The evolution of wing color: male mate choice opposes adaptive wing color divergence in Colias butterflies

Abstract Correlated evolution of mate signals and mate preference may be constrained if selection pressures acting on mate preference differ from those acting on mate signals. In particular, opposing selection pressures may act on mate preference and signals when traits have sexual as well as nonsexual functions. In the butterfly Colias philodice eriphyle , divergent selection on wing color across an elevational gradient in response to the thermal environment has led to increasing wing melanization at higher elevations. Wing color is also a long-range signal used by males in mate searching. We conducted experiments to test whether sexual selection on wing melanization via male mate choice acts in the same direction as natural selection on mate signals due to the thermal environment. We performed controlled mate choice experiments in the field over an elevational range of 1500 meters using decoy butterflies with different melanization levels. Also, we obtained a more direct estimate of the relation between wing color and sexual selection by measuring mating success in wild-caught females. Both our experiments showed that wing melanization is an important determinant of female mating success in C. p. eriphyle . However, a lack of elevational variation in male mate preference prevents coevolution of mate signals and mate preference, as males at all elevations prefer less-melanized females. We suggest that this apparently maladaptive mate choice may be maintained by differences in detectability between the morphs or by preservation of species recognition.     

The roles of wing color pattern and geography in the evolution of Neotropical Preponini butterflies

Diversification rates and evolutionary trajectories are known to be influenced by phenotypic traits and the geographic history of the landscapes that organisms inhabit. One of the most conspicuous traits in butterflies is their wing color pattern, which has been shown to be important in speciation. The evolution of many taxa in the Neotropics has also been influenced by major geological events. Using a dated, species‐level molecular phylogenetic hypothesis for Preponini, a colorful Neotropical butterfly tribe, we evaluated whether diversification rates were constant or varied through time, and how they were influenced by color pattern evolution and biogeographical events. We found that Preponini originated approximately 28 million years ago and that diversification has increased through time consistent with major periods of Andean uplift. Even though some clades show evolutionarily rapid transitions in coloration, contrary to our expectations, these shifts were not correlated with shifts in diversification. Involvement in mimicry with other butterfly groups might explain the rapid changes in dorsal color patterns in this tribe, but such changes have not increased species diversification in this group. However, we found evidence for an influence of major Miocene and Pliocene geological events on the tribe''s evolution. Preponini apparently originated within South America, and range evolution has since been dynamic, congruent with Andean geologic activity, closure of the Panama Isthmus, and Miocene climate variability.     

Specificity of acoustic signals and mate choice in the brown planthopper Nilaparvata lugens

Mate choice experiments were made between populations of N. lugens from the Philippines, Solomon Is. and northern Australia. Significant barriers to mating were found between the Australian insects and the other two populations. The acoustic signals of successful males in hybridisation experiments were recorded and their pulse repetition frequencies (PRFs) were compared with the mean PRF for a random sample from their own population. In crosses between insects from Australia and the Philippines or Solomon Is. succesful males were characterised by PRFs significantly different from their own populations and closer to those of the female populations in each cross than to their own. It is concluded that PRF of male calls is an important species recognition signal in N. lugens.

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Résumé La communication sexuelle de N. lugens s'effectue par signaux acoustiques transmis par le substrat. Quelques populations géographiquement définissables diffèrent par la fréquence des répétitions des impulsions (PRF) produits par les appels des mâles. Des populations des Philippines, des Iles Salomon et de l'Australie du Nord ont été étudiées.Des expériences de sélection sexuelle ont montré que des obstacles au transfert de spermatozoïdes apparaissaient dans les croisements qui impliquent un parent originaire de la population australienne. Des expériences dhybridation ont été répétées entre individus males et females de chacune des 3 populations étudiées. Le taux de succès étrait faible quand l'un des parents était originaire d'Australie. Le PRF des males de chaque croisement réussi a été déterminé et comparé au PRF moyen d'un échantillon constitué au hasard de males provenant de la même population. Pour les croisements impliquant un parent australien, le PRF des males victorieux différait de la moyenne et se rapprochait de celui des males de la population dont dérivait la female.On en a conclu que le PRF des appels males est important dans la reconnaissance spécifique de N. lugens, mais que chaque population montre un polymorphisme important pour ce caractère.

