Sneddon L.U., Braithwaite V.A., and Gentle M.J. (2003) Do fishes have nociceptors? Evidence for the evolution of a vertebrate sensory system. Proceedings of the Royal Society of London Series B-Biological Sciences. 270(1520): p. 1115-1121.
Halloy J., Sempo G., Caprari G., Rivault C., Asadpour M., Tache F., . . . Deneubourg J.L. (2007) Social Integration of Robots into Groups of Cockroaches to Control Self-Organized Choices. Science. 318(5853): p. 1155-1158 (group 9: Céline Aubry, Lucas Mauguin & Valentin Thouzeau).
Finger T. (2008) Sorting food from stones: the vagal taste system in Goldfish, Carassius auratus. Journal of Comparative Physiology A: Neuroethology, Sensory, Neural, and Behavioral Physiology. 194(2): p. 135-143 (group 12: Erwan de Gavelle & Stéphanie Guérin).
Devineni A.V. and Heberlein U. (2009) Preferential ethanol consumption in Drosophila models features of addiction. Current Biology. 19(24): p. 2126-2132.
Méry F., Varela S.A.M., Danchin E., Blanchet S., Parejo D., Coolen I., and Wagner R.H. (2009) Public versus personal information for mate copying in an invertebrate. Current Biology. 19(9): p. 730-734.
Skelhorn J. and Rowe C. (2009) Distastefulness as an antipredator defence strategy. Animal Behaviour. 78(3): p. 761-766.
Youngentob S.L. and Glendinning J.I. (2009) Fetal ethanol exposure increases ethanol intake by making it smell and taste better. Proceedings of the National Academy of Sciences of the United States of America. 106(13): p. 5359-5364. (group 5: Léna Bazin, Pauline Dumont & Anna Labarre)
Bateson M., Desire S., Gartside Sarah E., and Wright Geraldine A. (2011) Agitated Honeybees Exhibit Pessimistic Cognitive Biases. Current biology : CB. 21(12): p. 1070-1073. (group 2: Xavier Mesmin & Anaëlle Tanquerey-Cado)
Hayes J.E., Wallace M.R., Knopik V.S., Herbstman D.M., Bartoshuk L.M., and Duffy V.B. (2011) Allelic Variation in TAS2R Bitter Receptor Genes Associates with Variation in Sensations from and Ingestive Behaviors toward Common Bitter Beverages in Adults. Chemical Senses. 36(3): p. 311-319.
Kaun K.R., Azanchi R., Maung Z., Hirsh J., and Heberlein U. (2011) A Drosophila model for alcohol reward. Nature Neuroscience. 14(5): p. 612-U103.
Jiang P.H., Josue J., Li X., Glaser D., Li W.H., Brand J.G., . . . Beauchamp G.K. (2012) Major taste loss in carnivorous mammals. Proceedings of the National Academy of Sciences of the United States of America. 109(13): p. 4956-4961.
Milan N.F., Kacsoh B.Z., and Schlenke T.A. (2012) Alcohol Consumption as Self-Medication against Blood-Borne Parasites in the Fruit Fly. Current Biology. 22(6): p. 488-493.
Robinson Brooks G., Khurana S., Kuperman A., and Atkinson Nigel S. (2012) Neural Adaptation Leads to Cognitive Ethanol Dependence. Current Biology. 22(24): p. 2338-2341 (group 6: Victor Laratte & Simon Garret).
T. Agren, J. Engman, A. Frick, J. Bjorkstrand, E.-M. Larsson, T. Furmark, M. Fredrikson. Disruption of Reconsolidation Erases a Fear Memory Trace in the Human Amygdala. Science, 2012; 337 (6101): 1550 (group 3: Morgane Lélu & Mehdi Rakrouki)
Huang et al. Social Modulation during Songbird Courtship Potentiates Midbrain Dopaminergic Neurons. PLoS ONE, 2008; 3 (10): e3281 (group 1: Emilie Faure, Odile Piettre & Maud Thisse)
E. Jasarevic, P. T. Sieli, E. E. Twellman, T. H. Welsh, T. R. Schachtman, R. M. Roberts, D. C. Geary, C. S. Rosenfeld. Disruption of adult expression of sexually selected traits by developmental exposure to bisphenol A. Proceedings of the National Academy of Sciences, 2011; DOI: 10.1073/pnas.1107958108
Tomohiro Ishizu, Semir Zeki. Toward A Brain-Based Theory of Beauty. PLoS ONE, 2011; 6 (7): e21852 (group 11: Justine Barthod & Ariane Seitre)
Inbal Ben-Ami Bartal, Jean Decety, Peggy Mason. Empathy and Pro-Social Behavior in Rats. Science, 9 December 2011: Vol. 334 no. 6061 pp. 1427-1430 (group 7: Benjamin Debétencourt, Charlotte Morgant & Guillaume Oui)
Darby Proctor, Rebecca A. Williamson, Frans B. M. de Waal, and Sarah F. Brosnan. Chimpanzees play the ultimatum game. PNAS, January 14, 2013 (group 8: Zoé Beaumont, Pierre-Louis Choquet & Marie-Aude Natali)
Katharina Mahr, Matteo Griggio, Michela Granatiero and Herbert Hoi. Female attractiveness affects paternal investment: experimental evidence for male differential allocation in blue tits. Frontiers in Zoology, 2012 (group 10: Léonie Dusart, Coralie Ragueneau & Hélène Sundermann)
Suarez-Rodriguez M., Lopez-Rull I. & Macias Garcia C. (2012). Incorporation of cigarette butts into nests reduces nest ectoparasite load in urban birds: new ingredients for an old recipe?, Biology Letters, 9 (1) 931-931. (group 4: Paul Bertiaux & Elise Brilloux)
Amiel, Joshua J. & Shine, Richard (2012) Hotter nests produce smarter young lizards. Biology Letters: 8 (3) 372-374
--------------
Nociception is the detection of a noxious tissue-damaging stimulus and is sometimes accompanied by a reflex response such as withdrawal. Pain perception, as distinct from nociception, has been demonstrated in birds and mammals but has not been systematically studied in lower vertebrates. We assessed whether a fish possessed cutaneous nociceptors capable of detecting noxious stimuli and whether its behaviour was sufficiently adversely affected by the administration of a noxious stimulus. Electrophysiological recordings from trigeminal nerves identified polymodal nociceptors on the head of the trout with physiological properties similar to those described in higher vertebrates. These receptors responded to mechanical pressure, temperatures in the noxious range (more than 40 degreesC) and 1% acetic acid, a noxious substance. In higher vertebrates nociceptive nerves are either A-delta or C fibres with C fibres being the predominating fibre type. However, in the rainbow trout A-delta fibres were most common, and this offers insights into the evolution of nociceptive systems. Administration of noxious substances to the lips of the trout affected both the physiology and the behaviour of the animal and resulted in a significant increase in opercular beat rate and the time taken to resume feeding, as well as anomalous behaviours. This study provides significant evidence of nociception in telcost fishes and furthermore demonstrates that behaviour and physiology are affected over a prolonged period of time, suggesting discomfort.
