Skip to main content
Advertisement

Main menu

  • Home
  • Articles
    • Accepted manuscripts
    • Issue in progress
    • Latest complete issue
    • Issue archive
    • Archive by article type
    • Special issues
    • Subject collections
    • Interviews
    • Sign up for alerts
  • About us
    • About JEB
    • Editors and Board
    • Editor biographies
    • Travelling Fellowships
    • Grants and funding
    • Journal Meetings
    • Workshops
    • The Company of Biologists
    • Journal news
  • For authors
    • Submit a manuscript
    • Aims and scope
    • Presubmission enquiries
    • Article types
    • Manuscript preparation
    • Cover suggestions
    • Editorial process
    • Promoting your paper
    • Open Access
    • Outstanding paper prize
    • Biology Open transfer
  • Journal info
    • Journal policies
    • Rights and permissions
    • Media policies
    • Reviewer guide
    • Sign up for alerts
  • Contacts
    • Contact JEB
    • Subscriptions
    • Advertising
    • Feedback
  • COB
    • About The Company of Biologists
    • Development
    • Journal of Cell Science
    • Journal of Experimental Biology
    • Disease Models & Mechanisms
    • Biology Open

User menu

  • Log in

Search

  • Advanced search
Journal of Experimental Biology
  • COB
    • About The Company of Biologists
    • Development
    • Journal of Cell Science
    • Journal of Experimental Biology
    • Disease Models & Mechanisms
    • Biology Open

supporting biologistsinspiring biology

Journal of Experimental Biology

  • Log in
Advanced search

RSS  Twitter  Facebook  YouTube  

  • Home
  • Articles
    • Accepted manuscripts
    • Issue in progress
    • Latest complete issue
    • Issue archive
    • Archive by article type
    • Special issues
    • Subject collections
    • Interviews
    • Sign up for alerts
  • About us
    • About JEB
    • Editors and Board
    • Editor biographies
    • Travelling Fellowships
    • Grants and funding
    • Journal Meetings
    • Workshops
    • The Company of Biologists
    • Journal news
  • For authors
    • Submit a manuscript
    • Aims and scope
    • Presubmission enquiries
    • Article types
    • Manuscript preparation
    • Cover suggestions
    • Editorial process
    • Promoting your paper
    • Open Access
    • Outstanding paper prize
    • Biology Open transfer
  • Journal info
    • Journal policies
    • Rights and permissions
    • Media policies
    • Reviewer guide
    • Sign up for alerts
  • Contacts
    • Contact JEB
    • Subscriptions
    • Advertising
    • Feedback
COMMENTARY
The stalk-eyed fly as a model for aggression – is there a conserved role for 5-HT between vertebrates and invertebrates?
Andrew N. Bubak, Michael J. Watt, Jazmine D. W. Yaeger, Kenneth J. Renner, John G. Swallow
Journal of Experimental Biology 2020 223: jeb132159 doi: 10.1242/jeb.132159 Published 2 January 2020
Andrew N. Bubak
1Department of Neurology, University of Colorado School of Medicine, Aurora, CO 80045, USA
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
Michael J. Watt
2Department of Anatomy, University of Otago, Dunedin 9016, New Zealand
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
Jazmine D. W. Yaeger
3Department of Biology, University of South Dakota, Vermillion, SD 57069, USA
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
Kenneth J. Renner
3Department of Biology, University of South Dakota, Vermillion, SD 57069, USA
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
John G. Swallow
4Department of Integrative Biology, University of Colorado-Denver, Denver, CO 80217, USA
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
  • ORCID record for John G. Swallow
  • For correspondence: john.swallow@ucdenver.edu
  • Article
  • Figures & tables
  • Supp info
  • Info & metrics
  • PDF + SI
  • PDF
Loading

ABSTRACT

Serotonin (5-HT) has largely been accepted to be inhibitory to vertebrate aggression, whereas an opposing stimulatory role has been proposed for invertebrates. Herein, we argue that critical gaps in our understanding of the nuanced role of 5-HT in invertebrate systems drove this conclusion prematurely, and that emerging data suggest a previously unrecognized level of phylogenetic conservation with respect to neurochemical mechanisms regulating the expression of aggressive behaviors. This is especially apparent when considering the interplay among factors governing 5-HT activity, many of which share functional homology across taxa. We discuss recent findings using insect models, with an emphasis on the stalk-eyed fly, to demonstrate how particular 5-HT receptor subtypes mediate the intensity of aggression with respect to discrete stages of the interaction (initiation, escalation and termination), which mirrors the complex behavioral regulation currently recognized in vertebrates. Further similarities emerge when considering the contribution of neuropeptides, which interact with 5-HT to ultimately determine contest progression and outcome. Relative to knowledge in vertebrates, much less is known about the function of 5-HT receptors and neuropeptides in invertebrate aggression, particularly with respect to sex, species and context, prompting the need for further studies. Our Commentary highlights the need to consider multiple factors when determining potential taxonomic differences, and raises the possibility of more similarities than differences between vertebrates and invertebrates with regard to the modulatory effect of 5-HT on aggression.

Introduction

Aggressive behavior is ubiquitous for gaining access to desirable resources such as territory, food and mates (Edwards and Herberholz, 2005; Summers et al., 2005a,b), and hence aggression is critical for determining individual fitness. However, fighting is energetically costly and potentially injurious. As a consequence, diverse species have evolved signaling strategies during aggressive encounters with conspecifics to minimize physical engagement, often comprising elaborate displays incorporating various morphological ornaments and armaments. Across the majority of animal taxa, the ability to modulate aggressive responses appears to be governed by monoaminergic activity (Alekseyenko et al., 2013; Hoopfer, 2016; Rillich and Stevenson, 2014; Zhou et al., 2008), with serotonin (5-hydroxytryptamine, 5-HT) playing a key role (Bubak et al., 2015; Takahashi et al., 2012). In stalk-eyed flies, 5-HT appears to mediate appropriate behavioral responses upon perception of aggressive signals (Bubak et al., 2014a).

5-HT, 5-HT receptor structure and function, and the 5-HT transporter (SERT), which removes 5-HT from the synaptic cleft to terminate 5-HT signaling (Fig. 1), are phylogenetically conserved (Blenau and Baumann, 2001; Martin and Krantz, 2014). Despite this, 5-HT appears to play generally opposing roles in the generation of the complex behaviors associated with aggression in invertebrates and vertebrates (see Table S1). However, we propose that this seemingly contrasting role of 5-HT may be an overly simplistic generalization. In this Commentary, we will briefly outline the known functions of serotonergic signaling in aggression across invertebrates and vertebrates (for more comprehensive reviews, see Alekseyenko and Kravitz, 2015; de Boer et al., 2016; Takahashi et al., 2012), combined with findings from our stalk-eyed fly model (Box 1), to demonstrate that 5-HT plays a much more nuanced role when factors such as receptor subtype, other neuromodulators and specific phases within aggressive interactions are taken into consideration. The emerging picture suggests that the serotonergic mechanisms governing invertebrate aggression may be more reminiscent of those of vertebrates than previously thought.

Fig. 1.
  • Download figure
  • Open in new tab
  • Download powerpoint
Fig. 1.

A representative serotonin (5-HT) neuron and synapse. The figure shows predominant cellular locations of 5-HT receptors discussed in the text (5-HT1, 5-HT2 and 5-HT7), with their net effect on cellular activity denoted as excitatory (+) or inhibitory (−). The amino acid tryptophan is hydroxylated into 5-hydroxytryptophan (5-HTP), which then undergoes decarboxylation to produce serotonin (5-hydroxytryptamine, 5-HT). Once released, 5-HT can negatively modulate postsynaptic neurotransmission by binding to Gi-coupled 5-HT1A receptors, which inhibit adenylyl cyclase (AC) to restrict the production of cyclic AMP (cAMP) and dampen protein kinase A (PKA) activity. Excitatory postsynaptic effects can be mediated either by Gs-coupled 5-HT7 receptors (activate AC) or Gq/11-coupled 5-HT2A or 5-HT2C receptors that activate the phospholipase C (PLC)/inositol 1,4,5-trisphosphate (IP3)/diacylglycerol (DAG) pathway to increase cytosolic calcium (Ca2+) and stimulate protein kinase C (PKC). Presynaptic 5-HT1B (5-HT1D in humans) receptors located on 5-HT terminals are also Gi coupled, and serve as autoreceptors to limit further 5-HT release by closing Ca2+ channels and preventing docking of vesicles at the synaptic membrane. Note that 5-HT1B receptors can also be located on non-5-HT terminals, where they can act as heteroreceptors to similarly inhibit release of other neurotransmitters. The 5-HT transporter (SERT) takes 5-HT back up into the terminal, where it can be repackaged into vesicles for future use, and so plays a key role in regulating the duration of presynaptic or postsynaptic receptor activation by controlling extracellular 5-HT availability. Activation of somatodendritic 5-HT1A autoreceptors by 5-HT release at the level of the cell body inhibits neuronal firing by opening inwardly rectifying potassium (K+) channels, providing another mechanism to determine the amount of 5-HT released in terminal fields. For further reading, see Aggarwal and Mortensen (2017), Masson et al. (2012) and Sari (2004).

Box 1. The stalk-eyed fly as a model for aggression

Embedded Image

Stalk-eyed flies (Diptera; Diopsidae) provide an ideal model to study aggression, from both a neurophysiological and an evolutionary perspective. All species have eye bulbs displaced on the ends of eye stalks that serve as ornamental signals in both intrasexual and intersexual interactions (Wilkinson and Dodson, 1997; Wilkinson and Johns, 2005). In sexually dimorphic species, such as Teleopsis dalmanni, females prefer males with longer eye spans (Wilkinson et al., 1998; Burkhardt and de la Motte, 1988): (A) male and female T. dalmanni copulating (photo credit: Amy Worthington). Furthermore, males with larger eyespans typically win contests for food and mates (Lorch et al., 1993; Panhuis and Wilkinson, 1999; Egge et al., 2011): (B) males of the sexually dimorphic Teleopsis pallifacies fighting (photo credit: Jerry Wilkinson).

Like many species in the family, male T. dalmanni use eye stalks to both convey and assess aggressive intent in interactions with rivals. A contest typically comprises three distinct sequential stages: (1) initiation – one individual approaches the other, initiating the fight (de la Motte and Burkhardt, 1983; Panhuis and Wilkinson, 1999); (2) escalation – opponents line up their eyestalks, which appears to be mutual assessment (Bubak et al., 2016a; but see Brandt and Swallow, 2009), followed by low-intensity posturing behaviors that can escalate to higher-intensity physical contact exchanges; and (3) termination – one rival capitulates and retreats (Egge et al., 2011). Female T. dalmanni also engage in intrasexual contests, but at lower intensity, rarely escalating to high-intensity behaviors (Bath et al., 2015).

The easily characterized and quantifiable aggressive interactions in stalk-eyed flies provide a useful model to uncover proximate neurobiological mechanisms governing individual and sex differences in behavioral expression. By combining behavioral measurements with pharmacological treatments, measurements of brain neurochemistry and manipulations of endogenous 5-HT receptor subtypes in the stalk-eyed fly, we can test hypotheses relating to the role of 5-HT in modulating aggression in insects, and compare these results with findings from other taxa (Bubak et al., 2013; Bubak et al., 2019).

The role of 5-HT in vertebrate and invertebrate aggression

In most vertebrates, 5-HT is largely viewed as an inhibitory neuromodulator of aggression (Carrillo et al., 2009; de Almeida et al., 2015; Nelson and Chiavegatto, 2001; Summers et al., 2005a; but see de Boer et al., 2015, 2016). This interpretation is principally based upon studies showing that reductions in 5-HT in vertebrates typically increase aggression (Table S1; Audero et al., 2013; Caramaschi et al., 2008; Cervantes and Delville, 2007; Mosienko et al., 2012; Perez-Rodriguez et al., 2010). Conversely, augmenting 5-HT availability, through either dietary supplementation or reducing SERT-mediated 5-HT clearance, suppresses aggression (Höglund et al., 2005; Holmes et al., 2002).

In contrast to the effect in vertebrates, most studies suggest 5-HT increases aggression in invertebrates (Table S1). Acute 5-HT injection into the hemolymph of crustaceans induces subordinate males to re-engage in confrontations with dominant opponents while decreasing their willingness to retreat (Antonsen and Paul, 1997; Huber et al., 1997; Livingstone et al., 1980; Panksepp et al., 2003), and, in some species, increases the probability of winning a fight (Momohara et al., 2013). Retention of dominant status in crayfish is also enhanced by increasing synaptic 5-HT through SERT blockade (Huber et al., 1997; Momohara et al., 2013; Panksepp and Huber, 2002). However, the role of 5-HT is likely to be more complex than a simple enhancement of aggressive behavior. In paired fights with a size discrepancy between opponents, injection of 5-HT increases aggression in smaller crayfish while decreasing aggression in larger animals, suggesting that, as in vertebrates (Blanchard and Meyza, 2019), 5-HT may alter risk assessment (Bacqué-Cazenave et al., 2018). Manipulations that elevate 5-HT tend to increase aggression in several insect species (Alekseyenko et al., 2010; Bubak et al., 2014b; Dierick and Greenspan, 2007; Dyakonova and Krushinsky, 2013; Kostowski and Tarchalska, 1972; Szczuka et al., 2013). These studies, in which 5-HT is experimentally increased just prior to a conflict, may be consistent with the rapid and transient increase in endogenous 5-HT observed in highly aggressive individuals during vertebrate interactions (de Boer et al., 2015; Matter et al., 1998; Summers et al., 2005a; Takahashi et al., 2012). In contrast to findings in vertebrates, decreasing 5-HT function prior to interaction does not appear to affect subsequent expression of aggressive behavior in either male Drosophila or male crickets (Dierick and Greenspan, 2007; Rillich and Stevenson, 2018; Stevenson et al., 2000), suggesting 5-HT is permissive but not essential for invertebrate aggression.

