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Differences in gene expression and genetic variation underlying preference-performance mismatches: insights from a specialized native herbivore on an invasive toxic plant

Abstract

Specialist phytophagous insects have a narrow hostplant range for optimal development and survival. Mismatches between female oviposition preference and larval performance can lead to high fitness costs. Understanding the mechanistic basis of this decoupling can help us understand evolutionary constraints and aid in predicting outcomes of error-prone oviposition. We investigated the causes for preference-performance mismatches in a specialist native herbivore laying eggs on an invasive toxic plant. Transcriptomic analyses revealed host-plant-specific gene expression signatures in larvae feeding on different plants, while there was no differential gene expression in gustatory/olfactory organs of adult females with different oviposition preferences. However, genomic analysis revealed significant genetic differentiation in several genes underlying signal transduction in adult females with different oviposition preferences. The larvae feeding on toxic plants showed lower expression of specialized detoxification enzymes and higher expression of general digestive enzymes, indicating the inability of larvae to detoxify toxic compounds present in the toxic plants. We additionally found that genes related to successful detoxification and adaptive feeding were enriched in larvae feeding on native plants, while genes related to toxic responses, apoptosis, and accelerated development were enriched in larvae feeding on toxic plants. Our findings dissect the underlying mechanisms behind a preference-performance mismatch, quantifying the impact of error-prone oviposition on larval performance in a specialized species interaction.

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Fig. 1: Differential gene expression in Pieris macdunnoughii.
Fig. 2: Transcriptional differences in larval performance on different host plants.
Fig. 3: Genetic differences underlying female oviposition on T. arvense.
Fig. 4: Enrichment analysis of COG (Clusters of Orthologs) functional categories identified by OrthoDB for genes underlying differences in Pieris macdunnoughii female oviposition preference on C. cordifolia and T. arvense.
Fig. 5

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Data availability

The raw reads used in the project are deposited at NCBI under the Bioproject accession id PRJNA1076332. The source code and associated data files are available on GitHub https://github.com/nitinra/rna_seq_pieris_preference_performance#.

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Acknowledgements

We thank M. Olson, H. Walton, E. Wagner, O. Shrestha, and S. McDaniel for assisting with animal rearing. We thank R. Steward for providing advice on differential gene expression analysis. We thank R. Steward, W. Watt, J. Quattro, B. Hollis, P. Andolfatto, and M. Asher for providing comments on earlier versions of the manuscript, and several anonymous reviewers for productive suggestions or comments on the manuscript. This work was supported by the University of South Carolina to CLB and the Rocky Mountain Biological Laboratory (RMBL) graduate student fellowship to NR. Field research permits were arranged by RMBL.

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NR and CLB designed the research. NR conducted oviposition choice experiments in 2019 and 2020. NR and CLB conducted larval preference assays in 2019, and NR conducted the assays in 2020. NR did the molecular work and analyzed the data. NR wrote the draft manuscript. NR and CLB contributed to manuscript revisions. CLB provided oversight for all stages of the work.

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Correspondence to Nitin Ravikanthachari.

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Ravikanthachari, N., Boggs, C.L. Differences in gene expression and genetic variation underlying preference-performance mismatches: insights from a specialized native herbivore on an invasive toxic plant. Heredity (2025). https://doi.org/10.1038/s41437-025-00777-7

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