque environnemental lié au rejet de contaminants chimiques et sont devenus un champ de recherche important à développer en écotoxicologie. Centrés sur l'étude des capacités d'adaptation de l'amphipode d'eau douce Gammarus fossarum, les travaux présentés ici ont eu pour objectif d'avancer dans la compréhension des effets d'une exposition à long terme au cadmium à l'échelle populationnelle et en milieu naturel. En recourant à des méthodologies de biomonitoring par encagement, de culture et d'exposition au laboratoire et de suivi démographique in situ, une démarche couplant études a priori et rétrospectives sur populations naturelles, a permis d'identifier un phénomène d'augmentation de la tolérance et de modification de traits d'histoire de vie chez une population exposée historiquement au cadmium. Des approches de génétique quantitative conduites sur trois populations ont dans un deuxième temps mis en évidence (1) une faible héritabilité de la sensibilité au cadmium au sein de populations naïves ; et (2) un rôle majeur des effets parentaux induits par l'exposition comme mécanisme populationnel soutenant l'évolution de la tolérance chez cette espèce. Enfin, la caractérisation de la variabilité de la sensibilité au cadmium au sein du genre Gammarus (dix-sept populations) et la mise en regard de la divergence de la population tolérante vis-à-vis de cette variabilité, ont permis de discuter des implications de ces processus évolutifs induits par des expositions environnementales pour l'évaluation du risque lié aux substances chimiques. Ainsi, il apparaît nécessaire de prendre en compte les réponses adaptatives induites par la contamination des milieux comme source de variabilité et d'incertitude afin de proposer une évaluation du risque pertinente intégrant pleinement l'ensemble des impacts des contaminations environnementales sur les populations naturelles
Because they lead to changes in toxicological sensitivities and life history traits within field populations, evolutionary processes supporting adaptation to contamination challenge the relevance of environmental risk assessment of chemical contaminants. Hence their study becomes an important developing field of research in ecotoxicology. Focusing on the study of adaptive capacity of the freshwater amphipod Gammarus fossarum, this work aimed to gain insight into the effects of long term exposure to cadmium at the population scale in the field. By means of biomonitoring methodologies (caging), population demographic sampling, culture and exposure in the laboratory we identified a phenomenon of increased tolerance and modification of life history traits in a natural population historically exposed to cadmium. Quantitative genetics experiments conducted on three populations secondly demonstrated (1) a low heritability of sensitivity to cadmium in naïve populations ; and (2) a major role of parental effects induced by exposure as populational mechanism supporting the development of tolerance in this species. Finally, the characterization of the variability of cadmium sensitivity in the genus Gammarus (seventeen populations), and the analysis of the divergence of the tolerant population in comparison to this variability led us to discuss about the implications of these evolutionary processes induced by environmental exposure for risk assessment of chemicals. Thus, from these results it appears necessary to take into account adaptive responses induced by environmental contamination as a source of variability and uncertainty in order to provide a relevant risk assessment fully integrating all the impacts of environmental contamination on natural populations

Doutoramento em Biologia
As populações que vivem em ecossistemas de água doce extremamente contaminados por metais podem estar sujeitas a forte seleção e deriva genética. Este processo de erosão genética poderá ameaçar a sua sobrevivência a longo prazo, uma vez que a capacidade de adaptação das populações a alterações das condições ambientais está diretamente relacionada com os níveis de diversidade genética. Neste sentido, a procura por novos bioindicadores, que aumentem a relevância ecológica da avaliação de risco ambiental, tem levado a um crescente interesse pela toxicologia evolutiva e por medidas de diversidade genética. O trabalho aqui apresentado tem como objetivo último compreender de que forma os níveis de diversidade genética da espécie modelo em ecotoxicologia Chironomus riparius (Meigen) podem ser usados como indicadores de qualidade ecológica de sistemas de água doce. Para tal, avaliaram-se respostas microevolutivas à contaminação histórica por metais em populações de C. riparius, incluindo determinação dos níveis de diversidade genética, adaptação genética a metais e potenciais custos de fitness. A diversidade genética foi estimada com base na variação de sete marcadores de microssatélites enquanto que a adaptação genética a metais e potenciais custos de fitness foi avaliada através da tolerância aguda e crónica a diferentes stressores ambientais, medidas de balanço