Christopher N. Anderson

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.

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 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.

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.

Sexual selection in Hetaerina titia males: a possible key species to understand the evolution of pigmentation in calopterygid damselflies (Odonata: Zygoptera)

Hetaerina titia males bear wing pigmentation patterns similar to Hetaerina and Calopteryx (a derived sister genus of Hetaerina) species: black (typical of Calopteryx) and red (typical of Hetaerina). Sexual selection has operated on red (via male-male competition) and black (via male-male competition and female choice) in Hetaerina and Calopteryx, respectively. We investigated sexual behavior and pigmentation in H. titia to understand their evolution in both genera using H. titia as a possible evolutionary transitional stage. Similar to Calopteryx, the black pigmentation correlated with five male quality aspects: defending a territory, survival, immune ability, parasite resistance and fat reserves. We hypothesize that black pigmentation, but not red, may be used to signal energetic condition when males compete for a territory. The red pigmentation, despite indicating male quality in Hetaerina species, did not correlate with quality but showed a positive relation with parasite burden. These results suggest that the red lost its function which was gained by the black pigmentation, possibly via intrasexual competition, in the absence of female choice (as H. titia does not show male pre-copulatory courtship as in Calopteryx, during which females choose males based on black pigmentation). It is unknown why the red pigmentation was retained.

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.

An assessment of marking techniques for odonates in the family Calopterygidae

Author(s): Anderson, Christopher N; Cordoba-Aguilar, Alex; Drury, Jonathan P; Grether, Gregory F

Seasonal polyphenism in wing coloration affects species recognition in rubyspot damselflies (Hetaerina spp.)

Understanding how phenotypic plasticity evolves and in turn affects the course of evolution is a major challenge in modern biology. By definition, biological species are reproductively isolated, but many animals fail to distinguish between conspecifics and closely related heterospecifics. In some cases, phenotypic plasticity may interfere with species recognition. Here, we document a seasonal polyphenism in the degree of dark wing pigmentation in smoky rubyspot damselflies (Hetaerina titia) – a shift so pronounced that it led early researchers to classify different forms of H. titia as separate species. We further show how the seasonal colour shift impacts species recognition with the sympatric congener Hetaerina occisa. Interspecific aggression (territorial fights) and reproductive interference (mating attempts) are much more frequent early in the year, when H. titia more closely resembles H. occisa, compared to later in the year when the dark phase of H. titia predominates. Using wing colour manipulations of tethered damselflies, we show that the seasonal changes in interspecific interactions are caused not only by the seasonal colour shift but also by shifts in discriminatory behaviour in both species. We also experimentally tested and rejected the hypothesis that learning underlies the behavioural shifts in H. occisa. An alternative hypothesis, which remains to be tested, is that the seasonal polyphenism in H. titia wing coloration has resulted in the evolution of a corresponding seasonal polyphenism in species recognition in H. occisa. This study illustrates one of the many possible ways that plasticity in species recognition cues may influence the evolution of interspecific interactions.

Characterization of 12 microsatellite loci in the waterfall damselfly (Paraphlebia zoe) for use in population genetic applications

The waterfall damselfly, Paraphelbia zoe, is distributed in cloud forest areas in the Mexican states of Veracruz, Hidalgo, and San Luis Potosi. We developed twelve microsatellite loci for P. zoe from representative samples from the state of Veracruz. Microsatellites were tested for polymorphism on a panel of 24 individuals. The number of alleles ranged from 3 to 11, observed heterozygosity from 0.083 to 0.875, and the fixation index from 0.021 to 0.563. These loci are the first to be described and characterized for P. zoe and should prove useful for population genetics in support of the conservation of this vulnerable species.

Characterization of novel microsatellite loci for Hetaerina americana damselflies, and cross-amplification in other species

Hetaerina damselflies are distributed throughout the neotropics. We developed eleven microsatellite loci for the damselfly Hetaerina americana. Microsatellites were tested for polymorphism on a panel of 24 individuals. The number of alleles ranged from 2 to 6, observed heterozygosity from 0.080 to 0.701, and the fixation index from −0.266 to 1.000. Cross-amplification was tested in 7 different species in the genus Hetaerina from the United States and Mexico. These microsatellite loci will be useful for studies of population structure and gene flow in H. americana.