Host selection in insects: reproductive interference shapes behavior of ovipositing females

In nature, closely related species often utilize different host species, but it is still unclear what factors contribute to the evolution and maintenance of such diversified host selection. In this review, I describe how negative interspecific mating interactions (reproductive interference) can shape host selection by animals, focusing mainly on phytophagous and predatory insects. First, I explain an important premise of this hypothesis, which is that the adult reproductive site is the same as the feeding site for the offspring. Next, I describe several mathematical models and well-studied empirical systems to show that reproductive interference can sufficiently drive and maintain different host selection between phylogenetically related species. Then, I argue for the first time that reproductive interference can cause an oviposition preference in insects that is not optimal for the survival and development of the offspring, as a result of maternal adaptive behavior that maximizes the mother's own fitness. Furthermore, I argue that in insects, reproductive interference probably shapes oviposition behavior before the female alights on the host (e.g., habitat preference), without affecting post-alighting decision making. I would like to emphasize that these two arguments represent the novel approach to clarify the unrevealed pattern of complex insect oviposition behavior.     

Multifaceted determinants of host specificity in an aphid parasitoid

The host specificity of insect parasitoids and herbivores is thought to be shaped by a suite of traits that mediate host acceptance and host suitability. We conducted laboratory experiments to identify mechanisms shaping the host specificity of the aphid parasitoid Binodoxys communis. Twenty species of aphids were exposed to B. communis females in microcosms, and detailed observations and rearing studies of 15 of these species were done to determine whether patterns of host use resulted from variation in factors such as host acceptance or variation in host suitability. Six species of aphids exposed to B. communis showed no signs of parasitism. Four of these species were not recognized as hosts and two effectively defended themselves from attack by B. communis. Other aphid species into which parasitoids laid eggs had low suitability as hosts. Parasitoid mortality occurred in the egg or early larval stages for some of these hosts but for others it occurred in late larval stages. Two hypotheses explaining low suitability were investigated in separate experiments: the presence of endosymbiotic bacteria conferring resistance to parasitoids, and aphids feeding on toxic plants. An association between resistance and endosymbiont infection was found in one species (Aphis craccivora), and evidence for the toxic plant hypothesis was found for the milkweed aphids Aphis asclepiadis and Aphis nerii. This research highlights the multifaceted nature of factors determining host specificity in parasitoids.     

Oviposition Behavior and Conspecific Host Discrimination in Diachasmimorpha longicaudata (Hymenoptera: Braconidae), a Fruit Fly Parasitoid

We studied conspecific host discrimination and oviposition behavior of Diaschasmimorpha longicaudata (Ashmead), in third instar Anastrepha ludens (Loew) under laboratory conditions. The complete process of oviposition in D. longicaudata required an average of 29±11.7 s (Mean±SE), during which time the female remained completely immobile. This contrasts with attempts to oviposit for lesser durations (2-4 s), during which the female constantly moved her antennae and abdomen. In order to determine the host discrimination ability of this species (i.e., the capacity to distinguish between parasitized and non-parasitized hosts), third-instar A. ludens non-parasitized or parasitized 24 h earlier, were exposed simultaneously to individual female wasps with or without previous oviposition experience. An identical test was performed using larvae parasitized 48 h earlier. Both types of females showed a similar behavioral pattern of oviposition, but with significant differences in the number of eggs laid in parasitized and non-parasitized larvae. Experienced females showed reduced incidence of oviposition in parasitized larvae as well as a greater number of probes that did not lead to parasitism (rejection), although this difference was only significant in the 24-h test. This suggests that the host discrimination capacity of this parasitoid is innate and that previous oviposition experience increases the discrimination ability of females.     

