Impaired humidity sensing reduces tick survival by preventing water homeostasis

Authors: UHRAN, MELISSA - University Of Cincinnati; ONYEAGBA, KOSISOCHUKWU - University Of Cincinnati; SANDERSON, SHANIA - Old Dominion University; HOUQE, SYEDA - University Of Cincinnati; KELLEY, MELISSA - University Of Cincinnati; SMITH, EVAN - University Of Cincinnati; Oyen, Kennan; LEWIS, DAVID - University Of Cincinnati; BENTON-ANDERSON, AYESHA - University Of Cincinnati; ARYA, THOMAS - University Of Cincinnati; LEDEZMA, ARTURO - University Of Cincinnati; KENNEDY, JASMINE - University Of Cincinnati; FRIGARD, RONJA - University Of Cincinnati; CHEN, SHYH-CHI - University Of Cincinnati; Olafson, Pia; GAFF, HOLLY - Old Dominion University; BENOIT, JOSHUA - University Of Cincinnati

Submitted to: bioRxiv
Publication Type: Other
Publication Acceptance Date: 11/6/2024
Publication Date: 11/7/2024
Citation: Uhran, M.R., Onyeagba, K., Sanderson, S.M., Houqe, S.F., Kelley, M., Smith, E., Oyen, K.J., Lewis, D.L., Benton-Anderson, A., Arya, T., Ledezma, A., Kennedy, J., Frigard, R., Chen, S., Olafson, P.U., Gaff, H.D., Benoit, J.B. 2024. Impaired humidity sensing reduces tick survival by preventing water homeostasis. bioRxiv. https://doi.org/10.1101/2024.11.06.618166.
DOI: https://doi.org/10.1101/2024.11.06.618166

Interpretive Summary: Off-host periods are critical for ticks, representing a period when environmental stress, particularly dehydration, can impact tick survival. To prevent dehydration, ticks must be able to detect and move into high humidity areas to allow for water vapor uptake. Although the Haller's organ is suggested as the site of humidity detection in ticks, humidity detection has not been extensively examined. Here, we assessed the ability of ticks to sense humidity and how altered humidity detection impacts tick survival by manipulating the Haller’s organ. Permanent (cutting or heat ablation) or temporary blocking (silicone covering) of the Haller’s organ impairs the ability of the American dog tick to rest in areas necessary to maintain hydration. Impaired detection of humidity did not impact tick survival when individuals were held under stable optimal conditions. Still, variable conditions (low and high humidity gradient) reduced survival through dehydration stress and decreased energy reserves, as chronic water vapor uptake is energetically expensive. Field validation of these studies in the American dog tick confirmed that humidity detection is critical to tick survival. Lastly, modeling indicates impaired humidity detection will reduce questing tick populations, specifically in the adult stages. These studies confirm that the Haller’s organ is critical for humidity sensing in ticks. Without this ability, tick survival will be impaired by potential dehydration or more rapid depletion of energy reserves.

Technical Abstract: Off-host periods are critical for ticks, representing a period when environmental stress, particularly dehydration, can impact tick survival. To prevent dehydration, ticks must be able to detect and move into high humidity areas to allow for water vapor uptake. Ionotropic receptor 93a (Ir93a), which is highly expressed in the front forelegs (location of Haller’s organ), increases expression following dehydration, suggesting a role in humidity detection. Although the Haller's organ is suggested as the site of humidity detection in ticks, humidity detection has not been extensively examined. Here, we assessed the ability of ticks to sense humidity and how altered humidity detection impacts tick survival by manipulating the Haller’s organ. Permanent (cutting or heat ablation) or temporary blocking (silicone covering) of the Haller’s organ impairs the ability of the American dog tick, Dermacentor variabilis, to rest in areas necessary to maintain hydration. Impaired detection of humidity did not impact tick survival when individuals were held under stable optimal conditions. Still, variable conditions (low and high humidity gradient) reduced survival through dehydration stress and decreased energy reserves, as chronic water vapor uptake is energetically expensive. Field validation of these studies in D. variabilis confirmed that humidity detection is critical to tick survival. Lastly, modeling indicates impaired humidity detection will reduce questing tick populations, specifically in the adult stages. These studies confirm that the Haller’s organ is critical for humidity sensing in ticks. Without this ability, tick survival will be impaired by potential dehydration or more rapid depletion of energy reserves.