Caveats in understanding invertebrate 5-HT and aggression

There are a number of caveats that are problematic with respect to our understanding of the role of 5-HT in invertebrate aggression. First, although the 5-HT–aggression relationship has been well studied in a range of vertebrate models (de Boer et al., 2015, 2016; Table S1), relatively little attention has been paid to the role of 5-HT in aggression in invertebrates other than arthropods (but see Edsinger and Dölen, 2018). A second issue involves assessing behavioral changes following systemic injection of 5-HT. Insects and crustaceans have a hemolymph–blood barrier (HBB) that is functionally analogous to the vertebrate blood–brain barrier (Otopalik et al., 2012; Schirmeier and Klämbt, 2015), which should prevent diffusion of 5-HT from the hemolymph to the brain. However, systemic administration of 5-HT clearly influences aggression in lobsters (Antonsen and Paul, 1997; Bacqué-Cazenave et al., 2018; Huber et al., 1997; Momohara et al., 2013; Peeke et al., 2000) and ants (Kostowski and Tarchalska, 1972; Szczuka et al., 2013), suggesting that effects are modulated by mechanisms outside the brain, or that the invertebrate HBB is permeable to monoamines. The latter possibility is suggested by data from our laboratory showing that, in mantis shrimp (Neogonodactylus oerstedii), systemic dopamine and 5-HT both cross the HBB (K.J.R., unpublished results), and from studies indicating that systemically administered dopamine can directly alter nervous system development and locomotion in Drosophila larvae (Budnik et al., 1989; Wakabayashi-Ito et al., 2011). Thus, results obtained by systemically injecting 5-HT do not rule out potential confounds from neurohormonal or negative feedback effects rather than direct effects on the brain. Third, some vertebrate studies suggest that the degree to which 5-HT affects aggression may depend on individual social status established after repeated interactions. For example, aggression-reducing effects of elevating 5-HT in male lizards are only seen in dominant males (Summers et al., 2005b), and in hamsters and some teleost fish, 5-HT is associated with the acquisition and maintenance of subordinate status (Harvey et al., 2012; Backström and Winberg, 2017). Although differential actions of 5-HT following repeated fights and social status have been noted in crayfish (Huber et al., 1997) and male crickets (Rillich and Stevenson, 2018), the majority of invertebrate studies only utilize single interactions between unfamiliar opponents. Finally, most work on vertebrate aggression has focused on males, although there is some evidence suggesting 5-HT may increase or have minimal effects on aggression in female rodents (see Table S1; de Boer and Newman-Tancredi, 2016; Joppa et al., 1997; Terranova et al., 2016; Villalba et al., 1997; but see Heiming et al., 2013; Kästner et al., 2019). Even less is known about the role of 5-HT in female invertebrate aggression. Thus, there is a clear need for further studies using multiple species before conclusions about the activational or sex-specific role of 5-HT in aggression across invertebrates can be drawn. Such knowledge is crucial for understanding not only how individual or sex-specific aggression can be discretely modulated by 5-HT activity but also why functional homologies or differences in such a conserved neurotransmitter system would have evolved across vertebrates and invertebrates.

5-HT receptor subtypes and aggression

In vertebrates, progress has been made in understanding how 5-HT modulates aggression through differential binding of specific 5-HT receptors, with 5-HT1A, 5-HT1B, 5-HT2 and 5-HT3 subtypes being involved (Box 2; Juárez et al., 2013; Morrison et al., 2015; Popova et al., 2010; Takahashi et al., 2012). In general, systemic activation of each subtype dampens vertebrate aggression, but the opposite effect can be induced in mammals when these receptors are activated either in specific brain regions or during certain contexts such as maternal aggression or self-defense (de Almeida and Lucion, 1997; Takahashi et al., 2012). In contrast, the contribution of 5-HT receptor subtypes to invertebrate aggression is not as well understood. Of the seven known 5-HT receptor families in mammals, three (5-HT1, 5-HT2 and 5-HT7) have been described with notable sequence and functional homology in insects (Box 3; Tierney, 2018; Vleugels et al., 2013). As in vertebrates, adenylate cyclase activity and cAMP production are decreased by Gi-coupled 5-HT1-like receptors but increased by Gs-coupled 5-HT7-like receptors to exert inhibitory and excitatory effects, respectively, whereas excitatory 5-HT2-like receptors function through Gq proteins to stimulate phospholipase C and subsequently increase Ca2+ (Tierney, 2018; Fig. 1).

Box 2. Regulation of vertebrate aggression circuitry through serotonergic signaling

Embedded Image

(A) In rodents, aggression requires sensory activation of glutamatergic mitral cells of the main (MOB) and accessory olfactory bulbs (AOB) (Mandiyan et al., 2005; Stowers et al., 2002). This is enhanced by 5-HT2A binding in the MOB but dampened by 5-HT1A/B signaling in the AOB, whereas 5-HT2C receptor excitation of GABAergic interneurons inhibits both pathways (Huang et al., 2017). Net effects on cellular activity are denoted as excitatory (+) or inhibitory (−). (B) Excitatory olfactory bulb (OB) output is received by AMPA and NMDA receptors located on aggression-promoting GABAergic neurons in the posterior dorsal (pd) medial amygdala (MeA) that project to the hypothalamus (Hyp) (Hong et al., 2014). Anti-aggressive effects of 5-HT in the MeA (Puciłowski et al., 1985) may be mediated via 5-HT2A/C receptors on GABAergic interneurons (Asan et al., 2013) to inhibit MeA output. MeApd cells also contain aromatase (which converts testosterone to estrogen), and via androgen (AR) and estrogen receptors (ER) these steroids may have an organizational effect during puberty to dampen 5-HT signaling in the adult MeA and promote aggression (Grimes and Melloni, 2002; Puciłowski et al., 1985). Similarly, these steroids regulate activity of excitatory V1 vasopressin (AVP) receptors that enhance aggression (Koolhaas et al., 1990; Murakami et al., 2011). (C) In the anterior hypothalamus (ANH), V1 receptors promote aggression, which is countered by 5-HT1A binding (Ferris et al., 1997, 1999). The ventromedial hypothalamus (VMH) receives inhibitory projections from the ANH (Lo et al., 2019) and MeA (Canteras et al., 1995), which target GABAergic interneurons to disinhibit VMH output to the periaqueductal gray (PAG) and increase aggression (Lin et al., 2011). (D) In the cat PAG, 5-HT promotes or suppresses reactive aggression via 5-HT2C and 5-HT1A receptors, respectively (Shaikh et al., 1997). In contrast, both of these receptors in the PAG suppress maternal aggression in rats (de Almeida and Lucion, 1997; de Almeida et al., 2005). (E) Aggression decreases upon activation of inhibitory somatodendritic 5-HT1A autoreceptors (de Boer and Newman-Tancredi, 2016), suggesting the transient 5-HT increase seen at the initiation of aggression in many vertebrates is mediated by negative feedback at the dorsal raphe.

Box 3. Regulation of invertebrate aggression circuitry through serotonergic signaling

Embedded Image

(A) In Drosophila, male aggression is prompted by male pheromone activation of cholinergic olfactory receptor neurons (ORNs; Wang and Anderson, 2010), which is enhanced by 5-HT2B receptor binding (Sizemore and Dacks, 2016). Net effects on cellular activity are denoted as excitatory (+) or inhibitory (−). (B) Olfactory signals are processed by the antennal lobes (ALs), which comprise interconnected projection neurons (PNs) and local interneurons, most of which express different 5-HT receptor subtypes specific to neuronal type. Activation of excitatory cholinergic PNs by ORN afferents (Barbara et al., 2005) is enhanced by 5-HT2A and 5-HT7 receptors, whereas stimulation of inhibitory GABAergic PNs is dampened by 5-HT1A and 5-HT1B receptors (Sizemore and Dacks, 2016). Local inhibition of PNs and ORN terminals is provided by GABAergic and peptidergic [tachykinin (Tk) and myoinhibitory peptide (MIP)] interneurons (Bicker, 1999; Ignell et al., 2009). Peptidergic interneurons only express 5-HT1-type receptors (Sizemore and Dacks, 2016), and so are suppressed by 5-HT. In contrast, GABAergic interneurons express a combination of 5-HT1, 5-HT2 and 5-HT7 receptors (Sizemore and Dacks, 2016). In this manner, 5-HT can fine-tune AL output through both direct (stimulation/inhibition of PNs) and indirect (feedforward inhibition and disinhibition of PNs by interneurons) actions. (C) The AL targets the posterior lateral protocerebrum (PLP) (Tanaka et al., 2012), which contains densely arborized 5-HT neurons specifically implicated in male aggression (Alekseyenko et al., 2014) that may be modulated by incoming olfactory and visual information (Otsuna and Ito, 2006; Tanaka et al., 2012). (D) PLP 5-HT afferents regulate activity in the neighboring ventrolateral protocerebrum (VLP) to promote aggression, which may result from 5-HT1A receptor-mediated suppression of inhibitory GABAergic output neurons and concurrent disinhibition of excitatory cholinergic output (Alekseyenko et al., 2019). These cholinergic neurons also possess inhibitory short neuropeptide F (sNPF) receptors (Alekseyenko et al., 2019), which are functionally distinct from aggression-dampening NPF receptors (Dierick and Greenspan, 2007; Bubak et al., 2019) but possibly receive input from locomotion circuits (Nässel and Wegener, 2011) activated during aggression. (E) The PLP and VLP send descending projections, including aggression-promoting Tk neurons (Asahina et al., 2014), to the ventral nerve cord to control behavioral expression (Namiki et al., 2018).

Similar to findings in vertebrates, 5-HT1-like and 5-HT2-like receptor subtypes are implicated in insect aggression (see Table 1). In male Drosophila, aggression is reduced by 5-HT2 receptors but enhanced by activation of 5-HT1A receptors (Johnson et al., 2009). Further, the role of each subtype is specific to the type of aggressive behavior, with 5-HT1A receptors predominantly affecting low-intensity aggression seen at contest initiation, such as threat displays, whereas 5-HT2 receptors mediate high-intensity aggressive behaviors, such as lunging (Johnson et al., 2009). Our recent studies using the stalk-eyed fly (Teleopsis dalmanni) indicate a similar role for 5-HT1A and 5-HT2 receptors, respectively, in enhancing and reducing aggression (Bubak et al., 2019), suggesting receptor subtype activation as one mechanism to explain the generally opposing role of 5-HT in vertebrate versus invertebrate aggression. However, the story is not as simple as this; consideration of other factors points to more similarities than differences between invertebrates and vertebrates in how 5-HT can modulate aggression. In the following sections, we provide a summary of our work on aggression using the stalk-eyed fly. With this model, we hope to expand our knowledge of the role of 5-HT in altering aggressive behaviors with respect to discrete components of an aggressive interaction, such as contest initiation, intensity and termination, and we hope to determine how the actions of 5-HT may differ between the sexes (Box 1).

View this table:
  • View inline
  • View popup
  • Download powerpoint
Table 1.

Roles of serotonin receptor subtypes in insect aggression

The stalk-eyed fly (T. dalmanni) as a case study

Sex differences in 5-HT receptors and aggression

Pharmacologically increasing neural 5-HT using the precursor 5-hydroxytryptophan (5-HTP) increases high-intensity (defined by contact) behaviors in male stalk-eyed flies (Bubak et al., 2014b). This is consistent with studies demonstrating a positive relationship between increased 5-HT and aggression in other invertebrates (Table S1; Antonsen and Paul, 1997; Bubak et al., 2016b; Huber et al., 1997; Livingstone et al., 1980; Panksepp et al., 2003; Momohara et al., 2013; Dierick and Greenspan, 2007). However, females pretreated with 5-HTP exhibit no difference in either behavioral output or fight outcome (Bubak et al., 2019). Thus, as in some vertebrates (Joppa et al., 1997; Terranova et al., 2016; Villalba et al., 1997), there appears to be a sex difference in how 5-HT modulates aggression in stalk-eyed flies. This is supported by sex differences in components of 5-HT signaling, with males having higher 5-HT1A but lower 5-HT2 receptor expression, whereas 5-HT7 receptor expression is equivalent between the sexes (Bubak et al., 2019). In addition, males show much lower expression of SERT, which would presumably result in reduced 5-HT clearance. Combined, this suggests the higher levels of aggression displayed by males are a result of elevated levels of 5-HT acting at 5-HT1A receptors. Further, these findings indicate that 5-HT2 activation may inhibit aggression in male T. dalmanni. The fact that administration of selective 5-HT1A and 5-HT2 agonists increases or decreases, respectively, inter-male aggression in Drosophila supports this hypothesis (Johnson et al., 2009). Therefore, the lower expression of 5-HT1A and higher expression of 5-HT2 in female stalk-eyed flies may account for the difference in aggressive behavior seen between sexes of this species.

Results available from insect systems suggest some similarities in the role(s) of 5-HT receptors in modulating aggression when compared with vertebrates. In both vertebrates and arthropods, 5-HT2 receptors appear to dampen aggression (Bubak et al., 2019; Johnson et al., 2009; Muehlenkamp et al., 1995; Takahashi et al., 2011; Ten Eyck, 2008), but in contrast to the majority of rodent studies, 5-HT1A activation appears to increase insect aggression (Bubak et al., 2019; Johnson et al., 2009). However, this discrepancy in 5-HT1A modulation of aggression may owe more to whether the selected agonist is acting on somatodendritic 5-HT1A autoreceptors located presynaptically or on postsynaptic 5-HT1A heteroreceptors in terminal fields. For example, rodent aggression is reduced by 5-HT1A agonists when they are either injected directly into the dorsal raphe or given systemically (de Boer et al., 2016; Van der Vegt et al., 2003a,b; Calcagnoli et al., 2015), which seems contradictory, as activating autoreceptors in the raphe causes a reduction in 5-HT neuron firing and thus a decrease in 5-HT availability (Fig. 1), whereas activating postsynaptic 5-HT1A heteroreceptors mimics increased 5-HT signaling. Although the latter fits with an inhibitory role of 5-HT in vertebrate aggression, the anti-aggressive effects of autoreceptor activation suggest that 5-HT stimulates aggression. In support of this, social challenge in rodents and lizards is accompanied by rapid phasic increases in 5-HT in various brain regions (Watt et al., 2007; Nakazato, 2013; Takahashi et al., 2015). Combined, the overlap in functional effects of receptor subtypes again points to more similarities than differences between invertebrates and vertebrates in 5-HT-mediated modulation of aggression.

