Insect mating signal and mate preference phenotypes covary among host plant genotypes

Sexual selection acting on small initial differences in mating signals and mate preferences can enhance signal–preference codivergence and reproductive isolation during speciation. However, the origin of initial differences in sexual traits remains unclear. We asked whether biotic environments, a source of variation in sexual traits, may provide a general solution to this problem. Specifically, we asked whether genetic variation in biotic environments provided by host plants can result in signal–preference phenotypic covariance in a host‐specific, plant‐feeding insect. We used a member of the Enchenopa binotata species complex of treehoppers (Hemiptera: Membracidae) to assess patterns of variation in male mating signals and female mate preferences induced by genetic variation in host plants. We employed a novel implementation of a quantitative genetics method, rearing field‐collected treehoppers on a sample of naturally occurring replicated host plant clone lines. We found remarkably high signal–preference covariance among host plant genotypes. Thus, genetic variation in biotic environments influences the sexual phenotypes of organisms living on those environments in a way that promotes assortative mating among environments. This consequence arises from conditions likely to be common in nature (phenotypic plasticity and variation in biotic environments). It therefore offers a general answer to how divergent sexual selection may begin.     

Consumer trait variation influences tritrophic interactions in salt marsh communities

The importance of intraspecific variation has emerged as a key question in community ecology, helping to bridge the gap between ecology and evolution. Although much of this work has focused on plant species, recent syntheses have highlighted the prevalence and potential importance of morphological, behavioral, and life history variation within animals for ecological and evolutionary processes. Many small‐bodied consumers live on the plant that they consume, often resulting in host plant‐associated trait variation within and across consumer species. Given the central position of consumer species within tritrophic food webs, such consumer trait variation may play a particularly important role in mediating trophic dynamics, including trophic cascades. In this study, we used a series of field surveys and laboratory experiments to document intraspecific trait variation in a key consumer species, the marsh periwinkle Littoraria irrorata, based on its host plant species (Spartina alterniflora or Juncus roemerianus) in a mixed species assemblage. We then conducted a 12‐week mesocosm experiment to examine the effects of Littoraria trait variation on plant community structure and dynamics in a tritrophic salt marsh food web. Littoraria from different host plant species varied across a suite of morphological and behavioral traits. These consumer trait differences interacted with plant community composition and predator presence to affect overall plant stem height, as well as differentially alter the density and biomass of the two key plant species in this system. Whether due to genetic differences or phenotypic plasticity, trait differences between consumer types had significant ecological consequences for the tritrophic marsh food web over seasonal time scales. By altering the cascading effects of the top predator on plant community structure and dynamics, consumer differences may generate a feedback over longer time scales, which in turn influences the degree of trait divergence in subsequent consumer populations.     

Phenotypic Plasticity and Repeatability in the Mating Signals of Enchenopa Treehoppers, with Implications for Reduced Gene Flow among Host-Shifted Populations

Mate signaling systems, because of their role in assortative mating, have often been implicated in the origins of evolutionary independence between lineages. We investigated three sources of phenotypic plasticity in mating signals with potential relevance to assortative mating in a species in the Enchenopa binotata complex of treehoppers. This group has been a model for speciation in sympatry through shifts to novel host plants. Host shifts result in partial reproductive isolation in Enchenopa binotata because of their effects on life history timing, but interbreeding is still possible if there is dispersal and some overlap of mating periods. Courtship in these plant‐feeding insects is mediated by plant‐borne vibrational signals. We asked whether variation in male mate signaling behavior is influenced by plant substrate, age, or size, each of which may play a role in interactions among host‐shifted populations. Males produced fewer, shorter signals when on non‐hosts than when on hosts. However, there were no effects of age or size on signal variation. Significant repeatability of some signal features (carrier frequency and the number of signals produced in a signaling bout) is consistent with the presence of genetic variation and thus the potential to respond to selection. Our results suggest that plasticity in mate signaling systems, and in particular in male mate searching behavior on hosts and non‐hosts, may have the potential to reduce interbreeding between populations that use different species of host plant.     