     

Hybridization and transgressive exploration of colour pattern and wing morphology in Heliconius butterflies

Hybridization can generate novel phenotypes distinct from those of parental lineages, a phenomenon known as transgressive trait variation. Transgressive phenotypes might negatively or positively affect hybrid fitness, and increase available variation. Closely related species of Heliconius butterflies regularly produce hybrids in nature, and hybridization is thought to play a role in the diversification of novel wing colour patterns despite strong stabilizing selection due to interspecific mimicry. Here, we studied wing phenotypes in first‐ and second‐generation hybrids produced by controlled crosses between either two co‐mimetic species of Heliconius or between two nonmimetic species. We quantified wing size, shape and colour pattern variation and asked whether hybrids displayed transgressive wing phenotypes. Discrete traits underlain by major‐effect loci, such as the presence or absence of colour patches, generate novel phenotypes. For quantitative traits, such as wing shape or subtle colour pattern characters, hybrids only exceed the parental range in specific dimensions of the morphological space. Overall, our study addresses some of the challenges in defining and measuring phenotypic transgression for multivariate traits and our data suggest that the extent to which transgressive trait variation in hybrids contributes to phenotypic diversity depends on the complexity and the genetic architecture of the traits.     

Genetic control and evolution of acoustic signals in planthoppers (Homoptera: Delphacidae)

Acoustic signals are part of the specific mate recognition system of planthoppers. The genetic control of acoustic signal characters was studied in the planthopperRibautodelphax imitans. Artificial selection for interpulse interval in the female call revealed a large additive genetic component for this polygenic character. Other female call characters showed a correlated response. Some male call characters also appeared to be genetically correlated with the female character selected for, despite the rather different structure of male and female calls. Parent-offspring regression provided significant heritability estimates for those male call characters that also responded to artificial selection in the female call, one of which appeared to be influenced by sex-linked genes. It is argued that the differentiation of this mate recognition system in planthopper populations and species could be the result of founder effects, enabled by the genetic plasticity of the call characters and the existence of a wing length dimorphism in these animals.     

Character displacement from the receiver's perspective: species and mate recognition despite convergent signals in suboscine birds

Many social animals use long-distance signals to attract mates and defend territories. They face the twin challenges of discriminating between species to identify conspecific mates, and between individuals to recognize collaborators and competitors. It is therefore often assumed that long-distance signals are under strong selection for species-specificity and individual distinctiveness, and that this will drive character displacement when closely related species meet, particularly in noisy environments. However, the occurrence of signal stereotypy and convergence in rainforest species seems to contradict these ideas, and raises the question of whether receivers in these systems can recognize species or individuals by long-distance signals alone. Here, we test for acoustically mediated recognition in two sympatric antbird species that are known to have convergent songs. We show that male songs are stereotyped yet individually distinctive, and we use playback experiments to demonstrate that females can discriminate not only between conspecific and heterospecific males, but between mates and strangers. These findings provide clear evidence that stereotypy and convergence in male signals can be accommodated by fine tuning of perceptual abilities in female receivers, suggesting that the evolutionary forces driving divergent character displacement in animal signals are weaker than is typically assumed.     

The significance of wing pattern diversity in the Lycaenidae: mate discrimination by two recently diverged species

Closely related species of lycaenid butterflies are determinable, in part, by subtle differences in wing pattern. We found that female wing patterns can act as an effective mate‐recognition signal in some populations of two recently diverged species. In field experiments, we observed that males from a Lycaeides idas population and an alpine population of L. melissa preferentially initiate courtship with conspecific females. A morphometric study indicated that at least two wing pattern elements were important for distinguishing the two species: hindwing spots and orange crescent‐shaped pattern elements called aurorae. We deceived male L. idas into initiating courtship with computer generated paper models of heterospecific females when these pattern elements were manipulated, indicating that the wing pattern elements that define the diversity of this group can be effective mate recognition signals.     

