Inhibition of HSP90 causes morphological variation in the invasive ant Cardiocondyla obscurior

Abstract

Canalization underlies the expression of steady phenotypes in the face of unsteady environmental conditions or varying genetic backgrounds. The chaperone HSP90 has been identified as a key component of the molecular machinery regulating canalization and a growing body of research suggests that HSP90 could act as a general capacitator in evolution. However, empirical data about HSP90-dependent phenotypic variation and its evolutionary impact is still scarce, particularly for non-model species. Here we report how pharmacological suppression of HSP90 increases morphological variation up to 87% in the invasive ant Cardiocondyla obscurior. We show that workers treated with the HSP90 inhibitor 17-DMAG are significantly more diverse compared to untreated workers in two of four measured traits: maximal eye distance and maximal propodeal spine distance. We further find morphological differentiation between natural populations of C. obscurior in the same traits that responded to our pharmacological treatment. These findings add support for the putative impact of HSP90 on canalization, the modularity of phenotypic traits, and its potential role in morphological evolution of ants.

From egg to adult: a developmental table of the antMonomorium pharaonis

“…To date, empirical eco-evo-devo studies on ants have helped us to understand queen-worker caste differentiation (Wheeler 1986, Abouheif and Wray 2002, Sameshima et al 2004, Gotoh et al 2005, Khila and Abouheif 2008, Khila and Abouheif 2010, Miyazaki et al 2010, Penick et al 2012, Qui et al 2018, Chandra et al 2018, Nagel et al 2020, Qui et al 2022, Yan et al 2022, Trible et al 2023, epigenetic regulation (Alvarado et al 2015, LeBoeuf et al 2016, Simola et al 2016, Glastad et al 2021, Gospocic et al 2021, worker polymorphism (Wheeler and Nijhout 1981a, Wheeler and Nijhout 1981b, Klein et al 2018 , social behaviour (Teseo et al 2014, Trible et al 2017, Yan et al 2017, Glastad et al 2021, Gospocic et al 2021, Brahma et al 2023, Ju et al 2023, modularity (Yang and Abouheif 2011, Londe et al 2015, Hart et al 2024, evolutionary novelty (Rajakumar et al 2012, Favé et al 2015, Powell et al 2020, Rafiqi et al 2020, gene by environment interactions (Schrader et al 2014, Singh and Linksvayer 2020, Schrader et al 2021, ...…”

Chronic sublethal pesticide exposure affects brood production, morphology and endosymbionts, but not immunity in the ant, Cardiocondyla obscurior

“…We also saw increased variation in worker head width. Worker head size is more variable between populations of C. obscurior than other measured body parts (Schrader et al, 2021). Increased variation can result from inhibition of the HSP90 chaperone protein (Schrader et al, 2021), which is involved in canalization processes that keep the phenotype constant even under internal or external stressors (Schrader et al, 2021).…”

“…Worker head size is more variable between populations of C. obscurior than other measured body parts (Schrader et al, 2021). Increased variation can result from inhibition of the HSP90 chaperone protein (Schrader et al, 2021), which is involved in canalization processes that keep the phenotype constant even under internal or external stressors (Schrader et al, 2021). Our data suggest that stress induced by pesticide treatment may have similar effects, resulting in larger variation in worker phenotypes.…”

Morphogenetic Polyvariance in the Colonial Hydroid Dynamena pumila (L.)

“…The frequency of the manifestation of deviations from the norm in the Hsp90 mutant line was 1-2%, and the frequency of occurrence in the offspring indicated genetic fixation. The authors came to the conclusion of the existence of silent genes that predetermine abnormal morphological signs through variations in developmental pathways, using the example of a unitary [41] rather than a modular organism, in which this phenomenon would be easier to detect. The results of studies on morphovariations in the colonial hydroid D. pumila confirm this hypothesis.…”