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

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 PKAmediated behavioral plasticity resulting in an environmentally driven reorganization of a complex phenotype.phase change | phenotypic plasticity | Schistocerca gregaria H ow genetic information is integrated with environmental cues to control and coordinate complex phenotypes is a fundamental question in biology (1, 2). Environmental input can cause concerted changes in multiple traits to produce distinct phenotypic syndromes that are adaptive in particular conditions. Phase polyphenism in desert locusts (Schistocerca gregaria) is an extreme example. Locusts can reversibly transform between a solitarious phase and a gregarious phase that differ profoundly in morphology, physiology, and behavior (3-5). Solitarious locusts occur at low population densities and actively avoid conspecifics; they are cryptic in appearance and behavior; walk with a slow, creeping gait; and have restricted dietary preferences. The gregarious phase is characterized by increased activity and locomotion, an upright posture and gait, aposematic coloration, a broad dietary range, and, most critically, attraction to other locusts. Phase change is driven by huge changes in population density and is an adaptation to arid habitats where rains are infrequent and erratic. Transitory periods of verdure support rapid population growth, but after the rains cease, large numbers of solitarious locusts compete for...

Epigenetics and locust life phase transitions

“…Moreover, injection of serotonin (and its analogues) is sufficient to induce gregariousness in both S. gregaria and L. migratoria, whereas injecting serotonin antagonists inhibits tactile stimulation-induced phase transition (Anstey et al, 2009;Ma et al, 2011). These observations establish serotonin as an important regulatory agent in phase transition, an effect that is probably mediated through protein kinase A signalling (Ott et al, 2012). We note that other researchers report no influence on attraction/avoidance behaviour by serotonin (Tanaka and Nishide, 2013) or on darkening of hatchlings (Maeno et al, 2011) in S. gregaria.…”

Biological Mechanisms Determining the Success of RNA Interference in Insects

“…Therefore, locusts are attractive organisms for loss of function analyses, as already demonstrated in several studies (Badisco et al, 2011;He et al, 2006;Marchal et al, 2012;Ott et al, 2012;van Hoef et al, 2011;Van Wielendaele et al, 2012Wang et al, 2013;Zhao et al, 2013).…”

Toward a neurology of loneliness.

“…The fruit fly has been an attractive model due to its short lifespan and the simplicity of its neuroarchitecture. The desert locust, in contrast, has been an attractive model because of its natural ability to change from a solitary state to a gregarious state (Breuer, Hoste, & De Loof, 2003; Burrows, Rogers, & Ott, 2011; Ott & Rogers, 2010; Ott et al, 2012; Rahman et al, 2003; Rogers et al, 2004) and the problems (e.g., famine) that swarming desert locusts can cause when in the gregarious state.…”