Pheromonal and behavioral cues trigger male-to-female aggression in Drosophila

Appropriate displays of aggression rely on the ability to recognize potential competitors. As in most species, Drosophila males fight with other males and do not attack females. In insects, sex recognition is strongly dependent on chemosensory communication, mediated by cuticular hydrocarbons acting as pheromones. While the roles of chemical and other sensory cues in stimulating male to female courtship have been well characterized in Drosophila, the signals that elicit aggression remain unclear. Here we show that when female pheromones or behavior are masculinized, males recognize females as competitors and switch from courtship to aggression. To masculinize female pheromones, a transgene carrying dsRNA for the sex determination factor transformer (traIR) was targeted to the pheromone producing cells, the oenocytes. Shortly after copulation males attacked these females, indicating that pheromonal cues can override other sensory cues. Surprisingly, masculinization of female behavior by targeting traIR to the nervous system in an otherwise normal female also was sufficient to trigger male aggression. Simultaneous masculinization of both pheromones and behavior induced a complete switch in the normal male response to a female. Control males now fought rather than copulated with these females. In a reciprocal experiment, feminization of the oenocytes and nervous system in males by expression of transformer (traF) elicited high levels of courtship and little or no aggression from control males. Finally, when confronted with flies devoid of pheromones, control males attacked male but not female opponents, suggesting that aggression is not a default behavior in the absence of pheromonal cues. Thus, our results show that masculinization of either pheromones or behavior in females is sufficient to trigger male-to-female aggression. Moreover, by manipulating both the pheromonal profile and the fighting patterns displayed by the opponent, male behavioral responses towards males and females can be completely reversed. Therefore, both pheromonal and behavioral cues are used by Drosophila males in recognizing a conspecific as a competitor.     

DNA analysis on fox faeces and competition induced niche shifts

Interference competition can force inferior competitors to change their distribution patterns. It is, however, possible that the dominant competitor poses a higher threat during certain times of the year, for example during reproduction. In such cases, the inferior competitor is expected to change its distribution accordingly. We used a molecular species identification method on faeces to investigate how the spatial overlap between arctic and red foxes changes between seasons. The results show that arctic and red foxes are sympatric during winter, but allopatric in summer as arctic foxes retreat to higher altitudes further from the tree-line during the breeding season.     

Reproductive interference explains persistence of aggression between species

Interspecific territoriality occurs when individuals of different species fight over space, and may arise spontaneously when populations of closely related territorial species first come into contact. But defence of space is costly, and unless the benefits of excluding heterospecifics exceed the costs, natural selection should favour divergence in competitor recognition until the species no longer interact aggressively. Ordinarily males of different species do not compete for mates, but when males cannot distinguish females of sympatric species, females may effectively become a shared resource. We model how reproductive interference caused by undiscriminating males can prevent interspecific divergence, or even cause convergence, in traits used to recognize competitors. We then test the model in a genus of visually orienting insects and show that, as predicted by the model, differences between species pairs in the level of reproductive interference, which is causally related to species differences in female coloration, are strongly predictive of the current level of interspecific aggression. Interspecific reproductive interference is very common and we discuss how it may account for the persistence of interspecific aggression in many taxonomic groups.     

Lack of species discrimination based on chemical cues by male sailfin mollies, <Emphasis Type="Italic">Poecilia latipinna</Emphasis>

When making mating decisions, individuals may rely on multiple cues from either the same or multiple sensory modalities. Although the use of visual cues in sexual selection is well studied, fewer studies have examined the role of chemical cues in mate choice. In addition, few studies have examined how visual and/or chemical cues affect male mating decisions. Male mate choice is important in systems where males must avoid mating with heterospecific females, as is found in a mating complex of Poecilia. Male sailfin mollies, Poecilia latipinna, are sexually parasitized by gynogenetic Amazon mollies, P. formosa. Little is known about the mechanism by which male sailfin mollies base their mating decisions. Here we tested the hypothesis that male sailfin mollies from an allopatric and a sympatric population with Amazon mollies use multiple cues to distinguish between conspecific and heterospecific females. We found that male sailfin mollies recognized the chemical cues of conspecific females, but we found no support for the hypothesis that chemical cues are by themselves sufficient for species discrimination. Lack of discrimination based on chemical cues alone may be due to the close evolutionary history between P. latipinna and P. formosa. Males from populations sympatric with Amazon mollies did not differentially associate with females of either of the two species when given access to both visual and chemical cues of the females, yet males from the allopatric population did associate more with conspecific females than with heterospecific females in the presence of both chemical and visual cues. The lack of discrimination by males from the sympatric population between conspecific and heterospecific females based on both chemical and visual cues suggests that these males require more complex combinations of cues to distinguish species, possibly due to the close relatedness of these species.     

