Agonistic Character Displacement Research Articles

Competitive Displacement and Agonistic Character Displacement, or the Ghost of Interference Competition.

AbstractInterference competition can drive species apart in habitat use through competitive displacement in ecological time and agonistic character displacement (ACD) over evolutionary time. As predicted by ACD theory, sympatric species of rubyspot damselflies (Hetaerina spp.) that respond more aggressively to each other in staged encounters differ more in microhabitat use. However, the same pattern could arise from competitive displacement if dominant species actively exclude subordinate species from preferred microhabitats. The degree to which habitat partitioning is caused by competitive displacement can be assessed with removal experiments. We carried out removal experiments with three species pairs of rubyspot damselflies. With competitive displacement, removing dominant species should allow subordinate species to shift into the dominant species' microhabitat. Instead, we found that species-specific microhabitat use persisted after the experimental removals. Thus, the previously documented association between heterospecific aggression and microhabitat partitioning in this genus is most likely a product of divergence in habitat preferences caused by interference competition in the evolutionary past.

Mechanisms of reduced interspecific interference between territorial species

AbstractInterspecific territoriality has complex ecological and evolutionary consequences. Species that interact aggressively often exhibit spatial or temporal shifts in activity that reduce the frequency of costly encounters. We analyzed data collected over a 13-year period on 50 populations of rubyspot damselflies (Hetaerina spp.) to examine how rates of interspecific fighting covary with fine-scale habitat partitioning and to test for agonistic character displacement in microhabitat preferences. In most sympatric species, interspecific fights occur less frequently than expected based on the species’ relative densities. Incorporating measurements of spatial segregation and species discrimination into the calculation of expected frequencies accounted for most of the reduction in interspecific fighting (subtle differences in microhabitat preferences could account for the rest). In 23 of 25 sympatric population pairs, we found multivariate differences between species in territory microhabitat (perch height, stream width, current speed, and canopy cover). As predicted by the agonistic character displacement hypothesis, sympatric species that respond more aggressively to each other in direct encounters differ more in microhabitat use and have higher levels of spatial segregation. Previous work established that species with the lowest levels of interspecific fighting have diverged in territory signals and competitor recognition through agonistic character displacement. In the other species pairs, interspecific aggression appears to be maintained as an adaptive response to reproductive interference, but interspecific fighting is still costly. We now have robust evidence that evolved shifts in microhabitat preferences also reduce the frequency of interspecific fighting.

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.

Time spent together and time spent apart affect song, feather colour and range overlap in tinkerbirds

Abstract Most studies on the processes driving evolutionary diversification highlight the importance of genetic drift in geographical isolation and natural selection across ecological gradients. Direct interactions among related species have received much less attention, but they can lead to character displacement, with recent research identifying patterns of displacement attributed to either ecological or reproductive processes. Together, these processes could explain complex, trait-specific patterns of diversification. Few studies, however, have examined the possible effects of these processes together or compared the divergence in multiple traits between interacting species among contact zones. Here, we show how traits of two Pogoniulus tinkerbird species vary among regions across sub-Saharan Africa. However, in addition to variation between regions consistent with divergence in refugial isolation, both song and morphology diverge between the species where they coexist. In West Africa, where the species are more similar in plumage, there is possible competitive or reproductive exclusion. In Central and East Africa, patterns of variation are consistent with agonistic character displacement. Molecular analyses support the hypothesis that differences in the age of interaction among regions can explain why species have evolved phenotypic differences and coexist in some regions but not others. Our findings suggest that competitive interactions between species and the time spent interacting, in addition to the time spent in refugial isolation, play important roles in explaining patterns of species diversification.

Range-wide spatial mapping reveals convergent character displacement of bird song.

A long-held view in evolutionary biology is that character displacement generates divergent phenotypes in closely related coexisting species to avoid the costs of hybridization or ecological competition, whereas an alternative possibility is that signals of dominance or aggression may instead converge to facilitate coexistence among ecological competitors. Although this counterintuitive process-termed convergent agonistic character displacement-is supported by recent theoretical and empirical studies, the extent to which it drives spatial patterns of trait evolution at continental scales remains unclear. By modelling the variation in song structure of two ecologically similar species of Hypocnemis antbird across western Amazonia, we show that their territorial signals converge such that trait similarity peaks in the sympatric zone, where intense interspecific territoriality between these taxa has previously been demonstrated. We also use remote sensing data to show that signal convergence is not explained by environmental gradients and is thus unlikely to evolve by sensory drive (i.e. acoustic adaptation to the sound transmission properties of habitats). Our results suggest that agonistic character displacement driven by interspecific competition can generate spatial patterns opposite to those predicted by classic character displacement theory, and highlight the potential role of social selection in shaping geographical variation in signal phenotypes of ecological competitors.