Social isolation, 5-HT and insect aggression

Social isolation increases aggressive behavior in both vertebrates and invertebrates (Twenge et al., 2001; Wongwitdecha and Marsden, 1996; Alexander, 1961; Johnson et al., 2009). Male Drosophila reared in isolation also show changes in 5-HT receptor expression compared with group-housed males (Johnson et al., 2009). Similarly, socially isolated male stalk-eyed flies are more aggressive, performing more high-intensity behaviors and contest initiations than their socially reared opponent (Bubak et al., 2019). Socially isolated males also have lower 5-HT2 expression levels than their socially housed opponents, while expression of 5-HT1A and 5-HT7 receptors appears to be independent of rearing condition. This pattern of receptor expression changes is opposite to that seen in Drosophila, where isolation reduces expression of 5-HT1A while 5-HT2 expression increases (Johnson et al., 2009). In contrast, social isolation has no effect on the expression or intensity of aggressive behavior or the expression of any of the 5-HT receptor subtypes measured in female stalk-eyed flies (Bubak et al., 2019).

Social isolation has similar augmenting effects on aggression in rodents. For example, male rats reared in isolation exhibit abnormally high levels of unprovoked and contextually inappropriate violent aggression (Toth et al., 2011). Similarly, socially isolated arthropods express high levels of aggression (Johnson et al., 2009; Sibbald and Plowwright, 2014; Stevenson and Rillich, 2013) and abnormal high-intensity attacks (Bubak et al., 2019) relative to socially raised controls. Further, serotonergic modulation of aggressive responses through changes in the expression of 5-HT1A and/or 5-HT2 has been implicated for both socially isolated vertebrates (reviewed in Veneema, 2009) and invertebrates (Bubak et al., 2019; Johnson et al., 2009; Yeh et al., 1996). The role(s) of the 5-HT receptors appears to be species specific in insects (Johnson et al., 2009; Bubak et al., 2019). Similarly, in vertebrates, there are species differences in both 5-HT receptor subtype expression following social isolation as well as the brain region affected (Bibancos et al., 2007; Preece et al., 2004; Ross et al., 2019; Schiller et al., 2003).

5-HT2 receptors and aggression

Use of small interfering RNA (siRNA) to selectively knock down 5-HT2 receptors in stalk-eyed flies decreases the receptor expression by approximately 30% in males, similar to that observed following social isolation (Bubak et al., 2019). Behaviorally, siRNA-treated males initiate more fights but perform the same amount of high-intensity aggression compared with their vehicle-treated opponents. Female aggression, as with both isolation and 5-HTP pretreatment, does not change following reduction of 5-HT2 receptors (Bubak et al., 2019). These findings also suggest 5-HT2 may modulate the willingness of males to engage in a fight, whereas escalations to potentially injurious levels are mediated by a separate mechanism. This differs from Drosophila, where stimulation of 5-HT2 receptors in isolated males reduces high-intensity aggression but not fight initiation (Johnson et al., 2009). However, social isolation increases expression of 5-HT2 receptors in male Drosophila (Johnson et al., 2009), whereas the opposite effect is seen in stalk-eyed flies (Bubak et al., 2019). In male crickets, activation of 5-HT2 receptors inhibits aggression in subordinates, but only after they have fought (Rillich and Stevenson, 2018). In contrast, aggressiveness during honey bee colony defense appears to be increased by 5-HT2 activation (Nouvian et al., 2018). These differences among insects in how 5-HT2 receptors mediate the type of aggressive behavior expressed, along with social isolation effects on receptor expression, highlight the need for studying multiple species before making general conclusions about the role of 5-HT in invertebrate aggression.

The results discussed above suggest some similarity in the role of 5-HT2 receptors in vertebrates and invertebrates. In crickets, stalk-eyed flies and Drosophila, 5-HT2-like receptors appear to inhibit components of aggressive behavior such as fight initiation, intensity and reduction of aggression after defeat (Bubak et al., 2019; Johnson et al., 2009; Rillich et al., 2019). Similarly, selective 5-HT2 agonists are effective in decreasing aggression in several vertebrate species (Muehlenkamp et al., 1995; Ten Eyck, 2008; Takahashi et al., 2012; but see Juárez et al., 2013).

Interactions between 5-HT and neuropeptides in stalk-eyed fly aggression

Serotonin modulates a variety of other neurochemical systems, including the neuropeptides tachykinin (Tk; invertebrate equivalent to substance P) and neuropeptide F (NPF; invertebrate equivalent of neuropeptide Y), each of which has been linked to aggressive behavior in vertebrates and invertebrates (Katsouni et al., 2009; Takahashi et al., 2012). Other neuropeptides, such as oxytocin and vasopressin, have been shown to be important mediators of mammalian aggression (Caldwell, 2017); however, the role played by their functional orthologs (inotocin in insects; oxytocin/vasopressin-like peptide in crustaceans) in invertebrate aggression is largely unknown (Gruber, 2014; Liutkeviciute et al., 2016), although a recent study showed no relationship between the expression of inotocin receptors and aggression in mated ant queens (Chérasse and Aron, 2017). In contrast, Tk/substance P increases aggression across both taxa (Asahina et al., 2014; Halasz et al., 2009; Katsouni et al., 2009), whereas NPY/NPF suppresses aggression (Dierick and Greenspan, 2007; Karl et al., 2004). Both neuropeptides are influenced by 5-HT activity (Guiard et al., 2007; Hennessy et al., 2017; Karl et al., 2004; Sergeyev et al., 1999). In stalk-eyed flies, manipulation of serotonergic function alters the expression of Tk and NPF to modulate specific components of aggressive behavior, and effects differ as a function of sex and receptor subtype (Bubak et al., 2019).

Social isolation increases both contest initiation and escalation exclusively in male stalk-eyed flies. In addition, there is an increase in Tk expression in isolated males that is not evident in females (Bubak et al., 2019). Recent work in male mice also shows that social isolation increases the expression of a closely related neuropeptide, tachykinin 2, in portions of the limbic stress circuit, and increased fear and aggressive behaviors can be blocked in these animals by tachykinin 2 receptor antagonists (Zelikowsky et al., 2018). Pretreating socially raised male stalk-eyed flies with 5-HTP to increase 5-HT also increases Tk and high-intensity aggression, but does not affect contest initiation. Comparing the effects of isolation and 5-HTP treatment suggests that Tk may primarily control behaviors associated with fight escalation, but not necessarily affect other less-intense aggressive behaviors (Bubak et al., 2019). Similarly, reducing Tk signaling reduces high-intensity attacks but leaves milder aggressive behaviors unaffected in rats (Halasz et al., 2009). In Drosophila, sexually dimorphic Tk neurons also regulate male aggression, but this extends to both low- and high-intensity aggressive behaviors (Asahina et al., 2014), initially suggesting that Tk regulation of discrete types of aggression may represent an evolutionarily derived state possessed by vertebrates. However, the finding that Tk is most closely associated with high-intensity aggression in male T. dalmanni argues against this, and instead points to convergence in Tk function at the level of the species rather than phylum.

The association between Tk and 5-HT in mediating aggression in vertebrates versus invertebrates is less clear. Tachykinin receptors on 5-HT neurons in the mammalian hindbrain can directly modulate neuronal firing and release of 5-HT in terminal regions (Maejima et al., 2013), and there is evidence for 5-HT and Tk co-release from neurons in mammals (Chan-Palay et al., 1978). In contrast, Tk and 5-HT do not appear to be co-localized in neurons in the majority of invertebrates (Boyan et al., 2010; Boyer et al., 2007; Chamberlain et al., 1986; Langworthy et al., 1997). However, the finding that 5-HTP treatment elevates both Tk expression and high-intensity behaviors in male stalk-eyed flies (Bubak et al., 2019) implies an interaction between 5-HT, Tk and aggression. Whether this represents a direct functional interaction as opposed to an additive effect produced by independent actions of 5-HT and Tk is unknown. Serotonin neurons do appear to synapse on to Tk-immunoreactive terminals in desert locust brain (Ignell, 2001), suggesting a direct relationship via synaptic contact that may also be present in T. dalmanni.

Willingness to engage in a fight increases following administration of 5-HT2 siRNA in male but not female stalk-eyed flies, despite similar reductions in 5-HT2 expression levels in the two sexes. This may result, in part, from a sex-dependent interactive role between the 5-HT2 receptor and the NPF system, as knockdown of the 5-HT2 receptor only reduces NPF receptor expression in males (Bubak et al., 2019). Although this is consistent with an inhibitory role reported for NPF in modulating aggression in Drosophila and mice, decreases in NPF/NPY in these species specifically suppress high-intensity behaviors (Dierick and Greenspan, 2007; Karl et al., 2004). In contrast, reductions in NPF receptor expression following 5-HT2 siRNA treatment have no effect on expression of high-intensity aggression in male stalk-eyed flies (Bubak et al., 2019). Further, 5-HT and NPF pathways appear to act independently in regulating aggression in male Drosophila (Dierick and Greenspan, 2007) and mice (Karl et al., 2004), whereas a direct positive relationship between 5-HT2 receptors and NPF is indicated for male T. dalmanni.

Combined, the findings from the stalk-eyed fly system generate a complex picture of interplay among serotonergic and peptidergic pathways that may fine tune the expression of aggressive behavior as appropriate for that particular context. These studies suggest that although 5-HT has a critical role in male aggression, precisely how the confrontation proceeds is governed by selective activation of 5-HT receptor subtypes along with changes in activity of NPF and Tk. Reductions in 5-HT2 activation seem to promote the motivation to engage with an opponent, which may be potentiated by reductions in NPF signaling. Once committed, the two opponents typically express equivalent amounts of low-intensity aggressive behaviors, but a sharp increase in expression of high-intensity behaviors in the last stages of the confrontation is shown by those that eventually win the fight (Bubak et al., 2016a). Thus, while a balance of signaling in favor of 5-HT1A versus 5-HT2 receptor activation may be sufficient to initiate a confrontation and maintain expression of low-intensity aggression, the shift to high-intensity aggressive behaviors required for winning depends upon an additional mechanism, such as increased Tk signaling. In contrast, the lower levels of aggression in female stalk-eyed flies appear to be maintained by heightened 5-HT2 receptor activity, with NPF and Tk having no apparent function in this behavior. These findings suggest that 5-HT modulation of aggression in this species is permissive or inhibitory depending on receptor subtype, intensity of aggression, neuropeptide involvement and the sex of the individual.

Comparing the role of 5-HT in aggression in vertebrates and invertebrates – where do we go from here?

Several studies show that, as in invertebrates, increases in 5-HT in vertebrates are associated with enhanced aggression. For example, administration of 5-HTP to mice increases 5-HT turnover and aggression intensity (Kulikov et al., 2012). Similar results are obtained in insects following 5-HTP pretreatment (Dierick and Greenspan, 2007; Bubak et al., 2013). Other studies have shown that 5-HT increases in specific brain regions in several vertebrate species just before or during aggression (Summers et al., 2003; van der Vegt, et al., 2003a,b; Watt et al., 2007). Because 5-HT is an evolutionarily ancient neurotransmitter present in all animal lineages (Moutkine et al., 2019), it is perhaps not surprising that a broadly shared role in aggression has been retained in both phyla, as seen for modulation of other behaviors critical for survival such as feeding, motor control and reproduction (Weiger, 1997).

The 5-HT receptors that modulate aggression appear to be similar in structure and function in invertebrates and vertebrates (Tierney, 2018; Vleugels et al., 2013, 2015), although experiments studying the effects of 5-HT receptor function in invertebrate aggression are limited. In crickets, stalk-eyed flies and Drosophila, 5-HT2-like receptors appear to inhibit aggression, whereas 5-HT1A-like receptor activation increases aggression (Table 1), and these effects may be exerted postsynaptically (Alekseyenko and Kravitz, 2015). In vertebrates, these two receptor subtypes also appear to strongly influence the expression of aggression, but to have a dampening effect. As discussed above, the anti-aggressive effects of 5-HT1A agonists in rodents may result from a depression of serotonergic activity/release through actions at presynaptic somatodendritic autoreceptors (de Boer and Newman-Tracredi, 2016), implying that increased levels of 5-HT actually have a facilitatory role in vertebrate aggression similar to that demonstrated for arthropods. Further, it could be argued that what were presumed to be opposing effects of 5-HT1A receptors on aggression between invertebrates and vertebrates are largely dependent on the balance of presynaptic versus postsynaptic activation, and that activation of postsynaptic 5-HT1A receptors mimicking elevated 5-HT release should promote aggression in both groups. This premise is supported, in part, by the finding that infusion of 5-HT1A agonists into some 5-HT terminal regions of the rodent brain can enhance aggression (Takahashi et al., 2012). However, this is only seen with specific types of aggression, such as maternal defense or alcohol-enhanced aggression (Takahashi et al., 2012).

This raises an important point, in that the degree to which behavioral outputs differ between species may depend on the context in which the aggressive confrontation is taking place (e.g. Ling et al., 2010; Harvey et al., 2012; Backström and Winberg, 2017; Rillich and Stevenson, 2018), making it difficult to parse out specific mechanisms. Therefore, aggression should be investigated under different contexts and at different stages of the interaction (e.g. fight initiation, escalation, termination), particularly those relevant to the life history of the species or sex. For example, pitting female stalk-eyed flies in a forced-fight paradigm with food being the incentive may be a less powerful stimulus to provoke aggressive confrontations than access to egg-laying sites. To obtain a more fundamental understanding of how aggression is differentially modulated between the sexes by receptor subtypes, different combinations of selective knockdown or conditional gene overexpression could be linked with delivery of specific pharmacological agents. Work with Drosophila shows that strains can be created in which expression of genes controlling key aspects of neural signaling are restricted to particular brain regions, allowing fine-tuned analysis of how transmitters such as 5-HT mediate specific behaviors (Alekseyenko et al., 2014; Alekseyenko and Kravitz, 2015). Application of similar techniques to other arthropods could provide powerful tools for elucidating how and why aggression regulation by 5-HT has either diverged or remained similar in response to diverse evolutionary pressures.

