Merrill A. Peterson

The Influence of Dispersal and Diet Breadth on Patterns of Genetic Isolation by Distance in Phytophagous Insects

To determine the effects of dispersal ability and diet breadth on population‐genetic structure, we reviewed the allozyme literature and estimated genetic isolation by distance (IBD) for 43 species/host races of phytophagous insects. Subsequently, we tested two opposing hypotheses regarding the influence of dispersal ability on IBD: that IBD slopes do not vary with mobility, but that intercepts increase with mobility, and, alternatively, that IBD slopes vary with dispersal ability. We found that from tens of kilometers to more than 1,000 km, IBD is weak in sedentary and highly mobile species but pronounced in moderately mobile species. We attribute the weak IBD in strong dispersers to the homogenizing effects of gene flow, whereas in sedentary species, limited gene flow allows nearly all populations to diverge. In intermediate dispersers, genetic homogeneity is achieved at small spatial scales, but limited dispersal promotes genetic divergence over long distances. We also tested the hypothesis that IBD increases with decreasing diet breadth. We discovered no such pattern, casting doubt on the supposition that specialization promotes speciation by influencing population‐genetic subdivision. Finally, we found that the number of populations is a more important consideration than the number of polymorphic loci in studies of IBD.

BOTTOM-UP FORCES MEDIATE NATURAL-ENEMY IMPACT IN A PHYTOPHAGOUS INSECT COMMUNITY

We employed a combination of factorial experiments in the field and labo- ratory to investigate the relative magnitude and degree of interaction of bottom-up factors (two levels each of host-plant nutrition and vegetation complexity) and top-down forces (two levels of wolf-spider predation) on the population growth of Prokelisia planthoppers (P. dolus and P. marginata), the dominant insect herbivores on Spartina cordgrass through- out the intertidal marshes of North America. Treatments were designed to mimic combi- nations of plant characteristics and predator densities that occur naturally across habitats in the field. There were complex interactive effects between plant resources and spider predation on the population growth of planthoppers. The degree that spiders suppressed planthoppers depended on both plant nutrition and vegetation complexity, an interaction that was dem- onstrated both in the field and laboratory. Laboratory results showed that spiders checked planthopper populations most effectively on poor-quality Spartina with an associated matrix of thatch, all characteristics of high-marsh meadow habitats. It was also this combination of plant resources in concert with spiders that promoted the smallest populations of planthop- pers in our field experiment. Planthopper populations were most likely to escape the sup- pressing effects of predation on nutritious plants without thatch, a combination of factors associated with observed planthopper outbreaks in low-marsh habitats in the field. Thus, there is important spatial variation in the relative strength of forces with bottom-up factors dominating under low-marsh conditions and top-down forces increasing in strength at higher elevations on the marsh. Enhancing host-plant biomass and nutrition did not strengthen top-down effects on planthoppers, even though nitrogen-rich plants supported higher densities of wolf spiders and other invertebrate predators in the field. Rather, planthopper populations, particularly those of Prokelisia marginata, escaped predator restraint on high-quality plants, a result we attribute to its mobile life history, enhanced colonizing ability, and rapid growth rate. Thus, our results for Prokelisia planthoppers suggest that the life history strategy of a species is an important mediator of top-down and bottom-up impacts. In laboratory mesocosms, enhancing plant biomass and nutrition resulted in increased spider reproduction, a cascading effect associated with planthopper increases on high- quality plants. Although the adverse effects of spider predation on planthoppers cascaded down and fostered increased plant biomass in laboratory mesocosms, this result did not occur in the field where top-down effects attenuated. We attributed this outcome in part to the intraguild predation of other planthopper predators by wolf spiders. Overall, the general paradigm in this system is for bottom-up forces to dominate, and when predators do exert a significant suppressing effect on planthoppers, their impact is generally legislated by vegetation characteristics.

Feeding-induced changes in plant quality mediate interspecific competition between sap-feeding herbivores.

