GENETICS OF PHYSIOLOGICAL AND BEHAVIORAL RESISTANCE TO HOST FURANOCOUMARINS IN THE PARSNIP WEBWORM

Depressaria pastinacella, the parsnip webworm, feeds almost exclusively on the flowers and fruits of Pastinaca sativa, the wild parsnip. Resistance to webworms in wild parsnip populations is largely attributable to genetically based variation in furanocoumarin chemistry; by differentially reducing fruit set among chemical phenotypes, parsnip webworms may act as selective agents on wild parsnip populations. To determine whether wild parsnip chemistry can act as a selective agent on webworm populations, it is necessary to establish that resistance mechanisms in the webworm to furanocoumarins are genetically based. In this study, we estimated the amount of genetic variation in behavioral and physiological responses of webworms to parsnip furanocoumarins. Virtually no variation was found among webworm families for feeding preferences for diets varying as much as fourfold in furanocoumarin content. Nor was significant variation found for mean furanocoumarin intake over the assay period, except in one case, in which maternal effects may account for differences among families. In contrast, substantial familial variation existed for cytochrome P450–mediated metabolism of bergapten and xanthotoxin, two host furanocoumarins. The presence of additive genetic variation in metabolism, and the absence of such variation in discriminative feeding behavior, suggests that adaptation to changes in furanocoumarin chemistry, resulting either from changes in the distribution of chemical phenotypes in parsnip populations or from shifts to new chemically different host plants, is likely to be facilitated by physiological rather than behavioral means.     

Host plant, host plant chemistry and the polyembryonic parasitoid Copidosoma sosares: indirect effects in a tritrophic interaction

Host plant identity and host plant chemistry have often been shown to influence host finding and acceptance by natural enemies but comparatively less attention has been paid to the tritrophic effects of host plant and host plant chemistry on other natural enemy fitness correlates, such as survivorship, clutch size, body size, and sex ratio. Such studies are central to understanding both the selective impact of plants on natural enemies as well as the potential for reciprocal selective impact of natural enemies on plant traits. We examined the effects of host plant and host plant chemistry in a tritrophic system consisting of three apiaceous plants (Pastinaca sativa, Heracleum sphondylium and H. mantegazzianum), the parsnip webworm (Depressaria pastinacella) and the polyembryonic parasitic wasp Copidosoma sosares. All of these plants produce furanocoumarins, known resistance factors for parsnip webworms. Furanocoumarin concentrations were correlated neither with the presence nor the number of webworms on a given plant. Concentrations of two furanocoumarins were negatively associated with C. sosares fitness correlates: isopimpinellin with the likelihood that a given webworm would be parasitized and xanthotoxin with both within‐brood survivorship (of all‐male and mixed‐sex broods) and clutch size. Brood sex ratio and body sizes of individual wasps were not correlated with furanocoumarin chemistry. Because additive genetic variation exists in P. sativa for furanocoumarin chemical traits, these are subject to selection by webworms through herbivory. Third trophic level selective impacts on furanocoumarin traits may include selection for reduced production of those chemicals that affect parasitoid survivorship yet do not influence host plant choice by the herbivore. That such might be the case is suggested by patterns of furanocoumarin production in populations of P. sativa with different histories of infestation; in the Netherlands, where parasitism rates of webworms by C. sosares are high, plants produce lower levels of all linear furanocoumarins and proportionately less isopimpinellin than do midwestern U.S. populations of P. sativa, where natural enemies of the webworm are effectively absent.     

Evolution of tolerance in an invasive weed after reassociation with its specialist herbivore

The interaction between the European wild parsnip Pastinaca sativa and its coevolved florivore the parsnip webworm Depressaria pastinacella, established in North America for over 150 years, has resulted in evolution of local chemical phenotype matching. The recent invasion of New Zealand by webworms, exposing parsnips there to florivore selection for the first time, provided an opportunity to assess rates of adaptive response in a real‐time experiment. We planted reciprocal common gardens in the USA and NZ with seeds from (1) US populations with a long history of webworm association; (2) NZ populations that had never been infested and (3) NZ populations infested for 3 years (since 2007) or 6 years (since 2004). We measured impacts of florivory on realized fitness, reproductive effort and pollination success and measured phenotypic changes in infested NZ populations relative to uninfested NZ populations to determine whether rapid adaptive evolution in response to florivory occurred. Irrespective of country of origin or location, webworms significantly reduced plant fitness. Webworms reduced pollination success in small plants but not in larger plants. Although defence chemistry remained unchanged, plants in infested populations were larger after 3–6 years of webworm florivory. As plant size is a strong predictor of realized fitness, evolution of large size as a component of florivore tolerance may occur more rapidly than evolution of enhanced chemical defence.     

