No full-text available
To read the full-text of this research,
you can request a copy directly from the authors.
Mechanisms of experience dependent control of aggression in crickets
... size, strength, weaponry) 12-15 as well as on aggressive motivation 16 . The latter is a product of several factors, including the presence of resources 17-21 , social upbringing 22 , physical exertion 23 and experience in previous fights [24][25][26] . ...
... To date, relatively few model systems have been developed to shed light on how previous experience modifies aggressive behaviour in arthropods, mainly crickets 26 , drosophilid flies 43 and ants 28 (see also recent reviews 4,9,22,44 ). We propose a new model system, the olive fruit fly, Bactrocera oleae (Rossi) (Diptera: Tephritidae). ...
... Previous aggressive experience influences the outcome of conflicts, such that winners are more likely to win again and losers will more likely lose again 26,32,37,50 . In agreement with our first hypothesis, our data on the winner effect (Experiment 1) are consistent with earlier studies in other invertebrate species, in which aggression levels, fighting duration and/or probability of winning were higher in previous contest winners than in naïve ones (i.e. ...
In several animal species, aggressive experience influences the characteristics and outcomes of subsequent conflicts, such that winners are more likely to win again (the winner effect) and losers more likely to lose again (the loser effect). We tested the olive fruit fly, Bactrocera oleae (Diptera: Tephritidae), as a model system to evaluate the role of the winner and loser effects in male-male territorial contests. Further, we conducted experiments to test if winning and losing probabilities are affected only by the outcome of the previous contests, or whether the fighting experience itself is sufficient to induce an effect. Both winners and losers of two consecutive encounters displayed higher intensity of aggression and fought longer in subsequent contests. In both cases, they achieved higher fighting success than naïve males. The enhanced fighting performance of both winners and losers was stimulated by merely experiencing a contest, not necessarily by the relative outcome of previous fights. Overall, this study highlights the fact that previous victories and defeats both enhance aggressive behaviour in olive fruit flies, allowing them to achieve higher fighting success in subsequent contests against inexperienced males.
... Only a few insect models have been tested to study the effect of experience on aggressive behaviour, mainly crickets (Stevenson & Schildberger, 2013) and drosophilid flies (Yurkovic et al., 2010;Zwarts, Versteven, & Callaerts, 2012). True fruit flies (Diptera: Tephritidae) are good insect models for studying aggression. ...
... hyperaggressive performances, hereafter) in subsequent contests than naïve males. These findings are consistent with those of previous studies on several invertebrate species (Hsu et al., 2006;Stevenson & Schildberger, 2013), in which aggression intensity, fighting duration and/or probability of winning were higher in previous contest winners than in naïve contestants (i.e. cricket, Adamo & Hoy, 1995;crayfish, Bergman et al., 2003). ...
... To the best of our knowledge, this is the first evidence that consecutive defeats can reverse the loser effect, leading to higher fighting success. Although extensive research has been conducted to understand the role of social experience in affecting the outcomes of aggression, the ultimate and proximate causes for the existence of the winner and loser effects are unknown (Hsu et al., 2006;Rutte et al., 2006;Stevenson & Schildberger, 2013). Rutte et al. (2006) formulated two adaptive hypotheses to explain these effects, namely the 'social-cue hypothesis' (i.e. ...
In many animals, after experiencing an intraspecific aggressive interaction, winners are more likely to win again (the winner effect) and losers more likely to lose again (the loser effect). However, the winner and loser effect has been studied in few arthropod models, and comparative approaches between the sexes are hard to find. In this study, we evaluated the role of previous experience in male–male and female–female contests of Mediterranean fruit flies, Ceratitis capitata (Diptera: Tephritidae). In this species, lekking males fight for courtship territories, while females fight to maintain single oviposition sites, as well as for mates. We addressed the following questions. (1) Are winners more likely to win again and losers more likely to lose again? (2) Are different interfight intervals critical to detect experience-induced effects on aggression? (3) Are winning and losing probabilities affected solely by the outcome of the previous contests, or is fighting experience itself sufficient to induce the effect? (4) Does experience affect differently aggression displayed by males and females? Results showed reduced fighting success in males and females that experienced a single defeat, while individuals that experienced two previous victories or defeats had higher aggression rates and more wins in subsequent contests (i.e. hyperaggression). This was achieved merely by experiencing a contest, while the actual outcomes of previous fights did not affect the aggressiveness level. Some differences were documented between male–male and female–female contests (e.g. females fought longer than males), showing the value of a comparative approach between the sexes when studying experience-induced hyperaggression. This study highlights that both consecutive victories and defeats enhance fighting performances of fruit fly males and females defending courtship territories and oviposition sites, respectively. To the best of our knowledge, this is the first evidence about how repeated defeat experiences reverse the loser effect in animals, leading to higher fighting success.
... The monoamines serotonin (5-HT), dopamine (DA), and octopamine (OA), the invertebrate analogue to norepinephrine, regulate specific individual behaviors in a variety of invertebrate and vertebrate species [21][22][23][24][25][26][27][28][29][30][31][32]. For social insects, the monoamines modulate many behaviors important to ant colony function, including colony formation, reproductive dominance, division of labor, behavioral development, trophallaxis, predatory aggression, trail following, and nestmate recognition [21][22][23][24][25][26][27][28][29][30][31][32]. ...
... The monoamines serotonin (5-HT), dopamine (DA), and octopamine (OA), the invertebrate analogue to norepinephrine, regulate specific individual behaviors in a variety of invertebrate and vertebrate species [21][22][23][24][25][26][27][28][29][30][31][32]. For social insects, the monoamines modulate many behaviors important to ant colony function, including colony formation, reproductive dominance, division of labor, behavioral development, trophallaxis, predatory aggression, trail following, and nestmate recognition [21][22][23][24][25][26][27][28][29][30][31][32]. For example, neural 5-HT and DA have been shown to modulate social food flow among workers using trophallaxis as well as division of labor [21][22][23]. ...
Ant colonies are distributed systems that are regulated in a non-hierarchical manner. Without a central authority, individuals inform their decisions by comparing information in local cues to a set of inherent behavioral rules. Individual behavioral decisions collectively change colony behavior and lead to self-organization capable of solving complex problems such as the decision to engage in aggressive societal conflicts with neighbors. Despite the relevance to colony fitness, the mechanisms that drive individual decisions leading to cooperative behavior are not well understood. Here we show how sensory information , both tactile and chemical, and social context—isolation, nestmate interaction, or fighting non-nestmates—affects brain monoamine levels in pavement ants (Tetramorium caespitum). Our results provide evidence that changes in octopamine and serotonin in the brains of individuals are sufficient to alter the decision by pavement ants to be aggressive towards non-nestmate ants whereas increased brain levels of dopamine correlate to physical fighting. We propose a model in which the changes in brain states of many workers collectively lead to the self-organization of societal aggression between neighboring colonies of pavement ants.
... Special emphasis was placed on intraspecific behaviour. Additionally, some of the animals were administered octopamine hydrochloride or dopamine hydrochloride orally, as both substances are known to modulate competitive and task-related behaviour Stevenson & Schildberger, 2013;. Lastly, survival was tested under varying regimes of competition, host availability and amine treatment. ...
... Most of the studies into the role of OA in response thresholds and reward value have been conducted using sugar or other food rewards cementing the theory of OA being the modulator of reward. A reduction in competitive behaviour in OA-depleted individuals has been consequently explained as well by OA's role in reward assessment Stevenson & Schildberger, 2013). However, it has long been known that OA is essential in the activation of the energy metabolism as well and, accordingly, reduced aggressiveness in OA-depleted animals might have nothing to do with reward modulation, but rather be the result of deficiencies in the activation of energetic reserves . ...
Animals exploit complex environments in an optimal way, often with limited brain capacities. Interestingly, it is largely unknown, how they do so. This thesis comprises five studies investigating proximate mechanisms modulating the searching behaviour of parasitoid wasps. These organisms serve as excellent organisms for such questions due to their tight link of searching success and fitness. While the first study assumed a simple motor response to serve as a heuristic, yet effective, mechanism, the remaining studies focussed on the role of octopamine [OA] and dopamine [DA]. Both substances being essential in the assessment of reward and aversive stimuli, respectively. Neither the assumed motor response could be met nor did OA or DA reveal any consistent effects with respect to the assessment of rewards and costs. DA slightly impacted the movement pattern. Treatment with OA revealed numerous effects, in total indicating an influence on stress level. Both is in line with studies on other species. Yet, although OA significantly influences searching behaviour, the underlying mechanism is considerably more complex than initially assumed. Last, it was shown that a generalisation on the basis of a few studies and stimuli with respect to the role of OA in the integration of rewards is a simplification.
... Biogenic amines have also been implicated in the modulation of aggression in a number of invertebrate models (Kravitz and Huber 2003;Stevenson and Schildberger 2013;Alekseyenko and Kravitz 2014;Bubak et al. 2014a). The roles of OA, the invertebrate "fight or flight" neurotransmitter, and 5-HT have been extensively explored, especially in the social context-dependent initiation and escalation of fighting behavior and establishment of dominance. ...
... Intriguingly, the trend for higher brain DA in parental (breeding) females compared to nonbreeding females, and the lack of a similar trend in breeding males, may similarly reflect a role for DA in mediating the fine adjustments in the intensity of parental care activities between the sexes, and would be in accord with established behavioral sex differences, given that N. orbicollis females spend significantly more time provisioning larvae compared to males (Fetherston et al. 1990). The absence of a significant change in either OA or 5-HT brain levels in parental beetles is surprising, given that OA has been implicated in altering the threshold for task-related behavioral transitions (Schulz et al. 2002a(Schulz et al. , 2002b, while 5-HT linked to the modulation of social context-dependent aggression in a number of insects (Stevenson and Schildberger 2013;Alekseyenko and Kravitz 2014;Bubak et al. 2014a). ...
Burying beetles Nicrophorus orbicollis exhibit facultative biparental care of young. To reproduce, a male–female burying beetle pair bury and prepare a small vertebrate carcass as food for its altricial young. During a breeding bout, male and female behavior changes synchronously at appropriate times and is coordinated to provide effective care for offspring. Although the ecological and evolutionary factors that shape this remarkable reproductive plasticity are well characterized, the neuromodulation of parental behavior is poorly understood. Juvenile hormone levels rise dramatically at the time beetle parents accept and feed larvae, remain highly elevated during the stages of most active care and fall abruptly when care is terminated. However, hormonal fluctuations alone cannot account for this elaborate control of reproduction. The biogenic amines octopamine (OA), dopamine (DA), and serotonin (5-HT) mediate a diversity of insect reproductive and social behaviors. In this study, we measured whole brain monoamine levels in individual male and female burying beetles and compared OA, DA, and 5-HT profiles between breeding (parental) and nonbreeding, unmated beetles. Remarkably, after 24 h of care, when parental feeding rates begin to peak, DA brain levels increase in breeding beetles when compared to nonbreeding controls. In contrast, brain OA and 5-HT levels did not change significantly. These results provide the first evidence for a potential role of DA in the modulation of burying beetle parental behavior.
... In the present study in an attempt to have an insight for the role of biogenic amines, a significant elevation of DA and 5-HT in males and females on the 10 th , 20 th , and 30 th days of tunneling is implying the probable role of these neurotransmitters in nesting behaviour (Misof et al. 2014;Song et al. 2015;Kamhi et al. 2017). A marginal high titer of 5-HT in males compared to females (Trumbo 2019) can be correlated to the social context-dependent aggression in males during copulation (Stevenson and Schildberger 2013;Alekseyenko and Kravitz 2014). Parallel to the increase in 5-HT, an increased level of DA in males and females further reflects and proves the mitigating role of DA and its delicate adjustments in reinforcing the nesting activities (Rillich and Stevenson 2014;Guerra et al. 2016;Bhatt et al. 2018;Auletta 2019). ...
Dung beetles belonging to the subfamily Scarabaeinae are ecologically important organisms that feed primarily on mammalian dung for their nesting and brooding. The paracoprids are characterized for their complex tunnel-making behaviour. The present study revealed the role of neurotransmitters in the nesting behaviour of Digitonthophagus
gazella (Fabricius in Mantissa insectorum sistens species nuper detectas adiectis synonymis, observation ibus, descriptionibus, emendationibus, 1787) (Coleoptera: Scarabaeidae) under laboratory conditions. The development period was observed to be 31 days, comprising of four stages- egg, larva (1st instar, 2nd instar, and 3rd instar),
pupa, and adult. The nesting pattern of D. gazella showed a time dependent increase in the length (14.7 ± 0.1 cm,16.9 ± 0.1 cm and 19.8 ± 0.1 cm), and total depth (9.8 ± 0.1 cm, 12.9 ± 0.1 cm and 13.5 ± 0.1 cm) of the tunnel on 10th, 20th, and 30th day. Estimation of the neurotransmitters revealed that acetylcholine esterase (AChE), biogenic amines- 5-hydroxytryptamine serotonin (5-HT); dopamine (DA), and nitric oxide (NO) increased significantly (p < 0.01) in a time dependent manner in both male and female, suggesting their role in parental behaviour. These results provide the first evidence for a potential role of neurotransmitters in the modulation of nesting behaviour of the dung beetle; D. gazella.
... Interestingly, bystanders, who do not engage in overt confrontation but simply observe a contest, also change their winning and losing probabilities in future contests (Figure 1B-5; Johnsson and Åkerman, 1998;Silk, 1999;Oliveira et al., 2001; for review on the ''bystander effect'' and bystander-related phenomena, see Oliveira, 2005). Similar effects have been described in rodents ( Van de Poll et al., 1982;Fuxjager and Marler, 2010), humans (Page and Coates, 2017), and invertebrates (Van Wilgenburg et al., 2010;Stevenson and Schildberger, 2013;Benelli et al., 2015). Efforts have been made to uncover the mechanisms supporting these behavioral observations. ...