Feeding-induced plant resistance is a well-documented phenomenon for leaf- chewing insects. Furthermore, feeding-induced resistance provides the mechanistic basis for many cases of delayed interspecific competition, whereby previous feeding by one species diminishes the performance of other herbivores which attack the same plant later in the season. This phenomenon, however, has been very poorly investigated for sap-feeding insects. The results we present here for salt marsh-inhabiting planthoppers ( Prokelisia dolus and P. marginata) provide one of the few known examples of delayed, plant-mediated interspecific competition between two sap-feeding insects. Three lines of experimental evidence from the laboratory, field cages, and open field plots provide support for the detrimental effects of previous feeding by one planthopper species on the subsequent survival and performance of the other. Laboratory experiments showed that prior feeding on cordgrass by one congener resulted in reduced performance of the other in the following generation. However, the effect was asymmetric. Prior feeding by P. dolus resulted in prolonged development and reduced body size (a correlate of fecundity) in P. marginata, whereas only development was protracted in P. dolus when plants were previously exposed to P. marginata. Consequently, P. dolus appears to be the superior competitor in the context of delayed, plant-mediated interactions. The negative effects of previous feeding by P. dolus on the development time, body size, and survival of P. marginata obtained in the laboratory were confirmed both in cages and on cage-free islets of cordgrass in the field. Feeding-induced reductions in host-plant quality by P. dolus may provide additional impetus for P. marginata to migrate from shared habitats on the high marsh to nutritionally superior plants in the low marsh rarely occupied by P. dolus. The mechanism underlying the delayed competitive effects between Prokelisia plan- thoppers is most likely diminished plant nutrition, because feeding by P. dolus significantly reduces the concentration of essential amino acids in cordgrass. The asymmetry of plant- mediated competition between the Prokelisia species may be due to the ability of P. dolus to better tolerate feeding-depleted levels of plant nitrogen via compensatory feeding. Even though these two planthoppers do not suffer significant fitness reductions during contemporaneous interactions, they compete severely in the context of feeding-induced plant resistance which is expressed later in the season. This result, coupled with the fact that most studies of interspecific interaction between herbivorous insects are contempo- raneous, indicates that interspecific competition may be profoundly underestimated as a structuring force in phytophagous insect communities.

Habitat Persistence Underlies Intraspecific Variation in the Dispersal Strategies of Planthoppers

Dispersal is considered a vital life history characteristic for insects exploiting temporary habitats, and life history theorists have often hypothesized an inverse relationship between dispersal capability and habitat persistence. Most often, this hypothesis has been tested using interspecific comparisons of dispersal capability and qualitative estimates of habitat persistence. Consequently, most assessments have failed to control for possible phylogenetic nonindependence and they also lack quantitative rigor. We capitalized on existing intraspecific variation in the dispersal capability of Prokelisia planthoppers to examine the relationship between habitat persistence and dispersal, thereby minimizing possible phylogenetic effects. Two congeneric species (Prokelisia marginata and P. dolus) occur in the intertidal marshes of North America, where they feed exclusively on cordgrasses (Spartina). Because these planthoppers exhibit wing dimorphism, flight- capable adults (macropters with fully developed wings) are easily differentiated from flight- less adults (brachypters with reduced wings). Thus, dispersal capability can be readily estimated by the percentage of macropters in a population. At a regional spatial scale, we found a highly significant negative relationship between dispersal capability (percent macroptery) and habitat persistence. In this system, habitat persistence is influenced by a combination of marsh elevation, winter severity, and tidal range, which interact to determine the ability of planthoppers to endure through winter in their primary habitat for development. P. marginata develops primarily in low-marsh hab- itats during summer, habitats that can be subjected to pronounced winter disturbance due to ice scouring and/or extensive tidal inundation. Levels of winter disturbance of the low marsh are extreme along the Atlantic coast, intermediate along the Pacific, and low along the Gulf. Both the failure of P. marginata populations to remain through winter in this habitat, and the dispersal ability of these populations (92%, 29%, and 17% macroptery, respectively), are correlated with levels of disturbance. Thus, in regions where winter disturbance is high, levels of dispersal are correspondingly high to allow for recolonization of extirpated habitats from overwintering sites on the high marsh. Unlike P. marginata, P. dolus develops primarily in high-marsh habitats, which are much less disturbed on all coasts during winter. Consequently, this species remains year-round in its primary habitat for development, and most populations exhibit relatively low levels of macroptery (<10%). When raised under common garden conditions, many more macropters of both species were produced from Atlantic compared to Gulf populations. Thus the proportion of ma- cropters produced from the populations used in this experiment paralleled the incidence of macroptery measured in the field, providing evidence that the geographic variation in dispersal capability in both species has in part a genetic basis. The results of this study provide strong intraspecific evidence for an inverse relationship between the dispersal capability of insects and the persistence of their habitats.