Geographic variation and the evolution of song in Mesoamerican rufous‐naped wrens Campylorhynchus rufinucha

Speciation may be influenced by geographic variation in animal signals, particularly when those signals are important in reproductive decisions. Here, we describe patterns of geographic variation in the song of rufous‐naped wrens Campylorhynchus rufinucha. This species complex is a morphologically variable taxon confined to tropical dry forest areas from Mexico to northwestern Costa Rica. Morphological and genetic analyses suggest that there are at least three partially isolated groups within the complex, including a secondary‐contact zone in coastal western Chiapas between the subspecies C. r. humilus and C. r. nigricaudatus. Based on recordings throughout their geographic range, we investigate the effects of historical isolation on song structure and analyze whether genetic differences or climatic conditions explain observed patterns of variation. Our findings, based on a culturally‐transmitted and sexually‐selected trait, support the hypothesis that three evolutionary units exist within this taxon. Our results suggest that song differences between genetic groups were influenced by historical isolation. We report a strong relationship between vocal dissimilarity and genetic distance, suggesting that differences in vocal characteristics are probably affected by the same factors that drive genetic divergence. We argue that the evolution of song in this taxon is influenced by vicariant events, followed by accumulation of changes in song structure due to several possible factors: cultural drift in song structure; genetic drift in features related to song production; or natural selection acting on features that influence songs, such as body and beak size.     

Local‐ to continental‐scale variation in the richness and composition of an aquatic food web

Aim We investigated patterns of species richness and composition of the aquatic food web found in the liquid‐filled leaves of the North American purple pitcher plant, Sarracenia purpurea (Sarraceniaceae), from local to continental scales. Location We sampled 20 pitcher‐plant communities at each of 39 sites spanning the geographic range of S. purpurea– from northern Florida to Newfoundland and westward to eastern British Columbia. Methods Environmental predictors of variation in species composition and species richness were measured at two different spatial scales: among pitchers within sites and among sites. Hierarchical Bayesian models were used to examine correlates and similarities of species richness and abundance within and among sites. Results Ninety‐two taxa of arthropods, protozoa and bacteria were identified in the 780 pitcher samples. The variation in the species composition of this multi‐trophic level community across the broad geographic range of the host plant was lower than the variation among pitchers within host‐plant populations. Variation among food webs in richness and composition was related to climate, pore‐water chemistry, pitcher‐plant morphology and leaf age. Variation in the abundance of the five most common invertebrates was also strongly related to pitcher morphology and site‐specific climatic and other environmental variables. Main conclusions The surprising result that these communities are more variable within their host‐plant populations than across North America suggests that the food web in S. purpurea leaves consists of two groups of species: (1) a core group of mostly obligate pitcher‐plant residents that have evolved strong requirements for the host plant and that co‐occur consistently across North America, and (2) a larger set of relatively uncommon, generalist taxa that co‐occur patchily.     

Genetic variation in a host-parasite association: potential for coevolution and frequency-dependent selection

Abstract.— Models of host‐parasite coevolution assume the presence of genetic variation for host resistance and parasite infectivity, as well as genotype‐specific interactions. We used the freshwater crustacean Daphnia magna and its bacterial microparasite Pasteuria ramosa to study genetic variation for host susceptibility and parasite infectivity within each of two populations. We sought to answer the following questions: Do host clones differ in their susceptibility to parasite isolates? Do parasite isolates differ in their ability to infect different host clones? Are there host clone‐parasite isolate interactions? The analysis revealed considerable variation in both host resistance and parasite infectivity. There were significant host clone‐parasite isolate interactions, such that there was no single host clone that was superior to all other clones in the resistance to every parasite isolate. Likewise, there was no parasite isolate that was superior to all other isolates in infectivity to every host clone. This form of host clone‐parasite isolate interaction indicates the potential for coevolution based on frequency‐dependent selection. Infection success of original host clone‐parasite isolate combinations (i.e., those combinations that were isolated together) was significantly higher than infection success of novel host clone‐parasite isolate combinations (i.e., those combinations that were created in the laboratory). This finding is consistent with the idea that parasites track specific host genotypes under natural conditions. In addition, correspondence analysis revealed that some host clones, although distinguishable with neutral genetic markers, were susceptible to the same set of parasite isolates and thus probably shared resistance genes.     