Social status is recognized as a major determinant of social behavior and health among animals; however, the neural circuits supporting the formation and navigation of social hierarchies remain under extensive research. Available evidence suggests the prefrontal cortex is a keystone in this circuit, but upstream and downstream candidates are progressively emerging. In this review, we compare and integrate findings from rodent and primate studies to create a model of the neural and cellular networks supporting social hierarchies, both from a macro (i.e., circuits) to a micro-scale perspective (microcircuits and synapses). We start by summarizing the literature on the prefrontal cortex and other relevant brain regions to expand the current “prefrontal-centric” view of social hierarchy behaviors. Based on connectivity data we also discuss candidate regions that might inspire further investigation, as well as the caveats and strategies that have been used to further our understanding of the biological substrates underpinning social hierarchy and dominance.
... Our results suggest that mandible length of male G. firmus is a signal or indicator of RHP in addition to being important in physical combat. This result is in line with Rillich et al. (2007; see also Stevenson and Schildberger 2013) who found that male G. bimaculatus field crickets settle fights according to the cumulative assessment model (CAM), a form of persistence by self-assessment. In contrast, Briffa (2008) found that fights between male Acheta domesticus house crickets appear to be settled via mutual assessment, while Judge and Bonanno (2008) failed to meet any Fig. 4 Probability of larger rival winning a contest increases with increasing RHP asymmetry (absolute difference in trait size) between rivals (n= 414 contests) Statistical results are from generalized linear models having either a Gaussian (contest duration) or Poisson (contest intensity) family of errors. ...
The ability to win fights is expected to be influenced by the rearing and nutritional conditions experienced by individuals. We hypothesized that crowded rearing conditions would foreshadow intense competition for resources in adult male Gryllus firmus (Scudder) field crickets and thus favour greater investment in mandibular weaponry. In line with prediction, males developed relatively larger weapons in crowded rearing conditions but this investment did not translate into greater success in contests against size-matched males that were reared singly. Rather, we found that low-density males were more likely to defeat high-density males under some experimental conditions, possibly because low-density males are more aggressive. Overall, our strongest observed effect was that males with larger weaponry were more likely to win contests, independent of rearing density. We also manipulated the adult diet of males to test the hypothesis that greater fat loads, and thus potentially greater stamina, would improve success in contests. Contrary to prediction, increased fat load did not increase a male’s probability of winning a contest possibly because fights in field crickets are too short to invoke stamina. Broadly speaking, animals decide whether to give up in a fight by assessing either their own (self-assessment) resource-holding potential (RHP) or by assessing a combination of their own and their opponent’s RHP (mutual assessment). Our study lends some support to the hypothesis that male G. firmus crickets decide to persist in a fight by assessing their own RHP rather than via mutual assessment.
Significance statement
Animals fight each other for access to, and control of, resources that they require for survival and reproduction (e.g. food, shelter, and mates). Although considerable empirical research has shown that individuals having a larger body size or weapons generally possess greater fighting ability—resource-holding potential (RHP)—and are thus typically more successful in combat, the factors contributing to the development of an individual’s RHP have received less attention. One potential environmental factor dictating RHP is population density; however, the effect of density on RHP is difficult to predict. Developing under high density could cause individuals to invest more in RHP-related traits because these conditions might signal intense competition for mates in the near future. However, individuals reared under high density are often less aggressive than their low-density counterparts. The food available to an adult could also be important because the consumption of fat could improve an individual’s stamina, an RHP-related trait important in combat. Our study testing the impact of these two factors on male fighting ability in the sand field cricket (Gryllus firmus) found limited support for the hypothesis that rearing density and diet significantly influence a male’s ability to win a fight against another male. Instead we found stronger support for the notion that, all else being equal, males with larger mandibles, or weapons, than their opponent were more likely to win a fight.
... Cependant, les amines biogènes semblent également jouer un rôle dans l'agressivité durant les conflits. Chez les espèces nonsociales, principalement chez le grillon et les drosophiles, des recherches utilisant des approches pharmacologiques et génétiques suggèrent que l'OA est impliquée dans l'escalade des comportements agressifs lors de combats entre congénères (Adamo et al., 1995 ;Stevenson et al., 2000Stevenson et al., , 2005Hoyer et al., 2008 ;Zhou et al., 2008 ;Stevenson & Schildberger, 2013). Des études récentes utilisant des méthodes similaires pour modifier la 5-HT suggèrent que cette amine biogène pourrait également jouer un rôle important dans la modulation de l'agressivité chez ces espèces (Bubak et al., 2014), même si elle ne semble pas nécessaire au déclenchement des comportements agressifs (Dierick & Greenspan, 2007). ...
Within the animal kingdom, individuals of the same species are often in conflict for access to certain resources. In solitary parasitoids, females can compete directly for access to a host that is an essential resource for their reproductive success. During this thesis, we investigated the factors that influence the display of agonistic behaviour and the outcome of contest over host in females of the solitary parasitoid wasp Eupelmus vuilleti. More specifically, we investigated the effect of host value: a larva or pupa in the cowpea seed beetle, Callosobruchus maculatus. Moreover, we tested whether the genetic relatedness between contestants plays a role in the avoidance of competition and conflict resolution. We also investigated the hormonal mediation of aggressiveness during conflict, focusing on two families of hormones already known to regulate different life history traits and behaviours in adult insects: juvenile hormone and ecdysteroids.
... Mushroom body neurogenesis appears affected by NO which also increases the probability of calcium channel opening in the principal MB neurons the Kenyon cells; the mechanism here may involve PKG. Apparently submissive behavior in the cricket may involve NO [178][179][180][181][182][183]. The cockroach was utilized by researchers in group 12 (Periplaneta Americana) and Ott et al. demonstrate that in both the cockroach and locust sGC activity can be increased via an allosteric, NO-independent mechanism as observed in mammals. ...
Ever since the late-eighties when endothelium-derived relaxing factor was found to be the gas nitric oxide, endogenous nitric oxide production has been observed in virtually all animal groups tested and additionally in plants, diatoms, slime molds and bacteria. The fact that this new messenger was actually a gas and therefore didn’t obey the established rules of neurotransmission made it even more intriguing. In just 30 years there is now too much information for useful comprehensive reviews even if limited to animals alone. Therefore this review attempts to survey the actions of nitric oxide on development and neuronal function in selected major invertebrate models only so allowing some detailed discussion but still covering most of the primary references. Invertebrate model systems have some very useful advantages over more expensive and demanding animal models such as large, easily identifiable neurons and simple circuits in tissues that are typically far easier to keep viable. A table summarizing this information along with the major relevant references has been included for convenience.
... Previous experience can also influence the outcome of agonistic interactions and may explain the little effect of JH manipulation in Exp. 4. In many animals, older (but not too old) individuals are more likely to dominate younger opponents (Hughes and Strassmann, 1988;Khazraïe and Campan, 1999;Stevenson and Schildberger, 2013;Tsuji and Tsuji, 2005). More specific effects of previous agonistic interactions, known as "winner" and "looser" effects, reflect the increasing tendency of previous winners to win again, and of previous losers to be beaten in a conflict following a defeat (reviewed in Hsu et al., 2006, Kim et al., 2018, and were recently suggested to be also important in a social wasp (Bang and Gadagkar, 2016). ...
Juvenile hormone (JH) is a key regulator of insect development and reproduction. Given that JH commonly affects adult insect fertility, it has been hypothesized to also regulate behaviors such as dominance and aggression that are associated with reproduction. We tested this hypothesis in the bumblebee Bombus terrestris for which JH has been shown to be the major gonadotropin. We used the allatoxin precocene-I (P-I) to reduce hemolymph JH titers and replacement therapy with JH-III to revert this effect. In small orphan groups of workers with similar body size but mixed treatment, P-I treated bees showed lower aggressiveness, oogenesis, and dominance rank compared with control and replacement therapy treated bees. In similar groups in which all bees were treated similarly, there was a clear dominance hierarchy, even in P-I and replacement therapy groups in which the bees showed similar levels of ovarian activation. In a similar experiment in which bees differed in body size, larger bees were more likely to be dominant despite their similar JH treatment and ovarian state. In the last experiment, we show that JH manipulation does not affect dominance rank in groups that had already established a stable dominance hierarchy. These findings solve previous ambiguities concerning whether or not JH affects dominance in bumblebees. JH positively affects dominance, but bees with similar levels of JH can nevertheless establish dominance hierarchies. Thus, multiple factors including JH, body size, and previous experience affect dominance and aggression in social bumblebees.
Highlights of the study
In groups of orphan workers JH manipulation influences dominance rank
Orphan bumblebee workers with similar JH levels vary in aggressiveness and dominance rank
Body size influences dominance rank in groups of orphan workers with similar JH titers
JH, body size, and previous experience interact to determine dominance rank
... In the present study, to gain insights into the molecular evolution of the fruitless gene in basal hemimetabolous insects, I analysed a fruitless homologue in the two-spotted cricket, Gryllus bimaculatus, a basal hemimetabolous insect showing prominent sex-specific behaviours such as song production, courtship behaviour and aggressive behaviour (Adamo et al., 1995;Pollack, 2000;Hedwig, 2006;Stevenson and Schildberger, 2013). I first examined whether the Gryllus fruitless gene encodes sex-specific transcripts, as well as the occurrence of the distal promoter(s) that drive the expression of the sex-specific isoform. ...
In the brain of holometabolous insects such as the fruit fly Drosophila melanogaster, the fruitless gene produces sex‐specific gene products under the control of the sex‐specific splicing cascade and contributes to the formation of the sexually dimorphic circuits. Similar sex‐specific gene products of fruitless homolog have been identified in other holometabolous insects such as the mosquitos and the parasitic wasp, suggesting the fruitless‐dependent neural sex‐determination system is widely conserved among holometabolous insects. However, it remains obscure whether the fruitless‐dependent neural sex‐determination system is present in basal hemimetabolous insects. To address this issue, the identification, characterization, and expression analyses of the fruitless homolog were conducted in the two‐spotted cricket Gryllus bimaculatus as a model hemimetabolous insect. Gryllus fruitless gene encodes multiple isoforms with unique zinc finger domain, and does not encode a sex‐specific gene product. Gryllus Fruitless protein is broadly expressed in the neurons and glial cells in the brain, and there was no prominent sex‐related difference in the expression levels of Gryllus fruitless isoforms. The results suggest that the Gryllus fruitless gene is not involved in the neural sex‐determination in the cricket brain.
This article is protected by copyright. All rights reserved.
... In insects, the winner and loser effects have been well studied in several species, revealing that each species exhibits the effects to different magnitudes. For example, in the parasitoid wasp, Eupelmus vuilleti, a winner effect has been observed in the absence of any evident loser effect (Goubault and Decuignie're, 2012), while in crickets, Gryllus bimaculatus, both winner and loser effects exist; the winner effect is mediated by the action of octopamine (Stevenson and Schildberger, 2013), and aversive agonistic fighting experiences will invoke social defeat via the action of the NO/cGMP pathway (Rillich and Stevenson, T 2017). In the olive fruit fly, Bactrocera oleae, aggressive behavior could be enhanced by both previous victories and defeats to improve fighting success in subsequent contests against inexperienced males (Benelli et al., 2015). ...
In the context of animal aggression, the winner/loser effect is a cross-taxa phenomenon. In the present study, the effect of social contest experience on winning and losing subsequent encounters was investigated in the furious male lobster cockroach, Nauphoeta cinerea. Dominant and subordinate individuals were generated as the result of an encounter between two socially naïve males (SNMs); the winner and loser were designated as 1st encounter dominants and 1st encounter subordinates, respectively. With these dominants and subordinates, three experiments were conducted: (I) the original pair met in a re-encounter, (II) the 1st encounter dominants and subordinates were paired with an inexperienced SNM, (III) the 1st encounter dominants and subordinates were paired with an experienced individual of the same rank. Each experiment was conducted at 1 week, 2 weeks, 3 weeks, 4 weeks and 5 weeks after the 1st encounter fight. Juvenile hormone (JH) III titer was monitored in all individuals before and after each subsequent encounter. Our results showed that, in the original pairing and in the pairing with SNMs, the probability that a 1st encounter dominant (or subordinate) would win (or lose) the subsequent encounter fit well with the 95% confidence interval of the theoretical criteria proposed by Begin et al. (1969), indicating the existence of the winning/losing effect. However, this effect was inconsistent along the five-week observation period. For all 1st encounter dominants, at each week after the 1st encounter, the before subsequent encounter JH III titers distribution was significantly different from that on the 1st encounter day; the distributions of before subsequent encounter JH III titers could be further clustered into two groups, the higher JH III group and the lower JH III group, which were significantly correlated with subsequent winning and losing, respectively. For the 1st encounter subordinates, the distributions of before subsequent encounter JH III titers were not significantly different from that of SNMs, but the titer distributions were significantly shifted to a higher level compared to the 1st encounter day. Compared with before subsequent encounter, the after subsequent encounter hemolymph JH III level was significantly increased in winners and significantly decreased in losers. From these data, we propose that instability of the winner and loser effects may occur due to physiological costs and recovery; this instability may partly explain why the social hierarchy is unstable in this cockroach species.
... Recent progress in genetics allowed establishment of gene knockdown by RNA interference (RNAi) (Takahashi et al., 2009;Awata et al., 2016) and genome editing by the CRISPR/cas9 system (Awata et al., 2015) in crickets, adding to the well-established pharmacological methods (Unoki et al., 2005Matsumoto et al., , 2009Matsumoto et al., , 2016Mizunami et al., 2014;Sugimachi et al., 2016). Third, there has been a good accumulation of knowledge that bridges between the nervous system and behavior of crickets gained by extensive neuroethological studies in crickets (Stevenson and Schildberger, 2013;Hedwig, 2016). ...
Unraveling the molecular mechanisms underlying memory formation in insects and a comparison with those of mammals will contribute to a further understanding of the evolution of higher-brain functions. As it is for mammals, insect memory can be divided into at least two distinct phases: protein-independent short-term memory and protein-dependent long-term memory (LTM). We have been investigating the signaling pathway of LTM formation by behavioral-pharmacological experiments using the cricket Gryllus bimaculatus, whose olfactory learning and memory abilities are among the highest in insect species. Our studies revealed that the NO-cGMP signaling pathway, CaMKII and PKA play crucial roles in LTM formation in crickets. These LTM formation signaling pathways in crickets share a number of attributes with those of mammals, and thus we conclude that insects, with relatively simple brain structures and neural circuitry, will also be beneficial in exploratory experiments to predict the molecular mechanisms underlying memory formation in mammals.
