Manipulation of insulin signaling phenocopies evolution of a host-associated polyphenism

Abstract

Plasticity, the capacity of an organism to respond to its environment, is thought to evolve through changes in development altering the integration of environmental cues. In polyphenism, a discontinuous plastic response produces two or more phenotypic morphs. Here we describe evolutionary change in wing polyphenism and its underlying developmental regulation in natural populations of the red-shouldered soapberry bug, Jadera haematoloma (Insecta: Hemiptera: Rhopalidae) that have adapted to a novel host plant. We find differences in the fecundity of morphs in both sexes and in adult expression of insulin signaling components in the gonads. Further, the plastic response of ancestral-state bugs can be shifted to resemble the reaction norm of derived bugs by the introduction of exogenous insulin or RNA interference targeting the insulin signaling component encoded by FoxO. These results suggest that insulin signaling may be one pathway involved in the evolution of this polyphenism, allowing adaptation to a novel nutritional environment.

Insulin signalling's role in mediating tissue-specific nutritional plasticity and robustness in the horn-polyphenic beetleOnthophagus taurus

“…In conclusion, our results suggest that in the hornpolyphenic beetle O. taurus, both nutrition sensitivity and insensitivity may be regulated by diverse components of the IIS pathway and their interactions with dsx and Hh signalling across different body parts. The growing number of studies implicating diverse IIS components in both hemiand holometabolous insects supports the hypothesis that this pathway may be a hotspot for the evolution of nutrient-sensitive trait growth [5,18,19], including, as suggested by the results of this study, the evolutionary transition from linear to strongly sigmoidal allometries. However, the specific components of IIS and their interactions with other pathways (e.g.…”

“…By contrast, scarabaeine beetles may use the insulin receptor only to facilitate nutrition-insensitive growth of male genitalia and instead use Foxo-mediated differential inhibition in both horns and genitalia to enable different types of nutrition-responsive growth-polyphenic in the case of horns and largely nutritionally insensitive in the case of genitalia. A partly similar scenario appears to emerge from recent findings in hemipterans: while two InR paralogues are involved in the regulation of alternative wing polyphenic morphs in the planthopper N. lugens, evolutionary changes in Foxo function seem to underlie divergences in wing polyphenisms between populations of the soapberry bug J. haematoloma [18,19]. Our results thus generally support the broader significance of IIS in the evolutionary diversification of nutrition-responsive growth, but may call into question the claim that conserved insulin signalling is a universal mechanism of simple trait exaggeration.…”

“…25), but show that this discrepancy declines in Foxo RNAi males owing to both a reduction in fit of the sigmoidal model (AIC sigmoid ¼ 61. 19) and a commensurate increase in the linear model's fit (AIC linear ¼ 95. 15).…”

“…Furthermore, what role the IIS plays in the regulation of more complex scaling relationships such as polyphenisms is starting to be elucidated in hemipterans. Recent studies have shown that two InR paralogues are involved in the regulation of winged versus wingless morphs in the planthopper Nilaparvata lugens [18], whereas quantitative changes in Foxo function may be underlying the recent evolution of a novel reaction norm in the soapberry bug Jadera haematoloma [19]. These findings raise the possibility that this pathway may be a hotspot for the evolution of discontinuous and differentially responsive, nutrient-responsive organ growth [19].…”

“…Recent studies have shown that two InR paralogues are involved in the regulation of winged versus wingless morphs in the planthopper Nilaparvata lugens [18], whereas quantitative changes in Foxo function may be underlying the recent evolution of a novel reaction norm in the soapberry bug Jadera haematoloma [19]. These findings raise the possibility that this pathway may be a hotspot for the evolution of discontinuous and differentially responsive, nutrient-responsive organ growth [19]. Here, we use the polyphenic horned beetle Onthophagus taurus to investigate the role of IIS signalling in the development and evolution of extreme levels of nutritional responsiveness (horns) and robustness (genitalia).…”