Gregarious desert locusts have substantially larger brains with altered proportions compared with the solitarious phase

Abstract

The behavioural demands of group living and foraging have been implicated in both evolutionary and plastic changes in brain size. Desert locusts show extreme phenotypic plasticity, allowing brain morphology to be related to very different lifestyles in one species. At low population densities, locusts occur in a solitarious phase that avoids other locusts and is cryptic in appearance and behaviour. Crowding triggers the transformation into the highly active gregarious phase, which aggregates into dense migratory swarms. We found that the brains of gregarious locusts have very different proportions and are also 30 per cent larger overall than in solitarious locusts. To address whether brain proportions change with size through nonlinear scaling (allometry), we conducted the first comprehensive major axis regression analysis of scaling relations in an insect brain. This revealed that phase differences in brain proportions arise from a combination of allometric effects and deviations from the allometric expectation (grade shifts). In consequence, gregarious locusts had a larger midbrain : optic lobe ratio, a larger central complex and a 50 per cent larger ratio of the olfactory primary calyx to the first olfactory neuropile. Solitarious locusts invest more in low-level sensory processing, having disproportionally larger primary visual and olfactory neuropiles, possibly to gain sensitivity. The larger brains of gregarious locusts prioritize higher integration, which may support the behavioural demands of generalist foraging and living in dense and highly mobile swarms dominated by intense intraspecific competition.

Opsin expression, physiological characterization and identification of photoreceptor cells in the dorsal rim area and main retina of the desert locust,Schistocerca gregaria

“…Various differences in the visual system of solitarious and gregarious locusts have been reported, including differences in eye size, number of ommatidia and sensitivity to motion stimuli (Matheson et al, 2004;Ott and Rogers, 2010;Rogers et al, 2010;Gaten et al, 2012), while polarization-sensitive interneurons were not noticeably affected by locust phase (el Jundi and Homberg, 2012). Here we show differences in photoreceptor spectral sensitivities, particularly in the ventral eye as revealed by ERG recordings and in peak wavelength of blue peaking receptors found in intracellular recordings.…”

Parasitoidism, not sociality, is associated with the evolution of elaborate mushroom bodies in the brains of hymenopteran insects

“…Instead, the y-intercepts for these measurements were significantly different (F ¼ 93.83, p , 0.0001). This suggests a grade shift in the relationship between calyx volume and lobes þ pedunculus volume [51,52], in which for a given volume of lobes þ pedunculus, euhymenopterans have a significantly larger calyx, reflective of the expanded cup-shaped calyx morphology in these species.…”

Epigenetics and locust life phase transitions

“…Long-term gregarious desert locusts have a smaller body size, but their brain is substantially largerabout 30% -than that of long-term solitarious locusts (Ott and Rogers, 2010). In addition, Ott and Rogers reported that the relative distribution of brain regions differs between the two phases.…”

“…Solitarious locusts invest more in lower level sensory processing, reflected by their relatively large primary olfactory and visual neuropils. In contrast, the larger brains of gregarious locusts are more dedicated to the integration of sensory cues in higher level processing regions, which is thought to support their lifestyle as generalist foragers in dense, migratory swarms where competition among group members is high (Ott and Rogers, 2010). Other changes in brain functioning situate at the level of circuit activity and function (Ayali et al, 2004; Blackburn et al, 2010; Burrows et al, 2011;Fuchs et al, 2003).…”