Collective behavior based on self-organization has been shown in group-living animals from insects to vertebrates. These findings have stimulated engineers to investigate approaches for the coordination of autonomous multirobot systems based on self-organization. In this experimental study, we show collective decision-making by mixed groups of cockroaches and socially integrated autonomous robots, leading to shared shelter selection. Individuals, natural or artificial, are perceived as equivalent, and the collective decision emerges from nonlinear feedbacks based on local interactions. Even when in the minority, robots can modulate the collective decision-making process and produce a global pattern not observed in their absence. These results demonstrate the possibility of using intelligent autonomous devices to study and control self-organized behavioral patterns in group-living animals.
Many organisms use warning, or aposematic, coloration to signal their unprofitability to potential predators. Aposematically colored prey are highly visually conspicuous. There is considerable empirical support that conspicuousness promotes the effectiveness of the aposematic signal. From these experiments, it is well documented that conspicuous, unprofitable prey are detected sooner and aversion learned faster by the predator as compared with cryptic, unprofitable prey. Predators also retain memory of the aversion longer when prey is conspicuous. The present study focused on the elements of conspicuousness that confer these benefits of aposematic coloration. Drawing on current understanding of animal vision, we distinguish 2 features of warning coloration: high chromatic contrast and high brightness, or luminance, contrast. Previous investigations on aposematic signal efficacy have focused mainly on the role of high chromatic contrast between prey and background, whereas little research has investigated the role of high luminance contrast. Using the Chinese mantid as a model predator and gray-painted milkweed bugs as model prey, we found that increased prey luminance contrast increased detection of prey, facilitated predator aversion learning, and increased predator memory retention of the aversive response. Our results suggest that the luminance contrast component of aposematic coloration can be an effective warning signal between the prey and predator. Thus, warning coloration can even evolve as an effective signal to color blind predators.
Secretion of saliva to aid swallowing and digestion is an important physiological function found in many vertebrates and invertebrates. Pavlov reported classical conditioning of salivation in dogs a century ago. Conditioning of salivation, however, has been so far reported only in dogs and humans, and its underlying neural mechanisms remain elusive because of the complexity of the mammalian brain. We previously reported that, in cockroaches Periplaneta americana, salivary neurons that control salivation exhibited increased responses to an odor after conditioning trials in which the odor was paired with sucrose solution. However, no direct evidence of conditioning of salivation was obtained. In this study, we investigated the effects of conditioning trials on the level of salivation. Untrained cockroaches exhibited salivary responses to sucrose solution applied to the mouth but not to peppermint or vanilla odor applied to an antenna. After differential conditioning trials in which an odor was paired with sucrose solution and another odor was presented without pairing with sucrose solution, sucrose-associated odor induced an increase in the level of salivation, but the odor presented alone did not. The conditioning effect lasted for one day after conditioning trials. This study demonstrates, for the first time, classical conditioning of salivation in species other than dogs and humans, thereby providing the first evidence of sophisticated neural control of autonomic function in insects. The results provide a useful model system for studying cellular basis of conditioning of salivation in the simpler nervous system of insects.
The sense of taste, although a relatively undistinguished sensory modality in most mammals, is a highly developed sense in many fishes, e.g., catfish, gadids, and carps including goldfish. In these species, the amount of neural tissue devoted to this modality may approach 20% of the entire brain mass, reflecting an enormous number of taste buds scattered across the external surface of the animal as well as within the oral cavity. The primary sensory nuclei for taste form a longitudinal column of nuclei along the dorsomedial surface of the medulla. Within this column of gustatory nuclei, the sensory system is represented as a fine-grain somatotopic map, with external body parts being represented rostrally within the column, and oropharyngeal surfaces being represented caudally. Goldfish have a specialization of the oral cavity, the palatal organ, which enables them to sort food particles from particulate substrate material such as gravel. The palatal organ taste information reaches the large, vagal lobe with a complex laminar and columnar organization. This lobe also supports a radially-organized reflex system which activates the musculature of the palatal organ to effect the sorting operation. The stereotyped, laminated structure of this system in goldfish has facilitated studies of the circuitry and neurotransmitter systems underlying the goldfish’s ability to sort food from stones.
The brains of animals show chemical, anatomical, and functional differences, such as dopamine production and structure of sleep, between Amniota and older groups. In addition, play behavior, capacity to acquire taste aversion, sensory pleasure in decision making, and expression of emotional tachycardia and fever started also to be displayed by Amniota, suggesting that the brain may have began to work differently in early Amniota than in Lissamphibia and earlier vertebrates. Thus we propose that emotion, and more broadly speaking consciousness, emerged in the evolutionary line among the early Amniota. We also propose that consciousness is characterized by a common mental pathway that uses pleasure, or its counterpart displeasure, as a means to optimize behavior. (C) 2008 Elsevier B.V. All rights reserved.
