Sympatric shift in a male sexual ornament in the damselfly Calopteryx splendens

Character displacement is a process by which interactions between two species that exhibit similar traits, results in geographical patterns of trait divergence in one or both species. These traits evolve to reduce costs of interspecific interactions in sympatry and thus differ from their condition in allopatry. In male damselflies Calopteryx splendens, large wing spots are sexually selected. However, in sympatric populations with Calopteryx virgo, wing spot size decreases as C. virgo abundance increases. The stability of this pattern is unclear, because previous studies have focused on sympatric populations with potentially fluctuating relative abundances. We studied the wing spot sizes of C. splendens in both sympatric and allopatric populations. Our data show that male C. splendens’ wing spots are larger in allopatry than in sympatry with C. virgo. We suggest that both interspecific aggression and avoidance of interspecific reproductive interactions may result in this pattern, although their relative importance remains unclear.     

Interspecific aggression causes negative selection on sexual characters

Interspecific aggression originating from mistaken species recognition may cause selection on secondary sexual characters, but this hypothesis has remained untested. Here we report a field experiment designed to test directly whether interspecific aggression causes selection on secondary sexual characters, wing spots, in wild damselfly populations. Males of Calopteryx virgo are more aggressive toward males of C. splendens with large than with small wing spots. This differential interspecific aggression may cause negative selection on wing spot size. Indeed, our results show that directional survival selection on wing spot size of C. splendens males was changed by experimental removal of C. virgo males. Without removal, directional selection went from positive to negative with increasing relative abundance of C. virgo males. In populations where C. virgo males were removed, this relationship disappeared. These results verify that interspecific aggression can cause negative selection on sexual characters. Thus, interspecific aggression has the potential to cause divergence on these characters between two species offering an alternative explanation for reinforcement for generating character displacement in secondary sexual characters.     

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.     

Reproductive character displacement of female,but not male song discrimination in an avian hybrid zone

Divergence of male sexual signals and female preferences for those signals often maintains reproductive boundaries between closely related, co‐occurring species. However, contrasting sources of selection, such as interspecific competition, can lead to weak divergence or even convergence of sexual signals in sympatry. When signals converge, assortative mating can be maintained if the mating preferences of females diverge in sympatry (reproductive character displacement; RCD), but there are few explicit examples. Pied flycatchers (Ficedula hypoleuca) are sympatric with collared flycatchers (F. albicollis) on the Baltic island of Öland, where males from both species compete over nestboxes, their songs converge, and the two species occasionally hybridize. We compare song discrimination of male and female pied flycatchers on Öland and in an allopatric population on the Swedish mainland. Using field choice trials, we show that male pied flycatchers respond similarly to the songs of both species in sympatry and allopatry, while female pied flycatchers express stronger discrimination against heterospecific songs in sympatry than in allopatry. These results are consistent with RCD of song discrimination of female pied flycatchers where they co‐occur with collared flycatchers, which should maintain species assortative mating despite convergence of male sexual signals.     

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.     

The case for character displacement in plants

The evidence for character displacement as a widespread response to competition is now building. This progress is largely the result of the establishment of rigorous criteria for demonstrating character displacement in the animal literature. There are, however, relatively few well-supported examples of character displacement in plants. This review explores the potential for character displacement in plants by addressing the following questions: (1) Why aren''t examples of character displacement in plants more common? (2) What are the requirements for character displacement to occur and how do plant populations meet those requirements? (3) What are the criteria for testing the pattern and process of character displacement and what methods can and have been used to address these criteria in the plant literature? (4) What are some additional approaches for studying character displacement in plants? While more research is needed, the few plant systems in which character displacement hypotheses have been rigorously tested suggest that character displacement may play a role in shaping plant communities. Plants are especially amenable to character displacement studies because of the experimental ease with which they can be used in common gardens, selection analyses, and breeding designs. A deeper investigation of character displacement in plants is critical for a more complete understanding of the ecological and evolutionary processes that permit the coexistence of plant species.     

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.     

Reproductive character displacement and the genetics of gamete recognition in tropical sea urchins