Conclusions

So, does 5-HT have divergent or similar functions in aggression between invertebrates and vertebrates? Based on our studies using stalk-eyed flies, along with the available literature, the answer seems to depend on exactly how the question is posed. Systemically induced increases in 5-HT in invertebrates largely enhance components of aggressive behaviors (Table S1; Antonsen and Paul, 1997; Bubak et al., 2014a,b; Dierick and Greenspan, 2007; Huber et al., 1997; Livingstone et al., 1980; Panksepp et al., 2003; but see Stevenson and Rillich, 2017). In contrast, 5-HT historically has been viewed as an inhibitory neuromodulator of aggression in vertebrates (Table S1; Nelson and Chiavegatto, 2001; Summers et al., 2005a; Summers and Winberg, 2006). However, several studies suggest that the role of 5-HT in modulating aggression is more complicated, and depends on the subtype of 5-HT receptor activated, effects of 5-HT within specific brain regions, the type of aggression studied and the use of animal models selected for high aggression (de Boer et al., 2015, 2016; Nelson and Trainor, 2007; Takahashi et al., 2012). At least, elements of serotonergic function appear to be conserved phylogenetically.

The major classes of serotonergic receptors (5-HT1, 5-HT2 and 5-HT7) are estimated to have diverged over 800 million years ago (Peroutka and Howell, 1994), with a subsequent differentiation and appearance of new 5-HT receptors (including the 5-HT1A receptor) when ancestral vertebrates appeared some 600–700 million years ago (Peroutka and Howell, 1994; Blair and Hedges, 2005). Thus, there may truly be a broad phylogenetic divergence in how 5-HT1A receptors influence aggression, with the promoting effects in invertebrates representing a more ancestral state that has only been conserved in the vertebrate brain for mediating specific types of aggression. In contrast, the aggression-inhibiting role of the evolutionarily older 5-HT2 receptors appears to have been conserved phylogenetically. However, these hypotheses will remain speculative until additional studies with different invertebrate species are conducted. Further, there is some debate as to whether pharmacological agents used to manipulate specific 5-HT receptor subtypes in vertebrate studies are equally efficacious in their invertebrate orthologs (Vleugels et al., 2015; Tierney, 2018), and sophisticated genetic manipulations to target specific brain regions have primarily been restricted to Drosophila (Alekseyenko et al., 2014; Alekseyenko and Kravitz, 2015). Despite this, considerable evidence is steadily accumulating to suggest that there is indeed a shared facilitatory role for 5-HT in vertebrate and invertebrate aggression.

Acknowledgements

The authors appreciate the valuable comments and critiques from three reviewers and the editor Charlotte Rutledge, and help generating the figures and tables from Gabrielle Welsh.

FOOTNOTES

  • Competing interests

    The authors declare no competing or financial interests.

  • Funding

    This work was funded by National Science Foundation grants IOS 1256898 and 1656465 (J.G.S.), and IOS 1257679 (M.J.W.).

  • Supplementary information

    Supplementary information available online at http://jeb.biologists.org/lookup/doi/10.1242/jeb.132159.supplemental