Alcohol addiction is a common affliction with a strong genetic component [1]. Although mammalian studies have provided significant insight into the molecular mechanisms underlying ethanol consumption [2], other organisms such as Drosophila melanogaster are better suited for unbiased, forward genetic approaches to identify novel genes. Behavioral responses to ethanol, such as hyperactivity, sedation, and tolerance, are conserved between files and mammals [3, 4], as are the underlying molecular pathways [5-9]. However, few studies have investigated ethanol self-administration in flies [10]. Here we characterize ethanol consumption and preference in Drosophila. Files prefer to consume ethanol-containing food over regular food, and this preference increases over time. Files are attracted to the smell of ethanol, which partially mediates ethanol preference, but are averse to its taste. Preference for consuming ethanol is not entirely explained by attraction to either its sensory or caloric properties. We demonstrate that flies can exhibit features of alcohol addiction. First,flies self-administer ethanol to pharmacologically relevant concentrations. Second, flies will overcome an aversive stimulus in order to consume ethanol. Third, flies rapidly return to high levels of ethanol consumption after a period of imposed abstinence. Thus, ethanol preference in Drosophila provides a new model for studying aspects of addiction.
Organisms require information to make decisions about fitness-affecting resources, such as mates. Animals may extract "personal information" about potential mates by observing their physical characteristics or extract additional "public information" by observing their mating performance [1]. Mate copying by females [2-6] is a form of public information use that may reduce uncertainty about male quality, allowing more adaptive choices [2]. Experimental studies have produced evidence that female mate copying occurs in several species of fish [3], birds [5-7], and mammals [8], including humans [9]. We report the first evidence that a female invertebrate can exploit public information to select mates. In a first experiment, Drosophila melanogasterfemale prospectors increased their time in the attraction zones of poor-condition males, but not of good-condition males, after having observed them with a model female. This suggests that females appraised prospective mates by exploiting public information and did so mainly when it contrasted with personal information. In a second experiment, prospector females preferably mated with males of the color type they had previously observed copulating over males of the rejected color type, suggesting that female Drosophila can generalize socially learned information. The complexity of Drosophila decision-making suggests an unprecedented level of cognition in invertebrates. Our findings have implications for evolution given that socially learned mate preferences may lead to reproductive isolation, setting the stage for speciation [10].
Many prey species have evolved bitter-tasting toxins that effectively protect them from potential predators. While predators can learn to associate the taste of defended prey with the noxious effects of the toxins, it is unclear whether bitter tastes also function as deterrents. We explicitly tested the effectiveness of a nontoxic distasteful chemical as an antipredator defence. We gave four groups of European starlings, Sturnus vulgaris, a sequential colour discrimination task, where one colour signalled undefended mealworms, Tenebrio molitor, and the other signalled defended mealworms that had either been injected with or coated with either a high or a low concentration of Bitrex solution ( a nontoxic bitter-tasting solution). Birds ate all of the prey presented in this way, but performed disgust responses after eating prey coated in Bitrex solution. Birds were then given a series of trials in which they received defended and undefended prey items simultaneously. Birds that received prey injected with Bitrex attacked similar numbers of defended and undefended prey, whereas birds that received prey coated in Bitrex ate significantly fewer defended than undefended prey. Birds given prey coated in a high concentration of Bitrex showed a stronger preference for undefended prey than birds given prey coated in a low concentration of Bitrex. Our experiment demonstrates that a nontoxic distasteful chemical can protect insect prey from predation, but only under very specific conditions. (C) 2009 The Association for the Study of Animal Behaviour. Published by Elsevier Ltd. All rights reserved.
Human epidemiologic studies reveal that fetal ethanol exposure is highly predictive of adolescent ethanol avidity and abuse. Little is known about how fetal exposure produces these effects. It is hypothesized that fetal ethanol exposure results in stimulus-induced chemosensory plasticity. Here, we asked whether gestational ethanol exposure increases postnatal ethanol avidity in rats by altering its taste and odor. Experimental rats were exposed to ethanol in utero via the dam's diet, whereas control rats were either pair-fed an iso-caloric diet or given food ad libitum. We found that fetal ethanol exposure increased the taste-mediated acceptability of both ethanol and quinine hydrochloride (bitter), but not sucrose (sweet). Importantly, a significant proportion of the increased ethanol acceptability could be attributed directly to the attenuated aversion to ethanol's quinine-like taste quality. Fetal ethanol exposure also enhanced ethanol intake and the behavioral response to ethanol odor. Notably, the elevated intake of ethanol was also causally linked to the enhanced odor response. Our results demonstrate that fetal exposure specifically increases ethanol avidity by, in part, making it taste and smell better. More generally, they establish an epigenetic chemosensory mechanism by which maternal patterns of drug use can be transferred to offspring. Given that many licit (e.g., tobacco products) and illicit (e.g., marijuana) drugs have noteworthy chemosensory components, our findings have broad implications for the relationship between maternal patterns of drug use, child development, and postnatal vulnerability.
Whether animals experience human-like emotions is controversial and of immense societal concern [1 3]. Because animals cannot provide subjective reports of how they feel, emotional state can only be inferred using physiological, cognitive, and behavioral measures [4 8]. In humans, negative feelings are reliably correlated with pessimistic cognitive biases, defined as the increased expectation of bad outcomes [9 11]. Recently, mammals [12 16] and birds [17 20] with poor welfare have also been found to display pessimistic-like decision making, but cognitive biases have not thus far been explored in invertebrates. Here, we ask whether honeybees display a pessimistic cognitive bias when they are subjected to an anxiety-like state induced by vigorous shaking designed to simulate a predatory attack. We show for the first time that agitated bees are more likely to classify ambiguous stimuli as predicting punishment. Shaken bees also have lower levels of hemolymph dopamine, octopamine, and serotonin. In demonstrating state-dependent modulation of categorization in bees, and thereby a cognitive component of emotion, we show that the bees' response to a negatively valenced event has more in common with that of vertebrates than previously thought. This finding reinforces the use of cognitive bias as a measure of negative emotional states across species and suggests that honeybees could be regarded as exhibiting emotions. º Agitated honeybees display an increased expectation of bad outcomes º Hemolymph levels of dopamine, octopamine, and serotonin are reduced in agitated bees º Honeybees exhibit a vertebrate-like emotional state
Food contains complex blends of structurally diverse bitter compounds that trigger bitterness through activation of one or more of the similar to 25 human TAS2 bitter taste receptors. It remains unsolved, however, whether the perceived bitterness of binary bitter-compound mixtures can be considered an additive function of all bitter-inducing chemicals in the mouth, suggesting that little mutual interaction takes place among bitter substances or if mixture suppression and synergism occurs. Here we report on two natural sesquiterpene lactones from edible plants, which stimulate distinct sets of hTAS2Rs in transfected cells. Both chemicals also robustly inhibit different but overlapping subsets of agonist-activated hTAS2Rs. These findings demonstrate that mixtures of bitter compounds, because they normally occur in human foodstuff, likely elicit bitter perception in a complex and not in a merely additive manner. An unexpected implication of this discovery is that, during evolution, the naturally occurring bitter taste receptor antagonists have shaped some of the pharmacological properties of the receptors, such as overlapping recognition profiles and breadth of tuning.
