Life Cycle Simplifications in Aphids Drive Changes in Evolutionary Rates and Selection Regimes

Transitions toward simplified life cycles can reshape evolutionary trajectories, yet their impact on the rate of molecular evolution remains poorly understood. In aphids, host alternation (heteroecy) entails obligate seasonal migration between highly distinct plant hosts-typically woody and herbaceous species-and has been repeatedly lost, giving rise to monoecious species with simplified life cycles. Using comparative genomics across 46 aphid species, we tested whether transitions from heteroecy to monoecy alter evolutionary dynamics at the gene level. We identified 9,304 orthologs and estimated evolutionary rates (dN/dS) and shifts in selection regimes in the diverse Aphidinae subfamily. We found that 715 orthologs evolved faster in monoecious species, primarily due to relaxed selection, while heteroecious species showed signatures of intensified selection. Genes under relaxed selection in monoecious species were enriched for functions related to environmental sensing, signaling, nutritional adjustments, morph determination, and migration related-traits likely central for host alternation. These results suggest that the loss of a complex life cycle leads to reduced selective constraints as a consequence of ecological simplification. This study provides a robust evolutionary framework for understanding how life cycle transitions shape molecular evolution and drive gene decay following trait loss.

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Publication Details

Journal
Molecular Biology and Evolution
Published
2025-11-28
DOI
https://doi.org/10.1093/molbev/msaf307
Primary Topic
Insect-Plant Interactions and Control
Type
article
Field-Weighted Citation Impact
0.00

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article

Life Cycle Simplifications in Aphids Drive Changes in Evolutionary Rates and Selection Regimes

Fabrice Legeai, Julie Jaquiéry, Jean–Claude Simon, Aurelie Etier et al.
Molecular Biology and Evolution
Insect-Plant Interactions and Control
article

Life Cycle Simplifications in Aphids Drive Changes in Evolutionary Rates and Selection Regimes

Fabrice Legeai, Julie Jaquiéry, Jean–Claude Simon, Aurelie Etier, Théo Vericel, G. Gong
article en

Abstract

Transitions toward simplified life cycles can reshape evolutionary trajectories, yet their impact on the rate of molecular evolution remains poorly understood. In aphids, host alternation (heteroecy) entails obligate seasonal migration between highly distinct plant hosts-typically woody and herbaceous species-and has been repeatedly lost, giving rise to monoecious species with simplified life cycles. Using comparative genomics across 46 aphid species, we tested whether transitions from heteroecy to monoecy alter evolutionary dynamics at the gene level. We identified 9,304 orthologs and estimated evolutionary rates (dN/dS) and shifts in selection regimes in the diverse Aphidinae subfamily. We found that 715 orthologs evolved faster in monoecious species, primarily due to relaxed selection, while heteroecious species showed signatures of intensified selection. Genes under relaxed selection in monoecious species were enriched for functions related to environmental sensing, signaling, nutritional adjustments, morph determination, and migration related-traits likely central for host alternation. These results suggest that the loss of a complex life cycle leads to reduced selective constraints as a consequence of ecological simplification. This study provides a robust evolutionary framework for understanding how life cycle transitions shape molecular evolution and drive gene decay following trait loss.

Molecular Biology and EvolutionVol. 42(12)
Institut National de Recherche pour l'Agriculture, l'Alimentation et l'Environnement (FR), Institut de Génétique, Environnement et Protection des Plantes (FR)
Centre National de la Recherche Scientifique
Openalex Percentile: Top 66%
Insect-Plant Interactions and Control
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Life Cycle Simplifications in Aphids Drive Changes in Evolutionary Rates and Selection Regimes — Fabrice Legeai, Julie Jaquiéry, et al. · Molecular Biology and Evolution (2025) | TGRS Research Map | TGRS