Pollution going multimodal: the complex impact of the human-altered sensory environment on animal perception and performance

Anthropogenic sensory pollution is affecting ecosystems worldwide. Human actions generate acoustic noise, emanate artificial light and emit chemical substances. All of these pollutants are known to affect animals. Most studies on anthropogenic pollution address the impact of pollutants in unimodal sensory domains. High levels of anthropogenic noise, for example, have been shown to interfere with acoustic signals and cues. However, animals rely on multiple senses, and pollutants often co-occur. Thus, a full ecological assessment of the impact of anthropogenic activities requires a multimodal approach. We describe how sensory pollutants can co-occur and how covariance among pollutants may differ from natural situations. We review how animals combine information that arrives at their sensory systems through different modalities and outline how sensory conditions can interfere with multimodal perception. Finally, we describe how sensory pollutants can affect the perception, behaviour and endocrinology of animals within and across sensory modalities. We conclude that sensory pollution can affect animals in complex ways due to interactions among sensory stimuli, neural processing and behavioural and endocrinal feedback. We call for more empirical data on covariance among sensory conditions, for instance, data on correlated levels in noise and light pollution. Furthermore, we encourage researchers to test animal responses to a full-factorial set of sensory pollutants in the presence or the absence of ecologically important signals and cues. We realize that such approach is often time and energy consuming, but we think this is the only way to fully understand the multimodal impact of sensory pollution on animal performance and perception.     

Asymmetric interspecific competition drives shifts in signalling traits in fan-throated lizards

Interspecific competition can occur when species are unable to distinguish between conspecific and heterospecific mates or competitors when they occur in sympatry. Selection in response to interspecific competition can lead to shifts in signalling traits—a process called agonistic character displacement. In two fan-throated lizard species—Sitana laticeps and Sarada darwini—females are morphologically indistinguishable and male agonistic signalling behaviour is similar. Consequently, in areas where these species overlap, males engage in interspecific aggressive interactions. To test whether interspecific male aggression between Si. laticeps and Sa. darwini results in agonistic character displacement, we quantified species recognition and signalling behaviour using staged encounter assays with both conspecifics and heterospecifics across sympatric and allopatric populations of both species. We found an asymmetric pattern, wherein males of Si. laticeps but not Sa. darwini showed differences in competitor recognition and agonistic signalling traits (morphology and behaviour) in sympatry compared with allopatry. This asymmetric shift in traits is probably due to differences in competitive abilities between species and can minimize competitive interactions in zones of sympatry. Overall, our results support agonistic character displacement, and highlight the role of asymmetric interspecific competition in driving shifts in social signals.     

Olfactory mate recognition in a sympatric species pair of three-spined sticklebacks

Mate recognition is critical to the maintenance of reproductiveisolation, and animals use an array of sensory modalities toidentify conspecific mates. In particular, olfactory informationcan be an important component of mate recognition systems. Weinvestigated whether odor is involved in mate recognition ina sympatric benthic and limnetic species pair of three-spinedsticklebacks (Gasterosteus spp.), for which visual cues andsignals are known to play a role in premating isolation. Weallowed gravid females of each species to choose between waterscented by a heterospecific male and water scented by a conspecificmale. Benthic females preferred the conspecific male stimuluswater significantly more often than the heterospecific malestimulus water, whereas limnetic females showed no preference.These species thus differ in their odor and may also differin their use of olfaction to recognize conspecific mates. Thesedifferences are likely a consequence of adaptation to disparateenvironments. Differences in diet, foraging mode, habitat, andparasite exposure may explain our finding that odor might bean asymmetric isolating mechanism in these sympatric sticklebackspecies.     