  • © 2020. Published by The Company of Biologists Ltd

References

  1. ↵
    1. Aggarwal, S. and
    2. Mortensen, O. V.
    (2017). Overview of monoamine transporters. Curr. Protoc. Pharmacol. 79, 12.16.1-12.16.17. doi:10.1002/cpph.32
    OpenUrlCrossRef
  2. ↵
    1. Alekseyenko, O. V. and
    2. Kravitz, E. A.
    (2015). Serotonin and the search for the anatomical substrate of aggression. Fly (Austin) 8, 200-205. doi:10.1080/19336934.2015.1045171
    OpenUrlCrossRef
  3. ↵
    1. Alekseyenko, O. V.,
    2. Lee, C. and
    3. Kravitz, E. A.
    (2010). Targeted manipulation of serotonergic neurotransmission affects the escalation of aggression in adult male Drosophila melanogaster. PLoS ONE 5, e10806. doi:10.1371/journal.pone.0010806
    OpenUrlCrossRefPubMed
  4. ↵
    1. Alekseyenko, O. V.,
    2. Chan, Y. B.,
    3. Li, R. and
    4. Kravitz, E. A.
    (2013). Single dopaminergic neurons that modulate aggression in Drosophila. Proc. Natl. Acad. Sci. USA 110, 6151-6156. doi:10.1073/pnas.1303446110
    OpenUrlAbstract/FREE Full Text
  5. ↵
    1. Alekseyenko, O. V.,
    2. Chan, Y.-B.,
    3. Fernandez, M. P.,
    4. Bülow, T.,
    5. Pankratz, M. J. and
    6. Kravitz, E. A.
    (2014). Single serotonergic neurons that modulate aggression in drosophila. Curr. Biol. 24, 2700-2707. doi:10.1016/j.cub.2014.09.051
    OpenUrlCrossRefPubMed
  6. ↵
    1. Alekseyenko, O. V.,
    2. Chan, Y.-B.,
    3. Okaty, B. W.,
    4. Chang, Y. J.,
    5. Dymecki, S. M. and
    6. Kravitz, E. A.
    (2019). Serotonergic modulation of aggression in Drosophila involves GABAergic and cholinergic opposing pathways. Curr. Biol. 29, 2145-2156.e5. doi:10.1016/j.cub.2019.05.070
    OpenUrlCrossRef
  7. ↵
    1. Alexander, R. D.
    (1961). Aggressiveness, territoriality, and sexual behavior in field crickets (Orthoptera: Gryllidae). Behaviour 17, 130-223. doi:10.1163/156853961X00042
    OpenUrlCrossRef
  8. ↵
    1. Antonsen, B. L. and
    2. Paul, D. H.
    (1997). Serotonin and octopamine elicit stereotypical agonistic behaviors in the squat lobster Munida quadrispina (Anomura, Galatheidae). J Comp Physiol A 181, 501-510. doi:10.1007/s003590050134
    OpenUrlCrossRef
  9. ↵
    1. Asahina, K.,
    2. Watanabe, K.,
    3. Duistermars, B. J.,
    4. Hoopfer, E.,
    5. González, C. R.,
    6. Eyjólfsdóttir, E. A.,
    7. Perona, P. and
    8. Anderson, D. J.
    (2014). Tachykinin-expressing neurons control male-specific aggressive arousal in Drosophila. Cell 156, 221-235. doi:10.1016/j.cell.2013.11.045
    OpenUrlCrossRefPubMed
  10. ↵
    1. Asan, E.,
    2. Steinke, M. and
    3. Lesch, K.-P.
    (2013). Serotonergic innervation of the amygdala: targets, receptors, and implications for stress and anxiety. Histol. Cell Biol. 139, 785-813. doi:10.1007/s00418-013-1081-1
    OpenUrlCrossRefPubMed
  11. ↵
    1. Audero, E.,
    2. Mlinar, B.,
    3. Baccini, G.,
    4. Skachokova, Z. K.,
    5. Corradetti, R. and
    6. Gross, C.
    (2013). Suppression of serotonin neuron firing increases aggression in mice. J. Neurosci. 33, 8678-8688. doi:10.1523/JNEUROSCI.2067-12.2013
    OpenUrlAbstract/FREE Full Text
  12. ↵
    1. Backström, T. and
    2. Winberg, S.
    (2017). Serotonin coordinates responses to social stress-what we can learn from fish. Front. Neurosci. 11, 595. doi:10.3389/fnins.2017.00595
    OpenUrlCrossRef
  13. ↵
    1. Bacqué-Cazenave, J.,
    2. Cattaert, D.,
    3. Delbecque, J. P. and
    4. Fossat, P.
    (2018). Alteration of size perception: serotonin has opposite effects on the aggressiveness of crayfish confronting either a smaller or a larger rival. J. Exp. Biol. 221, jeb177840. doi:10.1242/jeb.177840
    OpenUrlAbstract/FREE Full Text
  14. ↵
    1. Barbara, G. S.,
    2. Zube, C.,
    3. Rybak, J.,
    4. Gauthier, M. and
    5. Grünewald, B.
    (2005). Acetylcholine, GABA and glutamate induce ionic currents in cultured antennal lobe neurons of the honeybee, Apis mellifera. J. Comp. Physiol. A 191, 823-836. doi:10.1007/s00359-005-0007-3
    OpenUrlCrossRefPubMedWeb of Science
  15. ↵
    1. Bath, E.,
    2. Wigby, S.,
    3. Vincent, C.,
    4. Tobias, J. A. and
    5. Seddon, N.
    (2015). Condition, not eyespan, predicts contest outcome in female stalk-eyed flies, Teleopsis dalmanni. Ecol. Evol. 5, 1826-1836. doi:10.1002/ece3.1467
    OpenUrlCrossRef
    1. Beiderbeck, D. I.,
    2. Neumann, I. D. and
    3. Veenema, A. H.
    (2007). Differences in intermale aggression are accompanied by opposite vasopressin release patterns within the septum in rats bred for low and high anxiety. Eur. J. Neurosci. 26, 3597-3605. doi:10.1111/j.1460-9568.2007.05974.x
    OpenUrlCrossRefPubMed
  16. ↵
    1. Bicker, G.
    (1999). Histochemistry of classical neurotransmitters in antennal lobes and mushroom bodies of the honeybee. Microsc. Res. Tech. 45, 174-183. doi:10.1002/(SICI)1097-0029(19990501)45:3<174::AID-JEMT5>3.0.CO;2-U
    OpenUrlCrossRefPubMedWeb of Science
  17. ↵
    1. Bibancos, T.,
    2. Jardim, D. L.,
    3. Aneas, I. and
    4. Chiavegatto, S.
    (2007). Social isolation and expression of serotonergic neurotransmission-related genes in several brain areas of male mice. Genes Brain Behav. 6, 529-539. doi:10.1111/j.1601-183X.2006.00280.x
    OpenUrlCrossRefPubMedWeb of Science
  18. ↵
    1. Blair, J. E. and
    2. Hedges, S. B.
    (2005). Molecular phylogeny and divergence times of deuterostome animals. Mol. Biol. Evol. 22, 2275-2284. doi:10.1093/molbev/msi225
    OpenUrlCrossRefPubMedWeb of Science
  19. ↵
    1. Blanchard, D. C. and
    2. Meyza, K.
    (2019). Risk assessment and serotonin: animal models and human psychopathologies. Behav. Brain Res. 14, 357-358. doi:10.1016/j.bbr.2017.07.008
    OpenUrlCrossRef
  20. ↵
    1. Blenau, W. and
    2. Baumann, A.
    (2001). Molecular and pharmacological properties of insect biogenic amine receptors: lessons from Drosophila melanogaster and Apis mellifera. Arch. Insect Biochem. Physiol. 48, 13-38. doi:10.1002/arch.1055
    OpenUrlCrossRefPubMedWeb of Science
  21. ↵
    1. Boyan, G.,
    2. Williams, L. and
    3. Herbert, Z.
    (2010). Multipotent neuroblasts generate a biochemical neuroarchitecture in the central complex of the grasshopper Schistocerca gregaria. Cell Tissue Res. 340, 13-28. doi:10.1007/s00441-009-0922-7
    OpenUrlCrossRefPubMed
  22. ↵
    1. Boyer, C.,
    2. Maubert, E.,
    3. Charnay, Y. and
    4. Chichery, R.
    (2007). Distribution of neurokinin A-like and serotonin immunoreactivities within the vertical lobe complex in Sepia officinalis. Brain Res. 1133, 53-66. doi:10.1016/j.brainres.2006.11.042
    OpenUrlCrossRefPubMed
  23. ↵
    1. Brandt, Y. and
    2. Swallow, J. G.
    (2009). Do the elongated eye stalks of diopsid flies facilitate rival assessment? Behav. Ecol. Sociobiol. 63, 1243-1246. doi:10.1007/s00265-009-0774-x
    OpenUrlCrossRefWeb of Science
  24. ↵
    1. Bubak, A. N.,
    2. Swallow, J. G. and
    3. Renner, K. J.
    (2013). Whole brain monoamine detection and manipulation in a stalk-eyed fly. J. Neurosci. Methods 219, 124-130. doi:10.1016/j.jneumeth.2013.07.006
    OpenUrlCrossRefPubMed
  25. ↵
    1. Bubak, A. N.,
    2. Grace, J. L.,
    3. Watt, M. J.,
    4. Renner, K. J. and
    5. Swallow, J. G.
    (2014a). Neurochemistry as a bridge between morphology and behavior: Perspectives on aggression in insects. Curr. Zool. 60, 778-790. doi:10.1093/czoolo/60.6.778
    OpenUrlCrossRef
  26. ↵
    1. Bubak, A. N.,
    2. Renner, K. J. and
    3. Swallow, J. G.
    (2014b). Heightened serotonin influences contest outcome and enhances expression of high-intensity aggressive behaviors. Behav. Brain Res. 259, 137-142. doi:10.1016/j.bbr.2013.10.050
    OpenUrlCrossRefPubMed
  27. ↵
    1. Bubak, A. N.,
    2. Rieger, N. S.,
    3. Watt, M. J.,
    4. Renner, K. J. and
    5. Swallow, J. G.
    (2015). David vs. Goliath: serotonin modulates opponent perception between smaller and larger rivals. Behav. Brain Res. 292, 521-527. doi:10.1016/j.bbr.2015.07.028
    OpenUrlCrossRefPubMed
  28. ↵
    1. Bubak, A. N.,
    2. Gerken, A. R.,
    3. Watt, M. J.,
    4. Costabile, J. D.,
    5. Renner, K. J. and
    6. Swallow, J. G.
    (2016a). Assessment strategies and fighting patterns in animal contests: a role for serotonin? Curr. Zool. 62, 257-263. doi:10.1093/cz/zow040
    OpenUrlCrossRef
  29. ↵
    1. Bubak, A. N.,
    2. Yaeger, J. D. W.,
    3. Renner, K. J.,
    4. Swallow, J. G., and
    5. Greene, M. J.
    (2016b). Neuromodulation of nestmate recognition decisions by pavement ants. PLoS One 11, e0166417.
    OpenUrl
  30. ↵
    1. Bubak, A. N.,
    2. Watt, M. J.,
    3. Renner, K. J.,
    4. Luman, A. A.,
    5. Costabile, J. D.,
    6. Sanders, E. J.,
    7. Grace, J. L. and
    8. Swallow, J. G.
    (2019). Sex differences in aggression: differential roles of 5-HT2, neuropeptide F and tachykinin. PLoS ONE 14, e0203980. doi:10.1371/journal.pone.0203980
    OpenUrlCrossRef
  31. ↵
    1. Budnik, V.,
    2. Wu, C. F. and
    3. White, K.
    (1989). Altered branching of serotonin-containing neurons in Drosophila mutants unable to synthesize serotonin and dopamine. J. Neurosci. 9, 2866-2877. doi:10.1523/JNEUROSCI.09-08-02866.1989
    OpenUrlAbstract/FREE Full Text
  32. ↵
    1. Burkhardt, D. and
    2. de la Motte, I.
    (1988). Big ‘antlers’ are favoured: female choice in stalk-eyed flies (Diptera, Insecta), field collected harems and laboratory experiments. J. Comp. Physiol. 162, 649-652. doi:10.1007/BF01342640
    OpenUrlCrossRef
  33. ↵
    1. Calcagnoli, F.,
    2. Stubbendorff, C.,
    3. Meyer, N.,
    4. de Boer, S. F.,
    5. Althaus, M. and
    6. Koolhaas, J. M.
    (2015). Oxytocin microinjected into the central amygdaloid nuclei exerts anti-aggressive effects in male rats. Neuropharmacology 90, 74-81. doi:10.1016/j.neuropharm.2014.11.012
    OpenUrlCrossRef
  34. ↵
    1. Caldwell, H. K.
    (2017). Oxytocin and vasopressin: powerful regulators of social behavior. Neuroscientist 23, 517-528. doi:10.1177/1073858417708284
    OpenUrlCrossRef
  35. ↵
    1. Canteras, N. S.,
    2. Simerly, R. B. and
    3. Swanson, L. W.
    (1995). Organization of projections from the medial nucleus of the amygdala: a PHAL study in the rat. J. Comp. Neurol. 360, 213-245. doi:10.1002/cne.903600203
    OpenUrlCrossRefPubMedWeb of Science
  36. ↵
    1. Caramaschi, D.,
    2. de Boer, S. F.,
    3. de Vries, H. and
    4. Koolhaas, J. M.
    (2008). Development of violence in mice through repeated victory along with changes in prefrontal cortex neurochemistry. Behav. Brain Res. 189, 263-272. doi:10.1016/j.bbr.2008.01.003
    OpenUrlCrossRefPubMedWeb of Science
  37. ↵
    1. Carrillo, M.,
    2. Ricci, L. A.,
    3. Coppersmith, G. A. and
    4. Melloni, R. H.
    (2009). The effect of increased serotonergic neurotransmission on aggression: a critical meta-analytical review of preclinical studies. Psychopharmacology 205, 349-368. doi:10.1007/s00213-009-1543-2
    OpenUrlCrossRefPubMed
  38. ↵
    1. Cervantes, M. C. and
    2. Delville, Y.
    (2007). Individual differences in offensive aggression in golden hamsters: a model of reactive and impulsive aggression? Neuroscience 150, 511-521. doi:10.1016/j.neuroscience.2007.09.034
    OpenUrlCrossRefPubMed
  39. ↵
    1. Chamberlain, S. C.,
    2. Pepper, J.,
    3. Battelle, B.-A.,
    4. Wyse, G. A. and
    5. Lewandowski, T. J.
    (1986). Immunoreactivity in Limulus. II. Studies of serotonin like immunoreactivity, endogenous serotonin, and serotonin synthesis in the brain and lateral eye. J. Comp. Neurol. 251, 363-375. doi:10.1002/cne.902510307
    OpenUrlCrossRefPubMed
  40. ↵
    1. Chan-Palay, V.,
    2. Jonsson, G. and
    3. Palay, S. L.
    (1978). Serotonin and substance P coexist in neurons of the rat's central nervous system. Proc. Natl Acad. Sci. USA 75, 1582-1586. doi:10.1073/pnas.75.3.1582
    OpenUrlAbstract/FREE Full Text
  41. ↵
    1. Chérasse, S. and
    2. Aron, S.
    (2017). Measuring inotocin receptor gene expression in chronological order in ant queens. Horm. Behav. 96, 116-121. doi:10.1016/j.yhbeh.2017.09.009
    OpenUrlCrossRef
  42. ↵
    1. de Almeida, R. M. M. and
    2. Lucion, A. B.
    (1997). 8-OH-DPAT in the median raphe, dorsal periaqueductal gray and corticomedial amygdala nucleus decreases, but in the medial septal area it can increase maternal aggressive behavior in rats. Psychopharmacology 134, 392-400. doi:10.1007/s002130050476
    OpenUrlCrossRefPubMed
  43. ↵
    1. de Almeida, R. M. M.,
    2. Giovenardi, M.,
    3. da Silva, S. P.,
    4. de Oliveira, V. P. and
    5. Stein, D. J.
    (2005). Maternal aggression in Wistar rats: effect of 5-HT2A/2C receptor agonist and antagonist microinjected into the dorsal periaqueductal gray matter and medial septum. Braz. J. Med. Biol. Res. 38, 597-602. doi:10.1590/S0100-879X2005000400014
    OpenUrlCrossRefPubMed
  44. ↵
    1. de Almeida, R. M. M.,
    2. Cabral, J. C. C. and
    3. Narvaes, R.
    (2015). Behavioural, hormonal and neurobiological mechanisms of aggressive behaviour in human and nonhuman primates. Physiol. Behav. 143, 121-135. doi:10.1016/j.physbeh.2015.02.053
    OpenUrlCrossRefPubMed
  45. ↵
    1. de Boer, S. F. and
    2. Newman-Tancredi, A.
    (2016). Anti-aggressive effects of the selective high-efficacy ‘biased’ 5-HT1A receptor agonists F15599 and F13714 in male WTG rats. Psychopharmacology 233, 9379-9347. doi:10.1007/s00213-015-4173-x
    OpenUrlCrossRef
  46. ↵
    1. de Boer, S. F.,
    2. Olivier, B.,
    3. Veening, J. and
    4. Koolhaas, J. M.
    (2015). The neurobiology of offensive aggression: revealing a modular view. Physiol. Behav. 146, 111-127. doi:10.1016/j.physbeh.2015.04.040
    OpenUrlCrossRefPubMed
  47. ↵
    1. de Boer, S. F.,
    2. Buwalda, B. and
    3. Koolhaas, J. M.
    (2016). Untangling the neurobiology of coping styles in rodents: towards neural mechanisms underlying individual differences in disease susceptibility. Neurosci. Biobehav. Rev. 74, 401-422. doi:10.1016/j.neubiorev.2016.07.008
    OpenUrlCrossRef
  48. ↵
    1. de la Motte, I. and
    2. Burkhardt, D.
    (1983). Portrait of an Asian stalk-eyed fly. Naturwiss 70, 451-461. doi:10.1007/BF01079611
    OpenUrlCrossRef
  49. ↵
    1. Dierick, H. A. and
    2. Greenspan, R. J.
    (2007). Serotonin and neuropeptide F have opposite modulatory effects on fly aggression. Nat. Genet. 39, 678-682. doi:10.1038/ng2029
    OpenUrlCrossRefPubMedWeb of Science
  50. ↵
    1. Dyakonova, V. E. and
    2. Krushinsky, A. L.
    (2013). Serotonin precursor (5-hydroxytryptophan) causes substantial changes in the fighting behavior of male crickets, Gryllus bimaculatus. J Comp Physiol A 199, 601-609. doi:10.1007/s00359-013-0804-z
    OpenUrlCrossRefPubMed
  51. ↵
    1. Edsinger, E. and
    2. Dölen, G.
    (2018). A conserved role for serotonergic neurotransmission in mediating social behavior in octopus. Curr. Biol. 28, 3136-3142.e4. doi:10.1016/j.cub.2018.07.061
    OpenUrlCrossRef
  52. ↵
    1. Edwards, D. H. and
    2. Herberholz, J.
    (2005). Crustacean models of aggression. In The Biology of Aggression (ed. R. J. Nelson), pp. 38–61. Oxford University Press.
  53. ↵
    1. Egge, A. R.,
    2. Brandt, Y. and
    3. Swallow, J. G.
    (2011). Sequential analysis of aggressive interactions in the stalk-eyed fly Teleopsis dalmanni. Behav. Ecol. Sociobiol. 65, 369-379. doi:10.1007/s00265-010-1054-5
    OpenUrlCrossRef
  54. ↵
    1. Ferris, C. F.,
    2. Melloni, Jr, R. H.,
    3. Koppel, G.,
    4. Perry, K. W.,
    5. Fuller, R. W. and
    6. Delville, Y.
    (1997). Vasopressin/serotonin interactions in the anterior hypothalamus control aggressive behavior in golden hamsters. J. Neurosci. 17, 4331-4340. doi:10.1523/JNEUROSCI.17-11-04331.1997
    OpenUrlAbstract/FREE Full Text
  55. ↵
    1. Ferris, C. F.,
