Periodic Reporting for period 1 - ALTEREVO (Evolutionary and Molecular Determinants of a Nutritional Polyphenism)
Période du rapport: 2022-11-01 au 2025-04-30
Organisms face constant environmental challenges, particularly in the face of rapid global change. To survive and thrive, they have evolved mechanisms that enable phenotypic plasticity—the ability to adjust their morphology, behavior, or physiology in response to changing conditions. One of the most striking examples of this adaptation is nutritional polyphenism, where a single organism produces distinct morphs, each specialized to exploit different food sources or ecological niches. This remarkable strategy allows species to anticipate resource degradation by switching to higher-quality food, ensuring their survival and reproductive success.
Despite its ecological and evolutionary significance, the mechanisms driving nutritional polyphenism remain poorly understood. Key questions persist: How do organisms detect environmental cues that trigger these phenotypic changes? What molecular and genetic pathways enable the induction and determination of alternative phenotypes? And how did this ability evolve? Moreover, recent discoveries suggest that symbiotic microorganisms, which often live in close association with their hosts, may play an overlooked but critical role in these processes.
The ALTEREVO project focuses on aphids, which are not only significant agricultural pests but also fascinating models for studying nutritional polyphenism. While many aphid species remain on the same host plant throughout their life cycle, others switch between distinct host plants—typically a woody plant for sexual reproduction and herbaceous plants for clonal reproduction—producing specialized morphs suited to the nutritional and ecological demands of each environment. This life cycle, characterized by an obligatory host alternation linked to seasonal changes, offers an ideal system for exploring the interplay between environmental triggers, molecular regulation, and evolutionary history.
ALTEREVO aims to unravel the evolutionary and molecular determinants of nutritional polyphenism in aphids by addressing the following objectives. First, the project aims to identify the specific plant compounds that act as environmental triggers, prompting aphids to develop morphs specialized for particular hosts. Next, it investigates the molecular pathways that control this polyphenism, focusing on receptors and signaling mechanisms that translate these environmental cues into phenotypic changes. Another objective is to explore the role of the aphid obligatory symbiont, Buchnera aphidicola, in regulating and possibly evolving alongside the polyphenism mechanism. Additionally, ALTEREVO examines the evolutionary origins of this trait, asking whether it arose through entirely new genetic innovations or by reconfiguring pre-existing pathways sensitive to environmental changes.
This interdisciplinary project integrates metabolomics, genomics, epigenetics, and bioinformatics to build a comprehensive understanding of nutritional polyphenism. By revealing the underlying mechanisms, ALTEREVO addresses fundamental questions about phenotypic plasticity’s role in adaptation and evolution. It also has practical implications, potentially identifying novel targets for sustainable pest management and informing strategies to mitigate agricultural damage caused by aphid crop pests.
Despite its ecological and evolutionary significance, the mechanisms driving nutritional polyphenism remain poorly understood. Key questions persist: How do organisms detect environmental cues that trigger these phenotypic changes? What molecular and genetic pathways enable the induction and determination of alternative phenotypes? And how did this ability evolve? Moreover, recent discoveries suggest that symbiotic microorganisms, which often live in close association with their hosts, may play an overlooked but critical role in these processes.
The ALTEREVO project focuses on aphids, which are not only significant agricultural pests but also fascinating models for studying nutritional polyphenism. While many aphid species remain on the same host plant throughout their life cycle, others switch between distinct host plants—typically a woody plant for sexual reproduction and herbaceous plants for clonal reproduction—producing specialized morphs suited to the nutritional and ecological demands of each environment. This life cycle, characterized by an obligatory host alternation linked to seasonal changes, offers an ideal system for exploring the interplay between environmental triggers, molecular regulation, and evolutionary history.
ALTEREVO aims to unravel the evolutionary and molecular determinants of nutritional polyphenism in aphids by addressing the following objectives. First, the project aims to identify the specific plant compounds that act as environmental triggers, prompting aphids to develop morphs specialized for particular hosts. Next, it investigates the molecular pathways that control this polyphenism, focusing on receptors and signaling mechanisms that translate these environmental cues into phenotypic changes. Another objective is to explore the role of the aphid obligatory symbiont, Buchnera aphidicola, in regulating and possibly evolving alongside the polyphenism mechanism. Additionally, ALTEREVO examines the evolutionary origins of this trait, asking whether it arose through entirely new genetic innovations or by reconfiguring pre-existing pathways sensitive to environmental changes.
This interdisciplinary project integrates metabolomics, genomics, epigenetics, and bioinformatics to build a comprehensive understanding of nutritional polyphenism. By revealing the underlying mechanisms, ALTEREVO addresses fundamental questions about phenotypic plasticity’s role in adaptation and evolution. It also has practical implications, potentially identifying novel targets for sustainable pest management and informing strategies to mitigate agricultural damage caused by aphid crop pests.
During the first two years of the ALTEREVO project, significant progress has been made in understanding nutritional polyphenism in aphids, particularly in the bird-cherry oat aphid (Rhopalosiphum padi). This aphid alternates between two distinct host plants: a primary host, the bird cherry (Prunus padus, Rosaceae family), where sexual reproduction occurs, and several secondary hosts from the Poaceae family, where clonal reproduction takes place. A key focus was on identifying plant cues that trigger the induction and determination of migrant morphs and the molecular mechanisms behind these phenotypic and physiological changes.
