Multiple Host Species Research Articles

Evolutionary Genetics of Borrelia.

The genus Borrelia consists of evolutionarily and genetically diverse bacterial species that cause a variety of diseases in humans and domestic animals. These vector-borne spirochetes can be classified into two major evolutionary groups, the Lyme borreliosis clade and the relapsing fever clade, both of which have complex transmission cycles during which they interact with multiple host species and arthropod vectors. Molecular, ecological, and evolutionary studies have each provided significant contributions towards our understanding of the natural history, biology and evolutionary genetics of Borrelia species; however, integration of these studies is required to identify the evolutionary causes and consequences of the genetic variation within and among Borrelia species. For example, molecular and genetic studies have identified the adaptations that maximize fitness components throughout the Borrelia lifecycle and enhance transmission efficacy but provide limited insights into the evolutionary pressures that have produced them. Ecological studies can identify interactions between Borrelia species and the vertebrate hosts and arthropod vectors they encounter and the resulting impact on the geographic distribution and abundance of spirochetes but not the genetic or molecular basis underlying these interactions. In this review we discuss recent findings on the evolutionary genetics from both of the evolutionarily distinct clades of Borrelia species. We focus on connecting molecular interactions to the ecological processes that have driven the evolution and diversification of Borrelia species in order to understand the current distribution of genetic and molecular variation within and between Borrelia species.

Stress resistance associated with multi-host transmission and enhanced biofilm formation at 42 °C among hyper-aerotolerant generalist Campylobacter jejuni

One of the emerging conundrums of Campylobacter food-borne illness is the bacterial ability to survive stressful environmental conditions. We evaluated the heterogeneity among 90 C. jejuni and 21 C. coli isolates from different sources in Egypt with respect to biofilm formation capabilities (under microaerobic and aerobic atmosphere) and resistance to a range of stressors encountered along the food chain (aerobic stress, refrigeration, freeze-thaw, heat, peracetic acid, and osmotic stress). High prevalence (63%) of hyper-aerotolerant (HAT) isolates was observed, exhibiting also a significantly high tolerance to heat, osmotic stress, refrigeration, and freeze-thaw stress, coupled with high biofilm formation ability which was clearly enhanced under aerobic conditions, suggesting a potential link between stress adaptation and biofilm formation. Most HAT multi-stress resistant and strong biofilm producing C. jejuni isolates belonged to host generalist clonal complexes (ST-21, ST-45, ST-48 and ST-206). These findings highlight the potential role of oxidative stress response systems in providing cross-protection (resistance to other multiple stress conditions) and enhancing biofilm formation in Campylobacter and suggest that selective pressures encountered in hostile environments have shaped the epidemiology of C. jejuni in Egypt by selecting the transmission of highly adapted isolates, thus promoting the colonization of multiple host species by important disease-causing lineages.

Toxoplasmosis: Recent Advances in Understanding the Link Between Infection and Host Behavior.

Humans, wildlife, and domestic animals are intimately linked through shared infections. Many parasites and pathogens use multiple host species, either opportunistically or sequentially, such that managing disease risk frequently requires a broader understanding of the ecological community. The coccidian protozoan Toxoplasma gondii infects more than one hundred species of vertebrates, ranging from bats to beluga whales. In humans, acute toxoplasmosis can have serious health consequences for immunocompromised individuals. Even amongst asymptomatic patients, however, toxoplasmosis has been linked to a range of behavioral alterations and conditions, such as changes in risk tolerance, neuroticism, mental illness, suicide, and accident proneness. Whether such links are causal or simply correlational has been the subject of intense study and debate; from an evolutionary standpoint, selection may favor parasite-induced alterations in host behavior that increase the likelihood a host is consumed by the definitive host-in this case a domestic or wild felid. Here, we examine current evidence for parasite-induced manipulations of host behavior, in both humans and other animals. We critically evaluate proposed mechanisms through which infection might influence host behavior, which range from inflammation in the brain to changes in hormones or neurotransmitters. Considering estimates that T. gondii may infect up to one-third of the global human population, we conclude by examining the implications of these changes for human behavior, individual fitness, and emergent cultural properties.