Agonistic character displacement of genetically based male colour patterns across darters.

Agonistic character displacement (ACD) occurs when selection to avoid maladaptive interspecific aggression leads to the evolution of agonistic signals and/or associated behavioural biases in sympatry. Here, we test for a pattern consistent with ACD in male colour pattern in darters (Percidae: Etheostoma). Male colour pattern has been shown to function in male-male competition rather than female mating preferences in several darter species. Additionally, males bias their aggression towards conspecific over heterospecific males in sympatry but not in allopatry, consistent with divergent ACD in male behavioural biases. We use a common garden approach to show that differences in male colour pattern among four closely related darter species are genetically based. Additionally, we demonstrate that some aspects of male colour pattern exhibit enhanced differences in sympatric compared to allopatric populations of two darter species, consistent with ACD. However, other male colour traits are more similar between species in sympatry compared with allopatry, indicating that not all signal components are under strong divergent selection in sympatry. This study provides evidence that interspecific male-male aggressive interactions alone can promote elaborate male signal evolution both between and within species. We discuss the implications this has for male-driven ACD and cascade ACD.

Male-driven reproductive and agonistic character displacement in darters and its implications for speciation in allopatry.

Selection against hybridization can cause mating traits to diverge between species in sympatry via reproductive character displacement (RCD). Additionally, selection against interspecific fighting can cause aggressive traits to diverge between sympatric species via agonistic character displacement (ACD). By directly affecting conspecific recognition traits, RCD and ACD between species can also incidentally cause divergence in mating and fighting traits among populations within a species [termed cascade RCD (CRCD) and cascade ACD]. Here, we demonstrate patterns consistent with male-driven RCD and ACD in 2 groups of darters (orangethroat darter clade Ceasia and rainbow darter Etheostoma caeruleum). In both groups, males that occur in sympatry (between Ceasia and E. caeruleum) have higher levels of preference for mating and fighting with conspecifics over heterospecifics than do males from allopatry. This is consistent with RCD and ACD. We also found patterns consistent with CRCD and cascade ACD among species of Ceasia. Ceasia males that are sympatric to E. caeruleum (but allopatric to one another) also have heightened preferences for mating and fighting with conspecific versus heterospecific Ceasia. In contrast, Ceasia males that are allopatric to E. caeruleum readily mate and fight with heterospecific Ceasia. We suggest that RCD and ACD between Ceasia and E. caeruleum has incidentally led to divergence in mating and fighting traits among Ceasia species. This study is unique in that male preferences evolve via both RCD (male preference for conspecific females) and ACD (male preference to fight conspecific males) which leads to subsequent divergence among allopatric lineages.

Agonistic character displacement in social cognition of advertisement signals.

Interspecific aggression between sibling species may enhance discrimination of competitors when recognition errors are costly, but proximate mechanisms mediating increased discriminative ability are unclear. We studied behavioral and neural mechanisms underlying responses to conspecific and heterospecific vocalizations in Alston's singing mouse (Scotinomys teguina), a species in which males sing to repel rivals. We performed playback experiments using males in allopatry and sympatry with a dominant heterospecific (Scotinomys xerampelinus) and examined song-evoked induction of egr-1 in the auditory system to examine how neural tuning modulates species-specific responses. Heterospecific songs elicited stronger neural responses in sympatry than in allopatry, despite eliciting less singing in sympatry. Our results refute the traditional neuroethological concept of a matched filter and instead suggest expansion of sensory sensitivity to mediate competitor recognition in sympatry.

Does competitive interaction drive species recognition in a house mouse secondary contact zone?