The evolution of novel host use is unlikely to be constrained by trade‐offs or a lack of genetic variation

The genetic and ecological factors that shape the evolution of animal diets remain poorly understood. For herbivorous insects, the expectation has been that trade‐offs exist, such that adaptation to one host plant reduces performance on other potential hosts. We investigated the genetic architecture of alternative host use by rearing individual Lycaeides melissa butterflies from two wild populations in a crossed design on two hosts (one native and one introduced) and analysing the genetic basis of differences in performance using genomic approaches. Survival during the experiment was highest when butterfly larvae were reared on their natal host plant, consistent with local adaptation. However, cross‐host correlations in performance among families (within populations) were not different from zero. We found that L. melissa populations possess genetic variation for larval performance and variation in performance had a polygenic basis. We documented very few genetic variants with trade‐offs that would inherently constrain diet breadth by preventing the optimization of performance across hosts. Instead, most genetic variants that affected performance on one host had little to no effect on the other host. In total, these results suggest that genetic trade‐offs are not the primary cause of dietary specialization in L. melissa butterflies.     

Effects of plant sex on insect abundance across three trophic levels in the perennial shrub Buddleja cordata

Although there is a growing interest in the effects of intra‐specific plant genetic variation on species interactions, the effects of plant sex, an important axis of genetic variation, have been less studied. In addition, previous work investigating plant sex effects on species interactions has frequently focused on bitrophic interactions (e.g., herbivory), usually ignoring plant sex effects on higher trophic levels (i.e., natural enemies). Here, we investigated the effects of plant sex on herbivore abundance and that of their natural enemies associated with the dioecious shrub Buddleja cordata Kunth (Scrophulariaceae). Furthermore, we measured a subset of plant traits frequently involved in herbivore resistance and the potentially underlying plant sex effects. To this end, we recorded the abundances of a specialist leaf‐chewing caterpillar [Acronyctodes mexicanaria Walker (Lepidoptera: Geometridae)] throughout an entire growing season. We also recorded information about the caterpillar’s parasitoids, as well as leaf water content, phenolic compounds, phosphorus, and nitrogen for male and female plants of B. cordata. Plant sex did not significantly influence caterpillar abundance but did have an effect on natural enemies, with parasitoid abundance being 2.4‐fold greater on female than on male plants. The effect of plant sex on parasitoids remained significant after accounting for caterpillar abundance, suggesting that it was underlain by a trait‐mediated (rather than density‐mediated) mechanism. Finally, we found that male plants had a higher concentration of phenolic compounds (other traits did not differ between plant sexes). These results provide valuable evidence for the extended effects of plant sex on the third trophic level and point at plant traits potentially mediating such effects.     

Variation in Plant Substrates and its Consequences for Insect Vibrational Communication

Many insects and other arthropods communicate using plant‐borne vibrational signals. Vibration transmission along plant stems imposes a frequency filter on signals, and may cause signal degradation from reflected waves. Furthermore, different plant species and plant parts can differ in their transmission properties. This variability in the communication channel may constrain the reliability of signals, with important consequences for the evolution of vibrational communication systems, as well as for researchers studying signal variation at an individual, population, or species level. In this study we estimate the magnitude of substrate‐related variation in the mate advertisement signals of a treehopper (Hemiptera: Membracidae: Umbonia crassicornis). We used laser vibrometry to record the signals produced by 25 adult males on two different plant species, one host and one non‐host. We recorded male signals on two plants per species; within each plant, signals were recorded simultaneously at two distances. We measured three spectral characteristics (dominant frequency, relative amplitude of the signals’ high and low frequency components, frequency at the end of the signal) and two temporal characteristics (signal duration and click repetition rate). Spectral characteristics were influenced by the distance at which the signal was recorded, and this influence varied among plant species and individuals. Temporal characteristics were less influenced, although signal length was influenced by distance, an effect that varied among individual plants. Overall, the magnitude of the effects was small. Furthermore, there was significant within‐individual repeatability of almost all signal traits across different plant substrates. Signal characteristics were thus reliably associated with individuals, even when they signaled on different plants.     