Emerging orthobunyaviruses associated with CNS disease.

The Orthobunyavirus genus comprises a wide range of arthropod-borne viruses which are prevalent worldwide and commonly associated with central nervous system (CNS) disease in humans and other vertebrates. Several orthobunyaviruses have recently emerged and increasingly more will likely do so in the future. Despite this large number, an overview of these viruses is currently lacking, making it challenging to determine importance from a One Health perspective. Causality is a key feature of determining importance, yet classical tools are unfit to evaluate the causality of orthobunyaviral CNS disease. Therefore, we aimed to provide an overview of orthobunyaviral CNS disease in vertebrates and objectify the causality strength of each virus. In total, we identified 27 orthobunyaviruses described in literature to be associated with CNS disease. Ten were associated with disease in multiple host species of which seven included humans. Seven viruses were associated with both congenital and postnatal CNS disease. CNS disease-associated orthobunyaviruses were spread across all known Orthobunyavirus serogroups by phylogenetic analyses. Taken together, these results indicate that orthobunyaviruses may have a common tendency to infect the CNS of vertebrates. Next, we developed six tailor-made causality indicators and evaluated the causality strength of each of the identified orthobunyaviruses. Nine viruses had a ‘strong’ causality score and were deemed causal. Eight had a ‘moderate’ and ten a ‘weak’ causality score. Notably, there was a lack of case-control studies, which was only available for one virus. We, therefore, stress the importance of proper case-control studies as a fundamental aspect of proving causality. This comprehensible overview can be used to identify orthobunyaviruses which may be considered causal, reveal research gaps for viruses with moderate to low causality scores, and provide a framework to evaluate the causality of orthobunyaviruses that may newly emerge in the future.

Harnessing genomics to trace the path of a viral outbreak in African lions.

Predicting the emergence of novel infectious diseases requires an understanding of how pathogens infect and efficiently spread in alternative naïve hosts. A pathogen's ability to adapt to a new host (i.e. host shift) oftentimes is constrained by host phylogeny, due to limits in the molecular mechanisms available to overcome host-specific immune defences (Longdon etal.,2014). Some pathogens, such as RNA viruses, however, have a propensity to jump hosts due to rapid mutation rates. For example, canine distemper virus (CDV) infects a broad range of terrestrial carnivores, as well as noncarnivore species worldwide, with a host range that is distributed across 5 orders and 22 families (Beineke etal.,2015). In 1993-1994, a severe CDV outbreak infected multiple carnivore host species in Serengeti National Park, causing widespread mortality and the subsequent decline of the African lion (Panthera leo) population (Roelke-Parker etal.,1996). While previous studies established domestic dogs (Canis lupus familiaris) as the disease reservoir, the precise route of transmission to lions remained a mystery, and a number of wild carnivore species could have facilitated viral evolution and spread. In this issue of Molecular Ecology, Weckworth etal.(2020) used whole-genome viral sequences obtained from four carnivore species during the CDV outbreak, in combination with epidemiological data, to illuminate the pathway and evolutionary mechanisms leading to disease emergence in Serengeti lions.

Empirical evidence of different egg morphs that match host eggs in the brush cuckoo (Cacomantis variolosus)