Chapter 6 – Density-Dependent Dispersal and Its Consequences for Population Dynamics

This chapter discusses a fundamental concern in insect ecology, that is, to determine the forces that dictate the temporal and spatial fluctuations of populations. Review of the literature found widespread evidence for density-dependent dispersal in the Thysanoptera, Homoptera, and Heteroptera. Intraplant dispersal was found for 20 species of sapfeeders, mostly the rather immobile nymphs of aphids, psyllids, and scale insects and the apterous adults of aphids. Another plant-mediated dispersal response occurred in two lygaeid species when feeding influenced the quantity of the seed resource. Support for density-dependent dispersal as a stabilizing force was provided by evidence either that high levels of dispersal contributed to population suppression or stabilization around some equilibrium level or that low levels of dispersal conferred little suppressing effect on the population. The maximum incidence of migratory forms was much higher (81%) for species in which dispersal was shown to be an important restraining process. An examination of the population biology of three species of wing-dimorphic planthoppers provides insight into the relationship between density-dependent dispersal and the density-dependent suppression of populations. When populations are small, births outweigh emigration and populations grow; in contrast, when populations are large, emigration exceeds birth and population growth is suppressed. Among the taxa reviewed, density-dependent dispersal occurred with similar frequency at the intraplant, interplant, and interhabitat spatial scales. It has been documented that populations of sap-feeding insects are overrepresented in the literature on interspecific competition, suggesting that sap-feeders, compared to other phytophages, may be more often limited by density-dependent processes in general.

RELATIVE ABUNDANCE AND THE SPECIES-SPECIFIC REINFORCEMENT OF MALE MATING PREFERENCE IN THE CHRYSOCHUS (COLEOPTERA: CHRYSOMELIDAE) HYBRID ZONE

Abstract Most studies of reinforcement have focused on the evolution of either female choice or male mating cues, following the long‐held view in sexual selection theory that mating mastakes are typically more costly for females than for males. However, factors such as conspecific sperm precedence can buffer females against the cost of mating mistakes, suggesting that in some hybrid zones mating mistakes may be more costly for males than for females. Thus, the historical bias in reinforcement research may underestimate its frequency. In this study, we present evidence that reinforcement has driven the evolution of male choice in a hybrid zone between teh highly promiscuous lealf beetles chyrsochus cobaltinus and C. auratus, the hybrids of which have extremely low fitness. In addition, there is evidence for male choice in these beetles and that male mating mistakes may be costly, due to reduced opportunities to mate with conspecific females. The present study combines laboratory and field methods to quantify the strenght of sexual isolation, test the hypothesis of reproductive character displacement, and assess the link between relative abundance and the strenght of selection against hybridization. We document that, while sexual isolation is weak, it is sufficient to produce positive assortative mating. In addtion, reproductive character displacement was only detected in the relatively rare species. The strong postzygotic barriers in this system are sufficient to generate the bimodality that characterizes this hybrid zone, but the weak sexual isolation is not, calling into question whether strong prezygotic isolation is necessary for the maintenance of bimodality. Growing evidence that the cost of mating mistakes is sufficient to shape the evolution of male mate choice suggests that the reinforecement of male mate choice may prove to be a widespread occurrence.