... However, conflicting observations have also been described in these animals (Peeke et al., 2000;Panksepp et al., 2003;Tricarico and Gherardi, 2007). Moreover, in insects, the effects of 5-HT appear to vary in different species: in crickets, 5-HT is able to decrease aggression and favor escape behavior (Stevenson and Rillich, 2012;Stevenson and Schildberger, 2013), but in ants, aggressiveness is weakly affected by exogenous 5-HT (Szczuka et al., 2013). In flies, aggressiveness is increased by the administration of a 5-HT precursor (Bubak et al., 2014) or by selective 5-HT neuron activation (Hoopfer, 2016). ...
We injected serotonin (5-HT) in adult male crayfish before pairing them with size-matched non-injected competitors, and we observed dyadic agonistic interactions. Paradoxically, 5-HT elicited opposite behavioral responses if the injected animal was opposed by a smaller or larger rival: the level of aggressiveness of the injected crayfish was higher in front of a larger rival but lower in front of a smaller rival. Our results indicate that the effects of 5-HT on aggressiveness are dependent on the perception of the relative size difference of the opponent. In both cases, however, 5-HT significantly delayed the decision to retreat. We conclude that 5-HT does not primarily act on aggressiveness but rather on the brain centers that integrate risk assessment and/or decision-making, which then modulate the aggressive response. Our study supports a reinterpretation of the role of 5-HT in crustacean agonistic behavior that may be of interest for other animals.
... Indeed, it can be stated that crickets are one of the best insect models for pharmacological analysis of learning and memory (Mizunami et al., 2013). Third, much information on the brain and behavior of crickets has been obtained as crickets have been used in diverse neuroethological studies (Stevenson and Schildberger, 2013;Hedwig, 2016). We first deal with the recent debate about whether appetite and aversive signals are conveyed by octopamine and dopamine neurons, respectively, as has been suggested in honey bees and crickets, or whether both appetitive and aversive signals are mediated by dopamine neurons, as has been suggested in fruit-flies. ...
Revealing neural systems that mediate appetite and aversive signals in associative learning is critical for understanding the brain mechanisms controlling adaptive behavior in animals. In mammals, it has been shown that some classes of dopamine neurons in the midbrain mediate prediction error signals that govern the learning process, whereas other classes of dopamine neurons control execution of learned actions. In this review, based on the results of our studies on Pavlovian conditioning in the cricket Gryllus bimaculatus and by referring to the findings in honey bees and fruit-flies, we argue that comparable aminergic systems exist in the insect brain. We found that administrations of octopamine (the invertebrate counterpart of noradrenaline) and dopamine receptor antagonists impair conditioning to associate an olfactory or visual conditioned stimulus (CS) with water or sodium chloride solution (appetitive or aversive unconditioned stimulus, US), respectively, suggesting that specific octopamine and dopamine neurons mediate appetitive and aversive signals, respectively, in conditioning in crickets. These findings differ from findings in fruit-flies. In fruit-flies, appetitive and aversive signals are mediated by different dopamine neuron subsets, suggesting diversity in neurotransmitters mediating appetitive signals in insects. We also found evidences of “blocking” and “auto-blocking” phenomena, which suggested that the prediction error, the discrepancy between actual US and predicted US, governs the conditioning in crickets and that octopamine neurons mediate prediction error signals for appetitive US. Our studies also showed that activations of octopamine and dopamine neurons are needed for the execution of an appetitive conditioned response (CR) and an aversive CR, respectively, and we, thus, proposed that these neurons mediate US prediction signals that drive appetitive and aversive CRs. Our findings suggest that the basic principles of functioning of aminergic systems in associative learning, i.e., to transmit prediction error signals for conditioning and to convey US prediction signals for execution of CR, are conserved among insects and mammals, on account of the fact that the organization of the insect brain is much simpler than that of the mammalian brain. Further investigation of aminergic systems that govern associative learning in insects should lead to a better understanding of commonalities and diversities of computational rules underlying associative learning in animals.
... Oecophylla smaragdina Kamhi, et al., 2015Kamhi, et al., 2015Linn and Roelofs, 1986 Gryllus bimaculatus Adamo, et al., 1995, Stevenson, et al., 2005, Stevenson and Rillich, 2017, Stevenson and Schildberger, 2013Mizunami, et al., 2009, Unoki, et al., 2005Abdoun, et al., 1995, Sakai, et al., 2017 Locusta migratoria Bacon, et al., 1995Ma, et al., 2015 Schistocerca americana Morris, et al., 1999, Orchard, et al., 1993, Sombati and Hoyle, 1984bSombati and Hoyle, 1984a SEROTONIN Activity Aggression Development Integration Nutrition Reproduction Sensorimotor function Social function ...
... Success rate of aggression can be influenced by several factors, such as physical disparities (e.g. size, strength and weapon) 41,42 , as well as physical exertion and experience in previous fights 43,44 . For example, different size of the parasitoid wasps has a different fighting propensity and weak-fighting ones usually stay hidden to avoid the stress of fighting 45 . ...
Acanthaspis cincticrus (Stål) is an assassin bug with a specialized camouflaging behavior to ambush ants in the nymphal stages. In this study, we comprehensively sequenced all the life stages of A. cincticrus, including the eggs, five nymph instars, female and male adults using Illumina HiSeq technology. We obtained 176 million clean sequence reads. The assembled 84,055 unigenes were annotated and classified functionally based on protein databases. Among the unigenes, 29.03% were annotated by one or more databases, suggesting their well-conserved functions. Comparison of the gene expression profiles in the egg, nymph and adult stages revealed certain bias. Functional enrichment analysis of significantly differentially expressed genes (SDEGs) showed positive correlation with specific physiological processes within each stage, including venom, aggression, olfactory recognition as well as growth and development. Relative expression of ten SDEGs involved in predation process was validated using quantitative real-time PCR (qRT-PCR).
... For social animals living in a nest, burrow or other type of physical home, the appearance of an intruder signifies that their home's location is known and vulnerable to attack, threatening the loss of group members and valuable stored resources. Thus, residents respond aggressively to intruders, and these responses also increase vigilance and intensify responses to future encounters with intruders (Hsu et al. 2006;Stevenson & Schildberger 2013;Yang et al. 2001). ...
Understanding how social experiences are represented in the brain and shape future responses is a major challenge in the study of behavior. We addressed this problem by studying behavioral, transcriptomic and epigenetic responses to intrusion in honey bees. Previous research showed that initial exposure to an intruder provokes an immediate attack; we now show that this also leads to longer-term changes in behavior in the response to a second intruder, with increases in the probability of responding aggressively and the intensity of aggression lasting two and one hours, respectively. Previous research also documented the whole-brain transcriptomic response; we now show that in the mushroom bodies (MB) there are two waves of gene expression, the first highlighted by genes related to cytoskeleton remodeling, and the second highlighted by genes related to hormones, stress response and transcription factors (TFs). Overall, 16 out of 37 (43%) of the TFs whose cis-motifs were enriched in the promoters of the differentially expressed genes were also predicted from transcriptional regulatory network analysis to regulate the MB transcriptional response, highlighting the strong role played by a relatively small subset of TFs in the MB's transcriptomic response to social challenge. Whole brain histone profiling revealed few changes in chromatin accessibility in response to social challenge; most differentially expressed genes were "ready" to be activated. These results demonstrate how biological embedding of a social challenge involves temporally dynamic changes in the neurogenomic state of a prominent region of the insect brain that are likely to influence future behavior.
... Larvae of 6th instar against 4th always had advantages in the contests between the species studied. Based on some animal behavior studies, the success of fighting is directly dependent on physical disparities like size, strength, and weaponry (Dodson 1986;Shelly 1999;Briffa 2008;Arnott and Elwood 2009), and the presence of resources, physical exertion, and experience in previous fights (Brown et al. 2006;Stevenson and Schildberger 2013). ...
The fall armyworm, Spodoptera frugiperda (J. E. Smith) and the corn earworm, Helicoverpa zea (Boddie) are among the main pests of maize. Both species exhibit cannibalistic behavior and quite often share the same feeding guild in maize (maize ears), which can result in several interspecific and intraspecific interactions. Paired interaction scenarios of intraspecific and interspecific larvae were assessed in arenas in the presence and absence of food to characterize movements resulting from interactions of these insects. There was a difference in the frequency of behavioral movements in all the interactions, except for S. frugiperda in the presence of food. Head touching and recoiling were the predominant movements in most of the interaction scenarios. Spodoptera frugiperda exhibited a predominance of defensive movements when competing against H. zea in the same instars. Cannibalism and predation occurred frequently in interactions involving 6th instar of H. zea against opponents in 4th instar. Larvae of H. zea show a higher aggressive movement than S. frugiperda. The larvae of S. frugiperda take advantage during the interactions, although they present more defensive movements compared to H. zea. This study provides relevant information regarding the interaction of these species and intraguild interaction, which might influence the population dynamics and the competitive displacement of pest species that share the same ecological niche.
... Based on this expectation of the social cue hypothesis, behavioural responses completely attributable to social experience should manifest as constant or even increased aggression and avoidance in repeated encounters, and tolerance should decrease accordingly (Stevenson et al., 2005;Rutte et al., 2006;Stevenson & Schildberger, 2013). Instead, avoidance in individuals that lost both trials and aggression in individuals that won both trials significantly decreased in the second trial, while all other behaviour types were unchanged between trials. ...
Dominance hierarchies represent some of nature’s most rudimentary social structures, and aggression is key to their establishment in many animal species. Previous studies have focused on the relative influences of prior experience and physiological traits of individuals in determining social rank through aggression. Here we examine the behavioural potential for dominance hierarchy formation in the subsocial small carpenter bee, Ceratina calcarata. Both physiological traits and social experience were found to play partial roles in predicting future interactive behaviour in this species. Our results suggest that individual size is associated with dominance in initial encounters, while prior experience plays a larger role in predicting dominance in subsequent encounters. Social systems in the early stages of social evolution may well have followed these same predictive factors and these factors are key targets for future studies of social evolution and the behavioural origins of dominance hierarchies.
... Studies across species have shown that altering levels of 5-HT has varying behavioral effects that consistently fall on an affiliative-agonistic axis . These observations have been made in a wide range of organisms including drosophila , lobsters (Kravitz, 2000), crickets (Stevenson and Schildberger, 2013) and zebrafish (Teles et al., 2013). ...
Regulation of social behaviors is necessary to achieve social inclusion, establish relationships and sustain those relationships through adversity. Impairments in socio-emotional function and competence are prominent and debilitating features of major depression, yet are not traditionally recognized as cardinal symptoms of the disease. However, these deficits often persist in patients whose other mood symptoms have remitted and can predict risk of relapse, indicating an important role as a vulnerability factor. Understanding the neurobiology of socioaffective dysfunction in depression is thus important for determining the pathology of the disorder and developing effective treatments. Human imaging studies of depressive patients have consistently reported abnormal activity in the ventromedial prefrontal cortex (vmPFC), an area important for emotional processing and social cognition. Tracing studies in animals and tractography in humans have shown that the dorsal raphe nucleus (DRN) is a major projection target of the vmPFC. The DRN contains the most serotonin (5-HT) producing neurons in the brain and its output has been shown to regulate behaviors along an affiliative-agonistic axis, however it is neuronally heterogeneous. This thesis investigated the cytoarchitecture of the vmPFC-DRN microcircuit and its relevance to socioaffective behaviors using genetic mapping, whole cell electrophysiology and optogenetics. I showed that GABAergic neurons, which are the primary non-serotonergic neuronal population in the DRN, mediated top-down projections from the vmPFC onto mood-regulating 5-HT neurons and demonstrated the relevance of this pathway in mediating socioaffective decisions using the chronic social defeat stress (CSDS) paradigm. In addition, I used deep brain stimulation of the vmPFC as an antidepressant model to show that therapeutic response may rely on restoring the excitatory/inhibitory balance of inputs to 5-HT neurons. Together, these results will provide a better understanding of socioaffective circuitry and could lead to the development of more effective and efficient strategies to treat mood disorders.
... According to our model, a cricket will flee the moment the accumulated sum of opponent actions raises the tendency to flee, via the action of NO, above the tendency to fight, set by octopamine. Modified and updated from Stevenson and Rilllich (2012); Stevenson and Schildberger (2013). ...
Aggression is a common behavioral strategy employed by animals to secure limited resources, but must be applied with restraint to limit potential costs including injury. How animals make the adaptive decision to fight or flee is barely known. Here, we review our work on crickets that reveals the roles of biogenic amines, primarily octopamine (the insect analog of noradrenaline) and nitric oxide (NO). Using aminergic drugs, we found that amines are not essential for actually initiating aggression. However, octopamine is necessary for mediating the aggression-promoting effects of potentially rewarding experiences including stimulation with a male antenna, physical exertion, winning, and resource possession. Hence, octopamine can be considered as the motivational component of aggression. Imposed handicaps that impede aggressive signaling revealed that the agonistic actions of an opponent perceived during fighting act to reduce aggression, and that crickets make the decision to flee the moment the accumulated sum of such aversive experiences exceeds some critical level. Treatment with nitridergic drugs revealed that the impact of the opponent’s aggressive actions is mediated by NO. NO acts to suppress aggression by promoting the tendency to flee and is primarily responsible for the depressed aggressiveness of subordinates after social defeat. Octopamine and dopamine can each restore aggression in subordinates, but only dopamine is necessary for normal recovery. The role of serotonin remains unclear, and is discussed. We conclude that octopamine and NO control the decision to fight or flee by mediating the effects of potentially rewarding and aversive experiences, respectively.
... Crickets exhibit spectacular fighting behavior (Alexander, 1961) and, as in mammals (Nelson, 2006), their aggressiveness is influenced by a wide variety of social and other experiences (e.g., Killian and Allen, 2008), and this is where OA plays a key role. We have shown that experiences as diverse as physical exertion (Stevenson et al., 2005), winning a fight , and resource possession each promote the expression of aggressive behavior via the activation of the octopaminergic system (reviews: Stevenson and Rillich, 2012;Stevenson and Schildberger, 2013;Simpson and Stevenson, 2014). ...
