Genetic variation in foraging traits among inbred lines of a predatory mite

Response of predators to herbivore-induced plant volatiles can affect the length of time a predator spends in a prey patch and the probability of a predator finding a new prey patch. Variation in response to herbivore-induced plant volatiles may lead to different foraging decisions among individuals, thereby affecting both within-patch dynamics and between-patch dispersal. We found significant phenotypic and additive genetic variation in two behavioral assays of response to herbivore-induced plant volatiles among inbred isofemale lines of the predatory mite, Phytoseiulus persimilis. In wind-tunnel tests to measure patch residence time, adult female predators from certain lines left prey patches sooner than others when a distant source of herbivore-induced plant volatiles was presented; whereas such variation disappeared when no distant volatiles were presented. In a measure of patch location, certain lines were more likely than others to locate a prey-infested leaf disc; again there was no difference when uninfested leaf discs were used. Patch location was negatively correlated with patch residence. That is, lines that were more likely to leave a prey patch in the presence of distant volatiles were also more likely to find an odor source (ie, prey patch) from a distance of 20 cm. These two foraging-related behaviors are heritable. A continuous distribution of both behaviors indicated that several to many loci may be responsible for these behavioral traits. Our line-crossing experiments suggested that maternal influence could be excluded. Substantial phenotypic variation in two other foraging-related traits, consumption and oviposition, were also detected among inbred lines. Consumption and oviposition were positively correlated; however, the relationship (slope) varied among inbred lines, suggesting that predatory mites vary in food conversion efficiency. A relationship was detected between patch residence and consumption. Patch location, as one important foraging trait, appeared to be negatively related to consumption, suggesting a trade-off between searching for patches and reproduction.     

Correlation between Olfactory Responses, Dispersal Tendencies, and Life-history Traits of the Predatory Mite Neoseiulus Womersleyi (Acari: Phytoseiidae) of Eight Local Populations

To investigate the relationship between foraging behavior and life-history traits of the predatory mite Neoseiulus womersleyi, the olfactory responses, dispersal ratios from a prey patch, predation rates, fecundity, and developmental times in eight local populations of N. womersleyi were investigated. Significant differences among local populations were found in all these traits except fecundity. None of the life-history traits correlated with foraging behavior. A significant positive correlation was found only between the olfactory response and the dispersal ratio. These results suggested that predatory mites with low olfactory responses would stay in a prey patch longer than predatory mites with high olfactory responses.     

Effects of Light on the Tritrophic Interaction Between Kidney Bean Plants, Two-Spotted Spider Mites and Predatory Mites, Amblyseius Womersleyi (Acari: Phytoseiidae)

By analyzing the volatiles from Tetranychus urticae-infested kidney bean plants (Phaseolus vulgaris) at different times for two days, we found that they were mainly produced in the light. Tetranychus urticae showed a higher oviposition rate and spent more time feeding during the day (in the light) than at night (in the dark). Infested leaves placed in the light attracted the predatory mite Amblyseius womersleyi, whereas those that were placed in the dark for at least 2h in daytime did not. This indicates that presence or absence of light affects the production of herbivore-induced plant volatiles. Amblyseius womersleyi dispersed more frequently and consumed more T. urticae eggs during the day (in the light) than at night (in the dark), whereas their oviposition rate did not differ between day and night. Presence or absence of herbivore-induced plant volatiles in the surroundings did not affect dispersal, predation or oviposition rates of A. womersleyi. These results show that A. womersleyis behavior coincides with the production pattern of herbivore-induced plant volatiles.     

Response of a phytoseiid predator to herbivore-Induced plant volatiles: Selection on attraction and effect on prey exploitation

Bean plants infested with herbivorous spider mites emit volatile chemicals that are attractive toP. persimilis, a predator of spider mites. In Y-tube olfactometer tests we evaluated involvement of a genetic component in predator response to herbivore-induced plant volatiles. Replicated bidirectional selection resulted in a significant increase in attraction after one generation of selection, but no decrease even after three generations of selection, indicating significant, but unbalanced, additive genetic variation in predator perception of, or response to, herbivore-induced plant volatiles. Selected lines responded differently than an unselected population to food deprivation, pointing to an interaction between their internal state and response to plant volatiles. Selected lines also differed from unselected ones in behaviors associated with local prey exploitation, such as residence time, prey consumption, and reproduction. At lower prey densities,P. persimilis from both “+” lines left spider mite-infested leaves more rapidly and consumed fewer prey eggs than an unselected population. Defining olfactory components of predator search behavior is one step in understanding the effect of plant volatiles on predator foraging efficiency. By selecting lines differing in their attraction to herbivore-induced plant volatiles we may experimentally investigate the link between this behavior, predator foraging efficiency, and local and regional predator-prey population dynamics. The impact of significant additive genetic variation in predator response to plant volatiles on evolution in a tritrophic context also remains to be uncovered.     

