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.     

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.     

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.     

Cues for Mate Recognition and the Effect of Prior Experience on Mate Recognition in Enallagma Damselflies

In many coenagrionid damselflies, sexually mature females exhibit color polymorphisms, with some females resembling conspecific males. Although it has been suggested that the latter function as male mimics, this does not appear to be the case for those in the genus Enallagma. We found that sexually dimorphic coloration of the female abdomen and thorax are important cues for sexual recognition by males. We demonstrate for the first time in the Odonata, that males learn to recognize andromorphs as potential mates. After 2 days in an enclosure, sexually mature males exposed to only andromorphic females initiated more sexual interactions with tethered andromorphs than with heteromorphs, the majority morph in the natural population. Exposure to only heteromorphic females tended to decrease males' sexual responses to andromorphs, but not significantly so. Because the frequency of female morphs often varies within a population, learned mate recognition would be advantageous for males that search for mates. Our results lead to a novel, frequency-dependent hypothesis for the occurrence and maintenance of female-limited color polymorphisms.     

The Impacts of Introduced Poeciliid Fish and Odonata on the Endemic Megalagrion (Odonata) Damselflies of Oahu Island, Hawaii

Since the beginning of this century there have been substantial declines in the distribution and abundance of native Megalagrion damselflies on the Hawaiian Island of Oahu. Native damselflies have also vanished from most low elevation areas on other Hawaiian Islands, although historically, lotic and wetland dwelling damselfly species were once common throughout the archipelago. It is hypothesized that poeciliid fish introduced for biological control have caused the decline of four stream-breeding damselfly species on Oahu, and the extinction or near-extinction of two other species in Hawaii. This study documents the presence of remnant Megalagrion populations in Oahu streams, wetlands and estuaries, and records the elevational distributions of introduced fish in each waterbody surveyed. The distributions of introduced Odonata are also recorded, because the seven species of damselflies and dragonflies introduced to Oahu since 1936 present another potential threat to native Hawaiian damselflies. Native damselfly and introduced poeciliid fish distributions were mutually exclusive on Oahu, and it is concluded that this is probably due to predation by the introduced fish. By contrast, even the rarest native Megalagrion damselflies were found in areas containing introduced damselflies and dragonflies.     

Limbic Neurons Shape Sex Recognition and Social Behavior in Sexually Naive Males

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Sexual Isolation Between Two Sympatric Types of the Butterfly Eurema hecabe (L.)

In Japan, the butterfly Eurema hecabe (L.) consists of two separate types. These types differ in wing fringe color (brown or yellow), which is linked with expression of seasonal wing morphs and with ability for host-plant use. It was recently found that these two types occur together on the subtropical Okinawa-jima Island (one of the Ryukyu Islands). In the present work we studied whether sexual isolation may exist between these sympatric types of E. hecabe on Okinawa-jima, using caged conditions. When living females (days 0, 1, and 7) were presented to males of the same or different type, females of the brown type received males of the same type and responded with a refusal posture to those of the yellow type. Females of the yellow type received males of the same type at all ages tested. However, when they were exposed to males of the brown type, the proportion of females showing a refusal posture changed with female age. The proportion was high at day 7 but relatively low at day 0 or day 1. When model females of the brown and yellow types were simultaneously presented to males of each type, males courted not only the model females of the same type, but also those of the different type. The results suggest that (1) sexual isolation exists between these types of E. hecabe on Okinawa-jima, although it is not perfect; (2) this isolation is mediated by female recognition but not male recognition; and (3) the sexual isolation system between two types is asymmetrical, depending on the female age after adult eclosion.     

Predator foolhardiness and morphological evolution in 17-year cicadas (Magicicada spp.)