Living organisms need to search for and ingest nutritional chemicals, and gustation plays a major role in detecting and discriminating between chemicals present in the environment. Using Drosophila as a model organism, we asked whether animals have the ability to evaluate the nutritional value of sugars. In flies, chemosensilla on the tarsi and labellum are the gustatory organs used to discriminate between edible and nonedible compounds [1, 2]. We noticed that Drosophila do not assign nutritional values to all sweet chemicals. D-arabinose is sweet to flies, but it provides them with no nutrition. By contrast, the sugar alcohol D-sorbitol is not sensed as sweet, but flies can live on it. We performed behavioral and electrophysiological measurements to confirm these gustatory and feeding responses. We found that Drosophila can learn the nutritional value of nonsweet D-sorbitol when it is associated with an odor cue. The learning process involved the synapsin molecule, suggesting that a neuronal mechanism is involved. We propose that Drosophila uses neural machinery to detect, evaluate, and learn the nutritional value of foods after ingestion.
The ability to respond to chemical stimuli is fundamental to the survival of motile organisms, but the strategies underlying odour tracking remain poorly understood. Here we show that chemotaxis in Drosophila melanogaster larvae is an active sampling process analogous to sniffing in vertebrates. Combining computer-vision algorithms with reconstructed olfactory environments, we establish that larvae orient in odour gradients through a sequential organization of stereotypical behaviours, including runs, stops, lateral head casts and directed turns. Negative gradients, integrated during runs, control the timing of turns. Positive gradients detected through high-amplitude head casts determine the direction of individual turns. By genetically manipulating the peripheral olfactory circuit, we examine how orientation adapts to losses and gains of function in olfactory input. Our findings suggest that larval chemotaxis represents an intermediate navigation strategy between the biased random walks of Escherichia Coli and the stereo-olfaction observed in rats and humans.
The 25 human bitter receptors and their respective genes (TAS2Rs) contain unusually high levels of allelic variation, which may influence response to bitter compounds in the food supply. Phenotypes based on the perceived bitterness of single bitter compounds were first linked to food preference over 50 years ago. The most studied phenotype is propylthiouracil bitterness, which is mediated primarily by the TAS2R38 gene and possibly others. In a laboratory-based study, we tested for associations between TAS2R variants and sensations, liking, or intake of bitter beverages among healthy adults who were primarily of European ancestry. A haploblock across TAS2R3, TAS2R4, and TAS2R5 explained some variability in the bitterness of espresso coffee. For grapefruit juice, variation at a TAS2R19 single nucleotide polymorphism (SNP) was associated with increased bitterness and decreased liking. An association between a TAS2R16 SNP and alcohol intake was identified, and the putative TAS2R38-alcohol relationship was confirmed, although these polymorphisms did not explain sensory or hedonic responses to sampled scotch whisky. In summary, TAS2R polymorphisms appear to influence the sensations, liking, or intake of common and nutritionally significant beverages. Studying perceptual and behavioral differences in vivo using real foods and beverages may potentially identify polymorphisms related to dietary behavior even in the absence of known ligands.
The rewarding properties of drugs contribute to the development of abuse and addiction. We developed a new assay for investigating the motivational properties of ethanol in the genetically tractable model Drosophila melanogaster. Flies learned to associate cues with ethanol intoxication and, although transiently aversive, the experience led to a long-lasting attraction for the ethanol-paired cue, implying that intoxication is rewarding. Temporally blocking transmission in dopaminergic neurons revealed that flies require activation of these neurons to express, but not develop, conditioned preference for ethanol-associated cues. Moreover, flies acquired, consolidated and retrieved these rewarding memories using distinct sets of neurons in the mushroom body. Finally, mutations in scabrous, encoding a fibrinogen-related peptide that regulates Notch signaling, disrupted the formation of memories for ethanol reward. Our results thus establish that Drosophila can be useful for understanding the molecular, genetic and neural mechanisms underling the rewarding properties of ethanol.
In 1991, Woods described the paradoxical nature of eating, specifically, that it produced aversive and negative effects. He noted in this analysis the multiple physiological and behavior adaptations, both learned and unlearned, that were aimed at regulating food intake and reducing its aversive, disruptive effects. From this position, he argued that consumption reflected a balance of the positive and aversive effects of eating. The present review extends this analysis to drug use and abuse, i.e., that drug taking itself also is a balance of reward and aversion. Although traditionally the analysis of drug use and abuse has focused on a drug's positive and negative rewarding effects, the present review highlights the aversive effects of these same drugs, e.g., cocaine, morphine, alcohol, and describes such effects as protective in nature. This balance and the manner by which it can be impacted by subject and experiential factors are described with a focus on genetic models of drug abuse using the Lewis and Fischer inbred rat strains. (C) 2010 Elsevier Inc. All rights reserved.