Profiles of cuticular hydrocarbons mediate male mate choice and sexual isolation between hybridising Chrysochus (Coleoptera: Chrysomelidae)

Summary.Chemical signals frequently underlie sexual isolation between insect species. Our understanding of the evolutionary forces influencing these signaling systems is known for very few systems, challenging both our efforts to understand insect speciation, and our ability to predict long-term changes in the chemical communication systems of insects. Thus, we are in need of more systems in which both the chemical signals causing sexual isolation and the evolutionary forces driving sexual isolation are understood. Sexual isolation in the hybrid zone between Chrysochus cobaltinus and C. auratus has apparently increased in response to natural selection against hybridisation (i.e. reinforcement). Previous experiments suggested that this isolation was due, at least in part, to male preferences for conspecific females. Here, we confirm this role of male choice, and document that male mate choice in this system is influenced by cuticular hydrocarbon (CHC) profiles. Specifically, male C. cobaltinus responses to control cadavers and conspecific female cadavers painted with different cuticular hexane extracts, together with analyses of the composition of those extracts, revealed that male mate choice is governed by CHC profiles. Multivariate analyses of GC profiles demonstrated that those profiles are indeed both sex- and species-specific. Although GC-MS enabled identification and quantification of the specific cuticular hydrocarbons, we have not yet determined which individual compounds govern mate choice. Having established that CHCs influence sexual isolation in this system, we can now assess the evolutionary lability of these cues, which will inform both our understanding of speciation, and of the conditions under which the chemical signaling systems that influence mate choice in insects can evolve.

Long-distance Gene Flow in the Sedentary Butterfly, Euphilotes enoptes (Lepidoptera: Lycaenidae)

The relationship between gene flow and geographic proximity has been assessed for many insect species, but dispersal distances are poorly known for most of these. Thus, we are able to assess the concordance between vagility and gene flow for only a few species. In this study, I documented variation at six allozyme loci among Washington and Oregon populations of the sedentary, patchily distributed, lycaenid butterfly, Euphilotes enoptes (Boisduval) to assess whether the relationship between gene flow and geographic distance is consistent with the dispersal biology of this species. Both a phenogram based on genetic distances between populations and a regression analysis of gene flow estimates on geographic distances showed a pattern consistent with genetic isolation by distance. Many estimates of gene flow among pairs of populations separated by more than 100 km exceeded the equivalent of 10 individuals exchanged per generation, a value much greater than would be predicted from the limited dispersal ability of this species. However, based on the allozyme data, genetic neighborhood size was estimated to be approximately 39 individuals, a value that is consistent with poor vagility. The results of this study speak to the power of stepping‐stone gene flow among populations and are compared to the results of other studies that have examined the relationship between dispersal and gene flow in sedentary insects.

Phenological Isolation, Gene Flow and Developmental Differences among Low- and High-elevation Populations of Euphilotes enoptes (Lepidoptera: Lycaenidae)

Populations of the specialist herbivore, Euphilotes enoptes (Lepidoptera: Lycaenidae), along three elevational transects in the mountains of central Washington state, differed markedly in the phenology of adult flight. In spite of this apparent limitation to gene flow, six allozyme loci revealed substantial gene exchange among populations along these gradients. The elevational difference, and thus the phenological difference, between populations has not influenced the extent of gene flow between them. Because the direct exchange of genes between low‐ and high‐elevation populations is very unlikely, gene flow between them has probably occurred in a stepwise fashion via intermediate populations. It is hypothesized that such gene flow has been biased in an uphill direction due to the combined effects of source size and oviposition behavior. Adult emergence times of populations in the same region are positively correlated with elevation in a nonlinear fashion, consistent with the hypothesis that gene flow from low‐elevation populations has been swamping selection at higher altitudes.

Apparent widespread gene flow in the predominantly flightless planthopper Tumidagena minuta

1. To determine whether dispersal biology can predict the pattern of population‐genetic variation among insect populations accurately, allozyme variation was assayed for populations of a saltmarsh planthopper, Tumidagena minuta, in which > 99% of the adults are flightless.