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PNAS 109 (7): 381-387

Copyright © 2012 by the National Academy of Sciences.

PNAS Plus


PNAS PLUS / BIOLOGICAL SCIENCES / AGRICULTURAL SCIENCES

Critical role for protein kinase A in the acquisition of gregarious behavior in the desert locust

Swidbert R. Otta,1,2, Heleen Verlindenb,1, Stephen M. Rogersa, Caroline H. Brightona, Pei Shan Quaha, Rut K. Vleugelsb, Rik Verdoncka,b, and Jozef Vanden Broeckb

aDepartment of Zoology, University of Cambridge, Cambridge CB2 3EJ, United Kingdom; and bDivision of Animal Physiology and Neurobiology, Zoological Institute, Katholieke Universiteit Leuven, B-3000 Leuven, Belgium

2To whom correspondence should be addressed. E-mail: s.r.ott{at}cantab.net.

Abstract: The mechanisms that integrate genetic and environmental information to coordinate the expression of complex phenotypes are little understood. We investigated the role of two protein kinases (PKs) in the population density-dependent transition to gregarious behavior that underlies swarm formation in desert locusts: the foraging gene product, a cGMP-dependent PK (PKG) implicated in switching between alternative group-related behaviors in several animal species; and cAMP-dependent PK (PKA), a signal transduction protein with a preeminent role in different forms of learning. Solitarious locusts acquire key behavioral characters of the swarming gregarious phase within just 1 to 4 h of forced crowding. Injecting the PKA inhibitor KT5720 before crowding prevented this transition, whereas injecting KT5823, an inhibitor of PKG, did not. Neither drug altered the behavior of long-term gregarious locusts. RNAi against foraging effectively reduced its expression in the central nervous system, but this did not prevent gregarization upon crowding. By contrast, solitarious locusts with an RNAi-induced reduction in PKA catalytic subunit C1 expression behaved less gregariously after crowding, and RNAi against the inhibitory R1 subunit promoted more extensive gregarization following a brief crowding period. A central role of PKA is congruent with the recent discovery that serotonin mediates gregarization in locusts and with findings in vertebrates that similarly implicate PKA in the capacity to cope with adverse life events. Our results show that PKA has been coopted into effecting the wide-ranging transformation from solitarious to gregarious behavior, with PKA-mediated behavioral plasticity resulting in an environmentally driven reorganization of a complex phenotype.

Key Words: phase change • phenotypic plasticity • Schistocerca gregaria


 

Freely available online through the PNAS open access option.

The authors declare no conflict of interest.

This article is a PNAS Direct Submission.

Data deposition: The sequences reported in this paper have been deposited in the GenBank database [accession nos. HM363020 (foraging), HM363018 (pkac1), and HM363019 (pkar1)].

See full research article on page E381 of www.pnas.org.

Cite this Author Summary as: PNAS 10.1073/pnas.1114990109.



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