Spots and stripes: ecology and colour pattern evolution in butterflyfishes

The incredible diversity of colour patterns in coral reef fishes has intrigued biologists for centuries. Yet, despite the many proposed explanations for this diversity in coloration, definitive tests of the role of ecological factors in shaping the evolution of particular colour pattern traits are absent. Patterns such as spots and eyespots (spots surrounded by concentric rings of contrasting colour) have often been assumed to function for predator defence by mimicking predators'' enemies'' eyes, deflecting attacks or intimidating predators, but the evolutionary processes underlying these functions have never been addressed. Striped body patterns have been suggested to serve for both social communication and predator defence, but the impact of ecological constraints remains unclear. We conducted the first comparative analysis of colour pattern diversity in butterflyfishes (Family: Chaetodontidae), fishes with conspicuous spots, eyespots and wide variation in coloration. Using a dated molecular phylogeny of 95 species (approx. 75% of the family), we tested whether spots and eyespots have evolved characteristics that are consistent with their proposed defensive function and whether the presence of spots and body stripes is linked with species'' body length, dietary complexity, habitat diversity or social behaviour. Contrary to our expectations, spots and eyespots appeared relatively recently in butterflyfish evolution and are highly evolutionarily labile, suggesting that they are unlikely to have played an important part in the evolutionary history of the group. Striped body patterns showed correlated evolution with a number of ecological factors including habitat type, sociality and dietary complexity. Our findings question the prevailing view that eyespots are an evolutionary response to predation pressure, providing a valuable counter example to the role of these markings as revealed in other taxa.     

The influence of ultraviolet reflectance differs between conspicuous aposematic signals in neotropical butterflies and poison frogs

Warning signals are often characterized by highly contrasting, distinctive, and memorable colors. Greater chromatic (hue) and achromatic (brightness) contrast have both been found to contribute to greater signal efficacy, making longwave colored signals (e.g., red and yellow), that are perceived by both chromatic and achromatic visual pathways, particularly common. Conversely, shortwave colors (e.g., blue and ultraviolet) do not contribute to luminance perception yet are also commonly found in warning signals. Our understanding of the role of UV in aposematic signals is currently incomplete as UV perception is not universal, and evidence for its utility is at best mixed. We used visual modeling to quantify how UV affects signal contrast in aposematic heliconiian butterflies and poison frogs both of which reflect UV wavelengths, occupy similar habitats, and share similar classes of predators. Previous work on butterflies has found that UV reflectance does not affect predation risk but is involved in mate choice. As the butterflies, but not the frogs, have UV‐sensitive vision, the function of UV reflectance in poison frogs is currently unknown. We found that despite showing up strongly in UV photographs, UV reflectance only appreciably affected visual contrast in the butterflies. As such, these results support the notion that although UV reflectance is associated with intraspecific communication in butterflies, it appears to be nonfunctional in frogs. Consequently, our data highlight that we should be careful when assigning a selection‐based benefit to the presence of UV reflectance.     

Specificity of sex pheromones, the role of host plant odour in the olfactory attraction of males, and mate recognition in the aphid Cryptomyzus

Abstract. Choice tests in an olfactometer showed that males of the aphid Cryptomyzus galeopsidis spent more time in the odour of conspecific females than of a sibling species or a more distantly related Cryptomyzus species, which all co-occur on red currant. Analysis of the pheromone-emissions of females showed the presence of a nepetalactol and a nepetalactone, two known aphid sex pheromone components. However, no interspecific difference in the ratio of the components ( c. 30:1) was found, and this ratio did not change as the females aged. Males were only slightly attracted by a synthetic 30:1 mixture of these two components, and in a choice test preferreď the odour of conspecific females. The sex pheromone of Cryptomyzus spp. must thus consist of more than two components, the first time this has been reported for aphids. Host plant odour did not attract males or enhance the activity of the pheromone.     