Parthenocarpic fruits in wild parsnip: Decoy defence against a specialist herbivore

Summary Parthenocarpy, the production of fruits without viable seeds, is a widespread phenomenon in plants. While failure to effect pollination or fertilization is often cited as the cause of parthenocarpy, this explanation alone is inadequate to explain why plants produce, maintain and further develop fruits. Wild parsnips (Pastinaca sativa) frequently produce parthenocarpic fruit. When parsnip webworms (Depressaria pastinacella), specialist feeders on wild parsnip, were given choices between normal fruit and parthenocarpic fruit, they exhibited a strong preference for parthenocarpic fruit. However, on parthenocarpic fruit, insects fed less efficiently and grew more slowly than insects fed normal fruit. Parthenocarpic fruits, then, may act as decoys that divert herbivores away from fruits that contain plant offspring.     

Chemical barriers to adaptation by a specialist herbivore

Summary Depressaria pastinacella, the parsnip webworm (Lepidoptera: Oecophoridae), feeds throughout eastern North America on Pastinaca sativa (wild parsnip) and few other species. The assumption that specialist herbivores such as the parsnip webworm are adapted to hostplant chemistry, and are therefore unaffected by chemical variation in hostplants, was tested. Flower buds from plants grown first in the greenhouse and then in the field were fed to ultimate instar webworms. Plant phenotype had a significant effect on virtually all webworm food utilization parameters. While nutritional factors (i.e., nitrogen content) were correlated with approximate digestibility, two constituents of the flowers — bergapten and xanthotoxin, both linear furanocoumarins — independently accounted for a significant amount of variation in food utilization indicies. The physiological effects of these furanocoumarins were confirmed in artificial diet experiments. Despite the fact that the two most important furanocoumarins in parsnip flowers relative to webworm feeding and growth are isomers, differing only in the positioning of a methoxy substituent, they have different physiological effects; while xanthotoxin in general has no effect on growth, bergapten decreases growth and digestibility of the diet. These results underscore the need in studies of plant-animal interactions to examine individual chemical components rather than classes of compounds.     

Reduced Aggressive Behavior: A Benefit of Silk-Spinning in the Parsnip Webworm, Depressaria pastinacella (Lepidoptera: Oecophoridae)

The parsnip webworm, Depressaria pastinacella, spins a silken web within the umbels of its host plant, the wild parsnip Pastinaca sativa, and aggressively defends this web against conspecifics. We first established experimentally that the number of aggressive interactions between caterpillars with their webs removed was significantly higher than for webworms with intact webs. In order to determine whether web-spinning acts to divide food resources and reduce aggressive interactions, we measured relative weight gain and total silk production of parsnip webworms isolated from one another, grouped together with webbing undisturbed, and grouped together with webbing removed daily. Parsnip webworms isolated from one another and therefore unable to engage in aggressive interactions attained the highest pupal weights and spun the smallest amount of silk; caterpillars with webs removed daily and therefore with frequent aggressive interactions until territories were reestablished had the lowest pupal weights and spun the greatest quantity of silk. Our findings indicate that, for the parsnip webworm, constructing a silken web reduces aggressive encounters among conspecifics.     