    2. Stolberg, T. and
    3. Delville, Y.
    (1999). Serotonin regulation of aggressive behavior in male golden hamsters (Mesocricetus auratus). Behav. Neurosci. 113, 804-815. doi:10.1037/0735-7044.113.4.804
    OpenUrlCrossRefPubMedWeb of Science
  56. ↵
    1. Grimes, J. M. and
    2. Melloni, R. H.
    (2002). Serotonin modulates offensive attack in adolescent anabolic steroid-treated hamsters. Pharmacol. Biochem. Behav. 73, 713-721. doi:10.1016/S0091-3057(02)00880-8
    OpenUrlCrossRefPubMed
  57. ↵
    1. Gruber, C. W.
    (2014). Physiology of invertebrate oxytocin and vasopressin neuropeptides. Exp. Physiol. 99, 55-61. doi:10.1113/expphysiol.2013.072561
    OpenUrlCrossRefPubMed
  58. ↵
    1. Guiard, B. P.,
    2. Guilloux, J.-P.,
    3. Reperant, C.,
    4. Hunt, S. P.,
    5. Toth, M. and
    6. Gardier, A. M.
    (2007). Substance P neurokinin 1 receptor activation within the dorsal raphe nucleus controls serotonin release in the mouse frontal cortex. Mol. Pharmacol. 72, 1411-1418. doi:10.1124/mol.107.040113
    OpenUrlAbstract/FREE Full Text
  59. ↵
    1. Halasz, J.,
    2. Zelena, D.,
    3. Toth, M.,
    4. Tulogdi, A.,
    5. Mikics, E. and
    6. Haller, J.
    (2009). Substance P neurotransmission and violent aggression: the role of tachykinin NK(1) receptors in the hypothalamic attack area. Eur. J. Pharmacol. 611, 35-43. doi:10.1016/j.ejphar.2009.03.050
    OpenUrlCrossRefPubMed
  60. ↵
    1. Harvey, M. L.,
    2. Swallows, C. L. and
    3. Cooper, M. A.
    (2012). A double dissociation in the effects of 5-HT2A and 5-HT2C receptors on the acquisition and expression of conditioned defeat in Syrian hamsters. Behav. Neurosci. 126, 530-537. doi:10.1037/a0029047
    OpenUrlCrossRefPubMed
  61. ↵
    1. Heiming, R. S.,
    2. Mönning, A.,
    3. Jansen, F.,
    4. Kloke, V.,
    5. Lesch, K.-P. and
    6. Sachser, N.
    (2013). To attack, or not to attack? The role of serotonin transporter genotype in the display of maternal aggression. Behav. Brain Res. 242, 135-141. doi:10.1016/j.bbr.2012.12.045
    OpenUrlCrossRefPubMed
  62. ↵
    1. Hennessy, M. L.,
    2. Corcoran, A. E.,
    3. Brust, R. D.,
    4. Chang, Y. J.,
    5. Nattie, E. E. and
    6. Dymecki, S. M.
    (2017). Activity of Tachykinin1-expressing Pet1 raphe neurons modulates the respiratory chemoreflex. J Neurosci 37, 1807-1181. doi:10.1523/JNEUROSCI.2316-16.2016
    OpenUrlAbstract/FREE Full Text
  63. ↵
    1. Höglund, E.,
    2. Bakke, M. J.,
    3. Øverli, Ø.,
    4. Winberg, S. and
    5. Nilsson, G. E.
    (2005). Suppression of aggressive behaviour in juvenile Atlantic cod (Gadus morhua) by L-tryptophan supplementation. Aquaculture 249, 525-531. doi:10.1016/j.aquaculture.2005.04.028
    OpenUrlCrossRefWeb of Science
  64. ↵
    1. Holmes, A.,
    2. Murphy, D. L. and
    3. Crawley, J. N.
    (2002). Reduced aggression in mice lacking the serotonin transporter. Psychopharmacology 161, 160-167. doi:10.1007/s00213-002-1024-3
    OpenUrlCrossRefPubMed
  65. ↵
    1. Hong, W.,
    2. Kim, D.-W. and
    3. Anderson, D. J.
    (2014). Antagonistic control of social versus repetitive self-grooming behaviors by separable amygdala neuronal subsets. Cell 158, 1348-1361. doi:10.1016/j.cell.2014.07.049
    OpenUrlCrossRefPubMed
  66. ↵
    1. Hoopfer, E. D.
    (2016). Neural control of aggression in Drosophila. Curr. Opin. Neurobiol. 38, 109-118. doi:10.1016/j.conb.2016.04.007
    OpenUrlCrossRef
  67. ↵
    1. Huang, Z.,
    2. Thiebaud, N. and
    3. Fadool, D. A.
    (2017). Differential serotonergic modulation across the main and accessory olfactory bulbs. J. Physiol. 595, 3515-3533. doi:10.1113/JP273945
    OpenUrlCrossRef
  68. ↵
    1. Huber, R.,
    2. Smith, K.,
    3. Delago, A.,
    4. Isaksson, K. and
    5. Kravitz, E. A.
    (1997). Serotonin and aggressive motivation in crustaceans: altering the decision to retreat. PNAS 94, 5939-5942. doi:10.1073/pnas.94.11.5939
    OpenUrlAbstract/FREE Full Text
  69. ↵
    1. Ignell, R.
    (2001). Monoamines and neuropeptides in antennal lobe interneurons of the desert locust, Schistocerca gregaria: an immunocytochemical study. Cell Tissue Res. 306, 143-156. doi:10.1007/s004410100434
    OpenUrlCrossRefPubMed
  70. ↵
    1. Ignell, R.,
    2. Root, C. M.,
    3. Birse, R. T.,
    4. Wang, J. W.,
    5. Nässel, D. R. and
    6. Winther, Å. M. E.
    (2009). Presynaptic peptidergic modulation of olfactory receptor neurons in Drosophila. Proc. Natl Acad. Sci. USA 106, 13070-13075. doi:10.1073/pnas.0813004106
    OpenUrlAbstract/FREE Full Text
  71. ↵
    1. Johnson, O.,
    2. Becnel, J. and
    3. Nichols, C. D.
    (2009). Serotonin 5-HT(2) and 5-HT(1A)-like receptors differentially modulate aggressive behaviors in Drosophila melanogaster. Neuroscience 158, 1292-1300. doi:10.1016/j.neuroscience.2008.10.055
    OpenUrlCrossRefPubMedWeb of Science
  72. ↵
    1. Joppa, M. A.,
    2. Rowe, R. K. and
    3. Meisel, R. L.
    (1997). Effects of serotonin 1A or 1B receptor agonists on social aggression in male and female Syrian hamsters. Pharmacol. Biochem. Behav. 58, 349-353. doi:10.1016/S0091-3057(97)00277-3
    OpenUrlCrossRefPubMedWeb of Science
  73. ↵
    1. Juárez, P.,
    2. Valdovinos, M. G.,
    3. May, M. E.,
    4. Lloyd, B. P.,
    5. Couppis, M. H. and
    6. Kennedy, C. H.
    (2013). Serotonin (2A/C) receptors mediate the aggressive phenotype of TLX gene knockout mice. Behav. Brain Res. 256, 354-361. doi:10.1016/j.bbr.2013.07.044
    OpenUrlCrossRef
  74. ↵
    1. Karl, T.,
    2. Lin, S.,
    3. Schwarzer, C.,
    4. Sainsbury, A.,
    5. Couzens, M.,
    6. Wittmann, W.,
    7. Boey, D.,
    8. von Horsten, S. and
    9. Herzog, H.
    (2004). Y1 receptors regulate aggressive behavior by modulating serotonin pathways. Proc. Natl. Acad. Sci. USA 101, 12742-12747. doi:10.1073/pnas.0404085101
    OpenUrlAbstract/FREE Full Text
  75. ↵
    1. Kästner, N.,
    2. Richter, S. H.,
    3. Urbanik, S.,
    4. Kunert, J.,
    5. Waider, J.,
    6. Lesch, K.-P.,
    7. Sylvia Kaiser, S. and
    8. Sachser, N.
    (2019). Brain serotonin deficiency affects female aggression. Sci. Rep. 9, 1366. doi:10.1038/s41598-018-37613-4
    OpenUrlCrossRef
  76. ↵
    1. Katsouni, E.,
    2. Sakkas, P.,
    3. Zarros, A.,
    4. Skandali, N. and
    5. Liapi, C.
    (2009). The involvement of substance P in the induction of aggressive behavior. Peptides 30, 1586-1591. doi:10.1016/j.peptides.2009.05.001
    OpenUrlCrossRefPubMedWeb of Science
  77. ↵
    1. Koolhaas, J. M.,
    2. Van den Brink, T.,
    3. Roozendaal, B. and
    4. Boorsma, F.
    (1990). Medial amygdala and aggressive behavior: Interaction between testosterone and vasopressin. Aggress. Behav. 16, 223-229.
    OpenUrl
  78. ↵
    1. Kostowski, W. and
    2. Tarchalska, B.
    (1972). The effects of some drugs affecting brain 5-HT on the aggressive behaviour and spontaneous electrical activity of the central nervous system of the ant, Formica rufa. Brain Res. 38, 143-149. doi:10.1016/0006-8993(72)90595-1
    OpenUrlCrossRefPubMedWeb of Science
  79. ↵
    1. Kulikov, A. V.,
    2. Osipova, D. V.,
    3. Naumenko, V. S.,
    4. Terenina, E.,
    5. Mormède, P. and
    6. Popova, N. K.
    (2012). A pharmacological evidence of positive association between mouse intermale aggression and brain serotonin metabolism. Behav. Brain Res. 233, 113-119. doi:10.1016/j.bbr.2012.04.031
    OpenUrlCrossRefPubMedWeb of Science
  80. ↵
    1. Langworthy, K.,
    2. Helluy, S.,
    3. Benton, J. and
    4. Beltz, B.
    (1997). Amines and peptides in the brain of the American lobster: immunocytochemical localization patterns and implications for brain function. Cell Tissue Res. 288, 191-206. doi:10.1007/s004410050806
    OpenUrlCrossRefPubMedWeb of Science
  81. ↵
    1. Lin, D.,
    2. Boyle, M. P.,
    3. Dollar, P.,
    4. Lee, H.,
    5. Lein, E. S.,
    6. Perona, P. and
    7. Anderson, D. J.
    (2011). Functional identification of an aggression locus in the mouse hypothalamus. Nature 470, 221. doi:10.1038/nature09736
    OpenUrlCrossRefPubMedWeb of Science
  82. ↵
    1. Ling, T. J.,
    2. Summers, C. H.,
    3. Renner, K. J. and
    4. Watt, M. J.
    (2010). Opponent recognition and social status differentiate rapid neuroendocrine responses to social challenge. Physiol. Behav. 99, 571-578. doi:10.1016/j.physbeh.2010.01.025
    OpenUrlCrossRefPubMed
  83. ↵
    1. Liutkeviciute, Z.,
    2. Koehbach, J.,
    3. Eder, T.,
    4. Gil-Mansilla, E. and
    5. Gruber, C. W.
    (2016). Global map of oxytocin/vasopressin-like neuropeptide signalling in insects. Sci. Rep. 6, 39177. doi:10.1038/srep39177
    OpenUrlCrossRef
  84. ↵
    1. Livingstone, M. S.,
    2. Harris-Warrick, R. M. and
    3. Kravitz, E. A.
    (1980). Serotonin and octopamine produce opposite postures in lobsters. Science 208, 76-79. doi:10.1126/science.208.4439.76
    OpenUrlAbstract/FREE Full Text
  85. ↵
    1. Lo, L.,
    2. Yao, S.,
    3. Kim, D.-W.,
    4. Cetin, A.,
    5. Harris, J.,
    6. Zeng, H.,
    7. Anderson, D. J. and
    8. Weissbourd, B.
    (2019). Connectional architecture of a mouse hypothalamic circuit node controlling social behavior. Proc. Natl Acad. Sci. USA 116, 7503-7512. doi:10.1073/pnas.1817503116
    OpenUrlAbstract/FREE Full Text
  86. ↵
    1. Lorch, P. D.,
    2. Wilkinson, G. S. and
    3. Reillo, P. R.
    (1993). Copulation duration and sperm precedence in the stalk-eyed fly, Cyrtodiopsis whitei (Diptera: Diopsidae). Behav. Ecol. Sociobiol. 32, 303-311. doi:10.1007/BF00183785
    OpenUrlCrossRefWeb of Science
  87. ↵
    1. Maejima, T.,
    2. Masseck, O. A.,
    3. Mark, M. D. and
    4. Herlitze, S.
    (2013). Modulation of firing and synaptic transmission of serotonergic neurons by intrinsic G protein-coupled receptors and ion channels. Front. Integr. Neurosci. 7, 40. doi:10.3389/fnint.2013.00040
    OpenUrlCrossRefPubMed
  88. ↵
    1. Mandiyan, V. S.,
    2. Coats, J. K. and
    3. Shah, N. M.
    (2005). Deficits in sexual and aggressive behaviors in Cnga2 mutant mice. Nat. Neurosci. 8, 1660-1662. doi:10.1038/nn1589
    OpenUrlCrossRefPubMedWeb of Science
  89. ↵
    1. Martin, C. A. and
    2. Krantz, D. E.
    (2014). Drosophila melanogaster as a genetic model system to study neurotransmitter transporters. Neurochem. Int. 73, 71-88. doi:10.1016/j.neuint.2014.03.015
    OpenUrlCrossRefPubMed
  90. ↵
    1. Masson, J.,
    2. Boris Emerit, M.,
    3. Hamon, M. D. and
    4. Darmon, M.
    (2012). Serotonergic signaling: multiple effectors and pleiotropic effects. Wiley Interdiscip. Rev. Membr. Transp. Signal. 1, 685-713. doi:10.1002/wmts.50
    OpenUrlCrossRef
  91. ↵
    1. Matter, J. M.,
    2. Ronan, P. J. and
    3. Summers, C. H.
    (1998). Central monoamines in free-ranging lizards: Differences associated with social roles and territoriality. Brain Behav. Evol. 51, 23-32. doi:10.1159/000006526
    OpenUrlCrossRefPubMedWeb of Science
  92. ↵
    1. Momohara, Y.,
    2. Kanai, A. and
    3. Nagayama, T.
    (2013). Aminergic control of social status in crayfish agonistic encounters. PLoS ONE 8, e74489. doi:10.1371/journal.pone.0074489
    OpenUrlCrossRefPubMed
  93. ↵
    1. Morrison, T. R.,
    2. Ricci, L. A. and
    3. Melloni, R. H. Jr.
    . (2015). Aggression and anxiety in adolescent AAS-treated hamsters: a role for 5HT3 receptors. Pharmacol. Biochem. Behav. 134, 85-91. doi:10.1016/j.pbb.2015.05.001
    OpenUrlCrossRef
  94. ↵
    1. Mosienko, V.,
    2. Bert, B.,
    3. Beis, D.,
    4. Matthes, S.,
    5. Fink, H.,
    6. Bader, M. and
    7. Alenina, N.
    (2012). Exaggerated aggression and decreased anxiety in mice deficient in brain serotonin. Transl. Psychiatry 2, e122. doi:10.1038/tp.2012.44
    OpenUrlCrossRefPubMed
  95. ↵
    1. Moutkine, I.,
    2. Collins, E. L.,
    3. Béchade, C. and
    4. Maroteaux, L.
    (2019). Evolutionary considerations on 5-HT2 receptors. Pharmacol. Res. 140, 14-20. doi:10.1016/j.phrs.2018.09.014
    OpenUrlCrossRef
  96. ↵
    1. Muehlenkamp, F.,
    2. Lucion, A. and
    3. Vogel, W. H.
    (1995). Effects of selective serotonergic agonists on aggressive behavior in rats. Pharmacol. Biochem. Behav. 50, 671-674. doi:10.1016/0091-3057(95)00351-7
    OpenUrlCrossRefPubMed
  97. ↵
    1. Murakami, G.,
    2. Hunter, R. G.,
    3. Fontaine, C.,
    4. Ribeiro, A. and
    5. Pfaff, D.
    (2011). Relationships among estrogen receptor, oxytocin and vasopressin gene expression and social interaction in male mice. Eur. J. Neurosci. 34, 469-477. doi:10.1111/j.1460-9568.2011.07761.x
    OpenUrlCrossRefPubMed
  98. ↵
    1. Namiki, S.,
    2. Dickinson, M. H.,
    3. Wong, A. M.,
    4. Korff, W. and
    5. Card, G. M.
    (2018). The functional organization of descending sensory-motor pathways in Drosophila. eLife 7, e34272. doi:10.7554/eLife.34272
    OpenUrlCrossRefPubMed
  99. ↵
    1. Nässel, D. R. and
    2. Wegener, C.
    (2011). A comparative review of short and long neuropeptide F signaling in invertebrates: any similarities to vertebrate neuropeptide Y signaling? Peptides 32, 1335-1355. doi:10.1016/j.peptides.2011.03.013
    OpenUrlCrossRefPubMed
  100. ↵
    1. Nakazato, T.
    (2013). Dual modes of extracellular serotonin changes in the rat ventral striatum modulate adaptation to a social stress environment, studied with wireless voltammetry. Exp. Brain Res. 230, 582-596. doi:10.1007/s00221-012-3168-7
    OpenUrlCrossRef
  101. ↵
    1. Nelson, R. J. and
    2. Chiavegatto, S.
    (2001). Molecular basis of aggression. Trends Neurosci. 24, 713-719. doi:10.1016/S0166-2236(00)01996-2
    OpenUrlCrossRefPubMedWeb of Science
  102. ↵
    1. Nelson, R. J. and
    2. Trainor, B. C.
    (2007). Neural mechanisms of aggression. Nat. Rev. Neurosci. 8, 536-546. doi:10.1038/nrn2174
    OpenUrlCrossRefPubMedWeb of Science
  103. ↵
    1. Nouvian, M.,
    2. Mandal, S.,
    3. Jamme, C.,
    4. Claudianos, C.,
    5. d'Ettorre, P.,
    6. Reinhard, J.,
    7. Barron, A. B. and
    8. Giurfa, M.
    (2018). Cooperative defence operates by social modulation of biogenic amine levels in the honey bee brain. Proc. R. Soc. B 285, 20172653. doi:10.1098/rspb.2017.2653
    OpenUrlCrossRefPubMed
  104. ↵
    1. Otopalik, A. G.,
    2. Shin, J.,
    3. Beltz, B. S.,
    4. Sandeman, D. C. and
    5. Kolodny, N. H.
    (2012). Differential uptake of MRI contrast agents indicates charge-selective blood-brain interface in the crayfish. Cell Tissue Res. 349, 493-503. doi:10.1007/s00441-012-1413-9
    OpenUrlCrossRefPubMed
  105. ↵
    1. Otsuna, H. and
    2. Ito, K.
    (2006). Systematic analysis of the visual projection neurons of Drosophila melanogaster. I. Lobula-specific pathways. J. Comp. Neurol. 497, 928-958. doi:10.1002/cne.21015
    OpenUrlCrossRefPubMedWeb of Science
  106. ↵
    1. Panhuis, T. M. and
    2. Wilkinson, G. S.
    (1999). Exaggerated male eye span influences contest outcome in stalk-eyed flies (Diopsidae). Behav. Ecol. Sociobiol. 46, 221-227. doi:10.1007/s002650050613
    OpenUrlCrossRefWeb of Science
  107. ↵
    1. Panksepp, J. B. and
    2. Huber, R.
    (2002). Chronic alterations in serotonin function: Dynamic neurochemical properties in agonistic behavior of the crayfish, Orconectes rusticus. J. Neurobiol. 50, 276-290. doi:10.1002/neu.10035
    OpenUrlCrossRefPubMed
  108. ↵
    1. Panksepp, J. B.,
    2. Yue, Z.,
    3. Drerup, C. and
    4. Huber, R.
    (2003). Amine neurochemistry and aggression in crayfish. Microsc. Res. Techniq. 60, 360-368. doi:10.1002/jemt.10274
    OpenUrlCrossRefPubMed
  109. ↵
    1. Peeke, H. V. S.,
    2. Blank, G. S.,
    3. Figler, M. H. and
    4. Chang, E. S.
    (2000). Effects of exogenous serotonin on a motor behavior and shelter competition in juvenile lobsters (Homarus americanus). J. Comp. Physiol. A 186, 575-582. doi:10.1007/s003590000113
    OpenUrlCrossRefPubMed
