Binotata Complex Research Articles

The function of prolonged copulations in Enchenopa treehoppers (Hemiptera: Membracidae).

Copulations are very brief in many species, sometimes taking only seconds, but in other species, they can be quite prolonged. Potential explanations for prolonged copulations include time requirements for the transfer of sperm and/or other ejaculate substances. Ejaculate substances could function to regulate female receptivity to subsequent matings, provide nutritional nuptial gifts, or hasten egg oviposition at a potential survival cost to the female. We investigated prolonged copulation in a member of the Enchenopa binotata complex of treehoppers (Hemiptera: Membracidae), in which females rarely remate and copulation can last several hours. We assigned females to treatments in which we interrupted copulation at different times. We also included a control where copulation was not interrupted. We found that females that experienced shorter copulations were more likely to be subsequently receptive to an attractive male. We also found that few females produced offspring when they engaged in short copulations compared to those with longer copulations. We did not find any differences in female survival. Our results support the sperm transfer and receptivity regulation hypotheses. We discuss potential reasons for why these processes should take so long in a species with low female remating.

You stay, but I Hop: Host shifting near and far co-dominated the evolution of Enchenopa treehoppers.

The importance and prevalence of phylogenetic tracking between hosts and dependent organisms caused by co‐evolution and shifting between closely related host species have been debated for decades. Most studies of phylogenetic tracking among phytophagous insects and their host plants have been limited to insects feeding on a narrow range of host species. However, narrow host ranges can confound phylogenetic tracking (phylogenetic tracking hypothesis) with host shifting between hosts of intermediate relationship (intermediate hypothesis). Here, we investigated the evolutionary history of the Enchenopa binotata complex of treehoppers. Each species in this complex has high host fidelity, but the entire complex uses hosts across eight plant orders. The phylogenies of E. binotata were reconstructed to evaluate whether (1) tracking host phylogeny; or (2) shifting between intermediately related host plants better explains the evolutionary history of E. binotata. Our results suggest that E. binotata primarily shifted between both distant and intermediate host plants regardless of host phylogeny and less frequently tracked the phylogeny of their hosts. These findings indicate that phytophagous insects with high host fidelity, such as E. binotata, are capable of adaptation not only to closely related host plants but also to novel hosts, likely with diverse phenology and defense mechanisms.

Variation in signal-preference genetic correlations in Enchenopa treehoppers (Hemiptera: Membracidae).

Fisherian selection is a within-population process that promotes signal–preference coevolution and speciation due to signal–preference genetic correlations. The importance of the contribution of Fisherian selection to speciation depends in part on the answer to two outstanding questions: What explains differences in the strength of signal–preference genetic correlations? And, how does the magnitude of within-species signal–preference covariation compare to species differences in signals and preferences? To address these questions, we tested for signal–preference genetic correlations in two members of the Enchenopa binotata complex, a clade of plant-feeding insects wherein speciation involves the colonization of novel host plants and signal–preference divergence. We used a full-sibling, split-family rearing experiment to estimate genetic correlations and to analyze the underlying patterns of variation in signals and preferences. Genetic correlations were weak or zero, but exploration of the underlying patterns of variation in signals and preferences revealed some full-sib families that varied by as much as 50% of the distance between similar species in the E. binotata complex. This result was stronger in the species that showed greater amounts of genetic variation in signals and preferences. We argue that some forms of weak signal–preference genetic correlation may have important evolutionary consequences.

Male Enchenopa treehoppers (Hemiptera: Membracidae) vary mate-searching behavior but not signaling behavior in response to spider silk

Finding and attracting mates can impose costs on males in terms of increased encounters with, and attraction of, predators. To decrease the likelihood of predation, males may modify mate-acquisition efforts in two main ways: they may reduce mate-searching efforts or they may reduce mate-attraction efforts. The specific behavior that males change in the presence of predator cues should depend upon the nature of risk imposed by the type of predator present in the environment. For example, sit-and-wait predators impose greater costs to males moving in search of mates. Here, we test whether cues of the presence of a sit-and-wait predator lead to a reduction in mate-searching but not mate-acquisition behavior. We used a member of the Enchenopa binotata complex of treehoppers-a clade of vibrationally communicating insects in which males fly in search of mates and produce mate-attraction signals when they land on plant stems. We tested for changes in mate-searching and signaling behaviors when silk from a web-building spider was present or absent. We found that males delayed flight when spider silk was present but only if they were actively searching for mates. These results suggest that males have been selected to reduce predation risk by adjusting how they move about their environment according to the cues of sit-and-wait predators.