Biogenic amines have widespread effects on numerous behaviors, but their natural functions are often unclear. We investigated the role of octopamine (OA), the invertebrate analog of noradrenaline, on initiation and maintenance of aggression in male crickets of different social status. The key-releasing stimulus for aggression is antennal fencing between males, a behavior occurring naturally on initial contact. We show that mechanical antennal stimulation (AS) alone is sufficient to initiate an aggressive response (mandible threat display). The efficacy of AS as an aggression releasing stimulus was augmented in winners of a previous fight, but unaffected in losers. The efficacy of AS was not, however, influenced by OA receptor (OAR) agonists or antagonists, regardless of social status. Additional experiments indicate that the efficacy of AS is also not influenced by dopamine (DA) or serotonin (5HT). In addition to initiating an aggressive response, prior AS enhanced aggression exhibited in subsequent fights, whereby AS with a male antenna was now necessary, indicating a role for male contact pheromones. This priming effect of male-AS on subsequent aggression was dependent on OA since it was blocked by OAR-antagonists, and enhanced by OAR-agonists. Together our data reveal that neither OA, DA nor 5HT are required for initiating aggression in crickets, nor do these amines influence the efficacy of the natural releasing stimulus to initiate aggression. OA’s natural function is restricted to promoting escalation and maintenance of aggression once initiated, and this can be invoked by numerous experiences, including prior contact with a male antenna as shown here.
... Crickets exhibit spectacular fighting behavior (Alexander, 1961) and, as in mammals (Nelson, 2006), their aggressiveness is influenced by a wide variety of social and other experiences (e.g., Killian and Allen, 2008), and this is where OA plays a key role. We have shown that experiences as diverse as physical exertion (Stevenson et al., 2005), winning a fight , and resource possession each promote the expression of aggressive behavior via the activation of the octopaminergic system (reviews: Stevenson and Rillich, 2012;Stevenson and Schildberger, 2013;Simpson and Stevenson, 2014). ...
Biogenic amines have widespread effects on numerous behaviors, but their natural functions are often unclear. We investigated the role of octopamine (OA), the invertebrate analogue of noradrenaline, on initiation and maintenance of aggression in male crickets of different social status. The key-releasing stimulus for aggression is antennal fencing between males, a behavior occurring naturally on initial contact. We show that mechanical antennal stimulation (AS) alone is sufficient to initiate an aggressive response (mandible threat display). The efficacy of AS was augmented in winners of a previous fight, but unaffected in losers. The efficacy of AS was not, however, influenced by OA receptor (OAR) agonists or antagonists, regardless of social status. Additional experiments indicate that the efficacy of AS is also not influenced by dopamine (DA) or serotonin (5HT). In addition to initiating an aggressive response, prior AS enhanced aggression exhibited in subsequent fights, whereby AS with a male antenna was now necessary, indicating a role for male contact pheromones. This priming effect of male-AS on subsequent aggression was dependent on OA since it was blocked by OAR-antagonists, and enhanced by OAR-agonists. Together our data reveal that neither OA, DA nor 5HT are required for initiating aggression in crickets, nor do these amines influence the efficacy of the natural releasing stimulus to initiate aggression. OA’s natural function is restricted to promoting escalation and maintenance of aggression once initiated, and this can be invoked by numerous experiences, including prior contact with a male antenna as shown here.
... Despite numerous behavioral theories (2,3), and insights into the neurochemical control of aggression in both vertebrates (4,5) and invertebrates (6,7), the mechanisms underlying the decision-making processes are barely known. Most behavioral assessment theories agree that the decision is based on information gathered from agonistic signals exchanged during fighting (2,8), but it is hotly debated who evaluates these signals (sender, receiver, or both), how they act on aggression (promote or suppress), and whether complex cognitive capacities are required (3,(9)(10)(11). Our earlier experiments (12) revealed that crickets simply add up the sensory impact of their opponent's agonistic signals during fighting, and flee when the sum exceeds some critical threshold, which is in full accord with the cumulative assessment model (8). Here, we investigate the role of the nitric oxide/cyclic guanosine 3′,5′-monophosphate (NO/cGMP) signaling pathway in opponent assessment. ...
Fighting is dangerous, which is why animals choose to flee once the costs outweigh the benefits, but the mechanisms underlying this decision-making process are unknown. By manipulating aggressive signaling and applying nitrergic drugs, we show that the evolutionarily conserved neuromodulator nitric oxide (NO), which has a suppressing effect on aggression in mammals, can play a decisive role. We found that crickets, which exhibit spectacular fighting behavior, flee once the sum of their opponent’s aversive actions accrued during fighting exceeds a critical amount. This effect of aversive experience is mediated by the NO signaling pathway. Rather than suppressing aggressive motivation, NO increases susceptibility to aversive stimuli and with it the likelihood to flee. NO’s effect is manifested in losers by pro- longed avoidance behavior, characteristic for social defeat in numerous species. Intriguingly, fighting experience also induces, via NO, a brief susceptible period to aversive stimuli in winners just after victory. Our findings thus reveal a key role for NO in the mechanism underlying the decision to flee and post-conflict depression in aggressive behavior.
... In a number of arthropod species experiencing aggression affects performance in subsequent contests. Current theory predicts that, after an intra-specific aggressive interaction, winners are more likely to win again and losers more likely to lose again [29,[103][104][105]. However, studying the olive fruit fly, it has been observed that both winners and losers of two consecutive encounters displayed higher intensity of aggression and fought longer in subsequent contests. ...
True fruit flies (Diptera: Tephritidae) include over 4000 species, many of which constitute enormous threats to fruit and vegetable production worldwide. A number of Tephritidae are lekking species, forming aggregations in which males fight to defend a small territory where they court females and mate. Male-male contests also occur in non-lekking species, characterized by resource defense polygyny. Tephritidae females display agonistic behavior to maintain single oviposition sites and reduce larval competition for food. Here, how, where, when and why aggressive interactions occur in Tephritidae flies is reviewed. A number of neglected issues deserving further research are highlighted, with a special focus on diel periodicity of aggression, cues evoking aggressive behavior, the role of previous experience on fighting success and the evolution of behavioral lateralization of aggressive displays. In the final section, future directions to exploit this knowledge in Integrated Pest Management, with particular emphasis on enhancement of Sterile Insect Technique and interspecific competitive displacement in the field are suggested.
... The octopaminergic system has been convincingly implicated in the motivation and escalation of aggressive behavior in some insect species Stevenson et al., 2000;Baier et al., 2002;Stevenson et al., 2005;Hoyer et al., 2008;Zhou et al., 2008;Rillich and Stevenson, 2011;Stevenson and Schildberger, 2013). Much of this research was conducted in crickets and fruit flies, utilizing both pharmacological and genetic approaches. ...
Aggression is a common behavioral trait shared in many animals, including both vertebrates and invertebrates. How-ever, the type and intensity of agonistic encounters and displays can vary widely both across and within species, resulting in complicated or subjective interpretations that create difficulties in developing theoretical models that can be widely applied. The need to easily and objectively identify quantifiable behaviors and their associated morphologies becomes especially important when attempting to decipher the neurological mechanisms underlying this complex behavior. Monoamines, neuropeptides, and pheromones have been implicated as important neuromodulators for agonistic displays in both invertebrates and vertebrates. Ad-ditionally, recent breakthroughs in insect research have revealed exciting proximate mechanisms important in aggression that may be broadly relevant, due to the relatively high conservation of these neurochemical systems across animal taxa. In this review, we present the latest research demonstrating the importance of monoamines, neuropeptides, and pheromones as neuromodulators for aggression across a variety of insect species. Additionally, we describe the stalk-eyed fly as a model system for studying aggres-sion, which integrates physiological, morphological, and neurochemical approaches in exploring detailed mechanisms responsi-ble for this common yet complex behavior. We conclude with our perspective on the most promising lines of future research aimed at understanding the proximate and ultimate mechanisms underlying aggressive behaviors [Current Zoology 60 (6): 778– 790, 2014 ].
... Octopamine and its precursor, tyramine, are commonly described as analogous to the vertebrate adrenergic system (Roeder, 2005). Octopamine is commonly associated with aggression and changes in response to contest outcomes and may even mediate the winnereloser effect in crickets (reviewed in Stevenson & Schildberger, 2013). In some social insects, dopamine is associated with social behaviours and decreases in the absence of interaction (Wada-Katsumata, Yamaoka, & Aonuma, 2011). ...
Many animals adapt to rapidly changing social environments by using social information to modulate their hormone titres. Modulation of hormone titres, as proposed by the challenge hypothesis, provides a mechanism by which individuals can match their behaviour to their current social environment and thereby avoid costs associated with prolonged high hormone titres. Thus far, most work on social responsiveness of hormone titres has focused on androgens in vertebrates. However, there is mounting evidence that insect hormones, especially juvenile hormone, may respond to social stimuli in ways that parallel androgens in vertebrates. This review will integrate work on social modulation of hormone titres in vertebrates and insects. First we review how the hormone-mediated trade-off between fecundity and life span may be a key selective force favouring socially responsive hormone titres in both systems. Then we review theoretical and empirical work in vertebrates and insects that address how factors such as social instability, dominance rank and mating system influence hormone titre responsiveness. These studies illustrate that (1) juvenile hormone (JH) is responsive to social stimuli in a range of insect taxa and (2) JH responses match key predictions of the challenge hypothesis. We conclude that there are strong similarities in endocrine responsiveness across vertebrate and insect taxa. The challenge hypothesis provides a useful conceptual framework for hypothesis-driven research in insect endocrinology. In addition, exploring areas of convergence and divergence across vertebrates and insects may help clarify how selection has shaped patterns of endocrine responsiveness.
... obs.]. These results suggest that OA induces aggressive responses to alien ants or increases discrimination of nonnestmates, corroborating studies implicating OA in aggression in Drosophila [Zhou et al., 2008] and crickets [Stevenson and Schildberger, 2013]. ...
The ecological dominance of ants has to a great extent been achieved through their collective action and complex social organization. Ants provide diverse model systems to examine the neural underpinnings of individual behavior and group action that contribute to their evolutionary success. Core elements of ant colony structure such as reproductive and ergonomic division of labor, task specialization, and social integration are beginning to be understood in terms of cellular neuroanatomy and neurochemistry. In this review we discuss the neuroethology of colony organization by focusing on the role of biogenic amines in the control of social behavior in ants. We examine the role of neuromodulation in significant sociobiological characteristics of ants, including reproductive hierarchies, colony foundation, social food flow, nestmate recognition, territoriality, and size- and age-related sensory perception and task performance as well as the involvement of monoamines in collective intelligence, the ultimate key to the global dominance of these remarkable superorganisms. We conclude by suggesting future directions for the analysis of the aminergic regulation of behavior and social complexity in ants. © 2013 S. Karger AG, Basel.
... To conclude this section, what is generally referred to as the decision to fight or flee could be accounted for in crickets by simply modulating relative behavioral thresholds (Figure 1; Stevenson & Rillich, 2012;Stevenson & Schildberger, 2013). Experiences evaluated as being in some way rewarding (winning, resource possession) promote the tendency to fight to a level determined by the modulatory action of octopamine, which can be considered as representing the motivational component of aggression. ...
We begin this review by introducing transformational concepts in neuromodulation and circuit function that have arisen from the study of insects and other invertebrates. These provide essential background not only to understanding behaviour in insects (social or otherwise), but also for the functioning of nervous systems in all animals. We next detail three (among many possible) examples, in which neuromodulation of social behaviour has been studied in depth. The first concerns the control of aggression and social dominance in crickets; the second involves swarming in locusts, and the third details the division of labour in honey bee societies. We conclude that insects have something profound to offer the study of psychology – not by providing direct analogues of human behaviour, but rather by illustrating the power of neuromodulation to generate behavioural complexity in simple systems, at the level of individuals and societies.
Adverse social experience impacts social structure by modifying the behavior of individuals, but the relationship between an individual's behavioral state and its response to adversity is poorly understood. We leveraged naturally occurring division of labor in honey bees and studied the biological embedding of environmental threat using laboratory assays and automated behavioral tracking of whole colonies. Guard bees showed low intrinsic levels of sociability compared to foragers and nurse bees, but large increases in sociability following exposure to a threat. Threat experience also modified the expression of caregiving-related genes in a brain region called the mushroom bodies. These results demonstrate that the biological embedding of environmental experience depends on an individual's societal role and in turn impacts its future sociability.
Genes expressed in response to increased neuronal activity are widely used as activity markers in recent behavioral neuroscience. In the present study, we established transgenic reporter system for whole-brain activity mapping in the two-spotted cricket Gryllus bimaculatus, a hemimetabolous insect used in neuroethology and behavioral ecology. In the cricket brain, a homolog of early growth response-1 (Gryllus egr-B) was rapidly induced as an immediate-early gene (IEG) in response to neuronal hyperexcitability. The upstream genomic fragment of Gryllus egr-B contains potential binding sites for transcription factors regulated by various intracellular signaling pathways, as well as core promoter elements conserved across insect/crustacean egr-B homologs. Using the upstream genomic fragment of Gryllus egr-B, we established an IEG promoter-driven transgenic reporter system in the cricket. In the brain of transgenic crickets, the reporter gene (a nuclear-targeted destabilized EYFP) was induced in response to neuronal hyperexcitability. Inducible expression of reporter protein was detected in almost all neurons after neuronal hyperexcitability. Using our novel reporter system, we successfully detected neuronal activation evoked by feeding in the cricket brain. Our IEG promoter-driven activity reporting system allows us to visualize behaviorally relevant neural circuits at cellular resolution in the cricket brain.