Experimental infections of the monogenean Gyrodactylus turnbulli indicate that it is not a strict specialist

Parasites represent a threat to endangered fish species, particularly when the parasite can host switch and the new host is vulnerable. If the parasite is highly host specific then successful host switching should be a rare occurrence; however, the host range of many parasites which are assumed to be specialists has never been tested. This includes the monogenean Gyrodactylus turnbulli, a well-studied ectoparasite found caudally on its known host, the guppy, Poecilia reticulata. In this study, we monitored parasite establishment and reproduction on a range of poeciliids and more distantly related fish. Individually maintained fish were experimentally infected with a single parasite and monitored daily to establish whether G. turnbulli could survive and reproduce on other fish species. Gyrodactylus turnbulli can infect a wider range of hosts than previously considered, highlighting the fact that host specificity can never be assumed unless experimentally tested. Our findings also have significant implications for parasite transmission to novel hosts and provide further insight into the evolutionary origins of this ubiquitous group of fish pathogens. Previous molecular evidence indicates that host switching is the key mechanism for speciation within the genus Gyrodactylus. Until recently, most Gyrodactylus spp. were assumed to be narrowly host specific. However, our findings suggest that even so-called specialist species, such as G. turnbulli, may represent a threat to vulnerable fish stocks. In view of the potential importance of host switching under artificial conditions, we propose to describe this as 'artificial ecological transfer' as opposed to 'natural ecological transfer', host switching under natural conditions.     

Semi-field demographic performance of the invasive planthopper,Orosanga japonica (Hemiptera: Ricaniidae) on two host plants

Orosanga japonica Melichar (Hemiptera: Ricaniidae) is an invasive polyphagous pest in Iran. The planthopper damaged host plants by sap-sucking and egg laying on new twigs. This study aimed to determine the life table parameters of O. japonica on Rubus ulmifolius Schoot (elm leaf blackberry) and Melia azedarach L. (chinaberry) under field conditions in Rudsar (North of Iran) during 2019–2020. The collected life history data were analyzed based on age-stage, two-sex life table theory. The results showed that the incubation period of O. japonica was too long (≈ 270 days) on both host plants. The nymphs emerged from mid-May 2020. The planthopper had five nymphal stages under field conditions. The nymphal duration was 41.39 ± 0.56 days and 38.13 ± 0.62 days on R. ulmifolius and M. azedarach, respectively. The total preadult survival rates were 53.2% and 51.7% on R. ulmifolius and M. azedarach, respectively. Based on the results, a significant shorter total developmental time was observed on M. azedarach. When adults emerged in late July, they laid eggs after 26.05 days and 26.75 days on R. ulmifolius and M. azedarach, respectively. The fecundity on M. azedarach (131.69 egg/female) was significantly higher than that on R. ulmifolius. However, the life table parameters were all not significantly different on the two host plants. The intrinsic rate of increase (r) were 0.0097 ± 0.0005 day⁻¹ and 0.0105 ± 0.0006 day⁻¹ on R. ulmifolius and M. azedarach, respectively. Generally, these findings could be helpful to establish an efficient management strategy for this exotic pest.     

Oviposition pattern of phytophagous insects: on the importance of host population heterogeneity

Frequency distributions of insect immatures per host are often fitted to contagious distributions, such as the negative binomial, to deduce oviposition pattern. However, different mechanisms can be involved for each theoretical distribution and additional biological information is needed to correctly interpret the fits. We chose the chestnut weevil Curculio elephas, a pest of the European chestnut Castanea sativa, as a model to illustrate the difficulties of inferring oviposition pattern from fits to theoretical distributions and from the variance/mean ratio. From field studies over 13–16 years, we show that 20 out of the 31 yearly distributions available fit a negative binomial and 25 a zero-inflated Poisson (ZIP). No distribution fits a Poisson distribution. The ZIP distribution assumes heterogeneity within the fruit population. There are two categories of host: the first comprises chestnuts unsuitable for weevil oviposition or in excess relative to the number of weevil females, and the second comprises suitable fruits in which oviposition behavior is random. Our results confirm this host heterogeneity. According to the ZIP distribution, the first category of hosts includes on average 74% of the chestnuts. A negative binomial distribution may be generated by either true or false contagion. We show that neither interference between weevil females, nor spatial variation in the infestation rate exist. Consequently, the observed distributions of immatures are not the result of false contagion. Nevertheless, we cannot totally exlude true contagion of immatures. In this paper we discuss the difficulty of testing true contagion in natural conditions. These results show that we cannot systematically conclude in favour of contagion when fitting a distribution such as the negative binomial or when a variance/mean ratio is higher than unity. Received: 22 September 1997 / Accepted: 15 December 1997     