Reproductive character displacement occurs when sympatric and allopatric populations of a species differ in traits crucial to reproduction, and it is commonly thought of as a signal of selection acting to limit hybridization. Most documented cases of reproductive character displacement involve characters that are poorly understood at the genetic level, and rejecting alternative hypotheses for biogeographic shifts in reproductive traits is often very difficult. In sea urchins, the gamete recognition protein bindin evolves under positive selection when species are broadly sympatric, suggesting character displacement may be operating in this system. We sampled sympatric and allopatric populations of two species in the sea urchin genus Echinometra for variation in bindin and for the mitochondrial cytochrome oxidase I to examine patterns of population differentiation and molecular evolution at a reproductive gene. We found a major shift in bindin alleles between central Pacific (allopatric) and western Pacific (sympatric) populations of E. oblonga. Allopatric populations of E. oblonga are polyphyletic with E. sp. C at bindin, whereas sympatric populations of the two species are reciprocally monophyletic. There is a strong signal of positive selection (P(N)/P(S) = 4.5) in the variable region of the first exon of bindin, which is associated with alleles found in sympatric populations of E. oblonga. These results indicate that there is a strong pattern of reproductive character displacement between E. oblonga and E. sp. C and that the divergence is driven by selection. There is much higher population structure in sympatric populations at the bindin locus than at the neutral mitochondrial locus, but this difference is not seen in allopatric populations. These data suggest a pattern of speciation driven by selection for local gamete coevolution as a result of interactions between sympatric species. Although this pattern is highly suggestive of speciation by reinforcement, further research into hybrid fitness and egg-sperm interactions is required to address this potential mechanism for character displacement.     

Asymmetrical reproductive character displacement in the house mouse

Our study addressed reproductive character displacement between two subspecies of the house mouse, Mus musculus musculus and Mus musculus domesticus that hybridize in Europe along a zone where selection against hybridization is known to occur. Based on a multi-population approach, we investigated spatial patterns of divergence of mate preference in the two taxa. Mate preference was significantly higher in the contact zone than in allopatry in both subspecies, suggesting that reproductive character displacement occurs. Moreover, patterns of preference were stronger in M. m. musculus than in M. m. domesticus, indicating an asymmetrical divergence between the two. In the context of selection against hybridization, our results may provide empirical support for the hypothesis of reinforcement in a parapatric hybrid zone. We discuss factors that could explain the asymmetrical pattern of divergence and the possible impact of a unimodal structure on the maintenance of premating divergence between the two subspecies.     

Directional mitochondrial introgression and character displacement due to reproductive interference in two closely related Pterostichus ground beetle species

Reproductive interference due to interspecific hybridization can lead to character displacement among related species with overlapping ranges. However, no studies have examined which reproductive traits are most important in reducing reproductive interference. We conducted molecular analyses of two nuclear genes (28S and Wingless) and a mitochondrial gene (COI) from two closely related ground beetle species, Pterostichus thunbergi and Pterostichus habui (Coleoptera: Carabidae), with overlapping distributions. In addition, we examined four reproductive traits (body size, organ morphologies of intromittent and non‐intromittent male genital organs, and female reproductive period) in sympatric and allopatric habitats. We compared male genital morphology using geometric morphometric analysis. The species determined by morphology were classified into separate groups based on the phylogenetic tree constructed by the nuclear gene (Wingless). However, according to the mitochondrial genes examined, P. thunbergi was not monophyletic, whereas at the sympatric sites, these species formed a monophyletic clade. This incongruence suggests that interspecific hybridization and subsequent mitochondrial introgression from P. habui to P. thunbergi have occurred. Concerning genital morphology, both of the intromittent and nonintromittent organs of P. thunbergi differed more from P. habui at the sympatric sites than between allopatric sites, suggesting reproductive character displacement. Pterostichus thunbergi, which likely arrived in P. habui habitat in small numbers, would have experienced stronger selection pressures than P. habui.     

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.     

Reproductive character displacement and speciation in periodical cicadas, with description of new species, 13-year Magicicada neotredecem

Abstract. Acoustic mate-attracting signals of related sympatric, synchronic species are always distinguishable, but those of related allopatric species sometimes are not, thus suggesting that such signals may evolve to "reinforce" premating species isolation when similar species become sympatric. This hypothesis predicts divergences restricted to regions of sympatry in partially overlapping species, but such "reproductive character displacement" has rarely been confirmed. We report such a case in the acoustic signals of a previously unrecognized 13-year periodical cicada species, Magicicada neotredecim , described here as a new species (see Appendix). Where M. neotredecim overlaps M. tredecim in the central United States, the dominant male call pitch (frequency) of M. neotredecim increases from approximately 1.4 kHz to 1.7 kHz, whereas that of M. tredecim remains comparatively stable. The average preferences of female M. neotredecim for call pitch show a similar geographic pattern, changing with the call pitch of conspecific males. Magicicada neotredecim differs from 13-year M. tredecim in abdomen coloration, mitochondrial DNA, and call pitch, but is not consistently distinguishable from 17-year M. septendecim ; thus, like other Magicicada species, M. neotredecim appears most closely related to a geographically adjacent counterpart with the alternative life cycle. Speciation in Magicicada may be facilitated by life-cycle changes that create temporal isolation, and reinforcement could play a role by fostering divergence in premating signals prior to speciation. We present two theories of Magicicada speciation by life-cycle evolution: "nurse-brood facilitation" and "life-cycle canalization."     

