An HSP90-regulated reduced-eye phenotype in Tribolium shows fitness benefits and thus provides evidence for evolutionary capacitance

Abstract

Evolution relies on genetic variation as the raw material for adaptation. The release of cryptic genetic variation (CGV), which can be regulated by the evolutionary capacitor heat shock protein 90 (HSP90), may thus be important for rapid adaptation. However, the fitness benefits of HSP90regulated phenotypes are still under debate. Here, we show in the important model insect Tribolium 5 castaneum that HSP90 impairment by two independent methods, RNA interference and chemical inhibition, revealed the same reduced-eye phenotype, which was stably inherited without further HSP90 inhibition. The penetrance and fitness of this trait increased under ambient light stress. This is the first demonstration that a phenotype released through HSP90 inhibition can be adaptive. 10 15 temporarily constrained (Flatt, 2005; Rohner et al., 2013; Sangster et al., 2008a). However, the availability of HSP90 may become limited, for example under stressful environmental situations, when HSP90 is needed as a chaperone by many proteins (Borkovich et al., 1989; Chen and Wagner, 2012; Peuss et al., 2015). Under such conditions, stored genetic variation is released, expressed as phenotypic differences, and selection can act on it. Therefore, HSP90 could be a 20 molecular mechanism underpinning the de-canalization and potential subsequent assimilation of traits (Queitsch et al.a., Klingler M. 2009. The red flour beetle, Tribolium castaneum (Coleoptera): A model for studies of development and pest biology.

Capturing the facets of evolvability in a mechanistic framework

“…Chaperoning can shield sequence mutations from selection, thus maintaining variation. This can later be released under stressful conditions [28,29]. Developmental canalization can affect evolvability in a similar manner, in that it allows the accumulation of cryptic genetic variation [30].…”