Generalist and specialist host–parasitoid associations respond differently to wild parsnip (Pastinaca sativa) defensive chemistry

1. Plant defensive chemistry is predicted to have a more negative effect on generalist herbivores and their parasitoids than on specialist herbivores and their parasitoids. 2. This prediction was examined by comparing the effects of the wild parsnip (Pastinaca sativa L.) toxin, xanthotoxin, on a generalist herbivore–parasitoid association [the cabbage looper, Trichoplusia ni Hübner, and its polyembryonic parasitoid, Copidosoma floridanum (Ashmead)] and a specialist herbivore–parasitoid association [the parsnip webworm, Depressaria pastinacella (Duponchel), and its polyembryonic parasitoid, Copidosoma sosares (Walker)]. 3. Copidosoma floridanum brood sizes were smaller and experienced lower survivorship when reared in a host feeding on an artificial diet containing a low concentration of xanthotoxin. No T. ni hosts, parasitised or unparasitised, survived on a diet high in xanthotoxin. In contrast, C. sosares brood size and survivorship were unaffected by the presence of low levels of xanthotoxin in the host diet. Copidosoma sosares experienced reduced brood size and survivorship only when its host consumed a diet containing 15 times the level of xanthotoxin as the diet adversely affecting its congener. 4. The differences in response to xanthotoxin exhibited by C. floridanum and C. sosares are explained partly by a differential reduction in host quality and partly by differential exposure to xanthotoxin in host haemolymph. Unlike D. pastinacella, T. ni experienced reduced pupal weight and survivorship and prolonged developmental time on a low‐xanthotoxin diet. More xanthotoxin passed unmetabolised into the haemolymph of T. ni than into the haemolymph of D. pastinacella.     

Effects of florivory on floral volatile emissions and pollination success in the wild parsnip

In addition to reducing fitness by consuming reproductive structures, florivores may also reduce plant fitness by altering interactions with pollinators. To date, the effects of florivore activity on the volatile profile of flowers and subsequent attractiveness to pollinators have not been extensively investigated. In this study, we had three specific objectives: to determine the impact of florivory by the parsnip webworm Depressaria pastinacella on the floral volatile profile of the wild parsnip Pastinaca sativa, to ascertain the mechanisms by which florivory changes the volatile profile, and to estimate the consequences of florivory on visitation by pollinators and eventual seed set. An overall indirect effect of webworms on seed set, that is, the effect of infestation on pollination success, was not detected. However, this overall lack of indirect effect masks the heterogeneity among individual plants. For seven of 14 plants examined, pollination success was altered by webworms, and in four of these plants the alteration in pollination success was consistent with webworm-altered visitation. Webworms significantly altered floral fragrance, in particular causing disproportionate increases in the emissions of octyl esters. Additionally, volatiles from webworm frass, which contains large amounts of the octyl ester metabolite n-octanol, may alter the floral fragrance in ways that change attractiveness of flowers to pollinators. This study suggests that the effects of florivores on plant fitness are not limited to the removal of floral units but may also involve alterations in floral volatile composition, through damage-induced release and detoxification of particular constituents, that affect visitation and pollination success. Handling Editor: Steve Johnson. An erratum to this article can be found at     

Geographic variation in performance of a widespread generalist insect herbivore

1. Generalist herbivores are often widespread and occur in a variety of environments. Due to their broad distribution, it is likely that some populations of generalists will encounter host plants with geographic variation in traits that could affect the herbivore's growth and survival (i.e. performance). However, the geographic pattern of performance has rarely been studied for generalists, especially across large geographic ranges. 2. This study used one of the most generalist herbivore species known, the fall webworm (Hyphantria cunea Drury 1773, Erebidae, Lepidoptera), to experimentally test how the performance of a local population of fall webworms varies with increasing geographic distance of the host plant population from the local herbivore population. Specifically, a transplant experiment was used to compare the performance of one fall webworm population feeding on its local host plants with its performance on host populations from two other locations, 1300 and 2600 km away. 3. It was found that fall webworms performed better on their local host plant populations than on populations from other regions, with performance at its lowest when reared on hosts of the same species from the farthest region. It was also found that local fall webworms do not perform well on hosts commonly used by fall webworms at the other two, more distant sites. 4. This study helps to elucidate how the performance of generalist herbivores varies along their geographic range and suggests possible local adaptation to different sets of hosts across sites.     

