Micro-evolutionary change and population dynamics of a brood parasite and its primary host: the intermittent arms race hypothesis

A long-term study of the interactions between a brood parasite, the great spotted cuckoo Clamator glandarius, and its primary host the magpie Pica pica, demonstrated local changes in the distribution of both magpies and cuckoos and a rapid increase of rejection of both mimetic and non-mimetic model eggs by the host. In rich areas, magpies improved three of their defensive mechanisms: nest density and breeding synchrony increased dramatically and rejection rate of cuckoo eggs increased more slowly. A stepwise multiple regression analysis showed that parasitism rate decreased as host density increased and cuckoo density decreased. A logistic regression analysis indicated that the probability of changes in magpie nest density in the study plots was significantly affected by the density of magpie nests during the previous year (positively) and the rejection rate of mimetic model eggs (negatively). These results are consistent with a hypothesis (the intermittent arms race hypothesis) of spatially structured cyclic changes in parasitism. During periods of parasitism, host defences continuously improve, and as a consequence, the fitness gains for parasites decrease. When host defences against parasites reach a high level, dispersing parasites have a selective advantage if they are able to emigrate to areas of low resistance. Once parasites have left an area hosts will lose their defensive adaptations due to their cost in the absence of parasitism. The scene is then set for re-colonization by great spotted cuckoos. Received: 7 May 1998 / Accepted: 24 August 1998     

The developmental strategies and related profitability of an idiobiont ectoparasitoid Sclerodermus pupariae vary with host size

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Costs of predator‐induced morphological defences in Daphnia

1. Inducible defences are advantageous because they protect the prey while limiting associated fitness costs. The presence of these costs is an essential component of this conditional strategy, since their absence would favour constitutive (fixed) defences. In some cases, however, these costs have been difficult to measure because of complex interactions between the defences themselves, resultant life history changes and the organism’s environment. 2. The pond‐dwelling water flea, Daphnia pulex, forms defensive neck spines in response to kairomones released by predatory larvae of the phantom midge, Chaoborus. This predator–prey interaction and the formation of these inducible defences have been well studied, but costs associated with the development of neck spines remain unclear. In this study, I address this problem by analysing the effect of Chaoborus kairomones on the life history responses (and fitness costs associated with these responses) of two clones of D. pulex that are from the same pond population, but differ greatly in their degree of neck spine development. 3. Both D. pulex clones exhibited the same predator‐induced shifts in life history: larger size at birth, reduced juvenile growth rate (producing a smaller size at maturity), delayed reproduction and a reduction in the number of neonates produced after the first clutch. Relative fitness decreased significantly and to the same degree (c. 10% reduction in r) in each clone. This observed fitness cost was not directly related to the neck spines per se since the cost was the same in both clones, despite their considerable differences in neck spine development. Rather, it appears to be indirectly related to this antipredator morphology via a combination of delayed reproduction and a set of life history trade‐offs (decreased growth rate, decreased reproduction after the first clutch) for increased neonate body size, which is necessary for neck spines to be effective defences. This suite of induced responses is probably a result of local adaptation of these two D. pulex clones to their common pond environment. 4. Costs of inducible defences do not always entail direct allocation costs associated with forming and maintaining a defence, but may also involve indirect life history responses that are specific to particular environmental situations. This local adaptation would explain the highly variable life history responses observed among D. pulex clones from different pond environments.     

Variation in costs of parasite resistance among natural host populations

Organisms that can resist parasitic infection often have lower fitness in the absence of parasites. These costs of resistance can mediate host evolution during parasite epidemics. For example, large epidemics will select for increased host resistance. In contrast, small epidemics (or no disease) can select for increased host susceptibility when costly resistance allows more susceptible hosts to outcompete their resistant counterparts. Despite their importance for evolution in host populations, costs of resistance (which are also known as resistance trade‐offs) have mainly been examined in laboratory‐based host–parasite systems. Very few examples come from field‐collected hosts. Furthermore, little is known about how resistance trade‐offs vary across natural populations. We addressed these gaps using the freshwater crustacean Daphnia dentifera and its natural yeast parasite, Metschnikowia bicuspidata. We found a cost of resistance in two of the five populations we studied – those with the most genetic variation in resistance and the smallest epidemics in the previous year. However, yeast epidemics in the current year did not alter slopes of these trade‐offs before and after epidemics. In contrast, the no‐cost populations showed little variation in resistance, possibly because large yeast epidemics eroded that variation in the previous year. Consequently, our results demonstrate variation in costs of resistance in wild host populations. This variation has important implications for host evolution during epidemics in nature.     

Effects of antagonistic coevolution on parasite‐mediated host coexistence

Parasites can promote diversity by mediating coexistence between a poorer and superior competitor, if the superior competitor is more susceptible to parasitism. However, hosts and parasites frequently undergo antagonistic coevolution. This process may result in the accumulation of pleiotropic fitness costs associated with host resistance, and could breakdown coexistence. We experimentally investigated parasite‐mediated coexistence of two genotypes of the bacterium Pseudomonas fluorescens, where one genotype underwent coevolution with a parasite (a virulent bacteriophage), whereas the other genotype was resistant to the evolving phages at all time points, but a poorer competitor. In the absence of phages, the resistant genotype was rapidly driven extinct in all populations. In the presence of the phages, the resistant genotype persisted in four of six populations and eventually reached higher frequencies than the sensitive genotype. The coevolving genotype showed a reduction in the growth rate, consistent with a cost of resistance, which may be responsible for a decline in its relative fitness. These results demonstrate that the stability of parasite‐mediated coexistence of resistant and susceptible species or genotypes is likely to be affected if parasites and susceptible hosts coevolve.     