Crickets have emerged as ideal model systems for investigating the mechanisms controlling intraspecific aggressive behaviour. As in many animals, male aggression in crickets is shaped by numerous experiences including physical exertion, past wins and defeats and the acquisition of resources. This chapter reviews work revealing that neuromodulators, primarily octopamine and nitric oxide, mediate such experience-dependent plasticity by modulating the relative behavioural thresholds to fight and to flee. Octopamine, the invertebrate analogue of noradrenaline, promotes the tendency to fight by mediating the effects of flying, winning and shelter occupancy and thus represents the motivational component of aggression. The gaseous neuromodulator nitric oxide, on the other hand, mediates the decision to flee and induces a period of prolonged submissiveness, which is characteristic for social defeat in many animals. Accumulating evidence also suggests a role for serotonin, dopamine and selected peptides in controlling insect aggression. The roles for neuromodulators in insect aggression are in essence similar to those emerging for corresponding signalling molecules in mammals, where their specific behavioural functions are less clear.
Like most animal species, fruit flies fight to obtain and defend resources essential to survival and reproduction. Aggressive behavior in Drosophila is genetically specified and also strongly influenced by the fly's social context, past experiences and internal states, making it an excellent framework for investigating the neural mechanisms that regulate complex social behaviors. Here, I summarize our current knowledge of the neural control of aggression in Drosophila and discuss recent advances in understanding the sensory pathways that influence the decision to fight or court, the neuromodulatory control of aggression, the neural basis by which internal states can influence both fighting and courtship, and how social experience modifies aggressive behavior.
Collective movement behaviours range from temporary aggregations to coordinated mass migrations with synchronous movement. Models show how complex collective patterns can arise from simple rules regulating local interactions between individuals. However, it is not always clear how these rules are implemented by real insects: even simple abstract rules contain non-trivial assumptions about the perceptual abilities of individuals. Here we review the underlying mechanisms of simple forms of aggregation and collective movement focussing on locusts using them as an example of system in which analyses of the underlying molecular and neural mechanisms have become feasible. These and similar studies promise to reveal the physiological rules governing these behaviours.
Social withdrawal, increased threat perception, and exaggerated reassurance seeking behaviors are prominent interpersonal symptoms in major depressive disorder (MDD). Altered serotonin (5-HT) systems and corticolimbic dysconnectivity have long been suspected to contribute to these symptomatic facets; however, the underlying circuits and intrinsic cellular mechanisms that control 5-HT output during socioemotional interactions remain poorly understood. We review literature that implicates a direct pathway between the ventromedial prefrontal cortex (vmPFC) and dorsal raphe nucleus (DRN) in the adaptive and pathological control of social approach–avoidance behaviors. Imaging and neuromodulation during approach–avoidance tasks in humans point to the cortical control of brainstem circuits as an essential regulator of socioemotional decisions and actions. Parallel rodent studies using viral-based connectomics and optogenetics are beginning to provide a cellular blueprint of the underlying circuitry. In these studies, manipulations of vmPFC synaptic inputs to the DRN have revealed bidirectional influences on socioaffective behaviors via direct monosynaptic excitation and indirect disynaptic inhibition of 5-HT neurons. Additionally, adverse social experiences that result in permanent avoidance biases, such as social defeat, drive long-lasting plasticity in this microcircuit, potentiating the indirect inhibition of 5-HT output. Conversely, neuromodulation of the vmPFC via deep brain stimulation (DBS) attenuates avoidance biases by restoring the direct excitatory drive of 5-HT neurons and strengthening a key subset of forebrain 5-HT projections. Better understanding the cellular organization of the vmPFC-DRN pathway and identifying molecular determinants of its neuroplasticity can open fundamentally novel avenues for the treatment of affective disorders.
Aggression plays a key role all across the Animal Kingdom, as it allows the acquisition and/or defence of limited resources (food, mates and territories) in a huge number of species. A large part of our knowledge on aggressive behaviour has been developed on insects of economic importance. How can this knowledge be exploited to enhance Integrated Pest Management? Here, I highlight how knowledge on intra-specific aggression can help IPM both in terms of insect pests (with a focus on the enhancement of the Sterile Insect Technique), and biological control agents (with a focus on mass-rearing optimisation). Then, I examine what implications for IPM can be outlined from knowledge about inter-specific aggressive behaviour. Besides predator-pest aggressive interactions predicted by classic biological control, I focus on what IPM can learn from (i) inter-specific aggression among pest species (with special reference to competitive displacement), (ii) defensive behaviour exhibited by prey against predaceous insects, and (iii) conflicts among predaceous arthropods sharing the same trophic niche (with special reference to learning/sensitisation practices and artificial manipulation of chemically-mediated interactions).
This article is protected by copyright. All rights reserved.
Social defeat, i.e. losing an agonistic dispute with a conspecific, is followed by a period of suppressed aggressiveness in many animal species, and is generally regarded as a major stressor, which may play a role in psychiatric disorders such as depression and post-traumatic stress disorder. Despite numerous animal models, the mechanisms underlying loser depression and subsequent recovery are largely unknown. This study on crickets is the first to show that a neuromodulator, dopamine (DA), is necessary for recovery of aggression after social defeat. Crickets avoid any conspecific male just after defeat, but regain their aggressiveness over 3 hours. This recovery was prohibited after depleting nervous stores of DA and octopamine (OA, the invertebrate analogue of noradrenaline) with α-methyl-tyrosine (AMT). Loser recovery was also prohibited by the insect DA-receptor (DAR) antagonist fluphenazine, but not the OA-receptor (OAR) blocker epinastine, or yohimbine, which blocks receptors for OA's precursor tyramine. Conversely, aggression was restored prematurely in both untreated and amine depleted losers given either chlordimeform (CDM), a tissue permeable OAR-agonist, or the DA-metabolite homovanillyl alcohol (HVA), a component of the honeybee queen mandibular pheromone. As in honeybees, HVA acts in crickets as a DAR-agonist since its aggression promoting effect on losers was selectively blocked by the DAR-antagonist, but not by the OAR-antagonist. Conversely, CDM's aggression promoting effect was selectively blocked by the OAR-antagonist, but not the DAR-antagonist. Hence, only DA is necessary for recovery of aggressiveness after social defeat, although OA can promote loser aggression independently to enable experience dependent adaptive responses.
Population density has profound influences on the physiology and behaviour of many animal species. Social isolation is generally reported to lead to increased aggressiveness, while grouping lowers it. We evaluated the effects of varying degrees of isolation and grouping on aggression in a territorial insect, the Mediterranean field cricket, Gryllusbimaculatus. Substantiating early observations, we show that dyadic contests between weight-matched, adult male crickets taken from groups rarely escalate beyond threat displays, whereas interactions between pairs of previously isolated crickets typically escalate to physical fights lasting several seconds. No significant differences were found between 1, 2 and 6-day isolates, or between individuals grouped for a few hours or lifelong. Unexpectedly, crickets grouped in immediate proximity within individual mesh cages that precluded fighting while permitting visual, olfactory and mechanical, antennal contact, were as aggressive as free isolates. This suggests that reduced aggression of grouped animals may be an acquired result of fighting. Supporting this notion, isolated crickets initially engage in vigorous fights when first grouped, but fighting intensity and duration rapidly decline to the level of life-long grouped crickets within only 10 min. Furthermore, grouped crickets become as aggressive as life-long isolates after only 3 hours of isolation, and on the same time course required for crickets to regain their aggressiveness after social defeat. We conclude that the reduced aggressiveness of grouped crickets is a manifestation of the loser effect resulting from social subjugation, while isolation allows recovery to a state of heightened aggressiveness, which in crickets can be considered as the default condition. Given the widespread occurrence of the loser effect in the Animal Kingdom, many effects generally attributed to social isolation are likely to be a consequence of recovery from social subjugation.
Octopamine (OCT) belongs to a group of compounds known as biogenic amines. OCT, a monohydroxylic analog of norepinephrine, is found in both vertebrate and invertebrate nervous systems. OCT is present in relatively high concentrations in the neuronal and non- neuronal tissues of most invertebrate species studied. However, OCT occurs as a trace amine in vertebrates where its physiological significance remains uncertain. OCT acts as a neurotransmit - ter, neuromodulator, and neurohormone in insect nervous systems where it prominently influences multiple physiological events. In the peripheral nervous system, OCT modulates the activity of flight muscles, peripheral organs, and most sense organs. In the central nervous system, OCT is essential for the regulation of motivation, desensitization of sensory inputs, arousal, initiation, and maintenance of various rhythmic behaviors, hygiene behavior, and complex social behaviors, including establishment of labor, as well as learning and memory. As a neurotransmitter, OCT regulates endocrine gland activity and controls the emission of light in the firefly lantern. As a neurohormone, OCT is released into hemolymph, transported to target tissues, and induces mobilization of lipids and carbohydrates, preparing insects for a period of extended activity or assisting recovery from a period of increased energy demand. OCT modulates hemocytic nodulation in nonimmune larvae and enhances phagocytosis as a neurohormone. OCT exerts its effects by binding to specific receptors belonging to the superfamily of G protein-coupled receptors and shares the structural motif of seven transmembrane domains. Activation of octo- paminergic receptor types is coupled with different second messenger pathways depending on the species, tissue source, receptor type, and cell line used for expression of the cloned receptor. OCT-mediated generation of second messengers is associated with changes in cellular response, affecting insect behaviors. This review describes the roles of OCT in insect nervous systems at the behavioral and molecular levels.
Animals often compete directly with conspecifics for food resources, and fighting success can be positively related to relative resource-holding power (RHP) and relative resource value (i.e., motivation to fight). Despite the ease of manipulating resource value during fights over food (by manipulating hunger levels), most studies have focused on male fighting in relation to gaining access to mates. In this study, pairwise contests over single food items were used to examine the effects of being the first to acquire a resource, relative body mass, relative body size (femur length), and relative level of food deprivation (i.e., hunger) on competitive feeding ability in male and female house crickets, Acheta domesticus. Only when the food pellet was movable did acquiring the resource first improve fighting success. When the pellet was fastened to the test arena, increased relative hunger level and high relative body mass both in - creased the likelihood of a takeover. However, the effects of body mass disappeared when scaled to body size. When the attacker and defender were equally hungry, larger relative body size increased takeover success but, when the at - tacker was either more or less hungry, body size had little effect on the likelihood of a takeover. Thus fight outcomes were dependent on an interaction between RHP and motivational asymmetries and on whether the resource was movable or stationary. Contest duration was not related to the magnitude of morphological differences between opponents, suggest - ing that assessment of fighting ability may be brief or nonexistent during time-limited animal contests over food items. Résumé : Les animaux d'une même espèce se font souvent une compétition directe pour les ressources alimentaires et le succès des combats peut être en corrélation positive avec leur pouvoir de rétention relatif de la ressource (RHP) et la
Summary The responses of single brain neurones to artificial calling song, to moving striped patterns and to air puffs were recorded while tethered crickets were walking on a sphere in such a way that their intended orientation to the stimuli could be measured. Local and descending brain neurones responsive to only one of the stimuli tested often encoded the directional information contained in the stimulus (e.g. the direction of the sound source or the direction of stripe movement). Brain neurones with little directional sensitivity responded with marked habituation to all stimuli, so that their responses primarily signalled changes in the overall stimulus situation. The responses of some neurones were stronger during walking than when the cricket was standing still. In the case of one descending neurone, which increased its level of activity shortly before and during the walking phases, the mean spike rate was correlated with the forward velocity. By altering the discharge rate of another descending neurone, it was possible to elicit walking in the manner typical of crickets. Maintenance and control of walking by such 'command neurones' is discussed.
We review current knowledge on octopaminergic systems in all major phyla with emphasis on arthropods. Octopaminergic systems occur in all triploblastic animals investigated. Close relationships of the octopamine-receptors in protostomes to vertebrate alpha-adrenergic receptors suggest an ancient common origin. Some evidence suggests that the octopaminergic system may be younger than the vertebrate adrenergic system. All octopaminergic systems are constructed from comparatively few neurons, and the cell populations in different representatives of a given phylum are clearly similar. Current data do not allow any conclusions on the relationships between molluscs and annelids (Lophotrochozoa) to nematodes and arthropods (Ecdysozoa). In chelicerates, including Limulus as a remaining xiphosuran, and crustaceans, octopaminergic neurons occur in pairs. All investigated winged insects (Pterygota) possess similar arrangements of octopaminergic cell populations, suggesting that their octopaminergic systems have been largely conserved during evolution. Unpaired octopaminergic neurons, with symmetrical, bilaterally projecting efferent axons in insects do not appear to have counterparts in other arthropods. Unpaired-octopaminergic neurons may thus be an autapomorphic feature of winged insects. Octopamine acts as an inhibitory neurotransmitter in gastropods, and as an excitatory transmitter controlling bioluminescence in fireflies. Octopamine is also implicated in controlling bioluminescence in other phyla. All critically examined triploblastic invertebrates release octopamine as a hormone, as a peripheral modulator and as a central neuromodulator in the nervous system, which exerts its action via evolutionary related G-protein-coupled receptors that activate cAMP. The evolution of the octopaminergic system seems fundamental for the evolution of efficient locomotory mechanisms, complex social interactions, and cognitive abilities of arthropods.
Crickets have traditional sex roles, where males compete aggressively for access to selective polyandrous females. However, in a laboratory experiment, we found that normally nonaggressive female Gryllus campestris fought each other vigorously in the presence of a courting male, resulting in a dominant female that gained a greater probability of receiving the spermatophore. Female–female fights included the same series of characteristic actions known from male–male fights, which demonstrates that the females can perform the full repertoire of agonistic actions except for the production of the aggressive rival song. Since females remained nonaggressive towards each other in the vicinity of a muted male, but were induced to fight each other in the complete absence of a male by the auditory experience of the courtship song, this song is both sufficient and necessary to induce female competition for males. Calling song was as effective as courtship song at inducing female aggression, whereas rival song was least effective. We therefore speculate that the calling and courtship songs may signal a male’s resource value. Ó 2008 The Association for the Study of Animal Behaviour. Published by Elsevier Ltd. All rights reserved.
It is thought that the adjustment of intraspecific aggression is an essential factor in the development of a social structure. To understand the natural laws for organizing the social structure, we focus on the fighting behavior of crickets, Gryllus bimaculatus, and investigate the neuronal mechanisms to adjust aggressiveness associated with a neuromodulatory biological amine: serotonin (5-HT).In this paper, we present a working theory of a neurophysiological mechanism based on the past biological studies on the 5-HT hypothesis, and a mathematical model of the mechanism. We analyzed this model and concluded that this neurophysiological mechanism makes the forgetting process slower. Next, we fitted our theoretical forgetting curve to an experimental curve and estimated the parameters of our model. These estimated values were in agreement with common belief in biological science.