ABSTRACT One of the most efficient defences against obligate brood parasitism in birds is egg ejection, where a host recognises and removes the parasitic egg from the nest. This defence often selects for egg mimicry in parasitic species to reduce the likelihood of egg ejection. If a parasite uses multiple host species with distinctive egg types, this could lead to the evolution of egg gentes (host-specific egg types) in the parasite. There is observational evidence that the brood parasitic Brush Cuckoo (Cacomantis variolosus) might exhibit egg gentes, but there has been no objective study conducted to determine how closely eggs of this cuckoo species resemble those of its hosts from a bird’s visual perspective. Using objective measurements to quantify egg appearance, we found that Brush Cuckoos exhibit at least two egg morphs that closely match the eggs of two of its primary hosts in colour, luminance and volume. While the determination of actual egg gentes in the Brush Cuckoo was beyond the scope of our study, our results are a first and necessary step in determining whether egg gentes might exist in this species. We suggest at least a third egg morph matching another primary host (or at least the genus of that host) might exist, but more data would be necessary to confirm this. Additionally, we provide a mechanism researchers can use to help distinguish between Brush Cuckoo eggs that are closely matched to their host eggs for future studies in this system.

Evolutionary ecology of Lyme Borrelia.

The bacterial genus, Borrelia, is comprised of vector-borne spirochete species that infect and are transmitted from multiple host species. Some Borrelia species cause highly-prevalent diseases in humans and domestic animals. Evolutionary, ecological, and molecular research on many Borrelia species have resulted in tremendous progress toward understanding the biology and natural history of these species. Yet, many outstanding questions, such as how Borrelia populations will be impacted by climate and land-use change, will require an interdisciplinary approach. The evolutionary ecology research framework incorporates theory and data from evolutionary, ecological, and molecular studies while overcoming common assumptions within each field that can hinder integration across these disciplines. Evolutionary ecology offers a framework to evaluate the ecological consequences of evolved traits and to predict how present-day ecological processes may result in further evolutionary change. Studies of microbes with complex transmission cycles, like Borrelia, which interact with multiple vertebrate hosts and arthropod vectors, are poised to leverage the power of the evolutionary ecology framework to identify the molecular interactions involved in ecological processes that result in evolutionary change. Using existing data, we outline how evolutionary ecology theory can delineate how interactions with other species and the physical environment create selective forces or impact migration of Borrelia populations and result in micro-evolutionary changes. We further discuss the ecological and molecular consequences of those micro-evolutionary changes. While many of the currently outstanding questions will necessitate new experimental designs and additional empirical data, many others can be addressed immediately by integrating existing molecular and ecological data within an evolutionary ecology framework.

Multilayer and Multiplex Networks: An Introduction to Their Use in Veterinary Epidemiology

Contact network analysis has become a vital tool for conceptualizing the spread of pathogens in animal populations and is particularly useful for understanding the implications of heterogeneity in contact patterns for transmission. However, the transmission of most pathogens cannot be simplified to a single mode of transmission and, thus, a single definition of contact. In addition, host-pathogen interactions occur in a community context, with many pathogens infecting multiple host species and most hosts being infected by multiple pathogens. Multilayer networks provide a formal framework for researching host-pathogen systems in which multiple types of transmission-relevant interactions, defined as network layers, can be analyzed jointly. Here, we provide an overview of multilayer network analysis and review applications of this novel method to epidemiological research questions. We then demonstrate the use of this technique to analyze heterogeneity in direct and indirect contact patterns amongst swine farms in the United States. When contact among nodes can be defined in multiple ways, a multilayer approach can advance our ability to use networks in epidemiological research by providing an improved approach for defining epidemiologically relevant groups of interacting nodes and changing the way we identify epidemiologically important individuals such as superspreaders.

The uneasy coexistence of predators and pathogens

.Disease and predation are both highly important in ecology, and pathogens with multiple host species have turned out to be common. Nonetheless, the interplay between multi-host epidemics and predation has received relatively little attention. Here, we analyse a model of a predator-prey system with disease in both prey and predator populations and determine reasonable parameter values using allometric mass scaling relations. Our analysis focuses on the possibility of extinction events rather than the linear stability of the model equations, and we derive approximate relations for the parameter values at which we expect these events to occur. We find that if the predator is a specialist, epidemics frequently drive the predator species to extinction. If the predator has an additional, immune prey species, predators will usually survive. Coexistence of predator and disease is impossible in the single-prey model. We conclude that for the prey species, carrying a pathogen can be an effective weapon against predators, and that being a generalist is a major advantage for a predator in the event of an epidemic affecting the prey or both species.Graphical abstract