Variation in the olfactory response of 13 populations of the predatory mite Amblyseius womersleyi to Tetranychus urticae-infested plant volatiles (Acari: Phytoseiidae, Tetranychidae)

We studied the response of the predatory mite Amblyseius womersleyi collected in 13 different sites in Japan toward Tetranychus urticae-infested kidney bean leaf volatiles in a Y-tube olfactometer. The predatory mites were collected from eight plant species infested by one of three tetranychid mite species. The predators' responses to the infested-leaf volatiles varied from 33% to 97% among the populations. The predators collected at 10 sites showed a significant preference for infested-leaf volatiles, whereas those collected at three tea plantations did not distinguish between the infested- and uninfested-leaf volatiles. We discussed the possible factors that affected the olfactory response of A. womersleyi towards the infested leaf volatiles.     

Genetic variations in a population of herbivorous mites Tetranychus urticae in the production of the induced volatiles by kidney bean plants

Abstract

This study tested whether a population of herbivorous mites Tetranychus urticae exhibits genetic variation in the production of induced plant volatiles in kidney bean plants (Phaseolus vulgaris L.). We selected two T. urticae genotypes based on their dispersal behavior (early- and late-disperser) in two plant lines (Line-1 and Line-2). In both lines, plants infested by the early-disperser produced large amounts of induced volatiles after the spider mite population peaked on the plants, whereas those infested by the late-disperser emitted the largest amount of induced volatiles at the population peak. The possible manipulation of the production of herbivore-induced plant volatiles by herbivores is discussed.     

Patch-Leaving Decision of the Predatory Mite Amblyseius womersleyi (Acari: Phytoseiidae) Based on Multiple Signals from Both Inside and Outside a Prey Patch

We compared the emigration rates of Amblyseius womersleyi from prey patches (leaf disks) of different conditions in airflow containing either infested plant volatiles (volatiles airflow) or uninfested plant volatiles (control airflow). Both airflow and prey patch conditions significantly affected the emigration rates. Emigration rates from patches carrying prey products (feces, exuviae, webs, etc.) and prey eggs were significantly lower in control airflow than in volatiles airflow. Under other patch conditions, the rates were lower in control airflow than in volatiles airflow, although the difference was not significant. In both airflows, the lowest emigration rates were observed when predators were in a heavily infested patch. Patches carrying prey products and prey eggs resulted in lower emigration rates than patches carrying eggs alone and patches emitting prey-infested plant volatiles but carrying no prey. Thus, A. womersleyi appears to decide the timing of emigration based on two criteria: prey products in the patch and prey-infested plant volatiles from outside.     

Do Herbivore-Induced Plant Volatiles Influence Predator Migration and Local Dynamics of Herbivorous and Predatory Mites?

If predators lack information on the prey's position, prey have more chance to escape predation and will therefore reach higher population densities. One of the many possible cues that predators may use to find their prey are herbivore-induced plant volatiles. Although their effects on the behaviour of foraging predators have been well studied, little is known about how these prey-related odours affect predator–prey dynamics on a plant. We hypothesise that herbivore-induced plant volatiles provide the major cue eliciting predator arrestment on prey-infested leaves and that the response to these volatiles ultimately leads to lower prey densities. To test this hypothesis experimentally, we created two types of odour-saturated environments: one with herbivore-induced plant volatiles (treatment), and one with green-leaf volatiles (control). An odour-free environment could not be tested because herbivores require plants for population growth. We measured the rate at which predatory mites (Phytoseiulus persimilis) immigrate, emigrate and exploit a single leaf infested by two-spotted spider mites (Tetranychus urticae). The experiments did not show a significant difference between treatment and control. At best, there was a somewhat higher rate of predator (and possibly also prey) emigration in the treatment. The lack of a pronounced difference between treatment and control indicates that at the spatial scale of the experiments random searching for prey was as effective as directional searching. Alternatively, predators were arrested in the prey patch by responding not merely to herbivore-induced plant volatiles, but also to other prey-related cues, such as web and faeces. Based on our current experience we advocate to increase the spatial scale of the experiment (>1m²) and we provide other suggestions for improving the set-up.     