The ALTEREVO team successfully established methodologies for collecting and analyzing phloem sap from different stages of the host plants, pinpointing specific amino acid and sugar fluctuations associated with leaf maturity. It was found that as leaves mature, declining amino acid levels in the primary host (P. padus) trigger the development of winged migratory morphs, enabling aphids to transition to herbaceous secondary hosts (grasses).
The project also advanced the understanding of genetic and molecular pathways regulating these changes. Using transcriptomic analyses, we identified key genes involved in morph induction and acclimation to the new host, highlighting the roles of salivary effectors and detoxifying genes in facilitating these transitions. Additionally, novel techniques, such as ATAC-Seq for chromatin accessibility studies, were implemented to study the epigenetic factors involved.
From an evolutionary perspective, comparative genomic analyses between heteroecious (host-alternating) and monoecious (non-host-alternating) aphid species revealed that monoecious species exhibit relaxed selection on specific genes, particularly salivary effector genes, which are critical for interactions with host plants. These findings shed light on the evolutionary pressures and genetic adaptations underlying host alternation.
Overall, ALTEREVO has achieved significant breakthroughs in understanding the environmental, molecular, and evolutionary mechanisms driving nutritional polyphenism in aphids, paving the way for further exploration of phenotypic plasticity and its broader ecological and evolutionary implications.
The ALTEREVO team successfully established methodologies for collecting and analyzing phloem sap from different stages of the host plants, pinpointing specific amino acid and sugar fluctuations associated with leaf maturity. It was found that as leaves mature, declining amino acid levels in the primary host (P. padus) trigger the development of winged migratory morphs, enabling aphids to transition to herbaceous secondary hosts (grasses).
The project also advanced the understanding of genetic and molecular pathways regulating these changes. Using transcriptomic analyses, we identified key genes involved in morph induction and acclimation to the new host, highlighting the roles of salivary effectors and detoxifying genes in facilitating these transitions. Additionally, novel techniques, such as ATAC-Seq for chromatin accessibility studies, were implemented to study the epigenetic factors involved.
From an evolutionary perspective, comparative genomic analyses between heteroecious (host-alternating) and monoecious (non-host-alternating) aphid species revealed that monoecious species exhibit relaxed selection on specific genes, particularly salivary effector genes, which are critical for interactions with host plants. These findings shed light on the evolutionary pressures and genetic adaptations underlying host alternation.
Overall, ALTEREVO has achieved significant breakthroughs in understanding the environmental, molecular, and evolutionary mechanisms driving nutritional polyphenism in aphids, paving the way for further exploration of phenotypic plasticity and its broader ecological and evolutionary implications.
The ALTEREVO project has made ground-breaking progress in deciphering nutritional polyphenism in aphids, particularly in the bird-cherry oat aphid (Rhopalosiphum padi). A significant achievement was identifying the specific maturity stage of leaves that triggers winged migratory morphs. This discovery highlights the critical role of plant cues in aphid development and provides a framework for further exploration of plant-aphid interactions.
Through advanced transcriptomic studies, the project uncovered key genes involved in stress response, salivary function, and detoxification, which facilitate aphid adaptation to their host plants. These findings highlight key genetic targets that may inform pest management strategies.
Comparative genomic analysis of host-alternating and non-host-alternating aphids provided evolutionary insights, showing that relaxed selection on certain genes, including salivary effectors, is associated with the loss of host alternation. These findings reveal how ecological pressures shape genome evolution.
The project enhanced our understanding of the genetic and molecular pathways that regulate phenotypic plasticity, as well as the evolutionary transitions that led to the emergence and loss of nutritional polyphenism across different aphid lineages. However, its potential impact extends beyond fundamental science. Unravelling the mechanisms of aphid polyphenism could lead to innovative, sustainable pest control solutions, reducing dependency on chemical pesticides and enhancing agricultural resilience. However, further research is needed to isolate the specific plant compounds and genetic factors responsible for these processes. Demonstrating the practical applications of these findings, such as identifying plant compounds that deter aphids or disrupt host alternation, will be crucial for successful implementation.
Through advanced transcriptomic studies, the project uncovered key genes involved in stress response, salivary function, and detoxification, which facilitate aphid adaptation to their host plants. These findings highlight key genetic targets that may inform pest management strategies.
Comparative genomic analysis of host-alternating and non-host-alternating aphids provided evolutionary insights, showing that relaxed selection on certain genes, including salivary effectors, is associated with the loss of host alternation. These findings reveal how ecological pressures shape genome evolution.
The project enhanced our understanding of the genetic and molecular pathways that regulate phenotypic plasticity, as well as the evolutionary transitions that led to the emergence and loss of nutritional polyphenism across different aphid lineages. However, its potential impact extends beyond fundamental science. Unravelling the mechanisms of aphid polyphenism could lead to innovative, sustainable pest control solutions, reducing dependency on chemical pesticides and enhancing agricultural resilience. However, further research is needed to isolate the specific plant compounds and genetic factors responsible for these processes. Demonstrating the practical applications of these findings, such as identifying plant compounds that deter aphids or disrupt host alternation, will be crucial for successful implementation.