Reproductive hormones mediate changes in the gut microbiome during pregnancy and lactation in Phayre\u2019s leaf monkeys

Studies in multiple host species have shown that gut microbial diversity and composition change during pregnancy and lactation. However, the specific mechanisms underlying these shifts are not well understood. Here, we use longitudinal data from wild Phayre’s leaf monkeys to test the hypothesis that fluctuations in reproductive hormone concentrations contribute to gut microbial shifts during pregnancy. We described the microbial taxonomic composition of 91 fecal samples from 15 females (n = 16 cycling, n = 36 pregnant, n = 39 lactating) using 16S rRNA gene amplicon sequencing and assessed whether the resulting data were better explained by overall reproductive stage or by fecal estrogen (fE) and progesterone (fP) concentrations. Our results indicate that while overall reproductive stage affected gut microbiome composition, the observed patterns were driven by reproductive hormones. Females had lower gut microbial diversity during pregnancy and fP concentrations were negatively correlated with diversity. Additionally, fP concentrations predicted both unweighted and weighted UniFrac distances, while reproductive state only predicted unweighted UniFrac distances. Seasonality (rainfall and periods of phytoprogestin consumption) additionally influenced gut microbial diversity and composition. Our results indicate that reproductive hormones, specifically progestagens, contribute to the shifts in the gut microbiome during pregnancy and lactation.

Diel activity patterns and arrestment behaviour in host associations of green mirids (Creontiades dilutus).

Many plant bugs (Miridae) are generalist herbivores that feed on multiple host species. The reasons these bugs move across hosts and the behavioural mechanisms responsible for their retention at specific hosts remain elusive. Green mirids (Creontiades dilutus) are endemic to Australia. These insects are important pests of cotton (Gossypium hirsutum) and even in low numbers can cause substantial damage to crops. These bugs are also present in relatively much higher numbers on pigeon pea (Cajanus cajan) planted alongside cotton fields, and evidence shows they move across these crops in both directions. Observations of these highly mobile insects in the field are challenging, but indirect evidence suggests that they may be nocturnal. This study evaluated: (1) the diel (24 h) period in which C. dilutus adults were most active, (2) whether they respond to plant volatiles immediately prior to landing on host substrates, and (3) if their presence on a host is in response to attraction or arrestment cues. The results suggest that C. dilutus bugs are typically most active early in the evenings, after remaining motionless during the day (unless disturbed). Their movement (at night) was arrested by hosts prior to touching plant tissues. There was no evidence to suggest that these bugs are attracted by volatiles beyond 2 cm. These outcomes demonstrate that insect behaviours need to be investigated within their typical activity periods, and that arrestment cues possibly play a central role in the host finding process of generalist C. dilutus and probably, therefore, other mirid species.

Host plant adaptation during contemporary range expansion in the monarch butterfly.

Herbivores that have recently expanded their host plant ranges provide opportunities to test hypotheses about the evolution of host plant specialization. Here, we take advantage of the contemporary global range expansion of the monarch butterfly (Danaus plexippus) and conduct a reciprocal rearing experiment involving monarch populations with divergent host plant assemblages. Specifically, we ask the following questions: (1) Do geographically disparate populations of monarch butterflies show evidence for local adaptation to their host plants? If so, what processes contribute to this pattern? (2) How is dietary breadth related to performance across multiple host species in monarch populations? (3) Does the coefficient of variation in performance vary across sympatric versus allopatric hosts? We find evidence for local adaptation in larval growth rate and survival based on sympatric/allopatric contrasts. Migratory North American monarchs, which have comparatively broad host breadth, have higher mean performance than derived nonmigratory populations across all host plant species. Monarchs reared on their sympatric host plants show lower coefficient of variation in performance than monarchs reared on allopatric hosts. We focus our discussion on possible mechanisms contributing to local adaptation to novel host plants and potential explanations for the reduction in performance that we observed in derived monarch populations.