Dopamine is synonymous with reward and motivation in mammals. However, only recently has dopamine been linked to motivated behaviour and rewarding reinforcement in fruitflies. Instead, octopamine has historically been considered to be the signal for reward in insects. Here we show, using temporal control of neural function in Drosophila, that only short-term appetitive memory is reinforced by octopamine. Moreover, octopamine-dependent memory formation requires signalling through dopamine neurons. Part of the octopamine signal requires the α-adrenergic-like OAMB receptor in an identified subset of mushroom-body-targeted dopamine neurons. Octopamine triggers an increase in intracellular calcium in these dopamine neurons, and their direct activation can substitute for sugar to form appetitive memory, even in flies lacking octopamine. Analysis of the β-adrenergic-like OCTβ2R receptor reveals that octopamine-dependent reinforcement also requires an interaction with dopamine neurons that control appetitive motivation. These data indicate that sweet taste engages a distributed octopamine signal that reinforces memory through discrete subsets of mushroom-body-targeted dopamine neurons. In addition, they reconcile previous findings with octopamine and dopamine and suggest that reinforcement systems in flies are more similar to mammals than previously thought.
Reward seeking is a major motivator and organizer of behavior, and animals readily learn to modify their behavior to more easily obtain reward, or to respond to stimuli that are predictive of reward. Here, we compare what is known of reward processing mechanisms in insects with the well-studied vertebrate reward systems. In insects almost all of what is known of reward processing is derived from studies of reward learning. This is localized to the mushroom bodies and antennal lobes and organized by a network of hierarchically arranged modulatory circuits, especially those involving octopamine and dopamine. Neurogenetic studies with Drosophila have identified distinct circuit elements for reward learning, "wanting," and possibly "liking" in Drosophila, suggesting a modular structure to the insect reward processing system, which broadly parallels that of the mammals in terms of functional organization. Expected final online publication date for the Annual Review of Entomology Volume 58 is December 03, 2013. Please see http://www.annualreviews.org/catalog/pubdates.aspx for revised estimates.
Insects possess miniature brains but exhibit a sophisticated behavioral repertoire (Menzel and Giurfa, 2001; Giurfa, 2003, 2007; Chittka and Niven, 2009; Srinivasan, 2010; Avargues-Weber et al., 2011; Dyer, 2012; Zhang et al., 2012). Recent studies have indicated that insects copy the behavior of conspecifics in contexts as diverse as foraging, in the case of bumblebees (Leadbeater and Chittka, 2005, 2008; Worden and Papaj, 2005), mate choice in the case of flies (Mery et al., 2009), and predator avoidance in the case of crickets (Coolen et al., 2005). These reports yield new light on the cognitive richness of insect behavior, which seems to transcend basic Pavlovian and operant learning, and have received a wide coverage, thereby inducing a reappraisal of insect learning capabilities. Yet, the critical question is not whether or not insects achieve “marvelous feats,” but, essentially, how do they achieve them. Here I focus on recent studies on social learning in insects and analyze to what extent these learning cases exceed elemental-learning interpretations, i.e., interpretations based on simple stimulus–stimulus (Pavlovian) or behavior-stimulus (operant) associations.
Ritualized fighting between conspecifics is an inherently dangerous behavioral strategy, optimized to secure limited resources at minimal cost and risk. To be adaptive, potential rewards, and costs of aggression must be assessed to decide when it would be more opportune to fight or flee. We summarize insights into the proximate mechanisms underlying this decision-making process in field crickets. As in other animals, cricket aggression is enhanced dramatically by motor activity, winning, and the possession of resources. Pharmacological manipulations provide evidence that these cases of experience dependent enhancement of aggression are each mediated by octopamine, the invertebrate counterpart to adrenaline/noradrenaline. The data suggest that both physical exertion and rewarding aspects of experiences can activate the octopaminergic system, which increases the propensity to fight. Octopamine thus represents the motivational component of aggression in insects. For the decision to flee, animals are thought to assess information from agonistic signals exchanged during fighting. Cricket fights conform to the cumulative assessment model, in that they persist in fighting until the sum of their opponent's actions accumulates to some threshold at which they withdraw. We discuss evidence that serotonin, nitric oxide, and some neuropeptides may promote an insect's tendency to flee. We propose that the decision to fight or flee in crickets is controlled simply by relative behavioral thresholds. Rewarding experiences increase the propensity to fight to a level determined by the modulatory action of octopamine. The animal will then flee only when the accumulated sum of the opponent's actions surpasses this level; serotonin and nitric oxide may be involved in this process. This concept is in line with the roles proposed for noradrenaline, serotonin, and nitric oxide in mammals and suggests that basic mechanisms of aggressive modulation may be conserved in phylogeny.
Both resource-holding potential (RHP) and experience in aggressive contests are known to affect future aggressive behaviour.
However, few studies have examined the effects of mating experience on agonistic behaviour, despite the fact that dominant
males usually acquire more matings. We investigated the effect of mating experience on male aggressive behaviour including
the relationship between RHP and fighting success in the fall field cricket, Gryllus pennsylvanicus. We formed pairs of size- and age-matched males that varied in RHP (relative weapon size) and conducted two experiments.
In the first, we varied male mating experience by allowing one male in a pair to either be (a) ‘mated’: court, be mounted
and copulate with a virgin female or (b) ‘experienced’: court, be mounted, but prevented from copulating. The second experiment
varied postcopulatory experience where the male was allowed (‘contact’) or prevented from (‘no-contact’) continued contact
with his recent mate. Following treatment, experimental males engaged in an aggressive contest with the naïve size- and age-matched
male. In our first experiment, we found that mated and experienced males were equally likely to escalate contests to combat
with a naïve opponent, but mated males were less likely than experienced males to win. There was no effect of mating on the
relationship between RHP and fighting success. In our second experiment, we found no effect of maintaining contact with the
female on the tendency to escalate or the probability of winning. As in the first experiment, males with relatively larger
heads again won more fights and this relationship was unaffected by male experience. These results suggest that mating is
itself detrimental to male success in aggressive contests, but that this effect is not sufficient to eliminate the effect
of RHP on fighting success.
KeywordsAggression-Sexual selection-Resource-holding potential-Social experience-Weaponry-Field cricket
An animal’s motivational state can significantly impact its behavior. We examined the effects of mating on the aggression
of male Acheta domesticus crickets. Pairs of males were allowed to establish dominance and subordinance and were then physically separated. Subordinate
males were then allowed to either copulate with a female or to have chemo-tactile contact with, but to not copulate with,
a female. Less than 15min after separation, all male pairs engaged in a second agonistic encounter. Subordinate males that
copulated with females were significantly more aggressive toward their dominant partners than un-mated subordinate males.
Many mated subordinates became dominant. Allowing a subordinate male to contact, but not copulate with, a female had a similar
effect, suggesting that chemo-tactile cues from the female are sufficient to elicit this change in aggression.
In crickets Gryllus bimaculatus, flight has been shown to be able to promote aggressive encounters between males and to suppress escape behavior. The aim
of this study was to examine the influence of flight on male behavior in male–female interactions. We found that flown males
demonstrate enhanced courtship behavior. The latency of calling song was significantly shorter, while the relative total duration
of singing as well as the duration of singing episodes longer in flown males than in the control. Mating rate was also significantly
higher in the experimental group containing flown males. The results suggest that, in addition to previously reported effects
on aggressiveness and escape, flying has a profound accelerating effect on male courtship behavior.
Aggressive behavior is widely present throughout the animal kingdom and is crucial to ensure survival and reproduction. Aggressive actions serve to acquire territory, food, or mates and in defense against predators or rivals; while in some species these behaviors are involved in establishing a social hierarchy. Aggression is a complex behavior, influenced by a broad range of genetic and environmental factors. Recent studies in Drosophila provide insight into the genetic basis and control of aggression. The state of the art on aggression in Drosophila and the many opportunities provided by this model organism to unravel the genetic and neurobiological basis of aggression are reviewed.
The function of aggressive signals, including both their information content and the circumstances under which they cause resolution or escalation of conflict, continues to be controversial. We studied the information content of aggressive songs in the house cricket, Acheta domesticus, to test their ability to inform opponents about fighting ability and motivation. We show that songs produced by individual males are highly repeatable and contain information about male resource holding potential, the ability of a male to win an aggressive contest. Temporal components of aggressive song were correlated with male body size, and size affected both the intensity and outcome of fights. In contrast, we found no components of song that signal motivation to fight. Although males with restricted access to mates were significantly more aggressive and won fights more often, their songs did not reflect the asymmetry in motivation to fight. We discuss possible reasons for the absence of signals of motivation during animal contests.
Previous interactions with conspecifics influenced the pattern, frequency and intensity of agonistic behaviour in the field cricket Gryllus bimaculatus. Tactile contact appeared to be the most important sensory cue responsible for the observed shifts in behaviour. Contact with other adult males promoted the production of aggressive song both during and after fights between males. However, individually housed males and males with restricted contact with conspecifics (once per day for 5 days) produced their aggressive song only at the end of an agonistic encounter. These two patterns of agonistic behaviour may reflect alternate fighting strategies. Prior experience influences whether sensory cues from a conspecific will initate agonistic behaviour. After males lost a fight, they displayed no further agonistic behaviour for 10 min but then gradually recovered their agonistic behaviour within an hour. This may be an important mechanism in preventing losing males from re-engaging a more powerful rival. Females were much less likely than males to attack conspecifics when food was plentiful. When food was scarce, females fought more often, and more successfully, than males for the contested resource.
In decision from experience, the source of probability information affects how probability is distorted in the decision task. Understanding how and why probability is distorted is a key issue in understanding the peculiar character of experience-based decision. We consider how probability information is used not just in decision-making but also in a wide variety of cognitive, perceptual, and motor tasks. Very similar patterns of distortion of probability/frequency information have been found in visual frequency estimation, frequency estimation based on memory, signal detection theory, and in the use of probability information in decision-making under risk and uncertainty. We show that distortion of probability in all cases is well captured as linear transformations of the log odds of frequency and/or probability, a model with a slope parameter, and an intercept parameter. We then consider how task and experience influence these two parameters and the resulting distortion of probability. We review how the probability distortions change in systematic ways with task and report three experiments on frequency distortion where the distortions change systematically in the same task. We found that the slope of frequency distortions decreases with the sample size, which is echoed by findings in decision from experience. We review previous models of the representation of uncertainty and find that none can account for the empirical findings.
Winning an agonistic interaction against a conspecific is known to heighten aggressiveness, but the underlying events and mechanism are poorly understood. We quantified the effect of experiencing successive wins on aggression in adult male crickets (Gryllus bimaculatus) by staging knockout tournaments and investigated its dependence on biogenic amines by treatment with amine receptor antagonists. For an inter-fight interval of 5 min, fights between winners escalated to higher levels of aggression and lasted significantly longer than the preceding round. This winner effect is transient, and no longer evident for an inter-fight interval of 20 min, indicating that it does not result from selecting individuals that were hyper-aggressive from the outset. A winner effect was also evident in crickets that experienced wins without physical exertion, or that engaged in fights that were interrupted before a win was experienced. Finally, the winner effect was abolished by prior treatment with epinastine, a highly selective octopamine receptor blocker, but not by propranolol, a ß-adrenergic receptor antagonist, nor by yohimbine, an insect tyramine receptor blocker nor by fluphenazine an insect dopamine-receptor blocker. Taken together our study in the cricket indicates that the physical exertion of fighting, together with some rewarding aspect of the actual winning experience, leads to a transient increase in aggressive motivation via activation of the octopaminergic system, the invertebrate equivalent to the adrenergic system of vertebrates.
Reduced levels of serotonin (5-HT) within prefrontal cortex (PFC)-amygdala circuits have long been implicated in impulsive aggression. However, whether lowering 5-HT alters the dynamic interplay between the PFC and the amygdala has not been directly tested in humans. It is known that manipulating 5-HT via acute tryptophan depletion (ATD) causes variable effects on brain responses to a variety of emotional stimuli, but it remains unclear whether ATD affects functional connectivity in neural networks involved in processing social signals of aggression (e.g., angry faces).
Thirty healthy individuals were enrolled in a randomized, double-blind, placebo-controlled ATD study. On each treatment, brain responses to angry, sad, and neutral faces were measured with functional magnetic resonance imaging. Two methods (psycho-physiological-interaction in a general linear model and dynamic causal modeling) were used to assess the impact of ATD on the functional connectivity between PFC and amygdala.
Data from 19 subjects were available for the final analyses. A whole-brain psycho-physiological-interaction in a general linear model showed that ATD significantly modulated the connectivity between the amygdala and two PFC regions (ventral anterior cingulate cortex and ventrolateral PFC) when processing angry vs. neutral and angry vs. sad but not sad vs. neutral faces. Dynamic causal modeling corroborated and extended these findings by showing that 5-HT depletion reduced the influence of processing angry vs. neutral faces on circuits within PFC and on PFC-amygdala pathways.
We provide strong support for neurobiological accounts positing that 5-HT significantly influences PFC-amygdala circuits implicated in aggression and other affective behaviors.
Sensory neurons are mostly studied in fixed animals, but their response properties might change when the animal is free to move. Indeed, recent studies found differences between responses of sensory neurons in resting versus moving insects. Since the dynamic range of visual motion stimuli strongly depends on the speed at which an animal is moving, we investigated whether the visual system adapts to such changes in stimulus dynamics as induced by self-motion. Lobula plate tangential cells of flies lend themselves well to study this question because they are known to code for ego-motion based on optic-flow. We recorded the responses of the lobula plate tangential cell H1 to a visual pattern moving at different velocities under three different conditions: fixed flies before and after application of the octopamine agonist chlordimeform (CDM) and tethered flying flies. CDM has been previously shown to induce arousal in flies. We found that flying as well as the application of CDM significantly broadens the velocity tuning of H1 toward higher velocities.