The role of interspecific interference competition in character displacement and the evolution of competitor recognition

The extent to which interspecific interference competition has contributed to character evolution is one of the most neglected problems in evolutionary biology. When formerly allopatric species come into secondary contact, aggressive interactions between the species can cause selection on traits that affect interspecific encounter rates (e.g. habitat preferences, activity schedules), competitor recognition (e.g. colouration, song), and fighting ability (e.g. weaponry, body size). We define agonistic character displacement (ACD) as the process of phenotypic evolution in a population caused by interference competition with one or more sympatric species and which results in shifts in traits that affect the rate, intensity or outcome of interspecific aggression. After clarifying the relationships between ACD and other evolutionary processes that may occur when species come into secondary contact, we develop an individual‐based, quantitative genetic model to examine how traits involved in competitor recognition would be expected to evolve under different secondary contact scenarios. Our simulation results show that both divergence and convergence are possible outcomes, depending on the intensity of interspecific exploitative competition, the costs associated with mutual versus unilateral recognition, and the extent of phenotypic differences prior to secondary contact. We then devise a set of eight criteria for evaluating putative examples of ACD and review the empirical literature to assess the strength of existing evidence and to identify promising avenues for future research. Our literature search revealed 33 putative examples of ACD across insects, fishes, bats, birds, lizards, and amphibians (15 divergence examples; 18 convergence examples). Only one example satisfies all eight criteria for demonstrating ACD, but most case studies satisfy four or more criteria. The current state of the evidence for ACD is similar to the state of the evidence for ecological character displacement just 10 years ago. We conclude by offering suggestions for further theoretical and empirical research on ACD.     

The mechanisms of kin discrimination and the evolution of kin recognition in vertebrates: a critical re-evaluation

I re-examine the four most widely proposed mechanisms of kin discrimination among vertebrates and conclude that the current categorization of kin discrimination mechanisms has been counterproductive because it has a hindered a clear understanding of the basic mechanisms by which animals discriminate kin. I suggest that there likely is only one authentic mechanism of kin discrimination and that this mechanism is learning, particularly associative learning and habituation. Observed differences in the way animals discriminate between kin and non-kin are due only to the cues (e.g., individually-distinctive, family-distinctive, or self) that are used, and not to different mechanisms per se. I also consider whether kin discrimination is mediated by specially evolved kin recognition systems, defined as neural mechanisms that allow animals to directly classify conspecifics as either kin or non-kin. A preliminary analysis of vertebrate recognition systems suggests that specialized neural, endocrine, and developmental mechanisms specifically for recognizing kin have not evolved. Rather, kin discrimination results from an extension of other, non-specialized sensory and cognitive abilities of animals, and may be derived from other forms of social recognition, such as individual, group, or species recognition.     

Courtship, aggression and avoidance: pheromones, receptors and neurons for social behaviors in Drosophila

Chemical communication between individual Drosophila is extremely important for social behaviors required for survival and reproduction, such as con-specific recognition, courtship, aggression and avoidance of odor from "stressed" flies. Characterization of the receptors and neural circuits that detect pheromone cues and an understanding of how these circuits are modulated by the social interactions are fundamental questions about the neurobiology of social behaviors. Recent years have seen important advances in the identification of chemoreceptors and sensory neurons that are involved in sensing pheromones. Here we present a brief review of the current understanding of the peripheral chemosensory systems that are involved in social behaviors.     

Eavesdropping in solitary large carnivores: Black bears advance and vocalize toward cougar playbacks