Food preference and performance of the larvae of a specialist herbivore: variation among and within host-plant populations

Specialist herbivores are suggested to be unaffected by or attracted to the defense compounds of their host-plants, and can even prefer higher levels of certain chemicals. Abrostola asclepiadis is a specialist herbivore whose larvae feed on the leaves of Vincetoxicum hirundinaria, which contains toxic alkaloids and is unpalatable to most generalist herbivores. The food choice, leaf consumption and growth of A. asclepiadis larvae were studied to determine whether there is variation among and within host-plant populations in their suitability for this specialist herbivore. There was significant variation in food preference and leaf consumption among host-plant populations, but no differences were found in larval growth and feeding on different host-plant populations. A. asclepiadis larvae preferred host-plant populations with higher alkaloid concentrations, but did not consume more leaf material from plants originating from such populations in a no-choice experiment. There was also some variation in food preference of larvae among host-plant individuals belonging to the same population, suggesting that there was variability in leaf chemistry also within populations. Such variation in larval preference among host-plant genotypes and populations may create potential for coevolutionary dynamics in a spatial mosaic.     

Preference and performance linkage of a leaf-mining moth on different Salicaceae species

The relationship between oviposition prefer-ence and offspring performance of a leaf-mining moth (Paraleucoptera sinuella) on four Salicaceae species was investigated in 1997 and 1998. We observed the egg distribution pattern on different plant species in the field and carried out oviposition experiments in the laboratory to determine the preference of ovipositing females. We also examined larval survival, pupal mass, and developmental time to compare larval performance on each plant species. Egg density in the field differed significantly among plant species. However, egg density was not correlated exactly with demonstrated oviposition preference. No larvae could develop on two Salix species. This finding indicated that larval survival is the most critical index of larval performance. Larval performance on each plant species was correlated well with oviposition preference that was revealed by a no-choice experiment in the laboratory. However, this correlation was not found in the field. These results indicate that the preference–performance linkage that was observed under laboratory conditions, was not always maintained in the field. Received: September 25, 2000 / Accepted: April 27, 2001     

Host-associated fitness variation in a seed beetle (Coleoptera: Bruchidae): evidence for local adaptation to a poor quality host

The geographic distributions of many generalist herbivores differ from those of their host plants, such that they experience coarse-grained spatial variation in natural selection on characters influencing adaptation to host plants. Thus, populations differing in host use are expected to differ in their ability to survive and grow on these host plants. We examine host-associated variation in larval performance (survivorship, development time, and adult body weight) and oviposition preference, within and between two populations ofStator limbatus (Coleoptera: Bruchidae) that differ in the hosts available to them in nature. In one population,Acacia greggii (Fabaceae: Mimosoideae) andCercidium microphyllum (Fabaceae: Caesalpininoideae) are each abundant, while in the second population onlyC. floridum andC. microphyllum are present. In both populations, egg-to-adult survivorship was less than 50% onC. floridum, while survivorship was greater than 90% onA. greggii. Most of the mortality onC. floridum occurred as larvae were burrowing through the seed coat; very low mortality occurred during penetration of the seed coat ofA. greggii. Significant variation was present between populations, and among families (within populations), in survivorship and egg-to-adult development time onC. floridum; beetles restricted toCercidium in nature, without access toC. floridum, survived better and developed faster onC. floridum than beetles that had access toA. greggii. Large host effects on body size were detected for female offspring: females reared onA. greggii were larger than those reared onC. floridum, whereas male offspring wee approximately the same size regardless of rearing host. Trade-offs between performance onC. floridum andC. floridum were not detected in this experiment. Instead, our data indicate that development time and survivorship onC. floridum may be largely independent of development time and survivorship onA. greggii. Patterns of oviposition preference corresponded to the observed patterns of host suitability: in laboratory preference tests, beetles with access toA. greggii in nature tended to prefer this host more than beetles without access to this host in nature.     