Felsenstein’s “one-allele model” of speciation: The role of philopatry in the initial stages of host plant mediated reproductive isolation in Enchenopa binotata

Abstract The study of speciation genetics is primarily concerned with identifying the genetic traits that allow divergent selection to overcome the homogenizing effects of gene flow. Felsenstein reviewed this race between gene flow and selection, concluding that speciation with gene flow was unlikely under a “two-allele model” (where two traits were necessary for reproductive isolation) but that divergence could occur quite easily under a “one-allele model.” Despite this finding, much of the sympatric speciation research involving phytophagous insects has relied on a two-trait model, where insects evolve both preferences for and increased performance on novel host plants. Philopatry (a tendency to remain where one was born) is known to occur in phytophagous insects and is a single trait isolation mechanism. However, it is traditionally invoked as simply augmenting reproductive isolation. Species in the Enchenopa binotata complex are believed to have speciated in sympatry. They exhibit host plant preferences, host specific performance advantages and strong philopatry. We experimentally shifted E. binotata to evolutionarily novel host plants. Previous research has demonstrated that the experimental population of insects possesses genetic variation in preference and performance to the novel host. The degree of philopatry at mating and egg-laying was assayed for the first four years under full choice conditions. Host plant preference and performance was assayed after eight years. Philopatry was an immediate and strong isolating mechanism, while preference for and performance on the novel host lagged. We therefore suggest that philopatry may be a more important mechanism in the early stages of a host shift than previously believed.

Host shifts and signal divergence: mating signals covary with host use in a complex of specialized plant-feeding insects

A combination of divergent natural and sexual selection is a powerful cause of speciation. This conjunction of evolutionary forces may often occur when divergence is initiated by ecological differences between populations because local adaptation to new resources can lead to changes in sexual selection. The hypothesis that differences in resource use contribute to the evolution of reproductive isolation by altering the nature of sexual selection predicts that: (1) differences in sexual traits, such as signals and preferences, are an important source of reproductive isolation between species using different resources; (2) there are identifiable sources of selection on sexual traits that differ between species using different resources; and (3) signals vary between populations using different resources to a larger extent than between populations using the same resource at different localities. Testing these predictions requires a group of closely-related species or populations that specialize on different resources and for which the traits involved in mate choice are known. The Enchenopa binotata species complex of treehoppers (Hemiptera: Membracidae) are host plant specialists in which speciation is associated with shifts to novel host plants. Mating in this complex is preceded by an exchange of vibrational signals transmitted through host plant stems, and the signal traits important for mate choice have been identified. In the E. binotata complex, previous work has supported the first two predictions: (1) signal differences between species are important in mate recognition and (2) host shifts can alter both the trait values favoured by sexual selection and the evolutionary response to that selection. In the present study, we tested the last prediction by conducting a large-scale study of mating signal variation within and between the 11 species in the complex. We find that differences in host use are strongly associated with differences in signal traits important for mate recognition. This result supports the hypothesis that hosts shifts have led to speciation in this group in part through their influence on divergence in mate communication systems.

Host shifts favor vibrational signal divergence in Enchenopa binotata treehoppers

For specialized herbivorous insects, shifts to novel host plants can have dramatic evolutionary consequences. If mating traits diverge, assortative mating can develop between ancestral and novel host populations and facilitate speciation. Mating signals may diverge under a variety of scenarios. Signal differences may be a consequence of divergence in correlated traits, such as body size. If local communication environments differ, mating signals may also diverge through selection for enhanced transmission. We tested these hypotheses using 2 closely related species in the Enchenopa binotata complex of treehoppers. Each member of this complex specializes on a different host plant species. Their communication modality may make signal divergence likely after a host shift: like many plant-dwelling insects, Enchenopa communicate using substrate-borne vibrations for which the plant itself is the transmission channel. Each species' mating signal is a relatively pure tone, and differences between species in signal frequency are critical for mate recognition. Whereas no support was found for a correlated selection hypothesis, we found support for a signal transmission hypothesis: both species use a signal frequency that transmits well in their contrasting communication environments, suggesting that host shifts may favor signal divergence and ultimately behavioral isolation.

Divergence in Female Duetting Signals in theEnchenopa binotataSpecies Complex of Treehoppers (Hemiptera: Membracidae)

AbstractSexual communication often involves signal exchanges between the sexes, or duetting, in which mate choice is expressed through response signals. With both sexes acting as signalers and receivers, variation in the signals of males and females may be important for mate choice, reproductive isolation, and divergence. In theEnchenopa binotataspecies complex – a case study of sympatric speciation in which vibrational duetting may have an important role – male signals are species‐specific, females choose among males on the basis of signal traits that reflect species and individual differences, and female preferences have exerted divergent selection on male signals. Here, we describe variation in female signals in theE. binotataspecies complex. We report substantial species differences in the spectral and temporal features of female signals, and in their timing relative to male signals. These differences were similar in range to differences in male signals in theE. binotatacomplex. We consider processes that might contribute to divergence in female signals, and suggest that signal evolution in theE. binotatacomplex may be influenced by mate choice in both sexes.

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

AbstractMate 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.

Signals and speciation in plant-feeding insects

Communication can play a role in speciation when differences in signaling systems reduce gene flow between diverging lineages. However, the observation that closely related species have different signals leaves open the question of cause and effect, because divergence in signals can also occur after speciation is completed. The relationship of signals and divergence is being investigated in the Enchenopa binotata species complex of treehoppers, a group of plant-feeding insects that communicate using substrate-borne vibrational signals. Speciation in the E. binotata complex is hypothesized to have resulted from repeated shifts to novel host plants. Sources of selection on the signals of these treehoppers can be studied not only in fully differentiated species, but also in experimental populations in the early stages of divergence. Some unique features of vibrational communication through plant stems will be discussed, as well as how shifts to novel host plants may influence signaling systems, and what role(s) communication may have played in the process of evolutionary divergence in this group.