Large carnivore behavioral responses to the cues of their competitors are rarely observed, but may mediate competition between these top predators. Playback experiments, currently limited to interactions involving group‐living large carnivores, demonstrate that attending to cues indicative of the immediate presence of heterospecific competitors plays a substantial role in influencing competition among these species. Group‐living species vocalize regularly to signal to one another, and competitors can readily “eavesdrop” on these acoustic cues. Solitary large carnivores also vocalize to conspecifics, but much less frequently, reducing the ease with which heterospecific competitors can eavesdrop. Eavesdropping could nonetheless play a substantive role in mediating competition among solitary large carnivores if the benefits of responding to the acoustic cues of heterospecific competitors (reducing risk or locating resources) are sufficiently large. Behavioral interactions between solitary large carnivore species are almost never observed, and there have been no experimental tests of their reactions to cues indicative of the immediate presence of other solitary large carnivores. We used an automated playback system to test the responses of a solitary large carnivore (black bear, Ursus americanus) to vocalizations of their similarly solitary competitor (cougar, Puma concolor), presenting both cougar and control vocalizations to free‐living bears foraging along shorelines in British Columbia, Canada. Both mothers with cubs and solitary bears were significantly more likely to advance and vocalize toward cougar than control playbacks, mothers producing one or both of two distinct vocalizations and solitary bears producing just one. Cougars could either represent a potential risk to bears (particularly cubs), or a source of resources, as bears are known to regularly scavenge cougar kills. Our results are consistent with bears eavesdropping on cougars for both these reasons. As with group‐living species, eavesdropping may be common among solitary large carnivores, and may be an important driver of competition between these species.     

Food availability and brood number do not influence intraspecific aggression in Argentine ants

Summary. Nestmate recognition cues can derive from both environmental and genetic factors, but can also be modulated in response to context-specific cues. Synchronous changes in nestmate recognition systems occur seasonally in some species of ants, however the mechanisms underlying these seasonal changes are often unknown. We studied two mechanisms, relative brood number and food availability, to determine if they generate temporal variation in intraspecific aggression in an introduced population of the Argentine ant, Linepithema humile. Using data from previous studies we found that seasonal increases in aggression levels correlate with seasonal increases in brood-to-worker ratios in the field. However, when we manipulated brood-to-worker ratios in paired experimental colonies, we found no direct evidence that relative brood numbers influenced aggression levels. To determine if food availability influenced aggression we conducted a second experiment in which we randomly assigned pairs of experimental colonies to starved or fed treatments and then measured aggression levels weekly for five weeks. We observed no difference in the level of aggression between these two treatment groups indicating that food availability also has no affect on aggression levels between hostile conspecific colonies.Received 24 August 2004; revised 15 September 2004; accepted 23 September 2004.     

Contact between supercolonies elevates aggression in Argentine ants

Complex recognition systems underlie the social organization of many organisms. In social insects the acceptance of other individuals as nestmates can involve a variety of different cues, but the relative importance of these cues can change in relation to the fitness costs of accepting or rejecting other individuals. In this study we investigate the mechanisms that underlie recognition behaviour in Argentine ants (Linepithema humile). Introduced populations of Argentine ants are characterized by a social structure known as unicoloniality where intraspecific aggression is absent over large distances resulting in the formation of expansive supercolonies. Recent research has identified sites where multiple, mutually aggressive supercolonies co-occur allowing an examination of Argentine ant behaviour at territorial boundaries. We found that workers from different supercolonies always interact aggressively with one another, but that neighbours from different colonies (i.e., workers from nests located in the immediate vicinity of territory borders) consistently exhibited higher levels of aggression compared to those displayed by non-neighbours from different colonies (i.e., workers from nests located far enough away from a territory border so that interactions are unlikely). This difference in the level of aggression displayed between neighbours and between non-neighbours from different supercolonies cannot be explained by differences in relatedness or genetic similarity. Instead our findings suggest that direct contact between mutually antagonistic colonies is sufficient to elevate aggression. A laboratory experiment in which we manipulated the extent to which colonies with no prior history of contact could interact with one another, revealed that aggression increased after colonies were permitted to interact, but dropped after connections between colonies were severed. Moreover, the mere presence of an aggressive supercolony was sufficient to elicit elevated aggression. Overall these patterns are opposite to the “dear enemy” phenomenon and could be the result of the intense territorial aggression exhibited by established supercolonies of this species. Received 8 January 2007; revised 27 March 2007; accepted 28 March 2007.     

