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Genetic and behavioral differences between above and below ground Culex pipiens bioforms

Heredity (2024)Cite this article

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Abstract

Efficiency of mosquito-borne disease transmission is dependent upon both the preference and fidelity of mosquitoes as they seek the blood of vertebrate hosts. While mosquitoes select their blood hosts through multi-modal integration of sensory cues, host-seeking is primarily an odor-guided behavior. Differences in mosquito responses to hosts and their odors have been demonstrated to have a genetic component, but the underlying genomic architecture of these responses has yet to be fully resolved. Here, we provide the first characterization of the genomic architecture of host preference in the polymorphic mosquito species, Culex pipiens. The species exists as two morphologically identical bioforms, each with distinct avian and mammalian host preferences. Cx. pipiens females with empirically measured host responses were prepared into reduced representation DNA libraries and sequenced to identify genomic regions associated with host preference. Multiple genomic regions associated with host preference were identified on all 3 Culex chromosomes, and these genomic regions contained clusters of chemosensory genes, as expected based on work in Anopheles gambiae complex mosquitoes and in Aedes aegypti. One odorant receptor and one odorant binding protein gene showed one-to-one orthologous relationships to differentially expressed genes in A. gambiae complex members with divergent host preferences. Overall, our work identifies a distinct set of odorant receptors and odorant binding proteins that may enable Cx. pipiens females to distinguish between their vertebrate blood host species, and opens avenues for future functional studies that could measure the unique contributions of each gene to host preference phenotypes.

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Fig. 1: Posterior probability distributions for host preference of Culex pipiens females tested in a multi-day behavioral assay.
Fig. 2: Genomic variation associated with Culex pipiens population and female host preference.
Fig. 3: Manhattan plot showing the distribution of −log10(p-values) resulting from a partialRDA of 24,529 SNPs in 115 Culex pipiens females with divergent host preferences.

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Data availability

Data for this study are available at: http://www.ncbi.nlm.nih.gov/bioproject/1068091. All scripts used to perform these analyses can be found at: https://github.com/katebell1987/CulexMS1 or upon request from corresponding authors.

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Acknowledgements

We thank Mervin Keith Cuadera and Lyra Morina for assistance with mosquito rearing. Gregorio Baek and Rebecca Kaminsky assisted during preference testing. We thank Chris Nice for providing GBS adapters with unique barcodes for use in our library preparation. We thank Texas State University for use of their LEAP computing cluster. We thank Jake Tu and Maria Sharakhova for production of the chromosome-scale publicly available Cx. quinquefasciatus assembly. Rong Guo and the laboratory of Carolyn McBride manually curated the OBP and OR gene families, respectively, without which aspects of this work would not have been possible.

Funding

Funding for this work was provided by the University of Maryland Brain and Behavior Initiative and National Institutes of Health R01AI125622A to MLF. Partial support for KLB was provided by the Modelscape Consortium with funding from the National Science Foundation (OIA-2019528).

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Authors and Affiliations

  1. Department of Biology, University of Nevada, Reno, NV, 89557, USA

    Katherine L. Bell

  2. Department of Entomology, University of Maryland, College Park, MD, 20742, USA

    Anna Noreuil & Megan L. Fritz

  3. Department of Computer Science, University of Maryland, College Park, MD, 20742, USA

    Erin K. Molloy

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Contributions

KLB and MLF designed the experiments. AN and KLB conducted the multi-day behavioral assays. KLB prepared the GBS libraries, and KLB, EKM, and MLF analyzed the data. KLB and MLF wrote the manuscript. All authors reviewed and approved the final manuscript.

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Correspondence to Katherine L. Bell or Megan L. Fritz.

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Use of animal subjects for behavioral tests was approved by the University of Maryland Institutional Animal Use and Care Committee under protocol number 1094335.

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Bell, K.L., Noreuil, A., Molloy, E.K. et al. Genetic and behavioral differences between above and below ground Culex pipiens bioforms. Heredity (2024). https://doi.org/10.1038/s41437-024-00675-4

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