CONSTRAINTS ON CHEMICAL COEVOLUTION: WILD PARSNIPS AND THE PARSNIP WEBWORM

The parsnip webworm (Depressaria pastinacella) and the wild parsnip (Pastinaca sativa) together represent a potentially “coevolved” system in that throughout their ranges the plant has relatively few other herbivores and the insect has virtually no other hosts. Individual wild parsnip plants within a central Illinois population vary in their content and composition of furanocoumarins, secondary compounds with insecticidal properties. Half-sib and parent-offspring regression estimates of the heritability of furanocoumarins demonstrate that this variation is genetically based. Wild parsnip plants also vary in their resistance to damage by the parsnip webworm, which feeds on flowers and developing seeds. In an experimental garden, seed production in the primary umbel ranged from 0 to 1,664 seeds among individuals, and mean seed production of half-sib families ranged from 3.7 seeds to 446.0 seeds. Approximately 75% of the variation in resistance among half-sib families to D. pastinacella was attributable to four furanocoumarin characteristics—resistance is positively related to the proportion of bergapten and the amount of sphondin in seeds, and negatively related to the amount of bergapten and the proportion of sphondin in leaves. Each of the four resistance factors had significant heritability. Thus, resistance in wild parsnip to the parsnip webworm is to a large extent chemically based and genetically controlled. Genetic correlations among fitness and resistance characters, however, tend to limit coevolutionary responses between herbivore and plant. In greenhouse plants protected from herbivory, several of the resistance factors have negative genetic correlations with potential seed production. Ostensibly, highly resistant plants in the absence of herbivory would be at a competitive disadvantage in the field. The selective impact of the herbivore is also limited in this population by a negative genetic correlation among resistance factors. Selection to increase one resistance factor (e.g., the proportion of bergapten in the seed) would at the same time decrease the amount of a second resistance factor (e.g., the amount of sphondin in the seed). The wild parsnip and the parsnip webworm, then, appear to have reached an evolutionary “stalemate” in the coevolutionary arms race.     

Impact of reassociation with a coevolved herbivore on oviposition deterrence in a hostplant

Although selection by herbivores for increased feeding deterrence in hostplants is well documented, selection for increased oviposition deterrence is rarely examined. We investigated chemical mediation of oviposition by the parsnip webworm (Depressaria pastinacella) on its principal hostplant Pastinaca sativa to determine whether ovipositing adults choose hostplants based on larval suitability and whether hostplants experience selection for increased oviposition deterrence. Webworms consume floral tissues and florivory selects for increased feeding deterrents; moths, however, oviposit on leaves of pre-bolting plants. Exclusive use of different plant parts for oviposition and larval feeding suggests oviposition should select for increased foliar deterrents. Recent webworm colonization of New Zealand (NZ) allowed us to assess phenotypic changes in foliar chemicals in response to webworm oviposition. In a common garden experiment, we compared NZ populations with and without a history of infestation from 2004 to 2006 for changes in leaf chemistry in response to oviposition. Three leaf volatiles, cis- and trans-ocimene, and β-farnesene, elicit strong responses in female moth antennae; these compounds were negatively associated with oviposition and are likely oviposition deterrents. Leaf β-farnesene was positively correlated with floral furanocoumarins that deter florivory; greater oviposition on plants with low floral furanocoumarins indicates that moths preferentially oviposit on parsnips most suitable for larval growth. Unlike florivory, high oviposition on leaves did not lower plant fitness, consistent with the fact that NZ parsnip foliar chemistry was unaffected by 3–6 years of webworm infestation. Thus, in this system, selection by ovipositing moths on foliar chemistry is weaker than selection by larvae on floral chemistry.     

Optimal defence, kin conflict and the distribution of furanocoumarins among offspring of wild parsnip