When two socially naive Drosophila males meet, they will fight. However, prior social grouping of males reduces their aggression. We found olfactory communication to be important for modulating Drosophila aggression. Although acute exposure to the male-specific pheromone 11-cis-vaccenyl acetate (cVA) elicited aggression through Or67d olfactory receptor neurons (ORNs), chronic cVA exposure reduced aggression through Or65a ORNs. Or65a ORNs were not acutely involved in aggression, but blockade of synaptic transmission of Or65a ORNs during social grouping or prior chronic cVA exposure eliminated social modulation of aggression. Artificial activation of Or65a ORNs by ectopic expression of the Drosophila gene TrpA1 was sufficient to reduce aggression. Social suppression of aggression requires subsets of local interneurons in the antennal lobe. Our results indicate that activation of Or65a ORNs is important for social modulation of male aggression, demonstrate that the acute and chronic effects of a single pheromone are mediated by two distinct types of ORNs, reveal a behaviorally important role for interneurons and suggest a chemical method to reduce aggression in animals.
Crickets use their long antennae as tactile sensors. Confronted with obstacles, conspecifics, or predators, antennal contacts trigger short-latency motor responses. To reveal the neuronal pathway underlying these antennal-guided locomotory reactions we identified descending interneurons that rapidly transmit antennal-tactile information from the head to the thorax in the cricket Gryllus bimaculatus. Antennae were stimulated with forces approximating those of naturally occurring antennal contacts. Responding interneurons were individually identified by intracellular axon recordings in the pro-mesothoracic connective and subsequent tracer injection. Simultaneous with the intracellular recordings, the overall spike response in the neck connectives was recorded extracellularly to reveal the precise response-timing of each individual neuron within the collective multiunit response. Here we describe four descending brain neurons and two with the soma in the subesophageal ganglion. All antennal-touch elicited action potentials apparent in the neck connective recordings within 10 ms after antennal-contact are generated by these six interneurons. Their dendrites ramify in primary antennal-mechanosensory neuropils of the head ganglia. Each of them consistently generated action potentials in response to antennal touching and three of them responded also to different visual stimulation (light-off, movement). Their descending axons conduct action potentials with 3-5 m/s to the thoracic ganglia where they send off side branches in dorsal neuropils. Their physiological and anatomical properties qualify them as descending giant fibers in the cricket and suggest an involvement in evoking fast locomotory reactions. They form a fast-mediating cephalo-thoracic pathway for antennal-tactile information, whereas all other antennal-tactile interneurons had response latencies exceeding 40 ms.
Aggression is a behavioural strategy for securing resources (food, mates and territory) and its expression is strongly influenced by their presence and value. While it is known that resource holders are generally highly aggressive towards intruding consexuals and usually defeat them, the underlying neuronal mechanisms are not known. In a novel intruder-resident paradigm for field crickets (Gryllus bimaculatus), we show that otherwise submissive losers of a preceding aggressive encounter readily fight and often defeat aggressive winners after occupying an artificial shelter. This aggression enhancing effect first became evident after 2 min residency, and was maximal after 15 min, but absent 15 min after shelter removal. The residency effect was abolished following non-selective depletion of biogenic amines from the central nervous system using reserpine, or semi-selective depletion of octopamine and dopamine using α-methyl-tyrosine, but not following serotonin depletion using α-methyl-tryptophan. The residency effect was also abolished by the treatment with phentolamine, an α-adrenergic receptor antagonist, or epinastine, a highly selective octopamine receptor blocker, but not by propranolol, a ß-adrenergic receptor antagonist, or by yohimbine, an insect tyramine receptor blocker. We conclude that crickets evaluate residency as a rewarding experience that promotes aggressive motivation via a mechanism involving octopamine, the invertebrate analogue of noradrenaline.
Situations requiring rapid decision-making in response to dynamic environmental demands occur repeatedly in natural environments. Neuromodulation can offer important flexibility to the output of neural networks in coping with changing conditions, but the contribution of individual neuromodulatory neurons in social behavior networks remains relatively unknown. Here we manipulate the Drosophila octopaminergic system and assay changes in adult male decision-making in courtship and aggression paradigms. When the functional state of OA neural circuits is enhanced, males exhibit elevated courtship behavior towards other males in both behavioral contexts. Eliminating the expression of the male form of the neural sex determination factor, Fruitless (Fru(M)), in three OA suboesophageal ganglia (SOG) neurons also leads to increased male-male courtship behavior in these same contexts. We analyzed the fine anatomical structure through confocal examination of labeled single neurons to determine the arborization patterns of each of the three Fru(M)-positive OA SOG neurons. These neurons send processes that display mirror symmetric, widely distributed arbors of endings within brain regions including the ventrolateral protocerebra, the SOG and the peri-esophageal complex. The results suggest that a small subset of OA neurons have the potential to provide male selective modulation of behavior at a single neuron level.
Summary The distribution of antennal afférents in the deutocerebrum of the cricket and the overlap of presumably mechanosensory terminals with the dendritic trees of some descending brain neurons was investigated. In double labelling experiments descending cells were filled retrogradely with Lucifer Yellow via the cervical connective, while fibers from the flagellum of the antenna were simultaneously stained with Neurobiotin. The results show three distinct termination areas of antennal receptors. These are the antennal lobe, dorsal lobe, and a third, newly described area in the ventral, lateral to medial, posterior deutocerebrum. In this region numerous, presumably mechanosensory fibers from the flagellum of the antenna terminate. These small fibers are closely packed and form a neuropile of dense appearance. The afférents enter this area in parallel bands, which might suggest a somatotopic map. The relative locations of the three areas of afferent antennal projections in the deutocerebrum of the cricket are summarized. One identified ipsilateral descending cell has a large, bifurcating dendritic tree that projects into the newly described neuropile. Another ipsilateral descending neuron only sends major branches into the anterior deutocerebrum, where another group of presumed mechanosensory, antennal afferent fibers is located. Moreover, some contralateral descending neurons also show overlap with presumed non-olfactory antennal terminals. These findings suggest rather close connections between presumed mechanosensory afférents and descending neurons. confocal laser scanning microscopy.
Single descending brain neurones were recorded and stained intracellularly in the neck connectives of crickets while they walked upon a styrofoam ball under open-loop conditions. The animal's translational and rotational velocities were measured simultaneously, and various stimuli were used to investigate the neuronal response characteristics. Stimulation with a moving grating or an artificial calling song of 5 kHz induced optomotor behaviour and positive phonotaxis. An acoustic stimulus of 20 kHz elicited negative phonotaxis.
We report the first clear evidence for behaviourally dependent gating of sensory responses of identified descending brain neurones. Most descending cells only responded to visual stimuli or to an artificial calling song of 5 kHz while the animal was walking, indicating that the responses to these stimuli were gated by the walking activity of the animal. In contrast to this, responses to stimuli that elicit negative phonotaxis, such as acoustic stimuli of 20 kHz, were not gated. This indicates that the gating of sensory responses in these cells depends on the behavioural context of the stimulus.
From these findings, we conclude that significant information about the properties of sensory processing in higher-order neurones can only be gained from tests in behaviourally relevant paradigms. Important characteristics might otherwise be missed, thus leading to misinterpretations regarding their function.
Animal personalities have become an established concept in animal behaviour. Despite this, the potential influence of early life experiences on adult personality is often overlooked. Juvenile exposure to environmental cues such as conspecific signalling or predator cues may provide relevant information regarding the make-up of the forthcoming environment. Individuals might be able to use these cues to adjust developmental trajectory and adult personality to prevent a personality-environment mismatch. Using the field cricket Gryllus integer, we show that individuals reared in the presence of conspecific acoustic sexual signals alter both growth rate and an adult personality trait. Males reared in the presence of acoustic sexual signals were less aggressive and less likely to become dominant relative to those reared in the absence of acoustic signals. Additionally, acoustic treatment interacted with juvenile body mass: large juveniles reared in the presence of acoustic signals were larger than small juveniles reared in the presence of acoustic signals and larger than all juveniles reared in silence. We discuss the potential adaptive significance of the observed developmental and personality differences.
Game theory predicts that at least some of the behaviour patterns displayed during aggressive encounters are used to assess asymmetries in variables that indicate fighting ability and resource value. Game theoretical models such as the sequential assessment game see assessment as the major activity during a fight. However, while these models acknowledge the existence of physical and motivational assessment parameters, there are only a few examples where a mechanism for the assessment of fighting readiness has been shown. In staged encounters between male Mediterranean field crickets, Gryllus bimaculatus, fighting behaviour follows a stereotyped escalation cascade with ritualized displays in the beginning and physical combat towards the end. Despite their larger size, heavier animals lost 30% of the encounters even if weight asymmetry was large. To examine whether the contestants provide assessment cues that might explain this surprising result, we analysed two stereotyped displays in detail (antennal fencing and mandible spreading). The duration of antennal fencing, which is necessary to initiate a fight, was independent of experience and weight asymmetry between the contestants, but was prolonged after shortening the antennae by almost 90%. Fights escalated only when antennal movement frequencies were high in both contestants. In blinded crickets few contests were settled by another ritualized display, mandible spreading, and fights that escalated beyond this stage were significantly shorter than in untreated crickets. We suggest that antennal fencing may be used to assess fighting readiness of the opponent, while mandible spreading may indicate fighting ability. We conclude that high willingness to fight may help crickets to overcome inferior fighting ability.
Various game theory models have been used to explain animal contests. Here we attend to the presumed cognitive abilities required by these models with respect to information gathering and consequent decision making. Some, such as the hawk/dove game and self-assessment models require very limited cognitive ability. By contrast, the broadly accepted sequential assessment model requires that contestants know their own abilities and compare them with information gathered about their opponent to determine which has the greater resource-holding power. However, evidence for assessment of relative abilities is sparse and we suggest that this complex ability is probably beyond most animals. Indeed, perceptual limitations may restrict information about an individual's own displays and thus preclude comparison. We take a parsimonious view and conclude that simple summation of causal factors accounts for changes in fight motivation without requiring mutual evaluation of relative abilities.
Experiments were carried out to study the effect of social conditioning (prior experience of dominance and submission) in dominance relationships between adult male Gryllus bimaculatus. The dominance status of a male cricket appears to be directly linked to its immediate prior agonistic experience. An experience of dominance increases the probability of victory and one of submission decreases it. The effect is maximum when one opponent has experienced dominance and one subordination. The aggressive behavior of males is significantly influenced by prior agonistic experience for 6 h and the effect disappears entirely after 24 h. The cost and benefit of a conflict appears to be dependent on the motivational state of each opponent, in turn modulated by the outcome of prior agonistic interactions.
DURING classical conditioning, animals learn to associate a neutral stimulus with a meaningful, or unconditioned, stimulus. The unconditioned stimulus is essential for forming associations, and modifications in the processing of the unconditioned stimulus are thought to underlie more complex learning forms1-4. Information on the neuronal representation of the unconditioned stimulus is therefore required for understanding both basic and higher-order features of conditioning. In honeybees, conditioning of the proboscis extension reflex occurs after a single pairing of an odour (conditioned stimulus) with food (unconditioned stimulus)5,6 and shows several higher-order features of conditioning6-8. I report here the identification of an interneuron that mediates the unconditioned stimulus in this associative learning. Its physiology is also compatible with a function in complex forms of associative learning. This neuron provides the first direct access to the cellular mechanisms underlying the reinforcing properties of the unconditioned stimulus pathway.
The assessment strategy used by adult male crickets, Gryllus bimaculatus (de Geer), during conspecific aggression was deduced from the effects of handicaps (disabled mandibles, blackened eyes, size) and altered aggressive motivation (after defeat and flying) on aggressiveness, fight duration and win probability under laboratory conditions. The contestants received either the same (symmetrical) or different (asymmetrical) treatments. Despite handicaps, all crickets showed essentially normal escalating fighting behaviour. In symmetrical contests, fights became even harsher and longer with multiple handicaps. In asymmetrical contests, neither disabling the mandibles nor blackening the eyes significantly influenced win probability. However, ‘blinded’ crickets nearly always defeated opponents with disabled mandibles that could not inflict bites. Furthermore, small crickets and losers showed physical fighting more frequently when prevented from seeing. Handicap effects became more pronounced when both contestants were flown, to maximize aggressive motivation, before fighting. Our findings conform to the cumulative assessment hypothesis. We conclude, first, that contestants need longer to accumulate the cues required to surpass a threshold to flee when visual and physical inputs are reduced. Second, the decision to flee is based solely on the opponent's actions. Third, flying enhances aggressiveness by reducing disparities in motivation, making other disparities, such as in weaponry, more decisive. Thus, a cricket's aggressiveness is a trade-off between its inherent, experience-dependent agonistic motivation and the accumulated perceived actions of the adversary.
The activity of four types of sound-sensitive descending brain neurons in the cricket Gryllus bimaculatus was recorded intracellularly while animals were standing or walking on an open-loop trackball system. In a neuron with a contralaterally descending axon, the male calling song elicited responses that copied the pulse pattern of the song during standing and walking. The accuracy of pulse copying increased during walking. Neurons with ipsilaterally descending axons responded weakly to sound only during standing. The responses were mainly to the first pulse of each chirp, whereas the complete pulse pattern of a chirp was not copied. During walking the auditory responses were suppressed in these neurons. The spiking activity of all four neuron types was significantly correlated to forward walking velocity, indicating their relevance for walking. Additionally, injection of depolarizing current elicited walking and/or steering in three of four neuron types described. In none of the neurons was the spiking activity both sufficient and necessary to elicit and maintain walking behaviour. Some neurons showed arborisations in the lateral accessory lobes, pointing to the relevance of this brain region for cricket audition and descending motor control.
All nervous systems are subject to neuromodulation. Neuromodulators can be delivered as local hormones, as cotransmitters in projection neurons, and through the general circulation. Because neuromodulators can transform the intrinsic firing properties of circuit neurons and alter effective synaptic strength, neuromodulatory substances reconfigure neuronal circuits, often massively altering their output. Thus, the anatomical connectome provides a minimal structure and the neuromodulatory environment constructs and specifies the functional circuits that give rise to behavior.