  110. ↵
    1. Perez-Rodriguez, M. M.,
    2. Weinstein, S.,
    3. New, A. S.,
    4. Bevilacqua, L.,
    5. Yuan, Q.,
    6. Zhou, Z.,
    7. Hodgkinson, C.,
    8. Goodman, M.,
    9. Koenigsberg, H. W.,
    10. Goldman, D. et al.
    (2010). Tryptophan-hydroxylase 2 haplotype association with borderline personality disorder and aggression in a sample of patients with personality disorders and healthy controls. J. Psychiatr. Res. 44, 1075-1081. doi:10.1016/j.jpsychires.2010.03.014
    OpenUrlCrossRefPubMed
  111. ↵
    1. Peroutka, S. J.
    2. Howell, T. A.
    (1994). The molecular evolution of G protein-coupled receptors: Focus on 5-hydroxytryptamine receptors. Neuropharmacology 33, 319-324. doi:10.1016/0028-3908(94)90060-4
    OpenUrlCrossRefPubMedWeb of Science
  112. ↵
    1. Popova, N. K.,
    2. Naumenko, V. S.,
    3. Cybko, A. S. and
    4. Bazovkina, D. V.
    (2010). Receptor-genes cross-talk: Effect of chronic 5-HT1A agonist 8-Hydroxy-2-(Di-N-Propylamino) Tetralin treatment on the expression of key genes in brain serotonin system and on behavior. Neuroscience 169, 229-235. doi:10.1016/j.neuroscience.2010.04.044
    OpenUrlCrossRef
  113. ↵
    1. Preece, M. A.,
    2. Dailey, J. W.,
    3. Theobald, D. E. H.,
    4. Robbins, T. W. and
    5. Reynolds, G. P.
    (2004). Region specific changes in forebrain 5-hydroxytryptamine1A and 5-hydroxytryptamine2A receptors in isolation-reared rats: an in vitro autoradiography study. Neuroscience 123, 725-732. doi:10.1016/j.neuroscience.2003.10.008
    OpenUrlCrossRefPubMedWeb of Science
  114. ↵
    1. Puciłowski, O.,
    2. Płaźnik, A. and
    3. Kostowski, W.
    (1985). Aggressive behavior inhibition by serotonin and quipazine injected into the amygdala in the rat. Behav. Neural Biol. 43, 58-68. doi:10.1016/S0163-1047(85)91496-7
    OpenUrlCrossRefPubMed
  115. ↵
    1. Rillich, J. and
    2. Stevenson, P. A.
    (2014). A fighter's comeback: dopamine is necessary for recovery of aggression after social defeat in crickets. Horm. Behav. 66, 696-704. doi:10.1016/j.yhbeh.2014.09.012
    OpenUrlCrossRef
  116. ↵
    1. Rillich, J. and
    2. Stevenson, P. A.
    (2018). Serotonin mediates depression of aggression after acute and chronic social defeat stress in a model insect. Front. Behav. Neurosci. 12, 233. doi:10.3389/fnbeh.2018.00233
    OpenUrlCrossRef
  117. ↵
    1. Rillich, J.,
    2. Rillich, B. and
    3. Stevenson, P. A.
    (2019). Differential modulation of courtship behavior and subsequent aggression by octopamine, dopamine and serotonin in male crickets. Horm. Behav. 114, 104542. doi:10.1016/j.yhbeh.2019.06.006
    OpenUrlCrossRef
  118. ↵
    1. Ross, A. P.,
    2. McCann, K. E.,
    3. Larkin, T. E.,
    4. Song, Z.,
    5. Grieb, Z. A.,
    6. Huhman, K. L. and
    7. Albers, H. E.
    (2019). Sex-dependent effects of social isolation on the regulation of arginine-vasopressin (AVP) V1a, oxytocin (OT) and serotonin (5HT) 1a receptor binding and aggression. Horm. Behav. 116, 104578. doi:10.1016/j.yhbeh.2019.104578
    OpenUrlCrossRef
  119. ↵
    1. Sari, Y.
    (2004). Serotonin receptors: from protein to physiological function and behavior. Neurosci. Biobehav. Rev. 28, 565-582. doi:10.1016/j.neubiorev.2004.08.008
    OpenUrlCrossRefPubMedWeb of Science
  120. ↵
    1. Schiller, L.,
    2. Jähkel, M.,
    3. Kretzschmar, M.,
    4. Brust, P. and
    5. Oehler, J.
    (2003). Autoradiographic analyses of 5-HT1A and 5-HT2A receptors after social isolation in mice. Brain Res. 980, 169-178. doi:10.1016/S0006-8993(03)02832-4
    OpenUrlCrossRefPubMed
  121. ↵
    1. Schirmeier, S. and
    2. Klämbt, C.
    (2015). The Drosophila blood-brain barrier as interface between neurons and hemolymph. Mech. Dev. 138, 50-55. doi:10.1016/j.mod.2015.06.002
    OpenUrlCrossRefPubMed
  122. ↵
    1. Sergeyev, V.,
    2. Hökfelt, T. and
    3. Hurd, Y.
    (1999). Serotonin and substance P co-exist in dorsal raphe neurons of the human brain. Neuroreport 10, 3967-3970. doi:10.1097/00001756-199912160-00044
    OpenUrlCrossRefPubMedWeb of Science
  123. ↵
    1. Shaikh, M. B.,
    2. De Lanerolle, N. C. and
    3. Siegel, A.
    (1997). Serotonin 5-HT1A and 5-HT2/1C receptors in the midbrain periaqueductal gray differentially modulate defensive rage behavior elicited from the medial hypothalamus of the cat. Brain Res. 765, 198-207. doi:10.1016/S0006-8993(97)00433-2
    OpenUrlCrossRefPubMed
  124. ↵
    1. Sibbald, E. D. and
    2. Plowwright, C. M. S.
    (2014). Social interactions and their connection to aggression and ovarian development in orphaned worker bumblebees (Bombus impatiens). Behav. Processes 103, 150-155. doi:10.1016/j.beproc.2013.11.012
    OpenUrlCrossRef
  125. ↵
    1. Sizemore, T. R. and
    2. Dacks, A. M.
    (2016). Serotonergic modulation differentially targets distinct network elements within the antennal lobe of Drosophila melanogaster. Sci. Rep. 6, 37119. doi:10.1038/srep37119
    OpenUrlCrossRefPubMed
  126. ↵
    1. Stevenson, P. A. and
    2. Rillich, J.
    (2013). Isolation associated aggression: a consequence of recovery from defeat in a territorial animal. PLoS One 9, e74965. doi:10.1371/journal.pone.0074965
    OpenUrlCrossRef
  127. ↵
    1. Stevenson, P. A. and
    2. Rillich, J.
    (2017). Neuromodulators and the control of aggression in crickets. In The Cricket as a Model Organism (ed. H. W. Horch, T. Mito, A. Popadic, H. Ohuhi and S. Noji), pp. 169-196. New York, NY; Berlin: Springer.
  128. ↵
    1. Stevenson, P. A.,
    2. Hofmann, H. A.,
    3. Schoch, K. and
    4. Schildberger, K.
    (2000). The fight and flight responses of crickets depleted of biogenic amines. J. Neurobiol. 43, 107-120. doi:10.1002/(SICI)1097-4695(200005)43:2<107::AID-NEU1>3.0.CO;2-C
    OpenUrlCrossRefPubMedWeb of Science
  129. ↵
    1. Stowers, L.,
    2. Holy, T. E.,
    3. Meister, M.,
    4. Dulac, C. and
    5. Koentges, G.
    (2002). Loss of sex discrimination and male-male aggression in mice deficient for TRP2. Science 295, 1493-1500. doi:10.1126/science.1069259
    OpenUrlAbstract/FREE Full Text
  130. ↵
    1. Summers, C. H. and
    2. Winberg, S.
    (2006). Interactions between the neural regulation of stress and aggression. J. Exp. Biol. 209, 4581-4589. doi:10.1242/jeb.02565
    OpenUrlAbstract/FREE Full Text
  131. ↵
    1. Summers, C. H.,
    2. Summers, T. R.,
    3. Moore, M. C.,
    4. Korzan, W. J.,
    5. Woodley, S. K.,
    6. Ronan, P. J.,
    7. Höglund, E.,
    8. Watt, M. J. and
    9. Greenberg, N.
    (2003). Temporal patterns of limbic monoamine and plasma corticosterone response during social stress. Neuroscience 116, 553-563. doi:10.1016/S0306-4522(02)00708-X
    OpenUrlCrossRefPubMedWeb of Science
  132. ↵
    1. Summers, C. H.,
    2. Korzan, W. J.,
    3. Lukkes, J. L.,
    4. Watt, M. J.,
    5. Forster, G. L.,
    6. Øverli, Ø.,
    7. Höglund, E.,
    8. Larson, E. T.,
    9. Ronan, P. J.,
    10. Matter, J. M. et al.
    (2005a). Does serotonin influence aggression? comparing regional activity before and during social interaction. Physiol. Biochem. Zool. 78, 679-694. doi:10.1086/432139
    OpenUrlCrossRefPubMedWeb of Science
  133. ↵
    1. Summers, C. H.,
    2. Forster, G. L.,
    3. Korzan, W. J.,
    4. Watt, M. J.,
    5. Larson, E. T.,
    6. Øverli, Ø.,
    7. Höglund, E.,
    8. Ronan, P. J.,
    9. Summers, T. R.,
    10. Renner, K. J.
    et al. (2005b). Dynamics and mechanics of social rank reversal. J. Comp. Physiol. A 191, 241-252. doi:10.1007/s00359-004-0554-z
    OpenUrlCrossRefPubMed
  134. ↵
    1. Szczuka, A.,
    2. Korczynska, J.,
    3. Wnuk, A.,
    4. Symonowicz, B.,
    5. Szwacka, A. G.,
    6. Mazurkiewicz, P.,
    7. Kostowski, W. and
    8. Godzinska, E. J.
    (2013). The effects of serotonin, dopamine, octopamine and tyramine on behavior of workers of the ant Formica polyctena during dyadic aggression tests. Acta Neurobiol. Exp. 73, 495-520. doi:10.1016/j.beproc.2014.07.009
    OpenUrlCrossRefPubMed
  135. ↵
    1. Takahashi, A.,
    2. Shiroishi, T. and
    3. Koide, T.
    (2011). Escalated aggression in Japanese wild-derived mouse strain MSM and brain 5-HT system. Genes Genet. Syst. 86, 403-403. doi:10.3389/fnins.2014.00156
    OpenUrlCrossRef
  136. ↵
    1. Takahashi, A.,
    2. Quadros, I. M.,
    3. de Almeida, R. M. M. and
    4. Micek, K. A.
    (2012). Behavioral and pharmacogenetics of aggressive behavior. Curr. Top. Behav. Neurosci. 12, 73-138. doi:10.1007/7854_2011_191
    OpenUrlCrossRef
  137. ↵
    1. Takahashi, A.,
    2. Lee, R. X.,
    3. Iwasato, T.,
    4. Itohara, S.,
    5. Arima, H.,
    6. Bettler, B.,
    7. Miczek, K. A. and
    8. Koide, T.
    (2015). Glutamate input in the dorsal raphe nucleus as a determinant of escalated aggression in male mice. J. Neurosci. 35, 6452-6463. doi:10.1523/JNEUROSCI.2450-14.2015
    OpenUrlAbstract/FREE Full Text
  138. ↵
    1. Tanaka, N. K.,
    2. Endo, K. and
    3. Ito, K.
    (2012). Organization of antennal lobe-associated neurons in adult Drosophila melanogaster brain. J. Comp. Neurol. 520, 4067-4130. doi:10.1002/cne.23142
    OpenUrlCrossRefPubMed
  139. ↵
    1. Ten Eyck, G. R.
    (2008). Serotonin modulates vocalizations and territorial behavior in an amphibian. Behav. Brain Res. 193, 144-147. doi:10.1016/j.bbr.2008.05.001
    OpenUrlCrossRefPubMed
  140. ↵
    1. Terranova, J. I.,
    2. Song, Z. M.,
    3. Larkin, T. E.,
    4. Hardcastle, N.,
    5. Norvelle, A.,
    6. Riaz, A. and
    7. Albers, H. E.
    (2016). Serotonin and arginine-vasopressin mediate sex differences in the regulation of dominance and aggression by the social brain. Proc. Natl. Acad. Sci. USA 113, 13233-13238. doi:10.1073/pnas.1610446113
    OpenUrlAbstract/FREE Full Text
  141. ↵
    1. Tierney, A. J.
    (2018). Invertebrate serotonin receptors: a molecular perspective on classification and pharmacology. J. Exp. Biol. 221, jeb184838. doi:10.1242/jeb.184838
    OpenUrlAbstract/FREE Full Text
  142. ↵
    1. Toth, M.,
    2. Mikics, E.,
    3. Tulogdi, A.,
    4. Aliczki, M. and
    5. Haller, J.
    (2011). Post-weaning social isolation induces abnormal forms of aggression in conjunction with increased glucocorticoid and autonomic stress responses. Horm. Behav. 60, 28-36. doi:10.1016/j.yhbeh.2011.02.003
    OpenUrlCrossRefPubMedWeb of Science
  143. ↵
    1. Twenge, J. M.,
    2. Baumeister, R. F.,
    3. Tice, D. M. and
    4. Stucke, T. S.
    (2001). If you can't join them, beat them: effects of social exclusion on aggressive behavior. J. Pers. Soc. Psychol. 81, 1058-1069. doi:10.1037/0022-3514.81.6.1058
    OpenUrlCrossRefPubMedWeb of Science
  144. ↵
    1. van der Vegt, B. J.,
    2. Lieuwes, N.,
    3. Cremers, T. I. F. H.,
    4. de Boer, S. F. and
    5. Koolhaas, J. M.
    (2003a). Cerebrospinal fluid monoamine and metabolite concentrations and aggression in rats. Horm. Behav. 44, 199-208. doi:10.1016/S0018-506X(03)00132-6
    OpenUrlCrossRefPubMedWeb of Science
  145. ↵
    1. van der Vegt, B. J.,
    2. Lieuwes, N.,
    3. van de Wall, E. H. E. M.,
    4. Kato, K.,
    5. Moya-Albiol, L.,
    6. Martínez-Sanchis, S.,
    7. de Boer, S. F. and
    8. Koolhaas, J. M.
    (2003b). Activation of serotonergic neurotransmission during the performance of aggressive behavior in rats. Behav. Neurosci. 117, 667-674. doi:10.1037/0735-7044.117.4.667
    OpenUrlCrossRefPubMedWeb of Science
  146. ↵
    1. Veneema, A. H.
    (2009). Early life stress, the development of aggression and neuroendocrine and neurobiological correlates: what can we learn from animal models? Front. Neuroendocrinol. 30, 497-518. doi:10.1016/j.yfrne.2009.03.003
    OpenUrlCrossRefPubMedWeb of Science
  147. ↵
    1. Villalba, C.,
    2. Boyle, P. A.,
    3. Caliguri, E. J. and
    4. De Vries, G. J.
    (1997). Effects of the selective serotonin reuptake inhibitor fluoxetine on social behaviors in male and female prairie voles (Microtus ochrogaster). Hormones Behav. 32, 184-191. doi:10.1006/hbeh.1997.1420
    OpenUrlCrossRefPubMed
  148. ↵
    1. Vleugels, R.,
    2. Lenaerts, C.,
    3. Baumann, A.,
    4. Vanden Broeck, J. and
    5. Verlinden, H.
    (2013). Pharmacological characterization of a 5-HT1-type serotonin receptor in the red flour beetle, Tribolium castaneum. PLoS ONE 8, e65052. doi:10.1371/journal.pone.0065052
    OpenUrlCrossRef
  149. ↵
    1. Vleugels, R.,
    2. Verlinden, H. and
    3. Vanden Broeck, J.
    (2015). Serotonin, serotonin receptors and their actions in insects. Neurotransmitter 2, 1-14.
    OpenUrl
    1. Wacker, D. and
    2. Ludwig, M.
    (2019). The role of vasopressin in olfactory and visual processing. Cell Tissue Res. 375, 201-215. doi:10.1007/s00441-018-2867-1
    OpenUrlCrossRef
  150. ↵
    1. Wakabayashi-Ito, N.,
    2. Doherty, O. M.,
    3. Moriyama, H.,
    4. Breakefield, X. O.,
    5. Gusella, J. F.,
    6. O'Donnell, J. M. and
    7. Ito, N.
    (2011). dtorsin, the Drosophila ortholog of the early-onset dystonia TOR1A (DYT1), plays a novel role in dopamine metabolism. PLoS ONE 6, e26183. doi:10.1371/journal.pone.0026183
    OpenUrlCrossRefPubMed
  151. ↵
    1. Wang, L. and
    2. Anderson, D. J.
    (2010). Identification of an aggression-promoting pheromone and its receptor neurons in Drosophila. Nature 463, 227-231. doi:10.1038/nature08678
    OpenUrlCrossRefPubMedWeb of Science
  152. ↵
    1. Watt, M. J.,
    2. Forster, G. L.,
    3. Korzan, W. J.,
    4. Renner, K. J. and
    5. Summers, C. H.
    (2007). Rapid neuroendocrine responses evoked at the onset of social challenge. Physiol. Behav. 90, 567-575. doi:10.1016/j.physbeh.2006.11.006
    OpenUrlCrossRefPubMed
  153. ↵
    1. Weiger, W. A.
    (1997). Serotonergic modulation of behaviour: a phylogenetic overview. Biol. Rev. 72, 61-95. doi:10.1017/S0006323196004975
    OpenUrlCrossRefPubMed
  154. ↵
    1. Wilkinson, G. S. and
    2. Dodson, G. N.
    (1997). Function and evolution of antlers and eye stalks in flies. In The Evolution of Mating Systems in Insects and Arachnids (ed. J. Choe and B. Crespi), pp. 310-328. Cambridge: Cambridge University Press.
  155. ↵
    1. Wilkinson, G. S. and
    2. Johns, P. M.
    (2005). Sexual selection and the evolution of fly mating systems. In The Biology of the Diptera (ed. D. K. Yeates and B. M. Weigmann), pp. 312-339. New York: Columbia University Press.
  156. ↵
    1. Wilkinson, G. S.,
    2. Kahler, H. and
    3. Baker, R. H.
    (1998). Evolution of female mating preferences in stalk-eyed flies. Behav. Ecol. 9, 525-533. doi:10.1093/beheco/9.5.525
    OpenUrlCrossRefWeb of Science
  157. ↵
    1. Wongwitdecha, N. and
    2. Marsden, C. A.
    (1996). Social isolation increases aggressive behaviour and alters the effects of diazepam in the rat social interaction test. Behav. Brain Res. 75, 27-32. doi:10.1016/0166-4328(96)00181-7
    OpenUrlCrossRefPubMed
  158. ↵
    1. Yeh, S.-R.,
    2. Fricke, R. A. and
    3. Edwards, D. H.
    (1996). The effect of social experience on serotonergic modulation of the escape circuit of crayfish. Science 271, 366-369. doi:10.1126/science.271.5247.366
    OpenUrlAbstract
  159. ↵
    1. Zelikowsky, M.,
    2. Hui, M.,
    3. Karigo, T.,
    4. Choe, A.,
    5. Yang, B.,
    6. Blanco, M. R.,
    7. Beadle, K.,
    8. Gradinaru, V.,
    9. Deverman, B. E. and
    10. Anderson, D. J.
    (2018). The neuropeptide Tac2 controls a distributed brain state induced by chronic social isolation stress. Cell 173, 1265-1279.e19. doi:10.1016/j.cell.2018.03.037
    OpenUrlCrossRefPubMed
  160. ↵
    1. Zhou, C.,
    2. Rao, Y. and
    3. Rao, Y.
    (2008). A subset of octopaminergic neurons are important for Drosophila aggression. Nat. Neurosci. 11, 1059-1067. doi:10.1038/nn.2164
    OpenUrlCrossRefPubMedWeb of Science
View Abstract
Previous ArticleNext Article
Back to top
Previous ArticleNext Article