energético e mecanismos de defesa após manter as diferentes populações durante várias gerações em condições laboratoriais controlo. Por fim, as respostas microevolutivas de C. riparius à contaminação por metais foram comparadas com a diversidade e composição das comunidades de macroinvertebrados. Para determinar a relação de causa-efeito entre respostas microevolutivas e contaminação, os efeitos da poluição por metais foram investigados em diferentes locais historicamente contaminados por metais e comparados com várias referências. Os resultados demonstraram elevados níveis de diversidade genética e uma considerável homogeneidade genética entre as populações monitorizadas em condições naturais. No entanto, observaram-se evidências de adaptação genética a metais nas populações de locais contaminados, incluindo maior tolerância à exposição aguda por metais e elevados níveis basais de glutationas e metalotioninas que possivelmente aumentam a capacidade de resposta das populações à exposição a metais. Além do mais, observaram-se maiores custos energéticos em populações de locais contaminados quando expostas a metais, enquanto que uma das populações de locais contaminados apresentou também custos de fitness em condições controlo. Finalmente, verificou-se que a diversidade e composição das comunidades de macroinvertebrados dos locais contaminados foi fortemente afetada e muitos grupos taxonómicos sensíveis à contaminação foram eliminados e substituídos por outros mais oportunistas, tais como C. riparius. De um modo geral, as medidas de diversidade genética de populações naturais de C. riparius não mostraram ser ferramentas de biomonitorização particularmente vantajosas per se uma vez que não refletiram as respostas microevolutivas das diferentes populações à poluição histórica por metais. Tal facto poderá estar relacionado com a elevada densidade populacional e dinamismo da espécie em condições naturais, uma vez que se observou uma considerável perda de diversidade genética quando as populações foram mantidas em laboratório durante períodos de tempo relativamente longos. Não obstante, algumas linhas de evidência do presente trabalho sugerem o uso de medidas de diversidade genética de C. riparius em diversas situações experimentais como sejam: deteção de hibridização interespecífica; estabelecimento de níveis mínimos de diversidade genética em laboratório; e, finalmente, uso integrativo de medidas de diversidade genética em programas de biomonitorização com um foco mais direcionado para os efeitos ao nível da comunidade de macroinvertebrados. Os resultados apresentados pretendem estimular a discussão acerca da adequabilidade de C. riparius como espécie modelo em toxicologia evolutiva bem como a sensibilidade e robustez das medidas de diversidade genética como indicadores de qualidade ambiental em avaliação de risco ecológico.
Natural populations inhabiting heavily metal impacted freshwater ecosystems may face intense selection and genetic drift that conduct populations to severe reductions of genetic diversity, the so-called process of genetic erosion. Because the ability of populations to adapt to environmental change is directly related to the levels of genetic diversity, contaminant-driven genetic erosion may threaten the long-term survival of populations. The search for more robust and context-driven bio-indicators that add ecological relevance to the environmental risk assessments has increased interest in evolutionary toxicology and measures of genetic diversity. The research described in the present thesis was performed with the ultimate goal of understanding whether the levels of genetic diversity of the model ecotoxicological species Chironomus riparius (Meigen) may be used as ecological indicators of the health of freshwater systems. For that, an integrative study was undertaken investigating microevolutionary responses of C. riparius towards historical metal pollution. This included assessments of levels of genetic diversity as well as determination of genetic adaptation to metals and associated fitness costs. Genetic diversity was estimated based on the variation of seven microsatellite markers. Genetic adaptation and associated fitness costs were investigated through acute and chronic exposures to different environmental stressors, measurements of energy budget and biochemical mechanisms of tolerance to metals, after maintaining populations for several generations under standard laboratory conditions. Microevolutionary responses of C. riparius to metal pollution were, afterwards, compared with macroinvertebrate diversity and composition metrics. To draw general conclusions of causal-relationship between microevolutionary responses and pollution history, effects were investigated across multiple metal polluted and reference site. Globally, the levels of genetic diversity were globally high and there was a remarkable genetic homogeneity among all C. riparius populations in the field. However, C. riparius populations from metal polluted sites showed signs of genetic adaptation to