The factors influencing the allocation of chemical defences to plant offspring have largely been unexplored, conceptually and experimentally. Because evolutionary interactions between maternal plants and their progeny can affect resource allocation patterns among sibling offspring, we suggest that kin conflict as well as herbivore–plant interaction theories need to be considered to predict chemical defence allocation patterns. Optimal defence theory predicts that maternal plants should defend more heavily those offspring in which resources have been disproportionately invested. In contrast, kin conflict theory predicts that natural selection will favour genotypes that can compete successfully for maternal defences irrespective of their quality, even at the expense of the fitness of siblings and the maternal plant. Evidence for these defence patterns were evaluated by examining the allocation of furanocoumarins to seeds of the wild parsnip (Pastinaca sativa, Apiaceae). Furanocoumarins are toxins that are localized within the oil tubes of the maternal tissues of seeds. We evaluated the role of offspring investment (endosperm mass) and seed genotype on furanocoumarin allocation by mating an array of pollen donors with pollen recipients. Furanocoumarins were found to be positively correlated with endosperm mass on one side of the seed, a result consistent with optimal defence theory; however, on the other side of the seed, furanocoumarin content was influenced by seed genotype and was unrelated to endosperm mass. These effects varied with maternal plant. Further experiments demonstrated that nearly 80% of furanocoumarin production occurs after pollination, when fertilization products are active. Although the amount of furanocoumarin influenced by the seed genotype is small relative to the total quantity in the seed, these furanocoumarins are the first line of defence against important predators, such as the parsnip webworm, Depressaria pastinacella (Lepidoptera: Oecophoridae). We found that parsnip webworm larvae were able to discriminate among genotypes within an inflorescence. In line with previous studies, these results suggest that a genotype's ability to influence furanocoumarin defence may affect its probability of survival. We conclude that the distribution of defences among plant offspring in wild parsnip is probably influenced by competition among seed genotypes that conflicts with maternal optimal defence. This revised version was published online in July 2006 with corrections to the Cover Date.     

The evolutionary response of predators to dangerous prey: hotspots and coldspots in the geographic mosaic of coevolution between garter snakes and newts

The "geographic mosaic" approach to understanding coevolution is predicated on the existence of variable selection across the landscape of an interaction between species. A range of ecological factors, from differences in resource availability to differences in community composition, can generate such a mosaic of selection among populations, and thereby differences in the strength of coevolution. The result is a mixture of hotspots, where reciprocal selection is strong, and coldspots, where reciprocal selection is weak or absent, throughout the ranges of species. Population subdivision further provides the opportunity for nonadaptive forces, including gene flow, drift, and metapopulation dynamics, to influence the coevolutionary interaction between species. Some predicted results of this geographic mosaic of coevolution include maladapted or mismatched phenotypes, maintenance of high levels of polymorphism, and prevention of stable equilibrium trait combinations. To evaluate the potential for the geographic mosaic to influence predator-prey coevolution, we investigated the geographic pattern of genetically determined TTX resistance in the garter snake Thamnophis sirtalis over much of the range of its ecological interaction with toxic newts of genus Taricha. We assayed TTX resistance in over 2900 garter snakes representing 333 families from 40 populations throughout western North America. Our results provide dramatic evidence that geographic structure is an important component in coevolutionary interactions between predators and prey. Resistance levels vary substantially (over three orders of magnitude) among populations and over short distances. The spatial array of variation is consistent with two areas of intense evolutionary response by predators ("hotspots") surrounded by clines of decreasing resistance. Some general predictions of the geographic mosaic process are supported, including clinal variation in phenotypes, polymorphism in some populations, and divergent outcomes of the interaction between predator and prey. Conversely, our data provide little support for one of the major predictions, mismatched values of interacting traits. Two lines of evidence suggest selection is paramount in determining population variation in resistance. First, phylogenetic information indicates that two hotspots of TTX resistance have evolved independently. Second, in the one region that TTX levels in prey have been quantified, resistance and toxicity levels match almost perfectly over a wide phenotypic and geographic range. However, these results do not preclude the role the nonadaptive forces in generating the overall geographic mosaic of TTX resistance. Much work remains to fill in the geographic pattern of variation among prey populations and, just as importantly, to explore the variation in the ecology of the interaction that occurs within populations.     

The influence of a competitor on the geographic mosaic of coevolution between crossbills and lodgepole pine