Periodical cicadas in the genus Magicicada have an unusual life history that includes an exceptionally long life cycle and a massive, synchronized emergence. Considerable effort has been put into research aimed at understanding the evolutionary history of periodical cicadas, but surprisingly little attention has been given to their morphological evolution. Their slow flight and approachability have been described as 'predator-foolhardy' behaviour. We quantified flight speeds for M. cassini, M. septendecim, and Tibicen chloromera (a nonperiodical cicada species) , and interpreted them in terms of thorax musculature, body proportions and wing size and shape in relation to body size. On average, T. chloromera flew three to four times faster than did the two Magicicada species. Using empirical relationships between flight speed and body length, body mass or wing loading, we determined M. cassini and M. septendecim to be unusually slow fliers for their body size, whereas T. chloromera was not. The relatively slow flight speeds of Magicicada species could be largely accounted for by relatively small thoracic muscle masses, as indicated by thorax length × width measurements, and low wing loadings. Aspect ratio differences were contributing factors. Male Magicicada and female Tibicen were more active in mate searching than was the opposite sex, and correspondingly had relatively large aspect ratios. We interpret the morphological traits responsible for the slow flight of Magicicada species as being adaptations to searching for mates in dense aggregations around the canopy of trees, relatively unconstrained by the per-capita risk of predation.  © 2007 The Linnean Society of London, Biological Journal of the Linnean Society , 2007, 90 , 1–13.     

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.     

Visual Cues in Mate Recognition by Males of the Damselfly, Coenagrion puella (L.) (Odonata: Coenagrionidae)

Coenagrion puella males search actively for mates and are not aggressive to other males. To study the role of visual cues in male–female discrimination, four types of models were used: (1) bodies of intact insects, (2) models of painted males, (3) models of male–female chimerae, and (4) models of female body parts. Abdomen coloration pattern and presence of wings were the most important cues for sexual recognition by males. Step-by-step elimination of male coloration pattern leads to an increase in the tandem response rate. A female model painted as a male repelled males like the intact male model. The absence of either the head or the thorax slightly decreased the number of tandem responses, but models without both the head and the thorax were not recognized as a mate. Abdomen thickness larger than that of a normal female decreased the attractiveness of the model. Models of the gynochrome female were significantly more attractive than models of the androchrome one. Female models containing male parts were less attractive than models without any structure at this place. Using principal-components analysis, it is shown that models repelling males usually were those containing an intact male abdomen or a female abdomen painted with blue. The results indicate that C. puella males can distinguish males from females visually by morphological structures and coloration pattern.     

Song diversification and complexity in canaries and seedeaters (Serinus spp.)

Bird song is a composite trait that shows great variation in syntax and phonology between taxa, which hampers the precise quantification of complexity. This should be more feasible for closely-related species that share aspects of song organization. We conducted a comparative study of song and syllable characteristics in the largest fringillid genus, Serinus (canaries and seedeaters), with two objectives: (1) to describe and quantify song complexity in the genus and (2) to assess evolutionary dynamics of song, in particular whether interspecific song diversification evolved along intraspecific lines of covariation between syllable characteristics. We document a pattern of intense, very labile evolution of song in the genus. Well-known vocal constraints such as the relationship between frequency and body size did not appear to limit this evolution, and intraspecific trade-offs between different aspects of syllable complexity did not constrain interspecific diversification. Factor analysis returned an axis of variation that comprehensively expresses song complexity in the genus, and is defined by song speed, repertoire size, and also various aspects of syllable phonology. The species body size is not related to this axis of complexity, but to a minor axis that may indicate better respiratory capacity of larger birds. We discuss the pattern of song evolution in Serinus spp. in the context of the evolutionary dynamics of sexually selected traits.  © 2007 The Linnean Society of London, Biological Journal of the Linnean Society , 2007, 92 , 183–194.     

Effects of developmental environment on signal-preference coupling in a Hawaiian cricket

Previous work has suggested that developmental temperature influences expression of the adult male calling song of the cricket, a sexually selected mate recognition signal. The role of developmental temperature in shaping female preference functions, and thus its influence on signal-preference coupling has not been investigated. In this study, the effects of developmental temperature are examined in both males and females of the Hawaiian cricket, Laupala cerasina, to determine the degree of signal-preference matching between male song and female preference due to developmental environment. We found that rearing females in different temperature environments affected adult female acoustic preference functions in the same direction as male calling song, thereby influencing variation in adult reproductive behavior in such a way that male and female components remain coordinated. However, we further demonstrate that for male song, the effect of the rearing environment is not permanent but appears only to exert influence for a period of days. This mid-term temperature effect is distinct from the effect of short-term ambient temperature, which influences song in a matter of minutes and has been well documented. Signal-preference coordination, and sexual selection pressures due to mismatching within natural populations, likely will be influenced by nymphal developmental environments of males and females, as well as by adult singing and preference environments.     