Phylogenetic analysis of avian paramyxoviruses 1 isolated in Taiwan from 2010 to 2018 and evidence for their intercontinental dispersal by migratory birds.

Avian paramyxovirus 1 (APMV-1), synonymous with Newcastle disease virus (NDV), is a worldwide viral agent that infects various avian species and responsible for outbreaks of Newcastle disease. In this study, 40 APMV-1 isolates collected from poultry, migratory birds, and resident birds during 2010–2018 in Taiwan were characterized genetically. Our phylogenetic analysis of complete fusion protein gene of the APMV-1 isolates revealed that 39 of the 40 Taiwanese isolates were closely related to APMV-1 of class I genotype 1 or class II genotypes I, VI or VII, and one isolate belonged to a group that can be classified as a novel genotype 2 within class I. The fusion protein gene sequences of a branch (former 1d) nested within class I sub-genotype 1.2 were closely related to those isolated from wild birds in North America. Viruses placed in class II sub-genotype VI.2.1.1.2.1 and sub-genotype VI.2.1.1.2.2 were the dominant pigeon paramyxovirus 1 (PPMV-1) circulating in the last decade in Taiwan. All the Newcastle disease outbreak-associated isolates belonged to class II sub-genotype VII.1.1, which was mainly responsible for the present epizootic of Newcastle disease in Taiwan. We conclude that at least five sub/genotypes of APMV-1 circulate in multiple avian host species in Taiwan. One genetically divergent group of APMV-1 should be considered as a novel genotype within class I. Migratory birds may play an important role in intercontinental spread of lentogenic APMV-1 between Eurasia and North America.

Contrasting impacts of a novel specialist vector on multihost viral pathogen epidemiology in wild and managed bees.

Typically, pathogens infect multiple host species. Such multihost pathogens can show considerable variation in their degree of infection and transmission specificity, which has important implications for potential disease emergence. Transmission of multihost pathogens can be driven by key host species and changes in such transmission networks can lead to disease emergence. We study two viruses that show contrasting patterns of prevalence and specificity in managed honeybees and wild bumblebees, black queen cell virus (BQCV) and slow bee paralysis virus (SBPV), in the context of the novel transmission route provided by the virus‐vectoring Varroa destructor. Our key result is that viral communities and RNA virus genetic variation are structured by location, not host species or V. destructor presence. Interspecific transmission is pervasive with the same viral variants circulating between pollinator hosts in each location; yet, we found virus‐specific host differences in prevalence and viral load. Importantly, V. destructor presence increases the prevalence in honeybees and, indirectly, in wild bumblebees, but in contrast to its impact on deformed wing virus (DWV), BQCV and SBPV viral loads are not increased by Varroa presence, and do not show genetic evidence of recent emergence. Effective control of Varroa in managed honeybee colonies is necessary to mitigate further disease emergence, and alleviate disease pressure on our vital wild bee populations. More generally, our results highlight the over‐riding importance of geographical location to the epidemiological outcome despite the complexity of multihost‐parasite interactions.

Generalising about generalists? A perspective on the role of pattern and process in investigating herbivorous insects that use multiple host species