Positive feedback between ecological and reproductive character displacement in a young avian hybrid zone

Character displacement can reduce costly interspecific interactions between young species. We investigated the mechanisms behind divergence in three key traits-breeding habitat choice, timing of breeding, and plumage coloration-in Ficedula flycatchers. We found that male pied flycatchers became expelled from the preferred deciduous habitat into mixed forest as the superior competitor, collared flycatchers, increased in numbers. The peak in food abundance differs between habitats, and the spatial segregation was paralleled by an increased divergence in timing of breeding between the two species. Male pied flycatchers vary from brown to black with brown coloration being more frequent in sympatry with collared flycatchers, a pattern often proposed to result from selection against hybridization, that is, reinforcement. In contrast to this view, we show that brown male pied flycatchers more often hybridize than black males. Male pied flycatcher plumage coloration influenced the territory obtained in areas of co-occurrence with collared flycatchers, and brown male pied flycatchers experienced higher relative fitness than black males when faced with heterospecific competition. We suggest that allopatric divergence in resource defense ability causes a feedback loop at secondary contact where male pied flycatchers with the most divergent strategy compared to collared flycatchers are favored by selection.     

Reproductive character displacement in the acoustic communication system of green tree frogs (Hyla cinerea)

Abstract Interactions between species can affect the evolution of their sexual signals, receiver selectivity, or both. One commonly expected outcome is reproductive character displacement, whereby adverse consequences of mismating select for greater differentiation of communication systems in areas of sympatry than in areas of allopatry. We found evidence of reproductive character displacement in the acoustic communication system of green tree frogs ( Hyla cinerea ). The strength of female preferences for the spectral properties of calls that distinguish conspecific calls from those of a closely related congener, H. gratiosa , was greater in areas of sympatry with H. gratiosa than in areas of allopatry. We also found subtle differences in advertisement calls and in the heights of male calling perches when we restricted our comparisons to localities in which H. gratiosa was also breeding (syntopy) with localities where this species was absent. Hyla cinerea and H. gratiosa show only weak genetic incompatibility, but the calls representative of interspecific hybrids were unattractive to females of both parental species. Hybrids might also be at an ecological disadvantage because of different habitat preferences of the two taxa. Thus, selection against production of less fit or less attractive hybrid or backcross offspring are probably the main causes responsible for the differences documented in this paper.     

Reproductive character displacement and potential underlying drivers in a species‐rich and florally diverse lineage of tropical angiosperms (Ruellia; Acanthaceae)

Reproductive character displacement is a pattern whereby sympatric lineages diverge more in reproductive character morphology than allopatric lineages. This pattern has been observed in many plant species, but comparably few have sought to disentangle underlying mechanisms. Here, in a diverse lineage of Neotropical plants (Ruellia; Acanthaceae), we present evidence of reproductive character displacement in a macroevolutionary framework (i.e., among species) and document mechanistic underpinnings. In a series of interspecific hand pollinations in a controlled glasshouse environment, we found that crosses between species that differed more in overall flower size, particularly in style length, were significantly less likely to produce viable seeds. Further, species pairs that failed to set seed were more likely to have sympatric distributions in nature. Competition for pollinators and reinforcement to avoid costly interspecific mating could both result in these patterns and are not mutually exclusive processes. Our results add to growing evidence that reproductive character displacement contributes to exceptional floral diversity of angiosperms.     

Ecological and community-wide character displacement: the next generation

Ecological character displacement, mostly seen as increased differences of size in sympatry between closely‐related or similar species, is a focal hypothesis assuming that species too similar to one another could not coexist without diverging, owing to interspecific competition. Thus, ecological character displacement and community‐wide character displacement (overdispersion in size of potential competitors within ecological guilds) were at the heart of the debate regarding the role of competition in structuring ecological communities. The debate has focused on the evidence presented in earlier studies and generated a new generation of rigorous, critical studies of communities. Character displacement research in the past two decades provides sound statistical support for the hypothesis in a wide variety of taxa, albeit with a phylogenetically skewed representation. A growing number of studies are strongly based in functional morphology, and some also demonstrate actual morphologically related resource partitioning. Phylogenetic models and experimental work have added to the scope and depth of earlier research, as have theoretical studies. However, many challenging ecological and evolutionary issues, regarding both selective forces (at the inter‐ and intraspecific level) and resultant patterns, remain to be addressed. Ecological character displacement and community‐wide character displacement are here to stay as the focus of much exciting research.     