Miscommunication may induce a high risk of unnecessary escalated fights between competitors (populations to species), resulting in selection favoring signal divergence through agonistic character displacement (ACD). When signals allowing discrimination between competitors are also involved in mate recognition, ACD could explain reproductive character displacement (RCD). We tested interference competition between males as a potential driver of RCD (here, subspecies recognition) in a secondary contact zone between two mouse subspecies (Mus musculus musculus and Mus musculus domesticus) displaying asymmetric dominance. Since such asymmetry could create a conflict between subspecies (compatibility) and quality (dominance) recognition in the contact zone, we tested for geographic variation in female preference for dominant males in the subordinate subspecies, musculus. We assessed competition between males and tested ACD during dyadic encounters comparing behavior displayed during trials between heterosubspecifics originating from populations close to the secondary contact (“contact”) and further away (“allopatric”). We also compared behavior of contact versus allopatric males during homosubspecific versus heterosubspecific trials to test whether subspecies discrimination evolved under competitive interference. Although domesticus dominated most heterosubspecific trials regardless of geographic origin, agonistic behavior was more marked (i.e., lower attack latencies) during contact than allopatric encounters, suggesting that ACD occurred. Comparing behavior during homosubspecific and heterosubspecific encounters, only allopatric musculus displayed differences, that is, higher attack latencies toward heterosubspecifics, indicating that discrimination between competitors did not evolve with ACD. Finally, although allopatric musculus females seemed to prefer dominant males, their contact counterparts did not, suggesting that “compatibility” may have outweighed “quality” under a risk of hybridization.

Interspecific territoriality in two songbird species: potential role of song convergence in male aggressive interactions

In animals, interspecific interference competition is often associated with their aggressive behaviour. The intensity of interspecific aggression and the outcomes of interference competition between closely related species might be substantially modified by copying of vocal signals used in territory defence. Here we tested the hypothesis that song convergence observed in a secondary contact zone of two songbird species, the common nightingale. Luscinia megarhynchos, and the thrush nightingale, Luscinia luscinia, might be an adaptive response to interspecific interference competition. These species are morphologically and ecologically very similar. However, the thrush nightingale is slightly larger and several lines of evidence indicate its competitive dominance. In the secondary contact zone most thrush nightingales incorporate common nightingale song types in their repertoires. Using playback experiments, we evaluated the strength of nonvocal aggressive responses of both species to conspecific and heterospecific stimuli. The species did not differ in aggressive responses to a heterospecific stimulus, suggesting that competitive dominance is not associated with higher interspecific aggressiveness in nightingales. Interestingly, while the common nightingale reacted significantly more aggressively to the conspecific than the heterospecific stimulus, the thrush nightingale showed similarly strong responses to both stimuli. We suggest that this similar level of interspecific and conspecific aggression in the thrush nightingale results from mixed singing of this species in sympatry, as males may not distinguish conspecifics from heterospecifics by song alone. Our results are consistent with the concept of convergent agonistic character displacement. According to this theory, vocal convergence might be adaptive in species that overlap broadly in resource use, as it leads to better distinction of territory boundaries between the species and thus reduces the level of interspecific competition.

Interspecific aggression, not interspecific mating, drives character displacement in the wing coloration of male rubyspot damselflies (Hetaerina).

Traits that mediate intraspecific social interactions may overlap in closely related sympatric species, resulting in costly between-species interactions. Such interactions have principally interested investigators studying the evolution of reproductive isolation via reproductive character displacement (RCD) or reinforcement, yet in addition to reproductive interference, interspecific trait overlap can lead to costly between-species aggression. Previous research on rubyspot damselflies (Hetaerina spp.) demonstrated that sympatric shifts in male wing colour patterns and competitor recognition reduce interspecific aggression, supporting the hypothesis that agonistic character displacement (ACD) drove trait shifts. However, a recent theoretical model shows that RCD overshadows ACD if the same male trait is used for both female mate recognition and male competitor recognition. To determine whether female mate recognition is based on male wing coloration in Hetaerina, we conducted a phenotype manipulation experiment. Compared to control males, male H. americana with wings manipulated to resemble a sympatric congener (H. titia) suffered no reduction in mating success. Thus, female mate recognition is not based on species differences in male wing coloration. Experimental males did, however, experience higher interspecific fighting rates and reduced survival compared to controls. These results greatly strengthen the case for ACD and highlight the mechanistic distinction between ACD and RCD.

Sympatric sexual signal divergence among North American Calopteryx damselflies is correlated with increased intra- and interspecific male–male aggression

Divergence of sexual signals in sympatry can arise as a consequence of (1) interspecific competition for resources, (2) selection against maladaptive hybridization, or (3) as a result of selection to reduce the cost of interspecific aggression; termed agonistic character displacement (ACD). Calopterygid damselflies have emerged as a model system for studying the evolution of divergent sexual signals due to the repeated evolution of sympatric species pairs with fully and partially melanized wings. Damselfly wing patterns function during both courtship and territory defense. However, the relative contributions of natural and sexual selection to phenotypic divergence and enhanced isolation in sympatry remain unclear in many cases. Here, we investigated the hypothesis that interference competition, in the form of increased interspecific male–male aggression, drives the evolution of character displacement in sympatry between two species of North American damselflies, Calopteryx aequabilis and Calopteryx maculata, that show no evidence of ecological divergence or ongoing hybridization. In paired behavioral trials, we found that interspecific male aggression related to territory defense varied between site, species, and as a function of the relative abundance of con- vs. hetero-specific males. Specifically, we found that large-spotted C. aequabilis males received increased intra- and interspecific aggression but that aggression against large-spotted males declined during the middle of the flight season when both species were equally abundant. Based on these results, we suggest that ACD leads to enhanced species recognition, and may be a common outcome of the antagonism between interspecific male–male competition and the countervailing force of intraspecific sexual selection favoring increased wing melanization among territorial damselfly species.