Effects of milfoil weevils and weather on the control of Eurasian watermilfoil

We examined the response of Eurasian watermilfoil (Myriophyllum spicatum) coverage on Manistee Lake, Michigan (U.S.A.) in the presence of milfoil weevils (Euhrychiopsis lecontei). Among 150 sites, milfoil presence declined from 2008 levels of 34 (23%) sites to 2 (1%) sites by 2015 coincident with cumulative stocking of 259,500 weevils from 2007 to 2014. Severe winter temperatures also were associated with milfoil declines. Each 1°C decline in average low temperature during the preceding winter was associated with 3.4 (95% CI 0.8–6.1) fewer sites with milfoil. Impacts of weevil herbivory on watermilfoil may be accentuated by severe winter temperatures. Lake managers should, when possible, integrate weather conditions with weevil stocking regimes to control Eurasian watermilfoil.     

Genetic architecture underlying convergent evolution of egg-laying behavior in a seed-feeding beetle

Independent populations subjected to similar environments often exhibit convergent evolution. An unresolved question is the frequency with which such convergence reflects parallel genetic mechanisms. We examined the convergent evolution of egg-laying behavior in the seed-feeding beetle Callosobruchus maculatus. Females avoid ovipositing on seeds bearing conspecific eggs, but the degree of host discrimination varies among geographic populations. In a previous experiment, replicate lines switched from a small host to a large one evolved reduced discrimination after 40 generations. We used line crosses to determine the genetic architecture underlying this rapid response. The most parsimonious genetic models included dominance and/or epistasis for all crosses. The genetic architecture underlying reduced discrimination in two lines was not significantly different from the architecture underlying differences between geographic populations, but the architecture underlying the divergence of a third line differed from all others. We conclude that convergence of this complex trait may in some cases involve parallel genetic mechanisms.     

Interactions between a specialist herbivore,Crocidosema plebejana,and its host plants Malva parviflora and cotton,Gossypium hirsutum: Oviposition preference

Ovipositional responses of gravid female Crocidosema plebejana Zeller (Lepidoptera: Tortricidae) to all stages of development of its host plants Malva parviflora L. and cotton, Gossypium hirsutum L., were studied in no-choice and choice experiments. In no-choice experiments the site of oviposition and the number of eggs laid reflected the suitability of the host plant for larval survival and development. The same was true of choice experiments although conclusions drawn from these are more tentative due to high levels of heterogeneity. Results from a natural (unplanned) choice experiment in the field, suggested flowering cotton was rejected as a site for oviposition by gravid females. Results from this paper and a previous paper by the authors are combined to explain the failure of tipworm populations to persist on cotton crops after flowering.     

Invaded habitat incompatibility affects the suitability of the potential biological control agent Listronotus sordidus for Sagittaria platyphylla in South Africa

Sagittaria platyphylla (Engelmann) J.G. Smith (Alismataceae) was first recorded in South Africa in 2008 and is considered to be an emerging weed with naturalised populations occurring throughout the country. A biological control programme was initiated in Australia and surveys conducted between 2010 and 2012 yielded potential agents, including the crown feeding weevil, Listronotus sordidus Gyllenhal (Coleoptera: Curculionidae). The potential of L. sordidus as a candidate biological control agent against S. platyphylla in South Africa was examined. Although adult feeding was recorded on a number of plant species, oviposition and larval development indicated a narrow host range restricted to the Alismataceae. In South Africa, S. platyphylla populations are primarily found in inundated systems. However, laboratory studies showed that L. sordidus did not oviposit on inundated plants, potentially nullifying the impact of the insect on South African populations. It is suggested that even though L. sordidus is a damaging, specific agent, its limited impact on inundated plant populations in South Africa does not justify the inherent risk associated with the release of a biological control agent.     