Sex,competition and mimicry: an eco-evolutionary model reveals unexpected impacts of ecological interactions on the evolution of phenotypes in sympatry

Phenotypic evolution in sympatric species can be strongly impacted by species interactions, either mutualistic or antagonistic. Heterospecific reproductive behaviours between sympatric species have been shown to favour phenotypic divergence of traits used as sexual cues. Those traits may also be involved in local adaptation or in other types of species interactions and, as a result, undergo complex evolutions across sympatric species. Here we focus on mimicry and study how reproductive interference may impair phenotypic convergence between species with various levels of defence. We use a deterministic model assuming two sympatric species where individuals can display two different warning colour patterns. This eco-evolutionary model explores how ecological interactions shape phenotypic evolution within sympatric species. We investigate the effect of 1) the opposing density-dependent selections exerted on colour patterns by predation and reproductive behaviour and 2) the impact of relative species and phenotype abundances on the fitness costs faced by each individual depending on their species and phenotype. Our model shows that reproductive interference may limit the convergent effect of mimetic interactions and may promote phenotypic divergence between Müllerian mimics. The divergent and convergent evolution of traits also strongly depends on the relative species and phenotype abundances and levels of trophic competition, highlighting how the eco-evolutionary feedbacks between phenotypic evolution and species abundances may result in strikingly different evolutionary routes.     

Social Reversal of Sex‐Biased Aggression and Dominance in a Biparental Cichlid Fish (Julidochromis marlieri)

In biparental species, aggression, dominance, and parental care are typically sexually dimorphic. While behavioral dimorphism is often strongly linked to gonadal sex, the environment—either social or ecological—may also influence sex‐biased behavior. In the biparental cichlid fish Julidochromis marlieri, the typical social environment for breeding pairs consists of large females paired with smaller males. While both sexes are capable of providing territory defense and parental care, the larger female provides the majority of defense for the pair, while the smaller male remains in the nest guarding their offspring. We examine the contributions of sex and relative mate size to these sex‐biased behaviors in monogamous J. marlieri pairs. Both female‐larger and male‐larger pairs were formed in the laboratory and were observed for territorial aggression (against conspecifics and heterospecifics), dominance, and parental care. In female‐larger pairs, territorial aggression and intra‐pair dominance were female‐biased, while in male‐larger pairs this bias was reversed. For both pairing types, the presence of an intruder amplified sex differences in territorial aggression, with the larger fish always attacking with greater frequency than its mate. Though less robust, there was evidence for plasticity of sex‐bias for some egg care related behaviors in the inverse direction. Our study suggests that relative mate size strongly influences the sex bias of aggression and dominance in J. marlieri and that this aspect of the social environment can override the influence of gonadal sex on an individual's behavior. The remarkable plasticity of this species makes Julidochromis an exciting model that could be used to address the relationship between proximate and ultimate mechanisms of behavioral plasticity.     

The evolution of female mating preferences: differentiation from species with promiscuous males can promote speciation

Females of many species are frequently courted by promiscuous males of their own and other closely related species. Such mating interactions may impose strong selection on female mating preferences to favor trait values in conspecific males that allow females to discriminate them from their heterospecific rivals. We explore the consequences of such selection in models of the evolution of female mating preferences when females must interact with heterospecific males from which they are completely postreproductively isolated. Specifically, we allow the values of both the most preferred male trait and the tolerance of females for males that deviate from this most preferred trait to evolve. Also, we consider situations in which females base their mating decisions on multiple male traits and must interact with males of multiple species. Females will rapidly differentiate in preference when they sometimes mistake heterospecific males for suitable mates, and the differentiation of female preference will select for conspecific male traits to differentiate as well. In most circumstances, this differentiation continues indefinitely, but slows substantially once females are differentiated enough to make mistakes rare. Populations of females with broader preference functions (i.e., broader tolerance for males with trait values that deviate from females' most preferred values) will evolve further to differentiate if the shape of the function cannot evolve. Also, the magnitude of separation that evolves is larger and achieved faster when conspecific males have lower relative abundance. The direction of differentiation is also very sensitive to initial conditions if females base their mate choices on multiple male traits. We discuss how these selection pressures on female mate choice may lead to speciation by generating differentiation among populations of a progenitor species that experiences different assemblages of heterospecifics. Opportunities for differentiation increase as the number of traits involved in mate choice increase and as the number of species involved increases. We suggest that this mode of speciation may have been particularly prevalent in response to the cycles of climatic change throughout the Quaternary that forced the assembly and disassembly of entire communities on a continentwide basis.     