Temperature coupling of mate attraction signals and female mate preferences in four populations of Enchenopa treehopper (Hemiptera: Membracidae)

Variation in temperature can affect the expression of a variety of important fitness‐related behaviours, including those involved with mate attraction and selection, with consequences for the coordination of mating across variable environments. We examined how temperature influences the expression of male mating signals and female mate preferences—as well as the relationship between how male signals and female mate preferences change across temperatures (signal–preference temperature coupling)—in Enchenopa binotata treehoppers. These small plant‐feeding insects communicate using plantborne vibrations, and our field surveys indicate they experience significant natural variation in temperature during the mating season. We tested for signal–preference temperature coupling in four populations of E. binotata by manipulating temperature in a controlled laboratory environment. We measured the frequency of male signals—the trait for which females show strongest preference—and female peak preference—the signal frequency most preferred by females—across a range of biologically relevant temperatures (18°C–36°C). We found a strong effect of temperature on both male signals and female preferences, which generated signal–preference temperature coupling within each population. Even in a population in which male signals mismatched female preferences, the temperature coupling reinforces predicted directional selection across all temperatures. Additionally, we found similar thermal sensitivity in signals and preferences across populations even though populations varied in the mean frequency of male signals and female peak preference. Together, these results suggest that temperature variation should not affect the action of sexual selection via female choice, but rather should reinforce stabilizing selection in populations with signal–preference matches, and directional selection in those with signal–preference mismatches. Finally, we do not predict that thermal variation will disrupt the coordination of mating in this species by generating signal–preference mismatches at thermal extremes.     

Male and female contributions to behavioral isolation in darters as a function of genetic distance and color distance

Determining which reproductive isolating barriers arise first between geographically isolated lineages is critical to understanding allopatric speciation. We examined behavioral isolation among four recently diverged allopatric species in the orangethroat darter clade (Etheostoma: Ceasia). We also examined behavioral isolation between each Ceasia species and the sympatric rainbow darter Etheostoma caeruleum. We asked (1) is behavioral isolation present between allopatric Ceasia species, and how does this compare to behavioral isolation with E. caeruleum, (2) does male color distance and/or genetic distance predict behavioral isolation between species, and (3) what are the relative contributions of female choice, male choice, and male competition to behavioral isolation? We found that behavioral isolation, genetic differentiation, and male color pattern differentiation were present between allopatric Ceasia species. Males, but not females, discerned between conspecific and heterospecific mates. Males also directed more aggression toward conspecific rival males. The high levels of behavioral isolation among Ceasia species showed no obvious pattern with genetic distance or male color distance. However, when the E. caeruleum was included in the analysis, an association between male aggression and male color distance was apparent. We discuss the possibility that reinforcement between Ceasia and E. caeruleum is driving behavioral isolation among allopatric Ceasia species.     

Spatial patterns of correlated scale size and scale color in relation to color pattern elements in butterfly wings

Complex butterfly wing color patterns are coordinated throughout a wing by unknown mechanisms that provide undifferentiated immature scale cells with positional information for scale color. Because there is a reasonable level of correspondence between the color pattern element and scale size at least in Junonia orithya and Junonia oenone, a single morphogenic signal may contain positional information for both color and size. However, this color–size relationship has not been demonstrated in other species of the family Nymphalidae. Here, we investigated the distribution patterns of scale size in relation to color pattern elements on the hindwings of the peacock pansy butterfly Junonia almana, together with other nymphalid butterflies, Vanessa indica and Danaus chrysippus. In these species, we observed a general decrease in scale size from the basal to the distal areas, although the size gradient was small in D. chrysippus. Scales of dark color in color pattern elements, including eyespot black rings, parafocal elements, and submarginal bands, were larger than those of their surroundings. Within an eyespot, the largest scales were found at the focal white area, although there were exceptional cases. Similarly, ectopic eyespots that were induced by physical damage on the J. almana background area had larger scales than in the surrounding area. These results are consistent with the previous finding that scale color and size coordinate to form color pattern elements. We propose a ploidy hypothesis to explain the color–size relationship in which the putative morphogenic signal induces the polyploidization (genome amplification) of immature scale cells and that the degrees of ploidy (gene dosage) determine scale color and scale size simultaneously in butterfly wings.     

