Rapid brain development and reduced neuromodulator titres correlate with host shifts in Rhagoletis pomonella

Host shifts are considered a key generator of insect biodiversity. For insects, adaptation to new host plants often requires changes in larval/pupal development and behavioural preference towards new hosts. Neurochemicals play key roles in both development and behaviour, and therefore provide a potential source for such synchronization. Here, we correlated life history timing, brain development, and corresponding levels of 14 neurochemicals in Rhagoletis pomonella (Diptera: Tephritidae), a species undergoing ecological speciation through an ongoing host shift from hawthorn to apple fruit. These races exhibit differences in pupal diapause timing as well as adult behavioural preference with respect to their hosts. This difference in behavioural preference is coupled with differences in neurophysiological response to host volatiles. We found that apple race pupae exhibited adult brain morphogenesis three weeks faster after an identical simulated winter than the hawthorn race, which correlated with significantly lower titres of several neurochemicals. In some cases, particularly biogenic amines, differences in titres were reflected in the mature adult stage, when host preference is exhibited. In summary, life history timing, neurochemical titre, and brain development can be coupled in this speciating system, providing new hypotheses for the origins of new species through host shifts.

寄主转换（host shift）被视为昆虫生物多样性形成的关键驱动因子。对于昆虫而言，适应新寄主植物往往需要调整幼虫/蛹的发育进程，以及对新寄主的行为偏好。神经化学物质（neurochemicals）在发育与行为调控中均发挥关键作用，因此为这类协同变化提供了潜在的分子基础。本研究以苹果绕实蝇（Rhagoletis pomonella，双翅目Diptera：实蝇科Tephritidae）为研究对象，该物种正通过从山楂向苹果果实的持续寄主转换过程，经历生态物种形成（ecological speciation）。我们将该物种的生活史时序、大脑发育水平，以及14种神经化学物质的对应含量进行了关联分析。该物种的不同寄主宗在蛹滞育时序以及针对各自寄主的成虫行为偏好上均存在差异，且这种行为偏好差异与其对寄主挥发物（host volatiles）的神经生理响应差异相耦合。研究发现，在经过相同的模拟越冬处理后，苹果寄主宗的蛹发育至成虫时的大脑形态建成过程较山楂寄主宗快3周，这一现象与多种神经化学物质的滴度显著降低存在相关性。在部分神经化学物质中，尤其是生物胺（biogenic amines），其滴度差异会在成虫成熟阶段——即成虫展现寄主偏好的阶段——得以体现。综上，在这一正经历物种形成的研究体系中，生活史时序、神经化学物质滴度与大脑发育三者可实现协同调控，这为理解寄主转换驱动新物种起源的机制提供了全新假说。