metals as suggested by the increased tolerance to acute concentrations of metal and high basal levels of glutathiones and metallothioneins that likely enhance the fitness of populations to cope with metal toxicity. Furthermore, populations from metals contaminated sites had higher energetic costs when exposed to metals and one of the populations from contaminated sites showed also a poorer performance under control clean conditions. Finally, diversity and composition of macroinvertebrate communities from metal polluted sites was strongly affected and many sensitive taxonomic groups were eliminated and replaced by more opportunistic ones such as C. riparius. Overall, measures of genetic diversity of C. riparius natural populations do not seem to be particularly advantageous biomonitoring tools per se once they did not reflect the underlying microevolutionary responses of natural populations to historical metal pollution. This is likely because of the large population densities together with the highly dynamic nature of C. riparius in the field as we observed genetic erosion in population reared under laboratory conditions over relatively long periods of time. However, several lines of evidence indicate that measures of genetic diversity may accrue valuable information in several experimental situations: detection of interspecific hybridization; establishment of minimum levels of genetic diversity in laboratory-reared C. riparius populations; finally, integrative use of measures of genetic diversity in biomonitoring programs with more community-level focus. The results presented in this thesis aim to stimulate discussion on the suitability of C. riparius as a model species in evolutionary ecotoxicology studies as well as the sensitivity and robustness of genetic diversity measures as indicators of environmental quality in ecological risk assessment.

Dans le milieu naturel, les poissons sont exposés à une multitude de facteurs de stress biotiques et abiotiques, mais leurs interactions sont encore mal connues. La hausse des températures et la contamination par les éléments trace métalliques (ETMs) sont des sources importantes de stress pour les poissons. Les parasites ont également des effets sur la physiologie de leur hôte, mais sont rarement considérés en tant que facteurs de stress. Ces trois facteurs de stress agissent via des voies physiologiques communes (immunité, stress oxydant, métabolisme) et sont donc susceptibles d'interagir de manière complexe (e.g. antagonisme, synergisme). De plus, il existe souvent une grande variabilité des réponses entre échelles biologiques, des molécules aux populations. Notamment, l'historique d'exposition des populations de poisson dans leur milieu naturel pourrait conditionner leur capacité de réponse au stress. La prise en compte de ces deux niveaux de variabilité (i.e. interactions entre stress et entre échelles d'organisation) représente donc un verrou scientifique majeur pour mieux comprendre les effets des stress multiples sur les populations de poissons d'eau douce. Cette thèse vise donc à évaluer les effets combinés de facteurs de stress abiotique (i.e. température, ETMs) et biotique (i.e. challenge immunitaire provoqué par le parasitisme) sur les réponses des poissons d'eau douce via une approche multi-échelles. Afin de remplir ces objectifs, le Goujon (Gobio occitaniae) a été utilisé comme espèce modèle dans le cadre de trois approches méthodologiques : (i) une approche transversale de terrain visant à comparer l'état de santé de population de poissons le long des gradients de stress ; puis, (ii) des expérimentations en conditions contrôlées afin de distinguer les effets des différents facteurs de stress simples dans différentes populations sauvages ; enfin (iii) une expérience de translocation réciproque (i.e. encagement sur le terrain) entre sites contaminés et peu contaminés afin de tester l'adaptation locale des populations. Les résultats montrent que les stress simples ont des effets importants aux échelles biologiques fines et induisent la mise en place de stratégies métaboliques de compensation : les poissons investissent dans les défenses immunitaires et antioxydantes, avec une réduction des réserves énergétiques. De plus, les ajustements comportementaux (i.e. activité de nage, recherche de nourriture) sont particulièrement importants sous stress simples, et permettent d'ajuster l'acquisition d'énergie ce qui limite les effets sur la survie et la croissance. Au contraire, les stress multiples ont peu d'effets aux échelles moléculaires et cellulaires, mais provoquent des réponses complexes à l'échelle individuelle, ce qui se traduit par des effets antagonistes sur le comportement et des effets négatifs sur la survie et la croissance. Ces résultats suggèrent que sous stress multiples, les capacités de réponse des poissons pourraient être dépassées, menant ainsi à une stratégie de conservation, avec des effets délétères sur la fitness. Cependant, les réponses observées étaient fortement variables selon la population considérée. [...]