Behavioral adaptations increase the value of enemy-free space for Heliothis subflexa,a specialist herbivore

We investigated the importance of specialized behaviors in the use of enemy-free space by comparing the host-use behavior of two closely related moths, Heliothis subflexa Guenee and H. virescens Fabricius. Heliothis subflexa is a specialist on plants in the genus Physalis, whereas H. virescens is an extreme generalist, feeding on plants in at least 14 families. Heliothis subflexa uses the inflated calyx surrounding Physalis fruits as enemy-free space, and field rates of parasitism for H. subflexa on Physalis are much lower than for H. virescens on tobacco and cotton, common hosts found in the same habitat as Physalis. If Physalis, architecture were solely responsible for H. subflexa's low rates of parasitism on Physalis, we predicted that H. virescens larvae experimentally induced to feed on Physalis would experience parasitism rates similar to those of H. subflexa. We found, however, that specialized host-use and host-acceptance behaviors are integral to the use of enemy-free space on Physalis and strongly augment the effects of the structural refuge. In laboratory assays, we found considerable differences between the larval behavior of the specialist. H. subflexa, and the generalist, H. virescens, and these contributed to H. subflexa's superior use of enemy-free space on Physalis. We tested the importance of these behavioral differences in the field by comparing parasitism of H. virescens on Physalis, H. virescens on tobacco, and H. subflexa on Physalis by Cardiochiles nigriceps Vierick, a specialist braconid parasitoid. For H. virescens, a threefold decrease in parasitism occurred when feeding on Physalis (mean parasitism +/- SEM = 13 +/- 4%) rather than tobacco (43 +/- 4%), a difference we attribute to the structural refuge provided by Physalis. However, parasitism of H. virescens on Physalis was more than ten times as great as that of H. subflexa on Pliv.salis (1 +/- 4%), supporting the hypothesis that specialized behaviors have a substantial impact on use of Physalis as enemy-free space. Behavioral adaptations may be central to the use of enemy-free space by phytophagous insects and may act as an important selective force in the evolution of dietary specialization.     

Yucca moth oviposition and pollination behavior is affected by past flower visitors: evidence for a host-marking pheromone

Insect larvae such as those of yucca moths that feed on small, patchily distributed food items often face an elevated risk of intraspecific competition or cannibalism. For this reason, ovipositing females may assess a potential oviposition site for prior conspecific eggs or larvae before deciding whether to oviposit. Selective abortion of yucca flowers with high egg numbers prevents competition among larvae of the yucca moth Tegeticula yuccasella, but the same mechanism should select for female detection of and fewer ovipositions in flowers that already contain eggs. Female yucca moths presented with either virgin or previously visited flowers laid significantly fewer eggs in the latter flowers and pollinated them less often. A significant negative association was found between number of previous oviposition attempts in a flower and number of additional attempts by a female, suggesting a quantitative assessment of prior egg load, but the correlation coefficient was low. Factors contributing to this low correlation may include variation in signal quality, poor detection capability, uncertainty contributed by a variable oviposition attempt to egg ratio, and a variable response criterion based on recent female experience and physiological status. Females rationed their pollen by pollinating at decreasing frequency during a bout within a flower, and by depositing smaller pollen loads during later pollinations within a flower. Females ovipositing into a previously visited flower pollinated as frequently as would a first female for a given oviposition attempt within a flower, i.e., the probability of pollination after the nth oviposition was independent of whether it was performed by a first or a later moth. Experimental presentation of virgin flowers marked with a homogenate from female abdomens induced the same oviposition and pollination behavior as seen on previously visited flowers, suggesting the presence of a host-marking pheromone. Given that all eggs within a selectively aborted flower die, there may be selection among some yucca moths for providing a strong signal of floral egg status to conspecific females. Received: 1 December 1998 / Accepted: 7 February 1999     

Relationship between physical leaf characteristics and growth and survival of polyphagous grasshopper nymphs, <Emphasis Type="Italic">Parapodisma subastris</Emphasis> (Orthoptera: Catantopidae)