A phylogenetic analysis of theEnchenopa binotataspecies complex (Homoptera: Membracidae) using nymphal characters

Abstract.Nymphal characters which distinguish the nine species of theEnchenopa binotatacomplex (key included) are delineated for future formal species descriptions. A phylogenetic tree using these characters is presented and compared to a tree derived from allozyme data. Three pairs of sister species are defined, two of these pairs meeting strict phylogenetic and biological criteria which suggest sympatric speciation through host shifts.

Macrogeographic Genetic Variation in the Enchenopa binotata Complex (Homoptera: Membracidae)

Starch gel electrophoresis was used to analyze biochemical genetic variation within six species of the Enchenopa binotata complex. Comparisons of heterogeneity within species indicate that significant differentiation exists between populations. Population structure data suggest that treehoppers from Ptelea are most differentiated (mean Nei genetic distance, 0.09; FST, 0.40), whereas those on Viburnum are most similar (mean Nei distance, 0.02; FST, 0.15). Gene flow estimates for Enchenopa from Ptelea (Nm*, 0.18) are lower than many wingless or troglobitic arthropods. Interspecific genetic distance estimates ranged from 0.02 to 0.43. Phenetic cluster algorithms position all but one of the 37 Enchenopa populations consistent with the host on which insects were collected.

Microgeographic Genetic Variation in the Enchenopa binotata Complex (Homoptera: Membracidae)

Biochemical genetic variation among populations of three species of the Enchenopa binotata complex was examined using starch gel electrophoresis. For each species of treehopper, comparisons were made among insect samples from different branches of the same tree and among pooled samples from different trees. Significant heterogeneity exists among nymphal samples taken from different branches of the same tree; differentiation also occurs between samples from trees within the same local areas. Enchenopa from different species of host plant exhibit minor differences in population structuring; FST is greatest for treehoppers on Juglans and approximately equal for insects on Ptelea and on Cercis .

ECOLOGICAL AND BEHAVIORAL BASIS FOR REPRODUCTIVE ISOLATION IN THE SYMPATRIC ENCHENOPA BINOTATA COMPLEX (HOMOPTERA. MEMBRACIDAE).

A pervasive question in evolutionary biology is whether sympatric speciation can be promoted by the exploitation of new plants or changes in life history. Recent studies (Maynard Smith, 1966; Alexander, 1968; Huettel and Bush, 1972; Knerer and Atwood, 1973; Bush, 1969, 1975; Tauber and Tauber, 1977a, 1977b; Edmunds and Alstad, 1978) have made sympatric speciation more readily accepted than in the past (Mayr, 1970) but it is still subject to debate (Futuyma and Mayer, 1980). Our past work (Wood, 1980; Guttman et al., 1981) with the treehopper Enchenopa binotata Say suggests that this insect diverged along plant lines into a complex of sympatric reproductively isolated species. Enchenopa is common in eastern North America on deciduous trees and shrubs as far south as Panama. Enchenopa from each of seven North American plants are all listed taxonomically as the same species (Metcalf and Wade, 1965), although they differ in nymphal coloration, oviposition site, egg froth composition, time of day they deposit eggs, and nymphal feeding sites. Females from a given species select that for oviposition when given a choice, and when confined to a single small cage select mates assortatively by plant species (Wood, 1980). Insects from each species are electrophoretically distinguishable although differences within host races can be found among samples collected from different conspecific trees. Enchenopa on Juglans nigra, Ptelea trifoliata, Robinia pseudoacacia, and Cercis canadensis are electrophoretically different from each other and from those on two species of Viburnum and Celastrus scandens, which are similar to each other (Guttman et al., 1981). Thus E. binotata is a complex of reproductively isolated species. The North American plants of Enchenopa represent evolutionarily diverse plants which are broadly and locally sympatric. When several species are found together Enchenopa may occur on each host. Females insert eggs into the branch of the plant and cover them with a secretion known as egg froth, which protects overwintering eggs (Wood and Patton, 1971), and contains an ovipositional attractant which is responsible for the clumping of egg masses on single branches. The large aggregations of nymphs that result attract mutualistic ants, which apparently increase nymphal survival (Wood and Seilkop, unpubl.). Wood (1980) suggested the following hypothesis based on the work of Bush (1975) to explain the divergence of the Enchenopa binotata complex. Based on present geographical distributions (Metcalf and Wade, 1965), plant and seasonal records in Costa Rica (Ballou, 1936) and observations by one of us (T.K.W.), the original stock was postulated to be tropical, polyphagous and multivoltine. As Enchenopa progenitors colonized north temperate climates they encountered deciduous hosts which promoted selection for coordination of treehopper life history