Glucose is a universal phagostimulant in many animal species, including the cockroach Blattella germanica. However, some natural populations of B. germanica have been found that are behaviorally deterred from eating glucose. In dose-response studies, glucose was a powerful phagostimulant for wild-type cockroaches, but it strongly deterred feeding in a glucose-averse strain. Both strains, however, exhibited identical dose-response curves to other phagostimulants and deterrents. As a lead to electrophysiological and molecular genetics studies to investigate the mechanisms that underlie glucose-aversion, we used 2 assay paradigms to delineate which chemosensory appendages on the head contribute to the reception of various phagostimulatory and deterrent chemicals. Both simultaneous dual stimulation of the antenna and mouthparts of the insects and 2-choice preference tests in surgically manipulated insects showed that the glucose-averse behavior could be elicited through the gustatory systems of the antennae and mouthparts. The paraglossae alone were sufficient for maximum sensitivity to both phagostimulants and deterrents, including glucose as a deterrent in the glucose-averse strain. In addition to the paraglossae, the labial palps were more important than the maxillary palps in the reception of deterrents (caffeine in both strains and glucose in the glucose-averse strain). The maxillary palps, on the other hand, played a more important role in the reception of phagostimulants (fructose in both strains and glucose in the wild-type strain). Our results suggest that distinct inputs from the chemosensory system mediate opposite feeding responses to glucose in the wild-type and glucose-averse strains.
Scent communication plays a central role in the mating behavior of many nonhuman mammals but has often been overlooked in the study of human mating. However, a growing body of evidence suggests that men may perceive women's high-fertility body scents (collected near ovulation) as more attractive than their low-fertility body scents. The present study provides a methodologically rigorous replication of this finding, while also examining several novel questions. Women collected samples of their natural body scent twice once on a low-fertility day and once on a high-fertility day of the ovulatory cycle. Tests of luteinizing hormone confirmed that women experienced ovulation within two days of their high-fertility session. Men smelled each woman's high- and low-fertility scent samples and completed discrimination and preference tasks. At above-chance levels, men accurately discriminated between women's high- and low-fertility scent samples (61%) and chose women's high-fertility scent samples as more attractive than their low-fertility scent samples (56%). Men also rated each scent sample on sexiness, pleasantness, and intensity, and estimated the physical attractiveness of the woman who had provided the sample. Multilevel modeling revealed that, when high- and low-fertility scent samples were easier to discriminate from each other, high-fertility scent samples received even more favorable ratings compared with low-fertility scent samples. This study builds on a growing body of evidence indicating that men are attracted to cues of impending ovulation in women and raises the intriguing question of whether women's cycling hormones influence men's attraction and sexual approach behavior.
Jiang, P. H., J. Josue, X. Li, D. Glaser, W. H. Li, J. G. Brand, . . . G. K. Beauchamp (2012). "Major taste loss in carnivorous mammals." Proceedings of the National Academy of Sciences of the United States of America 109(13): 4956-4961. [pdf]
Mammalian sweet taste is primarily mediated by the type 1 taste receptor Tas1r2/Tas1r3, whereas Tas1r1/Tas1r3 act as the principal umami taste receptor. Bitter taste is mediated by a different group of G protein-coupled receptors, the Tas2rs, numbering 3 to similar to 66, depending on the species. We showed previously that the behavioral indifference of cats toward sweet-tasting compounds can be explained by the pseudogenization of the Tas1r2 gene, which encodes the Tas1r2 receptor. To examine the generality of this finding, we sequenced the entire coding region of Tas1r2 from 12 species in the order Carnivora. Seven of these nonfeline species, all of which are exclusive meat eaters, also have independently pseudogenized Tas1r2 caused by ORF-disrupting mutations. Fittingly, the purifying selection pressure is markedly relaxed in these species with a pseudogenized Tas1r2. In behavioral tests, the Asian otter (defective Tas1r2) showed no preference for sweet compounds, but the spectacled bear (intact Tas1r2) did. In addition to the inactivation of Tas1r2, we found that sea lion Tas1r1 and Tas1r3 are also pseudogenized, consistent with their unique feeding behavior, which entails swallowing food whole without chewing. The extensive loss of Tas1r receptor function is not restricted to the sea lion: the bottlenose dolphin, which evolved independently from the sea lion but displays similar feeding behavior, also has all three Tas1rs inactivated, and may also lack functional bitter receptors. These data provide strong support for the view that loss of taste receptor function in mammals is widespread and directly related to feeding specializations.
In contrast to other apes, humans have relatively greater amounts of armpit hair, which is thought to retain signaling molecules. Although armpit shaving is widespread cross-culturally, its effect on body odor has been little investigated. In four experiments, we tested the effect of shaving and the subsequent regrowth of axillary hair. Armpit odors were collected from men who regularly shaved (group S) or who had never shaved (group N) their armpits before. The samples were subsequently rated by women for intensity, pleasantness, and attractiveness. In Experiments I, II (group N) and III, subjects firstly shaved one armpit and then let the hair regrow over 6 or 10 weeks. In Experiments I, II (group S) and IV, subjects shaved both armpits before the sampling and subsequently shaved one armpit during the same period, leaving the second armpit unshaved. Odors of the shaved armpits were rated more pleasant, attractive, and less intense compared to the unshaved armpits (Experiment I (group N)). However, no significant differences found in Experiments II and III (group N) suggest the effect of shaving is relatively minor. Moreover, there were no significant differences in odor comparing unshaved armpits with armpits after 1 week of regrowth (Experiments I, II (group N) and III) or comparing regularly shaved armpits with armpits after 1 or 3 weeks of regrowth (Experiments I, II (group S) and IV). The odor of shaved armpits was rated significantly more attractive compared to the armpits where hair had been regrowing for 6 or 10 weeks.
Context-dependent discrimination learning, a sophisticated form of nonelemental associative learning, has been found in many animals, including insects. The major purpose of this research is to establish a method for monitoring this form of nonelemental learning in rigidly restrained insects for investigation of underlying neural mechanisms. We report context-dependent olfactory learning (occasion-setting problem solving) of salivation, which can be monitored as activity changes of salivary neurons in immobilized cockroaches, Periplaneta americana. A group of cockroaches was trained to associate peppermint odor (conditioned stimulus, CS) with sucrose solution reward (unconditioned stimulus, US) while vanilla odor was presented alone without pairing with the US under a flickering light condition (1.0 Hz) and also trained to associate vanilla odor with sucrose reward while peppermint odor was presented alone under a steady light condition. After training, the responses of salivary neurons to the rewarded peppermint odor were significantly greater than those to the unrewarded vanilla odor under steady illumination and those to the rewarded vanilla odor was significantly greater than those to the unrewarded peppermint odor in the presence of flickering light. Similar context-dependent responses were observed in another group of cockroaches trained with the opposite stimulus arrangement. This study demonstrates context-dependent olfactory learning of salivation for the first time in any vertebrate and invertebrate species, which can be monitored by activity changes of salivary neurons in restrained cockroaches.