Common types of plant defense mechanisms are thought to affect the host ranges of polyphagous herbivorous insects, yet few studies have examined the relationship between host plant suitability for polyphagous insects and defense against them. We investigated the suitability of the 19 plant species growing in the habitat of the polyphagous grasshopper, Parapodisma subastris, to determine the relationship between the physical characteristics of leaves and the growth and survival of grasshopper nymphs. We examined leaf toughness, trichome density, and length. Nymph survival was greater on plants with characteristics ranging from soft leaves and dense trichomes to tough leaves and few trichomes than on plants with soft leaves and few trichomes. The exception was Rorippa indica, a plant with soft leaves and few trichomes that uses biotic defense, on which nymph survival was maximal. Higher-quality plants that share common physical characteristics over families may favor polyphagy by grasshoppers that possess ability to overcome the physical defense easily with their robust mandibles.An erratum to this article can be found at     

Effect of patch size and plant density of Paterson"s curse (Echium plantagineum) on the oviposition of a specialist weevil, Mogulones larvatus

This study examines the oviposition response of a specialist weevil (Mogulones larvatus) to patches of its host, the noxious weed Paterson"s curse/salvation Jane (Echium plantagineum). We simultaneously examined the effect of patch size and plant density (and their interaction), on the recorded oviposition patterns. Our results show that oviposition first occurred on the largest patches with the highest number of plants. However, there was no significant effect of patch size or number of plants per patch at the end of the experiment. At this time the level of attack per plant was negatively correlated with plant density. This negative effect of density on the level of oviposition was not mediated by a reduction in plant size at higher densities. The pattern observed may indicate a risk-spreading strategy by females. Received: 15 July 1999 / Accepted: 14 April 2000     

二化螟水稻类群和茭白类群成虫产卵与幼虫寄主选择行为的比较研究

实验室木箱条件下进行的二化螟水稻类群与茭白类群成虫产卵选择性试验结果表明,两类群在水稻与茭白上所产的卵块和卵粒的分布及孵化率无显著差异;但均有将不能孵化卵产在非本寄主上的倾向．通过Y形嗅觉仪进行的幼虫寄主选择行为的试验结果显示,除茭白类群1龄幼虫对水稻与茭白的趋性分别为30．00％与66．67％,有显著差异(P≤0．05)外,1龄幼虫对两寄主组织的趋性无显著差异;对水稻与茭白叶片、叶鞘的趋性反应中,水稻类群4龄、6龄幼虫对叶片,2龄、4龄幼虫对叶鞘差异显著,而茭白类群2—6龄幼虫均差异显著(P≤0．05)．研究结果表明,两类群已开始种下分化,其中茭白类群对本寄主的专化程度大于水稻类群。     

Influence of aphid size,age and behaviour on host choice by the parasitoid wasp Ephedrus californicus: a test of host-size models

Summary When host quality varies, parasitoid wasps are expected to oviposit selectively in high-quality hosts. We tested the assumption underlying host-size models that, for solitary species of wasps, quality is based on host size. Using Ephedrus californicus, a solitary endoparasitoid of the pea aphid, we evaluated the influence of aphid size (= mass), age and defensive behaviours on host selection. Experienced parasitoid females were given a choice among three classes of 5-day-old apterous nymphs: small aphids that had been starved daily for 4 h (S4) and 6 h (S6) respectively, and large aphids permitted to feed (F) normally. Wasps attacked more, and laid more eggs in, small than large aphids (S6>S4>F). This rank-order for attack did not change when females could choose among aphids of the same size that differed in age; however, wasps oviposited in all attacked aphids with equal probability. Host size did not influence parasitoid attack rates when aphids were anaesthetized so that they could not escape or defend themselves. As predicted by host-size models, wasp size increased with host size (F>S4; S6), but large wasps required longer to complete development than their smaller counterparts (S4E. californicus reflects a trade-off between maximization of fitness gains per egg and the economics of search-time allocation. Because large aphids are more likely to escape parasitization, a wasp must balance her potential gain in fitness by ovipositinng in a high-quality (large) aphid against her potential cost in terms of lost opportunity time if the attack fails.