Conditioned olfactory responses of a predatory mite, Neoseiulus womersleyi, to volatiles from prey-infested plants

To clarify the prey‐finding behavior of the predatory mite Neoseiulus womersleyi (Schicha) (Acari: Phytoseiidae), we studied its olfactory responses to volatiles from the prey‐infested plant on which the mites had been collected. We used a local N. womersleyi population called Kanaya collected from tea (Camellia sinensis L.) (Theaceae) plants infested by Tetranychus kanzawai Kishida (Acari: Tetranychidae) in Kanaya City, Japan. Neoseiulus womersleyi (Kanaya population) were more attracted to volatiles from tea plants infested with five female T. kanzawai per leaf for 7 days than to intact tea leaves in a Y‐tube olfactometer. Tetranychus kanzawai‐induced tea leaf volatiles were identified as (E)‐β‐ocimene, (E)‐4,8‐dimethyl‐1,3,7‐nonatriene, and (E,E)‐α‐farnesene. As olfactory responses are known to differ among local populations of N. womersleyi, we compared the responses of the Kanaya population with those of a Kikugawa population collected from tea plants infested by T. kanzawai in Kikugawa City. To test the influence of previous predation experience, we reared the two populations on tea plants infested by T. kanzawai or on kidney bean plants (Phaseolus vulgaris) infested by Tetranychus urticae Koch. The Kanaya population was more attracted to the volatiles from infested plants on which they had been reared. Because the Kanaya population was not attracted to the plant volatiles they had not previously experienced, the positive response to previously experienced volatiles might be the result of learning. By contrast, the Kikugawa population showed no preference for previously experienced volatiles from infested plants. The implications of this flexibility in foraging behavior are discussed.     

Innate responses of the predatory mite <Emphasis Type="Italic">Phytoseiulus persimilis</Emphasis> to a herbivore-induced plant volatile

The responses of the predatory mite P. persimilis to herbivore-induced plant volatiles are at least partly genetically determined. Thus, there is potential for the evolution of this behaviour by natural selection. We tested whether distinct predator genotypes with contrasting responses to a specific herbivore-induced plant volatile, i.e. methyl salicylate (MeSa), could be found in a base population collected in the field (Sicily). To this end, we imposed purifying selection on individuals within iso-female lines of P. persimilis such that the lines were propagated only via the individual that showed either a preference or avoidance of MeSa. The responses of the lines were characterized as the mean proportion of individuals choosing MeSa when given a choice between MeSa and clean air. Significant variation in predator responses was detected among iso-female lines, thus confirming the presence of a genetic component for this behaviour. Nevertheless, we did not find a significant difference in the response to MeSa between the lines that were selected to avoid MeSa and the lines selected to prefer MeSa. Instead, in the course of selection the lines selected to avoid MeSa shifted their mean response towards a preference for MeSa. An inverse, albeit weaker, shift was detected for the lines selected to prefer MeSa. We discuss the factors that may have caused the apparent lack of a response to selection within iso-female line in this study and propose experimental approaches that address them.     

Morphology of the olfactory system in the predatory mite Phytoseiulus Persimilis

The predatory mite Phytoseiulus persimilis locates its prey, the two-spotted spider mite, by means of herbivore-induced plant volatiles. The olfactory response to this quantitatively and qualitatively variable source of information is particularly well documented. The mites perform this task with a peripheral olfactory system that consists of just five putative olfactory sensilla that reside in a dorsal field at the tip of their first pair of legs. The receptor cells innervate a glomerular olfactory lobe just ventral of the first pedal ganglion. We have made a 3D reconstruction of the caudal half of the olfactory lobe in adult females. The glomerular organization as well as the glomerular innervation appears conserved across different individuals. The adult females have, by approximation, a 1:1 ratio of olfactory receptor cells to olfactory glomeruli.     