Insect antennae are multisensory probes which are used in many behavioural contexts, receiving sensory information from various modalities. Mechanoreceptors signal exteroreceptive cues like contact with another surface, flow or vibration of the surrounding medium, and proprioreceptive cues like joint angles and cuticular strain due to bending. Antennae can actively search the surrounding space, scan objects for surface properties, or transfer information between conspecifics by means of physical contact.We review insect behaviours involving antennal mechanosensory information, and passive or active antennal movements. Chemo- and thermoreception are only covered to the extent to which there is a direct connection to tactile sensing. Particular emphasis is given to model systems of invertebrate neuroscience, i.e. cockroach, cricket, locust, stick insect and the honeybee. For comparison, corresponding behaviours of crayfish and lobsters are discussed.The six sections deal with (a) the antennal motor system, kinematics, biomechanics, musculature and efferent innervation; (b) the sensory physiology of antennal mechanoreceptors, including mechanosensitive hairs, campaniform sensilla, chordotonal organs and stretch receptors; (c) the neuroanatomy of the brain structures processing antennal mechanosensory information, notably the deutocerebrum; (d) the neurophysiology of the afferents, local and descending interneurons, and motoneurons; (e) the behavioural physiology of passive and active sensing, including reflex behaviours, graviception, steering, escape, tactile exploration and localisation, pattern recognition, tactile learning and communication; and (f) some engineering aspects regarding the construction of artificial tactile antennae
Motivational asymmetry caused by differences in subjective resource value is a key component of strategic models of aggression. We study the role of motivational asymmetry in determining differential aggression and mating success of male house crickets, Acheta domesticus. We also assess the extent to which mating differences associated with motivational asymmetry are due to direct male–male fighting vs. male–female interactions. We manipulated male motivation to compete for a mating opportunity by providing males with either no access or nightly access to females for 4 d prior to the experiment. As predicted, when males from each treatment had to compete for the female, those with lower prior access were more aggressive and mated more often. In contrast, when males from each treatment were paired individually with females, there was no significant difference in the frequencies with which they pursued, courted or mated with females. We also found no evidence for female choice based on motivational asymmetry; the rate of successful courtship did not differ between treatments. We conclude that prior mate encounter rate can generate motivational asymmetry, leading to differential mating success mediated by direct male–male aggression.
1. There is a growing appreciation that male fighting ability is influenced by multiple traits. In particular, studies of male combat have identified a variety of performance capacities that predict victory in conflicts between conspecifics in several animal species. However, while multiple aspects of male fighting ability are often examined with a single study, the interactions among traits are rarely considered.
2. We conducted fight trials between size-matched males in the black field cricket, Teleogryllus commodus, with the aim of testing how two whole-organism performance traits, jumping ability and bite force, together with weight at eclosion, interact to determine combat outcomes. We then examined the relationships between these traits and the outcome of a fight using: a univariate framework, where we examined the difference between winners and losers for each trait separately; and, a multivariate framework known as response surface analysis, where we examined how the interactions among traits predict the outcome of a fight.
3. We show that males that won fights tended to exert significantly more force when biting, but were neither better jumpers nor heavier at eclosion than their rivals. However, when we examined the effects of these three traits while statistically controlling for one another in a multiple regression, we showed that overall fighting ability depends not only on contributions of individual traits to contest resolution but also on the interactions among traits and their relationship to the capabilities of rival males. We found that the probability of winning was highest for a male with the greatest positive difference from his rival in the combination of bite force, jump power and weight at eclosion.
4. These findings highlight how studying multiple performance capabilities in isolation from each other may obscure the importance of some variables. Our multivariate analyses revealed that the interactions between multiple dimensions of performance are important in male combat. We discuss the broader implications of these findings, including the potential role of whole-organism performance in determining male quality.
Male field crickets frequently engage in agonistic contests to establish dominance in social interactions and gain access to mate attraction territories. Crickets (Orthoptera: Gryllidae) are often used as a model taxon to study aggression, but limited documentation of aggression in some cricket species hinders our understanding of its evolutionary costs and benefits. Our study investigated cricket aggression at two scales: the within-species scale for two cricket species, Gryllus assimilis and G. veletis, whose aggression had not been adequately documented and the among-species scale to detect evolutionary patterns in species’ levels of aggression. In both G. veletis and G. assimilis, winners spent more time being aggressive than losers, but they were not larger or heavier. Collectively, our results reveal that G. veletis males are more aggressive than G. assimilis. Male G. veletis had higher aggression scores that male G. assimilis. The majority of G. veletis contests escalated to grappling (a highly aggressive behavior), while less than one quarter of G. assimilis contests escalated to grappling. Further, G. veletis males transitioned between two of the most aggressive behaviors most often while G. assimilis transitioned between two of the least aggressive behaviors most often. We integrate this new information on aggression for G. assimilis and G. veletis with previously documented aggression data for many cricket species to investigate aggression in a broader evolutionary context than previously possible. Within a phylogenetic context, we test the hypothesis that species whose males use burrows from which to call and attract females are more aggressive than species with non-burrowing males. We found evidence consistent with this hypothesis; species with burrowing males tended to be more aggressive than species with non-burrowing males. Together, our study provides fine-scale understanding of aggression in two cricket species and broad-scale evolutionary context for aggression across cricket species.
Biochemical investigations have demonstrated that nitric oxide synthase (NOS) is distributed widely in the olfactory system. However, little is known about the action of NO at the synaptic level on identified neurons in local circuits that process chemosensory signals. Here, using whole-cell recordings, the effect of NO on cholinergic synaptic input to olfactory projection neurons (PNs) is determined in the Drosophila antennal lobes (ALs), which has become an excellent model for studying early olfactory-processing mechanisms. We found that the NO donor SNP/SNAP or the NO precursor L-arginine significantly decreased the frequency of cholinergic spontaneous excitatory postsynaptic currents (sEPSCs) in PNs. Conversely, soluble guanylyl cyclase (sGC) inhibitor oxadiazolo-quinoxaline-one (ODQ) significantly increased the frequency of cholinergic sEPSCs in PNs. The subsequent application of 8-bromo-cGMP significantly attenuated the effects of ODQ, indicating the possible involvement of NO-cGMP signaling. To determine the role of NO in quantal release of acetylcholine (Ach) to PNs, cholinergic miniature excitatory postsynaptic currents (mEPSCs) were recorded. SNP significantly decreased the frequency of mEPSCs, but exhibited no effect on the amplitude or the decay time constant of mEPSCs in PNs. The effect of SNP on the frequency of mEPSCs could be eliminated by ODQ as well. Thus, these results suggest that elevated NO concentration decreased cholinergic synaptic input to PNs in a sGC-dependent manner. In this way, NO signaling is suited to fulfill a regulatory role to effectively fine-tune network activity in Drosophila ALs.
Antennae are one of the major organs to detect chemo- and mechanosensory cue in crickets. Little is known how crickets process and integrate different modality of information in the brain. We thus used a number of different anatomical techniques to gain an understanding of the neural pathways extending from the antennal sensory neurons up to centers in the brain. We identified seven antennal sensory tracts (assigned as T1-7) utilizing anterograde dye filling from the antennal nerve. Tracts T1-T4 project into the antennal lobe (AL), while tracts T5 and T6 course into the dorsal region of the deutocerebrum or the suboesophageal ganglion, and finally, tract T7 terminates in the ventral area of flagellar afferent (VFA). By analyzing autofluorescence images of the AL, we identified 49 sexually isomorphic glomeruli on the basis of shape, relative position and size. On the basis of our sensory-tract data, we assigned the glomeruli into one of four separate groups. We then three-dimensionally reconstructed the internal structures in the AL (glomeruli) and the VFA (layers). Next in the protocerebrum, we identified both the tracts and their terminations from the AL and VFA. We found that 10 tracts originate in the AL, whereas there are at least eight tracts from the VFA. Several tracts from the AL share their routes with those from the VFA, but their termination areas are segregated. We now have a better anatomical understanding of the pathways for the antennal information in cricket.
During contests the outcome is ultimately determined by the difference in fighting ability or resource holding potential (RHP) of opponents and the loser may make the decision to give up by comparing its own fighting ability to that of the eventual winner. Such ‘mutual assessment’, however, may not be possible in all cases and an alternative mechanism is to withdraw when the costs of remaining in the contest cross a threshold. Thus, in contests where the opponents do not impose direct costs on each other the decision to give up is based on the absolute RHP rather than the relative RHP of the loser. The possibility for ‘mutual’ or ‘self’ assessment is a feature that distinguishes between different theoretical models of contests. Here I analyse relationships between contest duration and relative and absolute measures of RHP to determine whether contests in the house cricket are settled on the basis of mutual or self assessment. Although body size may contribute to RHP, additional traits such as weapons and energetic status may also influence fighting ability. Therefore, in this study I aimed to determine which features contribute to RHP before analysis of the effects of relative and absolute RHP on contest duration. Energy and body size strongly differ between winners and losers but differences in weapon size are marginal. Analysis of contest duration supports the idea that mutual assessment is a feature of these contests but also suggests that individual thresholds of energetic cost contribute to the decision to give up.
Male field crickets (Gryllus integer; Orthoptera: Gryllidae) stridulate aggressively and fight vigorously in competition for females. We studied the degrees to which male-male aggression is influenced by time of night or day, sexual maturity, age and weight. Trials were observed between males matched for age and/or weight that had not previously been exposed to each other. Data were gathered on attack latency, aggressive stridulation, time spent in aggressive interactions and the winner of a trial. Aggression was equally likely to occur at any time of the day or night. Sexually mature males were more aggressive than adult males which had not yet produced a spermatophore. Age past sexual maturity did not greatly influence aggression, and heavy males were more aggressive than lighter ones. In repeated trials between the same males, one male in each pair won significantly more contests.
Females of the field cricket G. bimaculatus show multiple mating. Since such a strategy is likely to incur costs such as time and energy spent in orientation to calling males or increased susceptibility to predation, it must have certain selective advantages. This study shows that multiple mating is a potential mechanism of mate choice. Females removed the spermatophores of some males before complete insemination was achieved. Females also remained with large males in order to mate a second or third time. Since spermathecal morphology may limit last-male sperm precedence in this species, a function of multiple mating may be to dilute the sperm stored from previous matings with that of the current male, so increasing his representation in offspring production.
Males frequently remain in close proximity to their mate immediately postcopulation. This behavior has generally been interpreted as a guarding tactic designed to reduce the likelihood that a rival male can rapidly displace the ejaculate of the guarding male [1, 2]. Such attempts by males to control their mates represent a potential source of conflict [3-5], but guarding behaviors in species where it is difficult for males to control their mates suggest that conflict is not inevitable [6, 7]. We employed a network of infrared video cameras to study a wild population of individually marked and genotyped field crickets (Gryllus campestris). Lone females or males suffer similar rates of predation, but when a pair is attacked, the male allows the female priority access to their burrow, and in doing so dramatically increases his probability of being killed. In compensation for this increased predation risk, paired males mate more frequently and father more of the female's offspring. By staying with a male, females increase the sperm contribution of preferred males as well as reducing their predation risk. In contrast to conclusions based on previous lab studies, our field study suggests that mate guarding can evolve in a context of cooperation rather than conflict between the sexes.
Orthopteroid insects (cockroaches, crickets, locusts and related species) allow examination of active sensory processing in a comparative framework. Some orthopteroids possess long, mobile antennae endowed with many chemo- and mechanoreceptors. When the antennae are touched, an animal's response depends upon the identity of the stimulus. For example, contact with a predator may lead to escape, but contact with a conspecific may usually not. Active touch of an approaching object influences the likelihood that a discrimination of identity will be made. Using cockroaches, we have identified specific descending mechanosensory interneurons that trigger antennal-mediated escape. Crucial sensory input to these cells comes from chordotonal organs within the antennal base. However, information from other receptors on the base or the long antennal flagellum allows active touch to modulate escape probability based on stimulus identity. This is conveyed, at least to some extent, by textural information. Guidance of the antennae in active exploration depends on visual information. Some of the visual interneurons and the motor neurons necessary for visuomotor control have been identified. Comparisons across Orthoptera suggest an evolutionary model where subtle changes in the architecture of interneurons, and of sensorimotor control loops, may explain differing levels of vision-touch interaction in the active guidance of behaviour.
Previous winning experience increases the probability of winning a subsequent contest. However, it is not clear whether winning probability is affected only by the outcome of the contest (winning or losing) or whether fighting experience itself is also sufficient to induce this effect. We investigated this question in the East African cichlid fish Pundamilia spec. To create an unresolved conflict we allowed males to fight their own mirror image prior to a real fight against a size-matched non-mirror-stimulated control male. When males fight their own mirror image, the image's response corresponds to the action of the focal animal, creating symmetrical fighting conditions without the experience of losing or winning. We found that mirror-stimulated males were more likely to win an ensuing contest than control males. Interestingly, in this species mirror stimulation also induced an increase in circulating androgens, which is consistent with the hypothesis that stimulation of these sex steroids during aggressive encounters may prepare the animal for subsequent encounters. Our results suggest that fighting experience alone coupled with an androgen response, increases the likelihood of winning, even in the absence of a winning experience.
Many of the deleterious effects of chronic stress in vertebrates are caused by the long-term elevation of stress hormones. These negative effects are thought to be unavoidable by-products of sustained activation of the stress response, but the details remain unclear. A comparative perspective may help in understanding chronic stress. We exposed crickets (Gryllus texensis) to a mock predator. A single exposure to a mock predator induced a transient increase in the hemolymph (blood) concentration of the insect stress neurohormone, octopamine. Repeated exposure to the mock predator increased basal levels of octopamine, similar to the effects of chronic stress on the basal levels of vertebrate stress hormones. This study is the first to report an increase in the basal levels of an invertebrate stress hormone in response to repeated flight-or-fight stress. Chronic stress reduced weight gain, and decreased feeding and enhanced weight loss after food deprivation in adult female crickets. However, chronic stress also increased the tendency of crickets to produce sustained flight. Therefore, this study supports the hypothesis that increasing basal levels of stress hormones may be a phylogenetically common response to chronically stressful conditions. It also demonstrates that chronic stress has both positive and negative effects in insects.