Generalist insect herbivores, those recorded as using numerous hosts (tens or even hundreds of species), are not well understood ecologically. We suggest ways to investigate the ecology of these species beyond the practice of accumulating host records. We present reasons why multiple host use by herbivorous insects needs to be quantified in the field, both locally and geographically, and also through time. Further, the host use patterns generated must be based on certain knowledge that cryptic species are not conflated in the results as one species. Such results reveal a lot about the ecology of the species concerned and about generalist–host relationships more widely. This provides a sound basis for the functional significance of multiple host use to be interpreted and tested further. Structured sampling programs conducted previously in the field indicate that generalist insect herbivores are strongly associated with only a relatively small subset of their recorded host species, their primary host plants. A focus on these particular host plants is fundamental to (i) understanding the ecology of the herbivore species in question and (ii) investigating the sensory and behavioural mechanisms associated with host location. We conclude that the principal influence on patterns of multiple host use in the field is the mechanism by which herbivorous insects recognise cues from potential hosts and use them to localise plants. These mechanisms represent species-specific and species-wide adaptations to the usual environment of the species in question. Working from this perspective should contribute substantially to developing a strong and realistic interpretation of the origins and functional significance of multiple host use in herbivorous arthropods.

Antagonism between parasites within snail hosts impacts the transmission of human schistosomiasis.

Human disease agents exist within complex environments that have underappreciated effects on transmission, especially for parasites with multi-host life cycles. We examined the impact of multiple host and parasite species on transmission of the human parasite Schistosoma mansoni in Kenya. We show S. mansoni is impacted by cattle and wild vertebrates because of their role in supporting trematode parasites, the larvae of which have antagonistic interactions with S. mansoni in their shared Biomphalaria vector snails. We discovered the abundant cattle trematode, Calicophoron sukari, fails to develop in Biomphalaria pfeifferi unless S. mansoni larvae are present in the same snail. Further development of S. mansoni is subsequently prevented by C. sukari's presence. Modeling indicated that removal of C. sukari would increase S. mansoni-infected snails by two-fold. Predictable exploitation of aquatic habitats by humans and their cattle enable C. sukari to exploit S. mansoni, thereby limiting transmission of this human pathogen.

Argulus from the Pascagoula River, MS, USA, with an Emphasis on Those of the Threatened Gulf Sturgeon, Acipenser oxyrinchus desotoi

Species of Argulus (Branchiura Thorell, 1864) are common ectoparasites of freshwater, estuarine, and marine fishes. Argulid identification and taxonomy is often confusing because many species are reported to parasitize multiple host species, have similar morphological characters, and come from various salinity regimes. Gulf sturgeon is an anadromous fish natal to drainages in the north-central Gulf of Mexico, and as with many endangered species, has a poorly documented parasite community. During Gulf sturgeon tagging and monitoring studies (2016–2019) in the Pascagoula River, MS, USA, species of Argulus were collected from Gulf sturgeon as well as other incidentally captured fishes. Argulus flavescens Wilson, 1916 was found on Gulf sturgeon and flathead catfish, Argulus americanus Wilson, 1902 on bowfin, and Argulus bicolor Bere, 1936 on Atlantic stingray. We provide morphological details and measurements for these species as well as the first confirmed 28S rDNA molecular data. Argulus flavescens was more abundant and prevalent on larger Gulf sturgeon and on sturgeon captured in freshwater rather than estuarine habitats. Our results indicate that A. flacescens may not tolerate estuarine salinities and that the anadromous life-history pattern of Gulf sturgeon could help rid them of A. flavescens when they emigrate from their riverine habitats.

Persistence of single species of symbionts across multiple closely-related host species

Some symbiont species are highly host-specific, inhabiting only one or a very few host species, and typically have limited dispersal abilities. When they do occur on multiple host species, populations of such symbionts are expected to become genetically structured across these different host species, and this may eventually lead to new symbiont species over evolutionary timescales. However, a low number of dispersal events of symbionts between host species across time might be enough to prevent population structure and species divergence. Overall, processes of evolutionary divergence and the species status of most putative multi-host symbiont systems are yet to be investigated. Here, we used DNA metabarcoding data of 6,023 feather mites (a total of 2,225 OTU representative sequences) from 147 infracommunities (i.e., the assemblage consisting of all mites of different species collected from the same bird host individual) to investigate patterns of population genetic structure and species status of three different putative multi-host feather mite species Proctophyllodes macedo Vitzthum, 1922, Proctophyllodes motacillae Gaud, 1953, and Trouessartia jedliczkai (Zimmerman, 1894), each of which inhabits a variable number of different closely related wagtail host species (genus Motacilla). We show that mite populations from different host species represent a single species. This pattern was found in all the mite species, suggesting that each of these species is a multi-host species in which dispersal of mites among host species prevents species divergence. Also, we found evidence of limited evolutionary divergence manifested by a low but significant level of population genetic structure among symbiont populations inhabiting different host species. Our study agrees with previous studies showing a higher than expected colonization opportunities in host-specific symbionts. Indeed, our results support that these dispersal events would allow the persistence of multi-host species even in symbionts with limited dispersal capabilities, though additional factors such as the geographical structure of some bird populations may also play a role.