Reconstructing asymmetrical reproductive character displacement in a periodical cicada contact zone

Selection against costly reproductive interactions can lead to reproductive character displacement (RCD). We use information from patterns of displacement and inferences about predisplacement character states to investigate causes of RCD in periodical cicadas. The 13-year periodical cicada Magicicada neotredecim exhibits RCD and strong reproductive isolation in sympatry with a closely related 13-year species, Magicicada tredecim. Displacement is asymmetrical, because no corresponding pattern of character displacement exists within M. tredecim. Results from playback and hybridization experiments strongly suggest that sexual interactions between members of these species were possible at initial contact. Given these patterns, we evaluate potential sources of selection for displacement. One possible source is 'acoustical interference', or mate-location inefficiencies caused by the presence of heterospecifics. Acoustical interference combined with the species-specificity of song pitch and preference appears to predict the observed asymmetrical pattern of RCD in Magicicada. However, acoustical interference does not appear to be a complete explanation for displacement in Magicicada, because our experiments suggest a significant potential for direct sexual interactions between these species before displacement. Another possible source of selection for displacement is hybrid failure. We evaluate the attractiveness of inferred hybrid mating signals, and we examine the viability of hybrid eggs. Neither of these shows strong evidence of hybrid inferiority. We conclude by presenting a model of hybrid failure related to life cycle differences in Magicicada.     

Fine‐scale geographic patterns of gene flow and reproductive character displacement in Drosophila subquinaria and Drosophila recens

When two species are incompletely isolated, strengthening premating isolation barriers in response to the production of low fitness hybrids may complete the speciation process. Here, we use the sister species Drosophila subquinaria and Drosophila recens to study the conditions under which this reinforcement of species boundaries occurs in natural populations. We first extend the region of known sympatry between these species, and then we conduct a fine‐scale geographic survey of mate discrimination coupled with estimates of gene flow within and admixture between species. Within D. subquinaria, reinforcement is extremely effective: we find variation in mate discrimination both against D. recens males and against conspecific allopatric males on the scale of a few kilometres and in the face of gene flow both from conspecific populations and introgression from D. recens. In D. recens, we do not find evidence for increased mate discrimination in sympatry, even where D. recens is rare, consistent with substantial gene flow throughout the species’ range. Finally, we find that introgression between species is asymmetric, with more from D. recens into D. subquinaria than vice versa. Within each species, admixture is highest in the geographic region where it is rare relative to the other species, suggesting that when hybrids are produced they are of low fitness. In sum, reinforcement within D. subquinaria is effective at maintaining species boundaries, but even when reinforcing selection is strong it may not always result in a pattern of strong reproductive character displacement due to variation in the frequency of hybridization and gene flow from neighbouring populations.     

Character displacement and the evolution of mate choice: an artificial neural network approach

Interactions with heterospecifics can promote the evolution of divergent mating behaviours between populations that do and do not occur with heterospecifics. This process--reproductive character displacement--potentially results from selection to minimize the risk of mating with heterospecifics. We sought to determine whether heterospecific interactions lead to divergence of female preferences for aspects of conspecific male signals. We used artificial neural network models to simulate a mate recognition system in which females co-occur with different heterospecifics in different populations. Populations that evolved conspecific recognition in the presence of different heterospecifics varied in their preferences for aspects of conspecific male signals. When we tested networks for their preferences of conspecific versus heterospecific signals, however, we found that networks from allopatric populations were usually able to select against heterospecifics. We suggest that female preferences for aspects of conspecific male signals can result in a concomitant reduction in the likelihood that females will mate with heterospecifics. Consequently, even females in allopatry may discriminate against heterospecific mates depending on the nature of their preferences for conspecifics. Such a pattern could potentially explain cases where reproductive character displacement is expected, but not observed.     

Effects of cuticle structure and crystalline wax coverage on the coloration in young and old males of Calopteryx splendens and Calopteryx virgo

Male secondary sexual characters, such as color patterns, are often investigated at the macroscale level. However, micro- and nanoscale levels of morphological investigations may reveal functional features responsible for a particular coloration, thus providing more information, e.g., about the condition dependence of male sexual characters. The aim of this paper was to investigate cuticle color and its structure in males of two congeneric damselfly species, Calopteryx splendens and Calopteryx virgo, and reveal possible color changes with age. According to spectrometer measurements, C. splendens males were bluer and had a greater saturation of blue in their abdomen than C. virgo males, which were, in turn, greener and had more green saturation. Although the two species differed in the number of structural layers and the spacing of the layers, it seems that intactness of the wax crystals covering the epicuticle was most often the morphological trait which was related to the color parameters measured from males’ cuticles. The effect of the crystalline wax coverage on cuticle color was also confirmed by removing the wax using chloroform: after the treatment, the hue was bluer, the cuticle had a greater brightness and greater blue saturation, but less green saturation. Age differences influencing the color and structure of the cuticle were also observed: older males had more blue and green saturation and had more intact wax coverage than did younger males. Although multilayer reflection should be responsible for the iridescent color of males, our results suggest that wax coverage plays an important role in the color tuning of the male cuticle. This may have a considerable signal function, indicating the males’ viability to competing males or to females.