Multisensory Integration and Behavioral Plasticity in Sharks from Different Ecological Niches

The underwater sensory world and the sensory systems of aquatic animals have become better understood in recent decades, but typically have been studied one sense at a time. A comprehensive analysis of multisensory interactions during complex behavioral tasks has remained a subject of discussion without experimental evidence. We set out to generate a general model of multisensory information extraction by aquatic animals. For our model we chose to analyze the hierarchical, integrative, and sometimes alternate use of various sensory systems during the feeding sequence in three species of sharks that differ in sensory anatomy and behavioral ecology. By blocking senses in different combinations, we show that when some of their normal sensory cues were unavailable, sharks were often still capable of successfully detecting, tracking and capturing prey by switching to alternate sensory modalities. While there were significant species differences, odor was generally the first signal detected, leading to upstream swimming and wake tracking. Closer to the prey, as more sensory cues became available, the preferred sensory modalities varied among species, with vision, hydrodynamic imaging, electroreception, and touch being important for orienting to, striking at, and capturing the prey. Experimental deprivation of senses showed how sharks exploit the many signals that comprise their sensory world, each sense coming into play as they provide more accurate information during the behavioral sequence of hunting. The results may be applicable to aquatic hunting in general and, with appropriate modification, to other types of animal behavior.     

Paternal imprinting of mating preferences between natural populations of house mice (Mus musculus domesticus)

The evolutionary divergence of cues for mate recognition can contribute to early stages of population separation. We compare here two allopatric populations of house mice (Mus musculus domesticus) that have become separated about 3000 years ago. We have used paternity assignments in semi‐natural environments to study the degree of mutual mate recognition according to population origin under conditions of free choice and overlapping generations. Our results provide insights into the divergence of mating cues, but also for the mating system of house mice. We find frequent multiple mating, occurrence of inbreeding and formation of extended family groups. In addition, many animals show strong mate fidelity, that is, frequent choice of the same mating partners in successive breeding cycles, indicating a role for familiarity in mating preference. With respect to population divergence, we find evidence for assortative mating, but only under conditions where the animals had time to familiarize themselves with mating partners from their own population. Most interestingly, the first‐generation offspring born in the enclosure showed a specific mating pattern. Although matings between animals of hybrid population origin with animals of pure population origin should have occurred with equal frequency with respect to matching the paternal or maternal origin, paternal matching with mates from their own populations occurred much more often. Our findings suggest that paternally imprinted cues play a role in mate recognition between mice and that the cues evolve fast, such that animals of populations that are separated since not more than 3000 years can differentially recognize them.     

Predator selectivity alters the effect of dispersal on coexistence among apparent competitors

While the majority of studies on dispersal effects on patterns of coexistence among species in a metacommunity have focused on resource competitors, dispersal in systems with predator–prey interactions may provide very different results. Here, we use an analytical model to study the effect of dispersal rates on coexistence of two prey species sharing a predator (apparent competition), when the traits of that predator vary. Specifically, we explore the range in immigration rates where apparent competitors are able to coexist, and how that range changes with predator selectivity and efficiency. We find that if the inferior apparent competitor has a higher probability of being consumed, it will require less immigration to invade and to exclude the superior prey as the predator becomes more opportunistic. However, if the inferior apparent competitor has a lower probability of being consumed (and lower growth rates), higher immigration is required for the inferior prey to invade and exclude the superior prey as the predator becomes more opportunistic. We further find that the largest range of immigration rates where prey coexist occurs when predator selectivity is intermediate (i.e. they do not show much bias towards consuming one species or the other). Increasing predator efficiency generally reduces the immigration rates necessary for the inferior apparent competitor to invade and exclude the superior apparent competitor, but also reduces the range of immigration rates where the two apparent competitors can coexist. However, when the superior apparent competitor has a higher probability of being consumed, increased predator efficiency can increase the range of parameters where the species can coexist. Our results are consistent with some of the variation observed in the effect of dispersal on prey species richness in empirical systems with top predators.     

Generalization in response to mate recognition signals

Females usually exhibit strong and unequivocal recognition of conspecific mating signals and reject those of other sympatric heterospecifics. However, most species are allopatric with one another, and the degree to which females recognize mating signals of allopatric species is more varied. Such mating signals are often rejected but are sometimes falsely recognized as conspecific. We studied the dynamics of mate recognition in female túngara frogs (Physalaemus pustulosus) in response to a series of calls that were intermediate between the conspecific and each of five allopatric-heterospecific calls: two that elicited recognition from females in previous studies and three that did not. This study shows that females perceive variation in allopatric mating signals in acontinuous manner with no evidence of perceptual category formation. The strength of recognition is predicted by how different the target stimulus is from the conspecific call within a series of calls. But the differences in recognition responses among call series are not predicted by the similarity of the call series to the conspecific call. The latter result suggests that the strength of recognition of allopatric signals might be influenced by processes of stimulus generalization and past evolutionary history.     