Host tolerance and resistance to parasitic nest flies differs between two wild bird species.

Hosts have developed and evolved defense strategies to limit parasite damage. Hosts can reduce the damage that parasites cause by decreasing parasite fitness (resistance) or without affecting parasite fitness (tolerance). Because a parasite species can infect multiple host species, determining the effect of the parasite on these hosts and identifying host defense strategies can have important implications for multi‐host–parasite dynamics.Over 2 years, we experimentally manipulated parasitic flies (Protocalliphora sialia) in the nests of tree swallows (Tachycineta bicolor) and eastern bluebirds (Sialia sialis). We then determined the effects of the parasites on the survival of nestlings and compared defense strategies between host species. We compared resistance between host species by quantifying parasite densities (number of parasites per gram of host) and measured nestling antibody levels as a mechanism of resistance. We quantified tolerance by determining the relationship between parasite density and nestling survival and blood loss by measuring hemoglobin levels (as a proxy of blood recovery) and nestling provisioning rates (as a proxy of parental compensation for resources lost to the parasite) as potential mechanisms of tolerance.For bluebirds, parasite density was twice as high as for swallows. Both host species were tolerant to the effects of P. sialia on nestling survival at their respective parasite loads but neither species were tolerant to the blood loss to the parasite. However, swallows were more resistant to P. sialia compared to bluebirds, which was likely related to the higher antibody‐mediated immune response in swallow nestlings. Neither blood recovery nor parental compensation were mechanisms of tolerance.Overall, these results suggest that bluebirds and swallows are both tolerant of their respective parasite loads but swallows are more resistant to the parasites. These results demonstrate that different host species have evolved similar and different defenses against the same species of parasite.

The "sequential cues hypothesis": a conceptual model to explain host location and ranking by polyphagous herbivores.

Successfully locating a host plant is crucial for an insect herbivore to feed and/or oviposit. However, locating a host within a complex environment that may contain an array of different plant species is a difficult task. This is particularly the case for polyphagous herbivores, which must locate a host within environments that may simultaneously contain multiple suitable and unsuitable hosts. Here we review the mechanisms of host selection used by polyphagous herbivores, as well as exploring how prior experience may modify a generalist's response to host cues. We show that recent research demonstrates that polyphagous herbivores have the capacity to detect both common cues from multiple host species, as well as specific cues from individual host species. This creates a paradox in that generalists invariably rank hosts when given a choice, a finding at odds with the "neural limitations" hypothesis that says generalist insect herbivores should not have the neural capacity to identify cues specific to every possible host. To explain this paradox we propose a model, akin to parasitoid host location, that postulates that generalist herbivores use different cues sequentially in host location. We propose that initially common host cues, associated with all potential hosts, are used to place the herbivore within the host habitat and that, in the absence of any other host cues, these cues are sufficient in themselves to lead to host location. As such they are true "generalist" cues. However, once within the host habitat, we propose that the presence of a smaller group of cues may lead to further host searching and the location of preferred hosts: these are "specialist" cues. This model explains the current conflict in the literature where generalists can respond to both common and specific host-plant cues, while also exhibiting specialist and generalist host use behavior under different conditions.