Within‐Species Mate Preferences Do Not Contribute to the Maintenance of Sexually Monomorphic Mating Signals in Green Lacewings

We know much less about the evolutionary forces and constraints that maintain similar mating displays in females and males than we do about sexually dimorphic mating displays. Both female and male green lacewings have sexually monomorphic vibrational mating signals and are equally choosy against heterospecific mating signals. This similarity in between‐species sex roles may explain a large part of the presence of species‐specific female signals in these species, but does not necessarily predict why female and male signals are similar. We tested for within‐species sex‐specific similarities in mate preferences in Chrysoperla lucasina that may contribute to the maintenance of sexually monomorphic mating signals in this species. We found weak preferences and low levels of discrimination for signals with varying fine‐scale temporal features (volley duration, period, and volley‐duty cycle). The longer signals that both sexes produced in response to playback were sexually monomorphic, but some females and most males also produced shorter signals with significantly reduced volley durations and periods. Notably, all of these signals had indistinguishable volley‐duty cycles, the ratio of volley duration to volley period. We propose that mating signals in C. lucasina are maintained in both sexes because of similar between‐species mate preferences, but the sexually monomorphic mating signals cannot be attributed to significant within‐species mate preferences. What differences are present in within‐species sex roles may be resolved by a male‐biased signal polymorphism, in long and short signals that are hypothesized to have distinct functions during mate calling and courtship.     

Genetic variation of two species with different life‐history traits in the endangered renosterveld of South Africa – a comparative analysis of Eriocephalus africanus and Hemimeris racemosa

We tested the effects of life‐history traits on genetic variation and conducted a comparative analysis of two plant species with differing life‐history traits co‐occurring in the highly endangered renosterveld of South Africa. We selected eighteen renosterveld remnants with varying degrees of size and isolation where populations of the herbaceous, annual and insect‐pollinated Hemimeris racemosa and the shrubby perennial and both wind‐ and insect‐pollinated Eriocephalus africanus occurred. We postulated a lower genetic variation within populations and increased genetic variation between populations in the annual than in the perennial species. Genetic variation was lower within populations of H. racemosa than within E. africanus, as is typical for annual compared to perennial species. Variation within populations was, however, not correlated with fragment size or distance in either of the two species and genetic variation between populations of the two species was comparable (Φ_ST = 0.10, 0.09).     

SELECTION FOR ALTERNATIVE MALE REPRODUCTIVE TACTICS ALTERS INTRALOCUS SEXUAL CONFLICT

Intralocus sexual conflict (IASC) arises when fitness optima for a shared trait differ between the sexes; such conflict may help maintain genetic variation within populations. Sex‐limited expression of sexually antagonistic traits may help resolve the conflict, but the extent of this resolution remains a subject of debate. In species with alternative male reproductive tactics, unresolved conflict should manifest more in a more sexually dimorphic male phenotype. We tested this prediction in the bulb mite (Rhizoglyphus robini), a species in which aggressive fighters coexist with benign scramblers. To do this, we established replicated lines in which we increased the proportion of each of the alternative male morphs using artificial selection. After approximately 40 generations, the proportion of fighters and scramblers stabilized at >0.9 in fighter‐ and scrambler‐selected lines, respectively. We then measured several female fitness components. As predicted by IASC theory, female fecundity and longevity were lower in lines selected for fighters and higher in lines selected for scramblers. This finding indicates that sexually selected phenotypes are associated with an ontogenetic conflict that is not easily resolved. Furthermore, we suggest that IASC may be an important mechanism contributing to the maintenance of genetic variation in the expression of alternative reproductive tactics.     