The geographic mosaic theory of coevolution posits that the form of selection between interacting species varies across a landscape with coevolution important and active in some locations (i.e., coevolutionary hotspots) but not in others (i.e., coevolutionary coldspots). We tested the hypothesis that the presence of red squirrels (Tamiasciurus hudsonicus) affects the occurrence of coevolution between red crossbills (Loxia curvirostra complex) and Rocky Mountain lodgepole pine (Pinus contorta ssp. latifolia) and thereby provides a mechanism giving rise to a geographic mosaic of selection. Red squirrels are the predominant predispersal seed predator and selective agent on lodgepole pine cones. However, in four isolated mountain ranges east and west of the Rocky Mountains, red squirrels are absent and red crossbills are the main predispersal seed predator. These isolated populations of pine have apparently evolved without Tamiasciurus for about 10,000 to 12,000 years. Based on published morphological, genetic, and paleobotanical studies, we infer that cone traits in these isolated populations that show parallel differences from cones in the Rocky Mountains have changed in parallel. We used data on crossbill and conifer cone morphology and feeding preferences and efficiency to detect whether red crossbills and lodgepole pine exhibit reciprocal adaptations, which would imply coevolution. Cone traits that act to deter Tamiasciurus and result in high ratios of cone mass to seed mass were less developed in the isolated populations. Cone traits that act to deter crossbills include larger and thicker scales and perhaps increased overlap between successive scales and were enhanced in the isolated populations. In the larger, isolated mountain ranges crossbills have evolved deeper, shorter, and therefore more decurved bills to exploit these cones. This provides crossbills with higher feeding rates, and the change in bill shape has improved efficiency by reducing the concomitant increases in body mass and daily energy expenditures that would have resulted if only bill size had increased. These parallel adaptations and counter adaptations in red crossbills and lodgepole pine are interpreted as reciprocal adaptations and imply that these crossbills and pine are in coevolutionary arms races where red squirrels are absent (i.e., coevolutionary hotspots) but not where red squirrels are present (i.e., coevolutionary cold-spots).     

The geographic structure of selection on a coevolving interaction between social parasitic wasps and their hosts hampers social evolution

Social parasites exploit societies, rather than organisms, and rear their brood in social insect colonies at the expense of their hosts, triggering a coevolutionary process that may affect host social structure. The resulting coevolutionary trajectories may be further altered by selection imposed by predators, which exploit the abundant resources concentrated in these nests. Here, we show that geographic differences in selection imposed by predators affects the structure of selection on coevolving hosts and their social parasites. In a multiyear study, we monitored the fate of the annual breeding attempts of the solitary nesting foundresses of Polistes biglumis wasps in four geographically distinct populations that varied in levels of attack by the congeneric social parasite, P. atrimandibularis. Foundress fitness depended mostly on whether, during the long founding phase, a colony was invaded by social parasites or attacked by predators. Foundresses from each population differed in morphological traits and reproductive tactics that were consistent with selection imposed by their natural enemies and in ways that may affect host sociality. In turn, parasite traits were consistent with selection imposed locally by hosts, implying a geographic mosaic of coevolution in this brood parasitic interaction.     

Coevolution in temporally variable environments

Many potentially mutualistic interactions are conditional, with selection that varies between mutualism and antagonism over space and time. We develop a genetic model of temporally variable coevolution that incorporates stochastic fluctuations between mutualism and antagonism. We use this model to determine conditions necessary for the coevolution of matching traits between a host and a conditional mutualist. Using an analytical approximation, we show that matching traits will coevolve when the geometric mean interaction is mutualistic. When this condition does not hold, polymorphism and trait mismatching are maintained, and coevolutionary cycles may result. Numerical simulations verify this prediction and suggest that it remains robust in the presence of temporal autocorrelation. These results are compared with those from spatial models with unrestricted movement. The comparisons demonstrate that gene flow is unnecessary for generating empirical patterns predicted by the geographic mosaic theory of coevolution.     

Phylogeography and the geographic cline in the armament of a seed-predatory weevil: effects of historical events vs. natural selection from the host plant

Japanese camellia (Camellia japonica) and its seed predator, the camellia weevil (Curculio camelliae), provide a notable example of a geographic mosaic of coevolution. In the species interaction, the offensive trait of the weevil (rostrum length) and the defensive trait of the plant (pericarp thickness) are involved in a geographically-structured arms race, and these traits and selective pressures acting on the plant defence vary greatly across a geographical landscape. To further explore the geographical structure of this interspecific interaction, we tested whether the geographical variation in the weevil rostrum over an 800-km range along latitude is attributed to local natural selection or constrained by historical (phylogeographical) events of local populations. Phylogeographical analyses of the mitochondrial DNA sequences of the camellia weevil revealed that this species has experienced differentiation into two regions, with a population bottleneck and subsequent range and/or population expansion within each region. Although these phylogeographical factors have affected the variation in rostrum length, analyses of competing factors for the geographical variation revealed that this pattern is primarily determined by the defensive trait of the host plant rather than by the effects of historical events of populations and a climatic factor (annual mean temperature). Thus, our study suggests the overwhelming strength of coevolutionary selection against the effect of historical events, which may have limited local adaptation.     

