Origins of Aminergic Regulation of Behavior in Complex Insect Social Systems

Kamhi, J. Frances; Arganda, Sara; Moreau, Corrie S.; Traniello, James F. A.

doi:10.3389/fnsys.2017.00074

Cited by 74 publications

(73 citation statements)

References 142 publications

(161 reference statements)

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“…Although the effect of tyrosine enrichment in the brain is intriguing, however, undetectable level of tyrosine in the gut supports previous finding that the scavenging of toxic tyrosine from the gut is essential for the safeguard journey of blood fed mosquitoes [54]. A substantial body of literature suggests that the biogenic amines such as dopamine and serotonin are the critical regulator of feeding, host seeking and cognitive functions [3,[55][56][57][58][59]. Thus, an increase in the precursor molecules of dopamine i.e.…”

Section: Fig 4: Innate Physiological Status Differentially Modulatessupporting

confidence: 76%

Microbiome-Gut-Brain-Axis communication influences metabolic switch in the mosquitoAnopheles culicifacies

Sharma

Tevatiya

et al. 2019

Preprint

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A well coordinated neuro-olfactory regulation is essential for a successful host seeking and blood feeding behavior of adult female mosquitoes. Although, the crucial role of mosquito tiny brain during host selection/choice is of prime interest but how blood meal uptake modulate brain functions which consequently empower the cognition in mosquitoes remains unclear. Here we report that blood meal induced gut 'metabolic switch' shift brain function from external communication to inter-organ management. An exclusive induction of oxidation reduction associated proteins and enhancement of brain's energy metabolism indicate the active functioning of the brain probably to maintain physiological homeostasis. A spatial and temporal change in the expression pattern of neuro-signaling molecules and other neuro-modulators in the brain designate that a guided neuro-stimulation and endocrine regulation is enough to manage the brain-distant organ communication. Analogous to brain, significant modulation of the neuro-modulator receptor genes in the gut signifies its function as 'Second Brain' during metabolic switch in mosquitoes. Furthermore, quantitative analysis of neuro-transmitters (NTs)revealed that the gut of mosquitoes is one of the potent source of NTs during altered metabolic conditions. Finally, quantitative data on NTs dynamics of naïve and aseptic mosquitoes establish the concept of microbiome-gut-brainaxis communication in adult female mosquitoes. Graphical abstract:Introduction:Central nervous system i.e. the brain is a privileged organ in shaping animal's behavior from lower to higher taxa of which insect's tiny brain is famous for performing amazingly sophisticated behavior. Thus, insects are either enough smart to squeeze more information from limited number of neurons or they use some different algorithms to process information in their microscopic brain system [1]. In particular to mosquitoes, while navigating towards a vertebrate host for blood feeding the brain engagement of adult female mosquitoes is more complex than any other insect species [2][3][4][5]. A crucial interaction of olfactory derived odorant binding proteins (OBPs) and olfactory receptors (Ors) with the environmental guided chemical cues may have direct impact on mosquito's behavioural properties [6,7]. But how this chemical information influences decision Results & DiscussionHypothesis: Since, neuro system is a versatile centre of chemical information exchange, we hypothesize a minor change in the innate physiological status may have strong impact on mosquito's day to day life. Importantly blood meal uptake causes a drastic metabolic changes, which we named "gut metabolic switch", engages multiple organs simultaneously. We hypothesize that upon blood feeding mosquitoes' brain functions may shift from external communication to internal management such as (a) initiation of diuresis b) finding a resting site for digestion of blood meal in the midgut; (c) distribution of amino acids, generated through the degradation of protein rich blood meal; ...

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Section: Fig 4: Innate Physiological Status Differentially Modulatessupporting

confidence: 76%

Microbiome-Gut-Brain-Axis communication influences metabolic switch in the mosquitoAnopheles culicifacies

Sharma

Tevatiya

et al. 2019

Preprint

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“…In genes that now play roles in regulating worker behavior 30,105 , and conserved neuropeptides that have gained task-specific functions 32,65 . Recent evidence suggests that genetic pathways involved in generating sexually dimorphic morphology and behavior in solitary insects (e.g.…”

Section: Eusocial Colony Physiology: Hormonal Mechanisms and Evolutiomentioning

confidence: 99%

“…These predictions set a course for the integrated understanding of colony function as arising from nestmate specialization and decentralized physiological processes that have been shaped by millions of years of colony-level selection. All predictions and hypotheses should be carried out within a phylogenetic comparative framework to disentangle the relative importance of genomic, ecological, and behavioral constraints over evolutionary time 1,30,141,142 . Table 1 .…”

Section: Predictions For Eusocial Colony Physiologymentioning

confidence: 99%

Distributed physiology and the molecular basis of social life in eusocial insects