Geographic variation in sexual dimorphism in the barn owl Tyto alba: a role for direct selection or genetic correlation?

Geographic variation in sexually selected traits is commonly attributed to geographic variation in the net benefit accrued from bearing such traits. Although natural and sexual selection are potentially important in shaping geographic variation, genetic constraints may also play a role. Although a genetic correlation between two traits may itself be the outcome of natural or sexual selection, it may indirectly reinforce the establishment and maintenance of cline variation with respect to one particular trait when across the cline different values of other traits are selected. Using the barn owl Tyto alba, a species in which the plumage of females is more reddish‐brown and more marked with black spots than that of males, I report results that are consistent with the hypothesis that both direct selection and genetic constraints may help establish and maintain cline variation in sexual dichromatism. In this species, inter‐individual variation in plumage coloration and spottiness has a genetic basis, and these traits are not sensitive to the environment. Data, based on the measurement of skin specimens, is consistent with the hypothesis that the stronger European cline variation in male spottiness than in female spottiness depends on the combined effects of (1) the similar cline variation in male and female plumage coloration and (2) the more intense phenotypic correlation between plumage coloration and spottiness in males (darker birds are more heavily spotted in the two sexes, but especially males) which is a general feature among the globally distributed barn owls. In northern Europe, male and female T. a. guttata are reddish‐brown and heavily spotted, and in southern Europe male and female T. a. alba are white, but only females display many spots. Here, I discuss the relative importance of direct selection, genetic correlation and the post‐ice age invasion of Europe by T. alba, in generating sex‐specific cline variation in plumage spottiness and non‐sex‐specific cline variation in plumage coloration.     

Local population density and group composition influence the signal‐preference relationship in Enchenopa treehoppers (Hemiptera: Membracidae)

Many animals exhibit social plasticity – changes in phenotype or behaviour in response to experience with conspecifics that change how evolutionary processes like sexual selection play out. Here, we asked whether social plasticity arising from variation in local population density in male advertisement signals and female mate preferences influences the form of sexual selection. We manipulated local density and determined whether this changed how the distribution of male signals overlapped with female preferences – the signal preference relationship. We specifically look at the shape of female mate preference functions, which, when compared to signal distributions, provide hypotheses about the form of sexual selection. We used Enchenopa binotata treehoppers, a group of plant‐feeding insects that exhibit natural variation in local densities across individual host plants, populations, species and years. We measured male signal frequency and female preference functions across the density treatments. We found that male signals varied across local social groups, but not according to local density. By contrast, female preferences varied with local density – favouring higher signal frequencies in denser environments. Thus, local density changes the signal–preference relationship and, consequently, the expected form of sexual selection. We found no influence of sex ratio on the signal–preference relationship. Our findings suggest that plasticity arising from variation in local group density and composition can alter the form of sexual selection with potentially important consequences both for the maintenance of variation and for speciation.     

Geographic variation in male courtship acoustics and genetic divergence of populations of the Cotesia flavipes species complex

Courtship behaviors of insect populations can vary across the range of a species. Populations exhibiting divergent courtship behavior may indicate genetic divergence or cryptic species. Courtship acoustic signals produced by male wing fanning and genetic structure (using amplified fragment length polymorphisms) were examined for seven allopatric populations of the Cotesia flavipes (Hymenoptera: Braconidae) species complex, using four C. sesamiae (Cameron) and three C. flavipes Cameron populations. Members of this species complex parasitize lepidopteran pests in gramineous crops including sugarcane, maize, and rice . Significant variation was detected in courtship acoustic signals and genetic structure among populations of both species. For C. sesamiae, courtship acoustic signals varied more between populations of two biotypes that were collected near an area of sympatry. The two biotypes of C. sesamiae were also genetically divergent. For C. flavipes, significant differences in acoustic signals and genetic structure occurred among allopatric populations; these differences support the recent designation of one population as a new species. Courtship acoustics play a role in reproductive isolation in this species complex, and are likely used in conjunction with chemical signals. Ecological factors such as host range and host plant use may also influence the divergence of both courtship acoustic signals and genetic structure among populations in the C. flavipes complex.     