Utilization of a Photosystem by Drosophila melanogaster Larvae (Diptera: Drosophilidae)

Foraging-stage third-instar larvae from most wild-type (normal) Drosophila melanogaster stocks are generally repelled by light. To identify factors that affect the larval photoresponse, we elucidated the effects of age, temperature, and time on the photoresponse of larvae from a wild-type Canton-S stock. In addition, we analyzed the larvae from the LI2 isofemale line, which are unresponsive to light in a photoassay. To determine whether LI2 larvae behave abnormally on other behavioral paradigms, in comparison to Canton-S controls, we tested larvae in taste and olfactory assays and observed them to determine whether they dispersed in a food source. Like Canton-S larvae, LI2 larvae and other isofemale lines whose progenitors were collected from the same natural population are responsive to taste and olfactory stimuli. Moreover, LI2 larvae disperse in the food source, as do Canton-S larvae tested in the dark. Larvae expressing para^sbl mutations, which respond normally to light but not to chemical stimuli, do not disperse normally in the food source, suggesting that dispersal may be mediated by perception of chemical cues.     

Response of a complex foraging phenotype to artificial selection on its component traits

In nature, where predators must often track dynamic and dispersed prey populations, predator consumption rate, conversion efficiency, dispersal, and prey finding are likely to be important links between foraging and predator–prey population dynamics. Small differences in predator foraging caused by variation in any of the abovementioned traits might lead to significant differences in predator success as well as population dynamics. We used artificial selection to create lines of the predatory mite, Phytoseiulus persimilis in order to determine the potential for or constraints on the evolution of predator foraging behaviors. All four foraging traits demonstrated considerable phenotypic variation. They also exhibited significant realized heritabilities after artificial selection, except that prey finding did not respond to downward selection. Lines that responded to selection did so rapidly, and high-consumption, high-conversion efficiency, and high- and low-dispersal were stable for at least four generations after artificial selection was relaxed. There were some indirect responses to selection among the foraging traits. For example, there was positive correlation between consumption and dispersal. However, none of the correlated responses were of the magnitude of the direct responses we measured on the same trait. We also observed some correlations between foraging traits and life-history traits such as low-consumption and development time (negative), high-consumption and fecundity (positive), and high-conversion efficiency and fecundity (positive), but these were more likely to represent non-genetic constraints. Intrinsic rates of increase in low-consumption and low-conversion efficiency lines were lower than in their respective high lines and the unselected control, whereas rates of increase in dispersal and olfactory response lines did not differ from the unselected control. Thus, traits that make up foraging share partially overlapping genetic architectures with highly heritable phenotypic components, suggesting that each foraging trait will be able to respond rapidly to changes in the density and distribution of resources.     

Phenotypic plasticity and reaction norms of abdominal bristle number inDrosophila melanogaster

The phenotypic plasticity of abdominal bristle number (segments 3 and 4 in females) was investigated in 10 isofemale lines from a French population, grown at 7 constant temperatures, ranging from 12‡ to 31‡C. Overall concave reaction norms were obtained with a maximum around 20‡-21‡C. Intraclass correlation (isofemale line heritability) was not affected by temperature. Correlations between segments 3 and 4 strongly contrasted a low within-line phenotypic correlation (r = 0.39 ± 0.04) and a high, between-line genetic correlation (r = 0.89 ± 0.03). A significant decrease of the genetic correlation was observed when comparing more different temperatures. Finally, among 7 other morphometrical traits which were measured on the same set of lines, 3 provided a significant positive genetic correlation with abdominal bristles: thoracic bristles, abdomen pigmentation and thoracic pigmentation.     

The chemosensory basis for behavioral divergence involved in sympatric host shifts II: olfactory receptor neuron sensitivity and temporal firing pattern to individual key host volatiles

The Rhagoletis species complex has been a key player in the sympatric speciation debate for much of the last 50 years. Studies indicate that differences in olfactory preference for host fruit volatiles could be important in reproductively isolating flies infesting each type of fruit via premating barriers to gene flow. Single sensillum electrophysiology was used to compare the response characteristics of olfactory receptor neurons from apple, hawthorn, and flowering dogwood-origin populations of R. pomonella, as well as from the blueberry maggot, R. mendax (an outgroup). Eleven volatiles were selected as stimuli from behavioral/electroantennographic studies of the three R. pomonella host populations. Previously, we reported that differences in preference for host fruit volatile blends are not a function of alterations in the general class of receptor neurons tuned to key host volatiles. In the present study, population comparisons involving dose–response trials with the key volatiles revealed significant variability in olfactory receptor neuron sensitivity and temporal firing pattern both within and among Rhagoletis populations. It is concluded that such variability in peripheral sensitivity and temporal firing pattern could influence host preference and contribute to host fidelity and sympatric host shifts in the Rhagoletis complex.     