Role of visual stimuli in host and mate location of the Colorado potato beetle

Visual responses of adult male and female Colorado potato beetles CPB, Leptinotarsa decemlineata (Say) (Coleoptera, Chrysomelidae) to 10 × 20 cm coloured paper‐boards, beetle‐sized coloured beads or dead CPB, and to combinations of these in laboratory experiments in an arena of 52 cm diameter were investigated. In addition, visual discriminatory abilities of males exposed to female‐specific substances were also measured. The paths of the beetles were recorded on videotape by a computer‐aided motion detection system. Parameters of tracks were calculated and the tape‐recorded paths were further processed for behavioural analyses and for obtaining mean angular directions by circular statistics. Both sexes showed a strong preference for yellow‐black striped, yellow and light‐green boards and, to a lesser degree, were also attracted to yellow‐green, dark‐green, red and white boards, to beetle‐sized beads coloured either black or yellow‐black striped, and to some combinations of these. Males exposed to female substances immediately prior to entering the arena performed significantly more successful approaches to objects than did males of the control group. These results corroborate field observations on males' mate‐searching behaviour and increase our understanding of natural host‐ and mate‐finding processes.     

Geographical variation in acoustic signals of the planthopper, Nilaparvata bakeri (Muir), in Asia: species recognition and sexual selection

Populations of the planthopper .Nilaparvata bakeri (Muir) were sampled from the Philippines (Luzon), Indonesia (Bali), India (Bihar) and Sri Lanka (Central Province) from the grass Leersia hexandra (Schwartz), and cultured in Cardiff. Low intensity vibratory signals produced by males and females during mate location and courtship were recorded and analysed. Obvious differences were found between male calling songs of insects from the Philippines and those from the other three areas. Smaller differences were detected between the Indonesian, Indian and Sri Lankan populations. Hybrids between Philippine and Indonesian, and Indonesian and Sri Lankan, insects were obtained freely in the laboratory. Male calls of F, hybrids were variable and intermediate between parentals. Mate choice experiments showed no significant assortative mating between the different populations. There was no indication of reproductive isolation and therefore of different biological species. The assumption that different male calling songs necessarily indicate the presence of different biological species is not confirmed in this example.     

Variation in hostplant relations and courtship signals of weed-associated populations of the brown planthopper, Nilaparvata lugens (Stål), from Australia and Asia: a test of the recognition species concept

Populations of the morphological species, Nilaparvata lugens (Stål), were found to breed and feed on the grass, Leersia hexandra Schwartz, at six sites in Queensland, Australia. They differ from sympatric rice-feeding populations in characters of pulse repetition frequencies of male and female acoustic courtship signals. The two host-derived populations hybridize freely in the laboratory, but in mate choice experiments show very significant preferences for homogametic matings. No indication of field hybridization has been found, so that the two morphologically inseparable populations represent sympatric biological species in Australia.
Populations from L. hexandra are also reported from four localities in Sri Lanka and one in Orissa, India. These resemble previously studied populations from the Philippines. They differ significantly in courtship call characters, both from sympatric rice-associated populations and from allopatric Leersia -associated populations from Australia.
The geographical variation reported for acoustic signals is not consistent with Paterson's recognition concept of species, but may be interpreted in terms of theories of allopatric speciation involving sexual selection for mate recognition signals.     

Evolutionary constraints of warning signals: A genetic trade‐off between the efficacy of larval and adult warning coloration can maintain variation in signal expression

To predict evolutionary responses of warning signals under selection, we need to determine the inheritance pattern of the signals, and how they are genetically correlated with other traits contributing to fitness. Furthermore, protective coloration often undergoes remarkable changes within an individual's lifecycle, requiring us to quantify the genetic constraints of adaptive coloration across all the relevant life stages. Based on a 12 generation pedigree with > 11,000 individuals of the wood tiger moth (Arctia plantaginis), we show that high primary defense as a larva (large warning signal) results in weaker defenses as adult (less efficient warning color), due to the negative genetic correlation between the efficacy of larval and adult warning coloration. However, production of effective warning coloration as a larva did not incur any life‐history costs and was positively genetically correlated with reproductive output. These results provide novel insights into the evolutionary constraints on protective coloration in animals, and explain the maintenance of variation in the signal expression despite the strong directional selection by predators. By analyzing the genetic and environmental effects on warning signal and life‐history traits in all relevant life stages, we can accurately determine the mechanisms shaping the evolutionary responses of phenotypic traits under different selection environments.