Arms Race Coevolution: The Local and Geographical Structure of a Host–Parasite Interaction

Consideration of complex geographic patterns of reciprocal adaptation has provided insight into new features of the coevolutionary process. In this paper, we provide ecological, historical, and geographical evidence for coevolution under complex temporal and spatial scenarios that include intermittent selection, species turnover across localities, and a range of trait match/mismatch across populations. Our study focuses on a plant host–parasitic plant interaction endemic to arid and semiarid regions of Chile. The long spines of Chilean cacti have been suggested to evolve under parasite-mediated selection as a first line of defense against the mistletoe Tristerix aphyllus. The mistletoe, in turn, has evolved an extremely long morphological structure that emerges from the seed endosperm (radicle) to reach the host cuticle. When spine length was traced along cactus phylogenies, a significant association between spine length and parasitism was detected, indicating that defensive traits evolved in high correspondence with the presence or absence of parasitism in two cactus lineages. Assessment of spine-radicle matching across populations revealed a potential for coevolution in 50% of interaction pairs. Interestingly, hot spots for coevolution did not distribute at random across sites. On the contrary, interaction pairs showing high matching values occur mostly in the northern distribution of the interaction, suggesting a geographical structure for coevolution in this system. Only three sampled interaction pairs were so mismatched that reciprocal selection could not occur given current trait distributions. Overall, different lines of evidence indicate that arms-race coevolution is an ongoing phenomenon that occurs in the global system of interconnected populations.     

Epidemiological, evolutionary, and coevolutionary implications of context-dependent parasitism

Abstract Victims of infection are expected to suffer increasingly as parasite population growth increases. Yet, under some conditions, faster-growing parasites do not appear to cause more damage, and infections can be quite tolerable. We studied these conditions by assessing how the relationship between parasite population growth and host health is sensitive to environmental variation. In experimental infections of the crustacean Daphnia magna and its bacterial parasite Pasteuria ramosa, we show how easily an interaction can shift from a severe interaction, that is, when host fitness declines substantially with each unit of parasite growth, to a tolerable relationship by changing only simple environmental variables: temperature and food availability. We explored the evolutionary and epidemiological implications of such a shift by modeling pathogen evolution and disease spread under different levels of infection severity and found that environmental shifts that promote tolerance ultimately result in populations harboring more parasitized individuals. We also find that the opportunity for selection, as indicated by the variance around traits, varied considerably with the environmental treatment. Thus, our results suggest two mechanisms that could underlie coevolutionary hotspots and coldspots: spatial variation in tolerance and spatial variation in the opportunity for selection.     

Abundance trumps quality: bi‐trophic performance and parasitism risk fail to explain host use in the fall webworm

Factors including host abundance, quality, and the degree to which hosts provide enemy‐free space (EFS) may drive host plant choice by phytophagous insects. Herbivores may also experience fitness tradeoffs among hosts, promoting polyphagy. The fall webworm Hyphantria cunea is a dietary generalist that feeds on a broad array of trees across its geographic range. Here, we investigate the drivers of host tree use by the fall webworm in Connecticut (CT) and Maryland (MD). Neither caterpillar performance nor EFS was associated with the frequency with which host trees were used, and no tradeoff between host quality and EFS was identified. Vegetation surveys adjacent to host trees showed that at both localities, host use was non‐random with respect to tree species, and that the main predictor of use among suitable host trees was host tree abundance. This suggests that webworms are under selection to reduce search time for oviposition sites. Although we did not detect a tradeoff between host plant quality and availability in MD, we did identify that tradeoff in CT. This disparity amid otherwise similar patterns of host use between CT and MD may be explained by the relative rarity of high quality hosts in CT compared to MD. Our results illustrate that geographic mosaics in patterns of host use may arise in the absence of local adaptation if host use is based upon availability rather than host plant attributes.