Encoding olfactory signals via multiple chemosensory systems

Most animals have evolved multiple olfactory systems to detect general odors as well as social cues. The sophistication and interaction of these systems permit precise detection of food, danger, and mates, all crucial elements for survival. In most mammals, the nose contains two well described chemosensory apparatuses (the main olfactory epithelium and the vomeronasal organ), each of which comprises several subtypes of sensory neurons expressing distinct receptors and signal transduction machineries. In many species (e.g., rodents), the nasal cavity also includes two spatially segregated clusters of neurons forming the septal organ of Masera and the Grueneberg ganglion. Results of recent studies suggest that these chemosensory systems perceive diverse but overlapping olfactory cues and that some neurons may even detect the pressure changes carried by the airflow. This review provides an update on how chemosensory neurons transduce chemical (and possibly mechanical) stimuli into electrical signals, and what information each system brings into the brain. Future investigation will focus on the specific ligands that each system detects with a behavioral context and the processing networks that each system involves in the brain. Such studies will lead to a better understanding of how the multiple olfactory systems, acting in concert, offer a complete representation of the chemical world.     

Do novel weapons that degrade mycorrhizal mutualisms promote species invasion?

Non-native plants often dominate novel habitats where they did not co-evolve with the local species. The novel weapons hypothesis suggests that non-native plants bring competitive traits against which native species have not adapted defenses. Novel weapons may directly affect plant competitors by inhibiting germination or growth, or indirectly by attacking competitor plant mutualists (degraded mutualisms hypothesis). Japanese knotweed (Fallopia japonica) and European buckthorn (Rhamnus cathartica) are widespread plant invaders that produce potent secondary compounds that negatively impact plant competitors. We tested whether their impacts were consistent with a direct effect on the tree seedlings (novel weapons) or an indirect attack via degradation of seedling mutualists (degraded mutualism). We compared recruitment and performance using three Ulmus congeners and three Betula congeners treated with allelopathic root macerations from allopatric and sympatric ranges. Moreover, given that the allelopathic species would be less likely to degrade their own fungal symbiont types, we used arbuscular mycorrhizal (AMF) and ectomycorrhizal (ECM) tree species to investigate the effects of F. japonica (no mycorrhizal association) and Rhamnus cathartica (ECM association) on the different fungal types. We also investigated the effects of F. japonica and R. cathartica exudates on AMF root colonization. Our results suggest that the allelopathic plant exudates impact seedlings directly by inhibiting germination and indirectly by degrading fungal mutualists. Novel weapons inhibited allopatric seedling germination but sympatric species were unaffected. However, seedling survivorship and growth appeared more dependent on mycorrhizal fungi, and mycorrhizal fungi were inhibited by allopatric species. These results suggest that novel weapons promote plant invasion by directly inhibiting allopatric competitor germination and indirectly by inhibiting mutualist fungi necessary for growth and survival.     

The evolution of species recognition in competitive and mating contexts: the relative efficacy of alternative mechanisms of character displacement

Sympatric divergence in traits affecting species recognition can result from selection against cross‐species mating (reproductive character displacement, RCD) or interspecific aggression (agonistic character displacement, ACD). When the same traits are used for species recognition in both contexts, empirically disentangling the relative contributions of RCD and ACD to observed character shifts may be impossible. Here, we develop a theoretical framework for partitioning the effects of these processes. We show that when both mate and competitor recognition depend on the same trait, RCD sets the pace of character shifts. Moreover, RCD can cause divergence in competitor recognition, but ACD cannot cause divergence in mate recognition. This asymmetry arises because males with divergent recognition traits may avoid needless interspecific conflicts, but suffer reduced attractiveness to conspecific females. Therefore, the key empirical issue is whether the same or different traits are used for mate recognition and competitor recognition.