Genotype × environment interaction in the allometry of body,genitalia and signal traits in Enchenopa treehoppers (Hemiptera: Membracidae)

Developmental plasticity may promote divergence by exposing genetic variation to selection in novel ways in new environments. We tested for this effect in the static allometry (i.e. scaling on body size) of traits in advertisement signals, body and genitalia. We used a member of the Enchenopa binotata species complex of treehoppers – a clade of plant‐feeding insects in which speciation is associated with colonization of novel environments involving marked divergence in signals, subtle divergence in body size and shape, and no apparent divergence in genitalia. We found no change in mean allometric slopes across environments, but substantial genetic variation and genotype × environment interaction (G × E) in allometry. The allometry of signal traits showed the most genetic variation and G × E, and that of genitalia showed the weakest G × E. Our findings suggest that colonizing novel environments may have stronger diversifying consequences for signal allometry than for genitalia allometry. © 2011 The Linnean Society of London, Biological Journal of the Linnean Society, 2012, 105 , 187–196.     

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.     

Host‐plant genotypic diversity and community genetic interactions mediate aphid spatial distribution

Genetic variation in plants can influence the community structure of associated species, through both direct and indirect interactions. Herbivorous insects are known to feed on a restricted range of plants, and herbivore preference and performance can vary among host plants within a species due to genetically based traits of the plant (e.g., defensive compounds). In a natural system, we expect to find genetic variation within both plant and herbivore communities and we expect this variation to influence species interactions. Using a three‐species plant‐aphid model system, we investigated the effect of genetic diversity on genetic interactions among the community members. Our system involved a host plant (Hordeum vulgare) that was shared by an aphid (Sitobion avenae) and a hemi‐parasitic plant (Rhinanthus minor). We showed that aphids cluster more tightly in a genetically diverse host‐plant community than in a genetic monoculture, with host‐plant genetic diversity explaining up to 24% of the variation in aphid distribution. This is driven by differing preferences of the aphids to the different plant genotypes and their resulting performance on these plants. Within the two host‐plant diversity levels, aphid spatial distribution was influenced by an interaction among the aphid's own genotype, the genotype of a competing aphid, the origin of the parasitic plant population, and the host‐plant genotype. Thus, the overall outcome involves both direct (i.e., host plant to aphid) and indirect (i.e., parasitic plant to aphid) interactions across all these species. These results show that a complex genetic environment influences the distribution of herbivores among host plants. Thus, in genetically diverse systems, interspecific genetic interactions between the host plant and herbivore can influence the population dynamics of the system and could also structure local communities. We suggest that direct and indirect genotypic interactions among species can influence community structure and processes.     

THE IMPORTANCE OF FEMALE CHOICE,MALE–MALE COMPETITION,AND SIGNAL TRANSMISSION AS CAUSES OF SELECTION ON MALE MATING SIGNALS

Selection on advertisement signals arises from interacting sources including female choice, male–male competition, and the communication channel (i.e., the signaling environment). To identify the contribution of individual sources of selection, we used previously quantified relationships between signal traits and each putative source to predict relationships between signal variation and fitness in Enchenopa binotata treehoppers (Hemiptera: Membracidae). We then measured phenotypic selection on signals and compared predicted and realized relationships between signal traits and mating success. We recorded male signals, then measured lifetime mating success at two population densities in a realistic environment in which sources of selection could interact. We identified which sources best predicted the relationship between signal variation and mating success using a multiple regression approach. All signal traits were under selection in at least one of the two breeding seasons measured, and in some cases selection was variable between years. Female preference was the strongest source of selection shaping male signals. The E. binotata species complex is a model of ecological speciation initiated by host shifts. Signal and preference divergence contribute to behavioral isolation within the complex, and the finding that female mate preferences drive signal evolution suggests that speciation in this group results from both ecological divergence and sexual selection.