The evolution of courtship display repertoire size in the dabbling ducks (Anatini)

Many animals possess multiple ornaments or behaviours that seem to have evolved via sexual selection. A complete understanding of sexual selection requires an explanation for such multiple traits. The dabbling ducks (Tribe: Anatini) exhibit considerable variation among species in the number of displays in the male courtship repertoire. I tested five hypotheses concerning the evolution of the variation in display repertoire size of dabbling ducks: (1) species recognition, (2) courtship habitat, (3) sexual selection intensity, (4) display media tradeoff and (5) time constraints on pair formation. I tested these hypotheses, using an explicit phylogenetic hypothesis developed from DNA sequences for the dabbling ducks, with two types of statistical comparative methods (discrete and continuous character). The variation observed in male courtship display repertoire size in dabbling ducks was consistent with the courtship habitat and sexual selection intensity hypotheses. Specifically, the size of the display repertoire was larger in species that exhibit courtship exclusively on water and larger in species with dimorphic plumage. These results suggest that ecological (habitat) as well as social (sexual selection) factors may be important in driving the evolution of displays in the dabbling ducks.     

Evolution of territoriality in Hylinae treefrogs: Ecological and morphological correlates and lineage diversification

Given the diverse nature of traits involved in territorial defence, they may respond to different selective pressures and then exhibit distinct patterns of evolution. These selective pressures also may cause territorial behaviour to be associated with environmental and morphological variables. Such associations, however, have mostly been studied at the intraspecific level, being phylogenetic analyses of territoriality in a broad taxonomic framework rare in the literature. We used the anuran subfamily Hylinae to test (1) whether two territorial-behaviour traits with different levels of aggression—territorial call and physical combat—are evolutionarily more labile than a morphological trait used in physical combat—the spine-shaped prepollex; (2) whether reproduction in lentic waters and phytotelmata, as well as resource scarcity, might favour the occurrence of territoriality; (3) if physical combat is more important than territorial call for the evolution of body size and sexual size dimorphism and (4) the relationships between territorial-behaviour traits and lineage diversification. We mainly used the literature to build two datasets with different levels of certainty. Territorial-behaviour traits exhibited intermediate levels of phylogenetic signal in Hylinae, whereas the phylogenetic signal for the presence of the spine-shaped prepollex was strong. We found support for the hypothesis that reproduction in lentic water favours the occurrence of territorial behaviour, because the expression of territorial-behaviour traits was more associated with reproduction in lentic than in lotic waters. Territorial-behaviour traits were not correlated with annual precipitation nor with habitat complexity. Body size and sexual size dimorphism were not correlated with the presence of territorial call nor with physical combat. We identified negative correlations between diversification rates and physical combat. Relationships of territorial call and physical combat with diversification rates suggest that these territorial behaviours influence evolutionary processes in different ways.     

Antler size and fluctuating asymmetry in red deer (Cervus elaphus) stags and probability of becoming a harem holder in rut

Red deer hinds play a significant role in selecting stags for mating. We tested the hypotheses that in red deer ( Cervus elaphus ) the probability of becoming a harem holder (and hence achieving reproductive success) occurs in stags bearing larger, branched antlers and showing low fluctuating asymmetry (FA). Eleven antler characteristics were measured; absolute and relative FA were calculated on 51 cast antler sets from 19 individually recognized stags. Probability of becoming a harem holder (PBHH) was originally analysed separately, i.e. for antler size and FA of each antler characteristic and calculated factors for both antler size and FA. If analysed separately, large antler size and low relative but high absolute FA increased PBHH. When we combined antler size and FA of antler characteristics in one model using antler size and FA factors, however, PBHH and achieving reproductive success were mainly dependent on increasing antler size and enhanced antler branching rather than on FA. We conclude that in contrast to antler size, FA is unlikely to play any significant role in sexual selection as an indicator of individual quality.  © 2006 The Linnean Society of London, Biological Journal of the Linnean Society , 2006, 87 , 59–68.