Plants and fungi often produce toxic secondary metabolites that limit their consumption [1-4], but herbivores and fungi-vores that evolve resistance gain access to these resources and can also gain protection against nonresistant predators and parasites [3, 5-8]. Given that Drosophila melanogaster fruit fly larvae consume yeasts growing on rotting fruit and have evolved resistance to fermentation products [9, 10], we decided to test whether alcohol protects flies from one of their common natural parasites, endoparasitoid wasps [11-13]. Here, we show that exposure to ethanol reduces wasp oviposition into fruit fly larvae. Furthermore, if infected, ethanol consumption by fruit fly larvae causes increased death of wasp larvae growing in the hemocoel and increased fly survival without need of the stereotypical antiwasp immune response. This multifaceted protection afforded to fly larvae by ethanol is significantly more effective against a generalist wasp than a wasp that specializes on D. melanogaster. Finally, fly larvae seek out ethanol-containing food when infected, indicating that they use alcohol as an antiwasp medicine. Although the high resistance of D. melanogaster may make it uniquely suited to exploit curative properties of alcohol, it is possible that alcohol consumption may have similar protective effects in other organisms.
Physiological alcohol dependence is a key adaptation to chronic ethanol consumption that underlies withdrawal symptoms, is thought to directly contribute to alcohol addiction behaviors, and is associated with cognitive problems such as deficits in learning and memory [1 3]. Based on the idea that an ethanol-adapted (dependent) animal will perform better in a learning assay than an animal experiencing ethanol withdrawal will, we have used a learning paradigm to detect physiological ethanol dependence in Drosophila. Moderate ethanol consumption initially degrades the capacity of larvae to learn, but they eventually adapt and are able to learn as well as ethanol-naive animals. However, withholding ethanol from ethanol-adapted larvae impairs learning. Ethanol reinstatement restores the capacity to learn, thus demonstrating cognitive dependence on ethanol. The larval nervous system also shows ethanol-withdrawal hyperexcitability. Larvae reach ethanol concentrations equivalent to 0.05 to 0.08 blood-alcohol concentration levels that would be mildly intoxicating in humans. These ethanol-induced changes in learning are not the product of sensory deficits or state-dependent learning. This is the first demonstration of cognitive ethanol dependence in an invertebrate genetic model system. º Acute ethanol exposure impairs learning in Drosophila larvae º Prolonged ethanol consumption results in cognitive dependence on ethanol º Dependent larvae learn at a normal level only when ethanol is present.
Sweet-tasting compounds are recognized by a heterodimeric receptor composed of the taste receptor, type 1, members 2 (T1R2) and 3 (T1R3) located in the mouth. This receptor is also expressed in the gut where it is involved in intestinal absorption, metabolic regulation, and glucose homeostasis. These metabolic functions make the sweet taste receptor a potential novel therapeutic target for the treatment of obesity and related metabolic dysfunctions such as diabetes. Existing sweet taste inhibitors or blockers that are still in development would constitute promising therapeutic agents. In this review, we will summarize the current knowledge of sweet taste inhibitors, including a sweet-taste-suppressing protein named gurmarin, which is only active on rodent sweet taste receptors but not on that of humans. In addition, their potential applications as therapeutic tools are discussed.
Tracking distant odor sources is crucial to foraging, courtship and reproductive success for many animals including fish, flies and birds. Upon encountering a chemical plume in flight, Drosophila melanogaster integrates the spatial intensity gradient and temporal fluctuations over the two antennae, while simultaneously reducing the amplitude and frequency of rapid steering maneuvers, stabilizing the flight vector. There are infinite escape vectors away from a noxious source, in contrast to a single best tracking vector towards an attractive source. Attractive and aversive odors are segregated into parallel neuronal pathways in flies; therefore, the behavioral algorithms for avoidance may be categorically different from tracking. Do flies plot random ballistic or otherwise variable escape vectors? Or do they instead make use of temporally dynamic mechanisms for continuously and directly avoiding noxious odors in a manner similar to tracking appetitive ones? We examine this question using a magnetic tether flight simulator that permits free yaw movements, such that flies can actively orient within spatially defined odor plumes. We show that in-flight aversive flight behavior shares all of the key features of attraction such that flies continuously 'anti-track' the noxious source.
In vision, two mixtures, each containing an independent set of many different wavelengths, may produce a common color percept termed "white." In audition, two mixtures, each containing an independent set of many different frequencies, may produce a common perceptual hum termed "white noise." Visual and auditory whites emerge upon two conditions: when the mixture components span stimulus space, and when they are of equal intensity. We hypothesized that if we apply these same conditions to odorant mixtures, "whiteness" may emerge in olfaction as well. We selected 86 molecules that span olfactory stimulus space and individually diluted them to a point of about equal intensity. We then prepared various odorant mixtures, each containing various numbers of molecular components, and asked human participants to rate the perceptual similarity of such mixture pairs. We found that as we increased the number of nonoverlapping, equal-intensity components in odorant mixtures, the mixtures became more similar to each other, despite not having a single component in common. With similar to 30 components, most mixtures smelled alike. After participants were acquainted with a novel, arbitrarily named mixture of similar to 30 equal-intensity components, they later applied this name more readily to other novel mixtures of similar to 30 equal-intensity components spanning stimulus space, but not to mixtures containing fewer components or to mixtures that did not span stimulus space. We conclude that a common olfactory percept, "olfactory white," is associated with mixtures of similar to 30 or more equal-intensity components that span stimulus space, implying that olfactory representations are of features of molecules rather than of molecular identity.