The evolutionary consequences of interspecific aggression

Competition has always been a cornerstone of evolutionary biology, and aggression is the predominant form of direct competition in animals, but the evolutionary effects of aggression between species are curiously understudied. Only in the past few years, existing theoretical frameworks have been extended to include interspecific aggression, and significant empirical advances have been made. After arguing that agonistic character displacement (ACD) theory provides the most suitable theoretical framework, we review new empirical evidence for ACD and the results of mathematical models of the process. We consider how ACD can be distinguished empirically from ecological and reproductive character displacement and the additional challenges posed by developmental plasticity. We also provide the first taxonomically broad review of theoretical and empirical work on the effects of interspecific aggression on species coexistence and range limits. We conclude by highlighting promising directions for future research on the evolutionary effects of interspecific aggression.

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.

Male-Male Competition as a Force in Evolutionary Diversification: Evidence in Haplochromine Cichlid Fish

It has been suggested that intrasexual competition can be a source of negative frequency-dependent selection, causing agonistic character displacement and facilitating speciation and coexistence of (sibling) species. In this paper we synthesise the evidence that male-male and female-female competition contributes to cichlid diversification, showing that competition is stronger among same-coloured individuals than those with different colours. We argue that intrasexual selection is more complex because there are several examples where males do not bias aggression towards their own type. In addition, sibling species or colour morphs often show asymmetric dominance relationships. We briefly discuss potential mechanisms that might promote the maintenance of covariance between colour and aggression-related traits even in the face of gene-flow. We close by proposing several avenues for future studies that might shed more light on the role of intrasexual competition in cichlid diversification.

Multiple routes to reduced interspecific territorial fighting in Hetaerina damselflies

Multiple routes to reduced interspecific territorial fighting in Hetaerina damselflies

Character displacement in the fighting colours of Hetaerina damselflies.

Aggression between species is a seldom-considered but potentially widespread mechanism of character displacement in secondary sexual characters. Based on previous research showing that similarity in wing coloration directly influences interspecific territorial aggression in Hetaerina damselflies, we predicted that wing coloration would show a pattern of character displacement (divergence in sympatry). A geographical survey of four Hetaerina damselfly species in Mexico and Texas showed evidence for character displacement in both species pairs that regularly occurs sympatrically. Hetaerina titia, a species that typically has large black wing spots and small red wing spots, shifted to having even larger black spots and smaller red wing spots at sites where a congener with large red wing spots is numerically dominant (Hetaerina americana or Hetaerina occisa). Hetaerina americana showed the reverse pattern, shifting towards larger red wing spots where H. titia is numerically dominant. This pattern is consistent with the process of agonistic character displacement, but the ontogenetic basis of the shift remains to be demonstrated.

Interspecific aggression and character displacement of competitor recognition in Hetaerina damselflies

In zones of sympatry between closely related species, species recognition errors in a competitive context can cause character displacement in agonistic signals and competitor recognition functions, just as species recognition errors in a mating context can cause character displacement in mating signals and mate recognition. These two processes are difficult to distinguish because the same traits can serve as both agonistic and mating signals. One solution is to test for sympatric shifts in recognition functions. We studied competitor recognition in Hetaerina damselflies by challenging territory holders with live tethered conspecific and heterospecific intruders. Heterospecific intruders elicited less aggression than conspecific intruders in species pairs with dissimilar wing coloration (H. occisa/H. titia, H. americana/H. titia) but not in species pairs with similar wing coloration (H. occisa/H. cruentata, H. americana/H. cruentata). Natural variation in the area of black wing pigmentation on H. titia intruders correlated negatively with heterospecific aggression. To directly examine the role of wing coloration, we blackened the wings of H. occisa or H. americana intruders and measured responses of conspecific territory holders. This treatment reduced territorial aggression at multiple sites where H. titia is present, but not at allopatric sites. These results provide strong evidence for agonistic character displacement.

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.