This Issue

Keywords

  • Serotonin
  • 5-HT receptors
  • Monoamines

 Download PDF

Email

Thank you for your interest in spreading the word on Journal of Experimental Biology.

NOTE: We only request your email address so that the person you are recommending the page to knows that you wanted them to see it, and that it is not junk mail. We do not capture any email address.

Enter multiple addresses on separate lines or separate them with commas.
The stalk-eyed fly as a model for aggression – is there a conserved role for 5-HT between vertebrates and invertebrates?
(Your Name) has sent you a message from Journal of Experimental Biology
(Your Name) thought you would like to see the Journal of Experimental Biology web site.
CAPTCHA
This question is for testing whether or not you are a human visitor and to prevent automated spam submissions.
Share
COMMENTARY
The stalk-eyed fly as a model for aggression – is there a conserved role for 5-HT between vertebrates and invertebrates?
Andrew N. Bubak, Michael J. Watt, Jazmine D. W. Yaeger, Kenneth J. Renner, John G. Swallow
Journal of Experimental Biology 2020 223: jeb132159 doi: 10.1242/jeb.132159 Published 2 January 2020
del.icio.us logo Digg logo Reddit logo Twitter logo CiteULike logo Facebook logo Google logo Mendeley logo
Citation Tools
COMMENTARY
The stalk-eyed fly as a model for aggression – is there a conserved role for 5-HT between vertebrates and invertebrates?
Andrew N. Bubak, Michael J. Watt, Jazmine D. W. Yaeger, Kenneth J. Renner, John G. Swallow
Journal of Experimental Biology 2020 223: jeb132159 doi: 10.1242/jeb.132159 Published 2 January 2020

Citation Manager Formats

  • BibTeX
  • Bookends
  • EasyBib
  • EndNote (tagged)
  • EndNote 8 (xml)
  • Medlars
  • Mendeley
  • Papers
  • RefWorks Tagged
  • Ref Manager
  • RIS
  • Zotero
Alerts

Please log in to add an alert for this article.

Sign in to email alerts with your email address

Article navigation

  • Top
  • Article
    • ABSTRACT
    • Introduction
    • The role of 5-HT in vertebrate and invertebrate aggression
    • Caveats in understanding invertebrate 5-HT and aggression
    • 5-HT receptor subtypes and aggression
    • The stalk-eyed fly (T. dalmanni) as a case study
    • Comparing the role of 5-HT in aggression in vertebrates and invertebrates – where do we go from here?
    • Conclusions
    • Acknowledgements
    • FOOTNOTES
    • References
  • Figures & tables
  • Supp info
  • Info & metrics
  • PDF + SI
  • PDF

Related articles

Cited by...

More in this TOC section

  • Thermal robustness of biomechanical processes
  • Help, there are ‘omics’ in my comparative physiology!
  • Structural plasticity of the avian pectoralis: a case for geometry and the forgotten organelle
Show more COMMENTARY

Similar articles

Other journals from The Company of Biologists

Development

Journal of Cell Science

Disease Models & Mechanisms

Biology Open

Advertisement

Meet the Editors at SICB Virtual 2021

Reserve your place to join some of the journal editors, including Editor-in-Chief Craig Franklin, at our Meet the Editor session on 17 February at 2pm (EST). Don’t forget to view our SICB Subject Collection, featuring relevant JEB papers relating to some of the symposia sessions.


2020 at The Company of Biologists

Despite 2020's challenges, we were able to bring a number of long-term projects and new ventures to fruition. As we enter a new year, join us as we reflect on the triumphs of the last 12 months.


The Big Biology podcast

JEB author Christine Cooper talks to Big Biology about her research. In this fascinating JEB sponsored podcast she tells us how tough zebra finches adjust their physiology to cope with extreme climate events. 


Developmental and reproductive physiology of small mammals at high altitude

Cayleih Robertson and Kathryn Wilsterman focus on high-altitude populations of the North American deer mouse in their review of the challenges and evolutionary innovations of pregnant and nursing small mammals at high altitude.


Read & Publish participation extends worldwide

“Being able to publish Open Access articles free of charge means that my article gets maximum exposure and has maximum impact, and that all my peers can read it regardless of the agreements that their universities have with publishers.”

Professor Roi Holzman (Tel Aviv University) shares his experience of publishing Open Access as part of our growing Read & Publish initiative. We now have over 60 institutions in 12 countries taking part – find out more and view our full list of participating institutions.

Articles

  • Accepted manuscripts
  • Issue in progress
  • Latest complete issue
  • Issue archive
  • Archive by article type
  • Special issues
  • Subject collections
  • Interviews
  • Sign up for alerts

About us

  • About JEB
  • Editors and Board
  • Editor biographies
  • Travelling Fellowships
  • Grants and funding
  • Journal Meetings
  • Workshops
  • The Company of Biologists
  • Journal news

For Authors

  • Submit a manuscript
  • Aims and scope
  • Presubmission enquiries
  • Article types
  • Manuscript preparation
  • Cover suggestions
  • Editorial process
  • Promoting your paper
  • Open Access
  • Outstanding paper prize
  • Biology Open transfer

Journal Info

  • Journal policies
  • Rights and permissions
  • Media policies
  • Reviewer guide
  • Sign up for alerts

Contact

  • Contact JEB
  • Subscriptions
  • Advertising
  • Feedback

 Twitter   YouTube   LinkedIn

© 2021   The Company of Biologists Ltd   Registered Charity 277992