The domestication of dogs was an important episode in the development of human civilization. The precise timing and location of this event is debated and little is known about the genetic changes that accompanied the transformation of ancient wolves into domestic dogs. Here we conduct whole-genome resequencing of dogs and wolves to identify 3.8 million genetic variants used to identify 36 genomic regions that probably represent targets for selection during dog domestication. Nineteen of these regions contain genes important in brain function, eight of which belong to nervous system development pathways and potentially underlie behavioural changes central to dog domestication6. Ten genes with key roles in starch digestion and fat metabolism also show signals of selection. We identify candidate mutations in key genes and provide functional support for an increased starch digestion in dogs relative to wolves. Our results indicate that novel adaptations allowing the early ancestors of modern dogs to thrive on a diet rich in starch, relative to the carnivorous diet of wolves, constituted a crucial step in the early domestication of dogs.
When the moon is absent from the night sky, stars remain as celestial visual cues. Nonetheless, only birds [1, 2], seals [3], and humans [4] are known to use stars for orientation. African ball-rolling dung beetles exploit the sun, the moon, and the celestial polarization pattern to move along straight paths, away from the intense competition at the dung pile [5 9]. Even on clear moonless nights, many beetles still manage to orientate along straight paths [5]. This led us to hypothesize that dung beetles exploit the starry sky for orientation, a feat that has, to our knowledge, never been demonstrated in an insect. Here, we show that dung beetles transport their dung balls along straight paths under a starlit sky but lose this ability under overcast conditions. In a planetarium, the beetles orientate equally well when rolling under a full starlit sky as when only the Milky Way is present. The use of this bidirectional celestial cue for orientation has been proposed for vertebrates [10], spiders [11], and insects [5, 12], but never proven. This finding represents the first convincing demonstration for the use of the starry sky for orientation in insects and provides the first documented use of the Milky Way for orientation in the animal kingdom. º African dung beetles orient to the starry sky to move along straight paths º The beetles do not orientate to the individual stars, but to the Milky Way.
Many species defend themselves against enemies using repellent chemicals. An important but unanswered question is why investment in chemical defence is often variable within prey populations. One explanation is that some prey benefit by cheating, paying no costs of defence, but gaining a reduced attack rate because of the presence of defended conspecifics. Two important assumptions about predator behaviour must be met to explain cheating as a stable strategy: first, predators increase attack rates as cheats increase in frequency; second, defended prey survive attacks better than non-defended conspecifics. We lack data from wild predators that evaluate these hypotheses. Here, we examine how changes in the frequency of non-defended cheats affect predation by wild birds on a group of otherwise defended prey. We presented mealworm larvae that were either edible (cheats) or unpalatable (bitter tasting), and varied the proportion of cheats from 0 to 1 by increments of 0.25. We found strong frequency-dependent effects on the birds' foraging behaviour, with the proportion of prey attacked increasing nonlinearly with the frequency of cheats. We did not, however, observe that birds taste-rejected defended prey at the site of capture. One explanation is that wild birds may not assess prey palatability at the site of capture, but do this elsewhere. If so, defended and undefended prey may pay high costs of initial attack and relocation away from ecologically favourable locations. Alternatively, defended prey may not be taste-rejected because with acute time constraints, wild birds do not have time to make fine-grained decisions during feeding. We discuss the data in relation to the evolutionary ecology of prey defences.
Mammalian spermatogenesis and sperm maturation are susceptible to the effects of internal and external factors. However, how male germ cells interact with and respond to these elements including those potentially toxic substances is poorly understood. Here, we show that many bitter-taste receptors (T2rs), which are believed to function as gatekeepers in the oral cavity to detect and innately prevent the ingestion of poisonous bitter-tasting compounds, are expressed in mouse seminiferous tubules. Our in situ hybridization results indicate that Tas2r transcripts are expressed postmeiotically. Functional analysis showed that mouse spermatids and spermatozoa responded to both naturally occurring and synthetic bitter-tasting compounds by increasing intracellular free calcium concentrations, and individual male germ cells exhibited different ligand-activation profiles, indicating that each cell may express a unique subset of T2r receptors. These calcium responses could be suppressed by a specific bitter-tastant blocker or abolished by the knockout of the gene for the G protein subunit -gustducin. Taken together, our data strongly suggest that male germ cells, like taste bud cells in the oral cavity and solitary chemosensory cells in the airway, utilize T2r receptors to sense chemicals in the milieu that may affect sperm behavior and fertilization.
Memories become labile when recalled. In humans and rodents alike, reactivated fear memories can be attenuated by disrupting reconsolidation with extinction training. Using functional brain imaging, we found that, after a conditioned fear memory was formed, reactivation and reconsolidation left a memory trace in the basolateral amygdala that predicted subsequent fear expression and was tightly coupled to activity in the fear circuit of the brain. In contrast, reactivation followed by disrupted reconsolidation suppressed fear, abolished the memory trace, and attenuated fear-circuit connectivity. Thus, as previously demonstrated in rodents, fear memory suppression resulting from behavioral disruption of reconsolidation is amygdala-dependent also in humans, which supports an evolutionarily conserved memory-update mechanism.
Synaptic transmission onto dopaminergic neurons of the mammalian ventral tegmental area (VTA) can be potentiated by acute or chronic exposure to addictive drugs. Because rewarding behavior, such as social affiliation, can activate the same neural circuitry as addictive drugs, we tested whether the intense social interaction of songbird courtship may also potentiate VTA synaptic function. We recorded glutamatergic synaptic currents from VTA of male zebra finches who had experienced distinct social and behavioral conditions during the previous hour. The level of synaptic transmission to VTA neurons, as assayed by the ratio of a-amino-3-hydroxy-5-methyl-4-isoxazolepropionic acid (AMPA) to N-methyl-D-aspartic acid (NMDA) glutamate receptor mediated synaptic currents, was increased after males sang to females, and also after they saw females without singing, but not after they sang while alone. Potentiation after female exposure alone did not appear to result from stress, as it was not blocked by inhibition of glucocorticoid receptors. This potentiation was restricted to synapses of dopaminergic projection neurons, and appeared to be expressed postsynaptically. This study supports a model in which VTA dopaminergic neurons are more strongly activated during singing used for courtship than during noncourtship singing, and thus can provide social context-dependent modulation to forebrain areas. More generally, these results demonstrate that an intense social encounter can trigger the same pathways of neuronal plasticity as addictive drugs.