Aquatic ecosystems are increasingly exposed to multiple stressors. Among them, temperature increase and contamination by trace metal elements are major stressors for freshwater fish populations. In addition, parasites and their associated immune challenges can cause a wide range of responses in fish populations, but they are still rarely considered as biotic stressors. These three stressors trigger similar physiological pathways (i.e. immunity, oxidative stress and metabolism). Hence, they are likely to interact strongly but their combined effects (i.e. antagonism and synergism) are still poorly documented, thereby hindering our ability to predict the responses of wild populations to multiple stressors under global changes. In addition, responses to stressors could vary according to the level of organisation considered (i.e molecules, cells, individuals, populations). In particular, different populations could have different sensitivity to stressors depending on their past exposure in the wild. Thus it is essential to incorporate these levels of variability to better understand and predict the effects of multiple stressors in wild fish populations. This PhD project aimed at assessing the effects of a multiple abiotic (i.e. temperature, trace metal contamination) and biotic (i.e. immune challenge) stressors across biological levels of organisation, using the gudgeon fish (Gobio occitaniae) as a model species. First, I used a cross-sectional field study in 16 wild populations to compare fish health along stress gradients. Then, I used experimental approaches under controlled conditions to disentangle the role of each single and multiple stressors across levels of organisation in different fish populations. Finally, I used reciprocal translocation experiments between polluted vs. unpolluted rivers to test for local adaptation in response to multiple stressors. Taken together, results show that single stressors affect mostly the molecular and cellular levels, in accordance with a compensatory strategy. Indeed, costly physiological defences (immunity, anti-oxidant responses) were set up and behavioural adjustments (i.e. changes in activity and foraging) enable fish to increase energy acquisition and respond adequately to single stressors, with limited deleterious effects on survival and growth. On the contrary, multiple stressors affected mostly the individual level, in accordance with a conservation metabolic strategy. Indeed, multiple stressors lead to complex antagonistic effects between stressors (i.e. antagonistic inhibition of behavioural responses), potentially due to the high energy demand incurred, resulting in deleterious effects on survival or growth. This suggests that physiological and behavioural responses might be exceeded under multiple stressors with deleterious consequences on fitness, thereby raising concerns about the effects of multiple global changes on wild populations. [...]

Mayflies are important macroinvertebrate members of steam communities and are highly sensitive to agricultural insecticides. In this dissertation I sought to explore whether Heptageniidae mayflies in Indiana have evolved greater tolerance to clothianidin, a neonicotinoid insecticide that has been widely applied over the predominant corn and soybean crops of the state for the last 20 years. Over the five chapters of this dissertation, I investigate different aspects of the effects of clothianidin on mayfly populations. First, I collected mayfly populations from streams around the state across a gradient of agricultural landscape to see if proximity to corn and soybean crops was associated with tolerance to the insecticide. I found significant variation in tolerance between the populations but only connected it to land use for one species and one insecticide. Second, I investigated the potential for increases in predation rates due to exposure to low concentrations of clothianidin by both a vertebrate and invertebrate predator. Sublethal exposure did increase the risk of predation by the invertebrate predator but not the vertebrate. Third, I collected four populations of mayflies and placed them in a common stream which is heavily impacted by agricultural runoff. The most tolerant of the four populations had the highest survival rates and was native to the polluted stream, suggesting that it was best adapted to the local conditions. Finally, the last chapter is a discussion of the factors influencing the evolution of contaminant tolerance, the implications for biomonitoring, and a series of recommendations for incorporating evolved tolerance into biomonitoring practices. Collectively, this work suggests that the lethal and sublethal effects of clothianidin exposure create conditions suitable for the evolution of tolerance in Heptageniid mayflies. While there are already differences in tolerance between populations, it seems likely that mayfly pesticide tolerance will continue to increase as pesticides continue to impact aquatic ecosystems.