Friedman

Johnson

Linksvayer

2020

Hormones and Behavior

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The traditional focus of physiological and functional genomic research is on molecular processes that play out within a single body. In contrast, when social interactions occur, molecular and behavioral responses in interacting individuals can lead to physiological processes that are distributed across multiple individuals. In eusocial insect colonies, such multi-body processes are tightly integrated, involving social communication mechanisms that regulate the physiology of colony members. As a result, conserved physiological mechanisms, for example related to pheromone detection and neural signaling pathways, are deployed in novel contexts and regulate emergent colony traits during the evolutionary origin and elaboration of social complexity. Here we review conceptual frameworks for organismal and colony physiology, and highlight functional genomic, physiological, and behavioral research exploring how colony-level traits arise from physical and chemical interactions among nestmates. We highlight mechanistic work exploring how colony traits arise from physical and chemical interactions among physiologically-specialized nestmates of 1 various developmental stages. We consider similarities and differences between organismal and colony physiology, and make specific predictions based on a decentralized perspective on the function and evolution of colony traits. Integrated models of colony physiological function will be useful to address fundamental questions related to the evolution and ecology of collective behavior in natural systems. Colony Organization = Social Anatomy + Social PhysiologyEusocial colonial insects, such as ants, termites, and honey bees, thrive across almost all terrestrial ecosystems 1,2 . The ecological success of these species rests in their use of colony traits, such as nest architecture 3,4 and collective foraging behavior 5-7 , which are functionally absent in solitary insects yet keenly developed in eusocial taxa. In the eusocial insects, division of labor (DOL) describes how nestmates vary in their form and function. DOL formalizes the extent of specialization among nestmates in the performance of tasks, usually with a physiological or morphological basis or arising from nestmate age (temporal polyethism) and experience [8][9][10][11] . We build off of the conceptual framework of Johnson & Linksvayer 12 that considers eusocial colony organization from the perspective of social anatomy & social physiology : Social anatomy is the notion that colonies are composed of specialized parts with limited roles, like the organs of an individual animal. Specialized colony anatomy allows for greater productivity and efficiency for the completion of many tasks.Physiological specialization exists at multiple levels within the colony. Queen-worker specialization allows for an increased reproductive output of queens alongside increased work output from workers, from the same diploid female genome 13 .Subspecialization among workers can manifest as permanent variation in body morphology 14 , temporal polyet...

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“…We therefore also subjected colonies to an experimental manipulation of carbohydrate availability (high and low sugar) and octopamine (OA), both of which can influence insect behaviour. OA is a major biogenic amine in invertebrates known to influence foraging behaviour and aggression in social insects, among many other neuroactive compounds such as dopamine (Kamhi, Arganda, Moreau, & Traniello, 2017). In honeybees, the role of OA in modulating division of labour and foraging activity is well established (Schulz, Barron, & Robinson, 2002;Schulz & Robinson, 2001).…”

Section: Introductionmentioning

confidence: 99%

Behavioural variation and plasticity along an invasive ant introduction pathway

Felden

Paris

Chapple

et al. 2018

Journal of Animal Ecology

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Once established in new areas, introduced species may exhibit changes in their biology due to phenotypic plasticity, novel selection pressures and genetic drift. Moreover, the introduction process itself has been hypothesised to act as a selective filter for traits that promote invasiveness. We tested the hypothesis that behaviours thought to promote invasiveness-such as increased foraging activity and aggression-are selected for during invasion by comparing traits among native and introduced populations of the widespread Argentine ant (Linepithema humile). We studied Argentine ant populations in the native range in Argentina and in three invaded regions along an introduction pathway: California, Australia and New Zealand. In each region, we set up 32 experimental colonies to measure foraging activity and interspecific aggression in a subset of the study regions. These colonies were subject to experimental manipulation of carbohydrate availability and octopamine, a biogenic amine known to modulate behaviour in insects, to measure variation in behavioural plasticity. We found variation in foraging activity among populations, but this variation was not consistent with selection on behaviour in relation to the invasion process. We found that colonies with limited access to carbohydrates exhibited unchanged exploratory behaviour, but higher exploitation activity and lower aggression. Colonies given octopamine consistently increased foraging behaviour (both exploration and exploitation), as well as aggression when also sugar-deprived. There was no difference in the degree of behavioural response to our experimental treatments along the introduction pathway. We did not find support for selection of behavioural traits associated with invasiveness along the Argentine ant's introduction pathway or clear evidence for an association between the introduction process and variation in behavioural plasticity. These results indicate that mechanisms promote behavioural variation in a similar fashion both in native and introduced ranges. Our results challenge the assumption that introduced populations always perform better in key behavioural traits hypothesised to be associated with invasion success.

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Origins of Aminergic Regulation of Behavior in Complex Insect Social Systems

Cited by 74 publications

References 142 publications

Microbiome-Gut-Brain-Axis communication influences metabolic switch in the mosquitoAnopheles culicifacies

Microbiome-Gut-Brain-Axis communication influences metabolic switch in the mosquitoAnopheles culicifacies

Distributed physiology and the molecular basis of social life in eusocial insects

Behavioural variation and plasticity along an invasive ant introduction pathway

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