The Role of Dopamine in the Collective Regulation of Foraging in Harvester Ants

Friedman, Daniel; Pilko, Anna; Skowronska‐Krawczyk, Dorota; Krasinska, Karolina; Parker, Jacqueline W.; Hirsh, Jay; Gordon, Deborah M.

doi:10.1016/j.isci.2018.09.001

Cited by 38 publications

(47 citation statements)

References 105 publications

(157 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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“…Future studies should focus on identifying the mechanisms by which genes function to influence collective behavior and how variation in these genes affects patterns of variation for collective behavior within populations. Candidate gene approaches have been used successfully to demonstrate the roles of the ant ortholog of the foraging gene (ppfor; Lucas & Sokolowski 2009) and dopamine (Friedman et al 2018). In addition to candidate gene approaches, future studies should utilize unbiased approaches such as quantitative trait locus (QTL) mapping in mapping populations (e.g., Hunt et al 1998;2007) such as ours, and association mapping in natural populations (e.g., Kocher et al 2018)…”

Section: Discussionmentioning

confidence: 99%

Ant collective behavior is heritable and shaped by selection

Walsh

Garnier

Linksvayer

2019

Preprint

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11Collective behaviors are widespread in nature and usually assumed to be strongly shaped 12 by natural selection. However, the degree to which variation in collective behavior is heritable 13 and has fitness consequences --the two prerequisites for evolution by natural selection --is 14 largely unknown. We used a new pharaoh ant (Monomorium pharaonis) mapping population to 15 estimate the heritability, genetic correlations, and fitness consequences of three collective 16 behaviors (foraging, aggression, and exploration) as well as body size, sex ratio, and caste ratio. 17Heritability estimates for the collective behaviors were moderate, ranging from 0.17 to 0.32, but 18 lower than our estimates for the heritability of caste ratio, sex ratio, and the body size of new 19 workers, queens, and males. Moreover, variation among colonies in collective behaviors was 20 phenotypically correlated, suggesting that selection may shape multiple colony collective 21 behaviors simultaneously. Finally, we found evidence for directional selection that was similar in 22 strength to estimates of selection in natural populations. Altogether, our study begins to elucidate 23 the genetic architecture of collective behavior and is one of the first studies to demonstrate that it 24 is shaped by selection. 25

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“…In the context of biological invasions, variation in biogenic amine pathways could be associated with the regulation of behavioural syndromes that contribute to the success of introduced species. In social insects, expression of genes associated with biogenic amines, has been suggested to be associated with variation in social behaviour, including foraging and aggression (Liang et al 2012(Liang et al , 2014Kamhi et al 2017;Friedman et al 2018). Some of these genes have been shown to exhibit genetic variation associated with behavioural syndromes (e.g.…”

Section: Introductionmentioning

confidence: 99%

Native and introduced Argentine ant populations are characterised by distinct transcriptomic signatures associated with behaviour and immunity

Felden

Paris

Chapple³

et al. 2019

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Biological invasions can be influenced by trait variation in the invader, such as behavioural traits and ecological factors, such as variation in pathogen pressure. High-throughput nucleotide sequencing has increased our capacity to investigate the genomic basis of the functional changes associated with biological invasions. Here, we used RNA-sequencing in Argentina and California, Australia and New Zealand to investigate if native and introduced Argentine ant populations were characterised by distinct transcriptomic signatures. We focused our analysis on viral pressure and immunity, as well as genes associated with biogenic amines known to modulate key behaviour in social insects. Using a combination of differential expression analysis, gene co-expression network analysis and candidate gene approach, we show that native and introduced populations have distinct transcriptomic signatures. Genes associated with biogenic amines were overall up-regulated in the native range compared to introduced populations. Although we found no significant variation in overall viral loads amongst regions for viruses known to infect Argentine ants, viral diversity was lower in most of the introduced range which was interestingly associated with down-regulation of the RNAi immune pathway, primarily directed against viruses. Altogether, our data show that Argentine ant populations exhibit range-specific transcriptomic signatures, perhaps reflecting regional adaptations that may contribute to the ecological success of introduced populations.

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The Role of Dopamine in the Collective Regulation of Foraging in Harvester Ants

Cited by 38 publications

References 105 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

Ant collective behavior is heritable and shaped by selection

Native and introduced Argentine ant populations are characterised by distinct transcriptomic signatures associated with behaviour and immunity

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