Intraspecific variation ofDrosophila buzzatii larval breeding success onOpuntia: A yeast-plant-insect relationship

The cactophilic species,Drosophila buzzatii, normally breeds in decaying pockets ofOpuntia cladodes, in which there is a complex interaction with the microbial flora, especially yeast species. Isofemale lines were used to estimate genetic variation among larvae reared on their natural feeding substrate. Four naturally occurring cactophilic yeast species isolated from the same Tunisian oasis as theDrosophila population were used. Two fitness components were studied for each line, viability and developmental time. Genetic variations amongD. buzzatii lines were observed for both traits. A significant yeast species x isofemale line interaction for viability was also evidenced, suggesting the occurrence of specialized genotypes for the utilization of breeding substrates. This genetic heterogeneity in the natural population may favor a better adaptation to the patchily distribution of yeasts.     

Quantitative Genetic Variation of Odor-Guided Behavior in a Natural Population of Drosophila Melanogaster

Quantitative genetic variation in behavioral response to the odorant, benzaldehyde, was assessed among a sample of 43 X and 35 third chromosomes extracted from a natural population and substituted into a common inbred background. Significant genetic variation among chromosome lines was detected. Heritability estimates for olfactory response, however, were low, as is typical for traits under natural selection. Furthermore, the loci affecting naturally occurring variation in olfactory response to benzaldehyde were not the same in males and females, since the genetic correlation between the sexes was low and not significantly different from zero for the chromosome 3 lines. Competitive fitness, viability and fertility of the chromosome 3 lines were estimated using the balancer equilibrium technique. Genetic correlations between fitness and odor-guided behavior were not significantly different from zero, suggesting the number of loci causing variation in olfactory response is small relative to the number of loci causing variation in fitness. Since different genes affect variation in olfactory response in males and females, genetic variation for olfactory response could be maintained by genotype X sex environment interaction. This unusual genetic architecture implies that divergent evolutionary trajectories for olfactory behavior may occur in males and females.     

Variation in flight response of the specialist parasitoidMacrocentrus grandii goidanich to odours from food plants of its European corn borer host

The specialist parasitoidMacrocentrus grandii Goidanich (Hymenoptera: Braconidae) appears to parasitize its polyphagous host, European corn borer (Ostrinia nubilalis (Hübner)) (Lepidoptera: Pyralidae), in only certain habitats. To determine whether it differed in its olfactory response to host-habitat odours, volatiles from four plants were isolated using Tenax. Wind tunnel bioassays of the extracts revealed that, besides corn which was tested in an earlier study, olfactory stimuli for attraction ofM. grandii females were present in potato and snap bean but not in pepper or soybean. To further characterize the response to pepper and soybean, these extracts were bioassayed in combination with an attractive extract. The results indicated that pepper volatiles evoked a neutral response inM. grandii while response to soybean volatiles appeared to be neutral or slightly negative. The innate response to soybean volatiles was altered to one of attraction after oviposition experience on soybean. Seven days after oviposition, experienced females continued to respond positively to soybean volatiles. Components of soybean volatiles responsible for the change in flight behaviour resulting from oviposition experience were eluted by nonpolar and slightly polar solvents. These results support the idea that plant odour may be a factor determining the range of plants on whichM. grandii parasitizes its host. The study indicates the occurrence of associative learning of plant-related volatiles during oviposition inM. grandii, and suggests the involvement of diverse plant compounds in the learning process.     

Genetic variation inMeloidogyne incognita virulence against the tomatoMi resistance gene: evidence from isofemale line selection studies

Resistance to the parthenogenetic root-knot nematodeMeloidogyne incognita is controlled in tomato by the single dominant geneMi, against which virulent pathotypes are able to develop. Isofemale lines (i.e., families) were established from a natural avirulent isolate ofM. incognita in order to study the genetic variability and inheritance of the nematode virulence. From the progeny of individual females, the production of egg masses on the root system of theMi-resistant tomato Piersol was analyzed in artificial selection experiments. A family analysis revealed, after two successive generations, a strongly significant variation between the 63 isofemale lines tested, and the results obtained for the mothers and their daughters were also significantly correlated. These results together clearly demonstrate the existence of a genetic variability and inheritance for this character. In a second experiment, a four-generation selection was performed on 31 other isofemale lines. The results revealed a significant response to selection apparently limited only to the two families able to produce, in first generation, a significant minimal egg-mass number on the resistant cultivar.