Exposure to endocrine disrupting compounds (EDCs), such as bisphenol A (BPA), may cause adverse health effects in wildlife and humans, but controversy remains as to what traits are most sensitive to EDCs and might serve as barometers of exposure. Expression of sexually selected traits that have evolved through intrasexual competition for mates and intersexual choice of mating partner are more dependent on developmental and physical condition of an animal than naturally selected traits and thus might be particularly vulnerable to disruption by developmental exposure to EDCs. We have used the deer mouse (Peromyscus maniculatus) as a model to test this hypothesis. Adult male–male competition for mates in this species is supported by enhanced spatial navigational and exploratory abilities, which enable males to search for prospective, widely dispersed females. Male deer mice exposed to BPA or ethinyl estradiol (EE) through maternal diet showed no changes in external phenotype, sensory development, or adult circulating concentrations of testosterone and corticosterone, but spatial learning abilities and exploratory behaviors were severely compromised compared with control males. Because these traits are not sexually selected in females, BPA exposure predictably had no effect, although EE-exposed females demonstrated enhanced spatial navigational abilities. Both BPA-exposed and control females preferred control males to BPA-exposed males. Our demonstration that developmental exposure to BPA compromises cognitive abilities and behaviors essential for males to reproduce successfully has broad implications for other species, including our own. Thus, sexually selected traits might provide useful biomarkers to assess risk of environmental contamination in animal and human populations.
We wanted to learn whether activity in the same area(s) of the brain correlate with the experience of beauty derived from different sources. 21 subjects took part in a brain-scanning experiment using functional magnetic resonance imaging. Prior to the experiment, they viewed pictures of paintings and listened to musical excerpts, both of which they rated on a scale of 1–9, with 9 being the most beautiful. This allowed us to select three sets of stimuli–beautiful, indifferent and ugly–which subjects viewed and heard in the scanner, and rated at the end of each presentation. The results of a conjunction analysis of brain activity showed that, of the several areas that were active with each type of stimulus, only one cortical area, located in the medial orbito-frontal cortex (mOFC), was active during the experience of musical and visual beauty, with the activity produced by the experience of beauty derived from either source overlapping almost completely within it. The strength of activation in this part of the mOFC was proportional to the strength of the declared intensity of the experience of beauty. We conclude that, as far as activity in the brain is concerned, there is a faculty of beauty that is not dependent on the modality through which it is conveyed but which can be activated by at least two sources–musical and visual–and probably by other sources as well. This has led us to formulate a brain-based theory of beauty.
Whereas human pro-social behavior is often driven by empathic concern for another, it is unclear whether nonprimate mammals experience a similar motivational state. To test for empathically motivated pro-social behavior in rodents, we placed a free rat in an arena with a cagemate trapped in a restrainer. After several sessions, the free rat learned to intentionally and quickly open the restrainer and free the cagemate. Rats did not open empty or object-containing restrainers. They freed cagemates even when social contact was prevented. When liberating a cagemate was pitted against chocolate contained within a second restrainer, rats opened both restrainers and typically shared the chocolate. Thus, rats behave pro-socially in response to a conspecific’s distress, providing strong evidence for biological roots of empathically motivated helping behavior.
A hatchling reptile’s sex, body size and shape, and locomotor performance can be influenced not only by its genes, but also by the temperature that it experiences during incubation. Can incubation temperature also affect a hatchling’s cognitive skills? In the scincid lizard Bassiana duperreyi, higher incubation temperatures enhanced the resultant hatchling’s learning performance. Hence, factors such asmaternal nest-site selection and climate change affect not only the size, shape and athletic abilities of hatchling reptiles, but also their ability to learn novel tasks.
Is the sense of fairness uniquely human? Human reactions to reward division are often studied by means of the ultimatum game, in which both partners need to agree on a distribution for both to receive rewards. Humans typically offer generous portions of the reward to their partner, a tendency our close primate relatives have thus far failed to show in experiments. Here we tested chimpanzees (Pan troglodytes) and human children on a modified ultimatum game. One individual chose between two tokens that, with their partner’s cooperation, could be exchanged for rewards. One token offered equal rewards to both players, whereas the other token favored the chooser. Both apes and children responded like humans typically do. If their partner’s cooperation was required, they split the rewards equally. However, with passive partners—a situation akin to the so-called dictator game—they preferred the selfish option. Thus, humans and chimpanzees show similar preferences regarding reward division, suggesting a long evolutionary history to the human sense of fairness.
Introduction: The differential allocation hypothesis (DAH) predicts that individuals should adjust their parental investment to their current mate’s quality. Although in principle the DAH holds for both sexes, male adjustment of parental investment has only been tested in a few experimental studies, revealing contradictory results. We conducted a field experiment to test whether male blue tits (Cyanistes caeruleus) allocate their parental effort in relation to female ornamentation (ultraviolet colouration of the crown), as predicted by the DAH. Results: We reduced the UV reflectance in a sample of females and compared parental care by their mates with that of males paired to sham-manipulated control females. As predicted by the DAH our results demonstrate that males paired with UV-reduced females invested less in feeding effort but did not defend the chicks less than males paired with control females. Conclusions: To our knowledge, this is one of the first studies providing support for male differential allocation in response to female ornamentation.
Birds are known to respond to nest-dwelling parasites by altering behaviours. Some bird species, for example, bring fresh plants to the nest, which contain volatile compounds that repel parasites. There is evidence that some birds living in cities incorporate cigarette butts into their nests, but the effect (if any) of this behaviour remains unclear. Butts from smoked cigarettes retain substantial amounts of nicotine and other compounds that may also act as arthropod repellents. We provide the first evidence that smoked cigarette butts may function as a parasite repellent in urban bird nests. The amount of cellulose acetate from butts in nests of two widely distributed urban birds was negatively associated with the number of nest-dwelling parasites. Moreover, when parasites were attracted to heat traps containing smoked or non-smoked cigarette butts, fewer parasites reached the former, presumably due to the presence of nicotine. Because urbanization changes the abundance and type of resources upon which birds depend, including nesting materials and plants involved in self-medication, our results are consistent with the view that urbanization imposes new challenges on birds that are dealt with using adaptations evolved elsewhere. 1.