Effects of the introduced ectoparasite Philornis downsi on haemoglobin level and nestling survival in Darwin's Small Ground Finch (Geospiza fuliginosa)

Abstract: The physiological impacts and fitness costs of parasitism by an introduced ectoparasitic fly, Philornis downsi (Muscidae), were studied in nestlings of Darwin's Small Ground Finch, Geospiza fuliginosa (Geospizinae), on the Galápagos Archipelago. Whole blood haemoglobin (Hb) concentration was used to measure host response to ectoparasitism due to its high repeatability and validity, as well as for its key role in aerobic activities that affect fitness, such as flight capacity and nestling begging intensity. Increased numbers of ectoparasitic larvae of P. downsi were strongly correlated with lower Hb levels in nestlings in the absence of blood parasites. Furthermore, immature red blood cell counts were negatively correlated with Hb level and positively correlated with P. downsi intensity. Nestlings with high levels of parasitism suffered higher mortality, which varied with clutch size. Our results provide evidence that endemic Galápagos bird populations are physiologically compromised by P. downsi and experience substantial fitness costs due to ectoparasitism.     

The evolution of acceptance and tolerance in hosts of avian brood parasites

Avian brood parasites lay their eggs in the nests of their hosts, which rear the parasite's progeny. The costs of parasitism have selected for the evolution of defence strategies in many host species. Most research has focused on resistance strategies, where hosts minimize the number of successful parasitism events using defences such as mobbing of adult brood parasites or rejection of parasite eggs. However, many hosts do not exhibit resistance. Here we explore why some hosts accept parasite eggs in their nests and how this is related to the virulence of the parasite. We also explore the extent to which acceptance of parasites can be explained by the evolution of tolerance; a strategy in which the host accepts the parasite but adjusts its life history or other traits to minimize the costs of parasitism. We review examples of tolerance in hosts of brood parasites (such as modifications to clutch size and multi‐broodedness), and utilize the literature on host–pathogen interactions and plant herbivory to analyse the prevalence of each type of defence (tolerance or resistance) and their evolution. We conclude that (i) the interactions between brood parasites and their hosts provide a highly tractable system for studying the evolution of tolerance, (ii) studies of host defences against brood parasites should investigate both resistance and tolerance, and (iii) tolerance and resistance can lead to contrasting evolutionary scenarios.     

Fitness consequences of host plant choice: a field experiment

Determining the relative contributions of different ecological factors for herbivore fitness is one key to understanding the ecology and evolution of host plant choice by herbivores. Natural enemies are increasingly being recognized as an important factor: host plants of inferior quality for development may still be used by herbivores if they provide enemy‐free space (EFS). Here we used the tobacco hornworm, Manduca sexta, to experimentally disentangle the effects of natural enemies from the potentially confounding factors of host plant quality, competition and microhabitat. We explored the consequences for both individual components of fitness and total fitness of M. sexta feeding on a typical high quality host plant, tobacco Nicotiana tabacum and a novel, low quality host plant, devil's claw Proboscidea louisianica in an experimental field environment in the presence of a parasitoid natural enemy, Cotesia congregata. Although early larval survival, development and growth rates, final body size and fecundity were all reduced for M. sexta feeding on devil's claw, a high rate of parasitism on tobacco and an absence of parasitism on devil's claw contributed to similar total fitness (net reproductive rate, R₀) across the two host plant species. Our results suggest M. sexta has adopted a novel host plant (devil's claw) outside its typical host range because this host plant provides enemy free space. In addition, oviposition behavior of adult female M. sexta appears to be well suited to exploiting the enemy‐free space on devil's claw; oviposition by M. sexta on devil's claw appears to correspond with seasonal variation in parasitoid abundance.     

Tritrophic effects of organic and conventional fertilisers on a cereal‐aphid‐parasitoid system

The impact of parasitoids on pests varies between conventional and low‐intensity agricultural systems. Although the impacts on parasitoid natural enemies of many practices within these agricultural systems are well understood, the role of fertilisers has been less well studied. The effects of organic‐based and conventional fertilisers on Hordeum vulgare L. (Poaceae), the aphid Metopolophium dirhodum Walker (Hemiptera: Aphididae), and its parasitoid Aphidius ervi Haliday (Hymenoptera: Braconidae) was investigated using cage release experiments and measures of aphid and parasitoid fitness were taken. Barley tiller number and aphid weight were increased by fertilisers, particularly under conventional treatments. Adult parasitoid size correlated positively with that of the host, M. dirhodum, whereas percentage parasitism was not affected by fertiliser treatment or host size. The results suggest that the increased parasitoid impact observed in some low‐intensity or organic systems is not a direct result of fertiliser treatment. Our results indicate that fertiliser treatments that improve cereal‐aphid fitness will improve parasitoid fitness as measured by parasitoid size but may not influence percentage parasitism.     

Long‐term coevolution between avian brood parasites and their hosts

Coevolutionary theory predicts that the most common long‐term outcome of the relationships between brood parasites and their hosts should be coevolutionary cycles based on a dynamic change selecting the currently least‐defended host species, given that when well‐defended hosts are abandoned, hosts will be selected to decrease their defences as these are usually assumed to be costly. This is assumed to be the case also in brood parasite‐host systems. Here I examine the frequency of the three potential long‐term outcomes of brood parasite–host coevolution (coevolutionary cycles, lack of rejection, and successful resistance) in 182 host species. The results of simple exploratory comparisons show that coevolutionary cycles are very scarce while the lack of rejection and successful resistance, which are considered evolutionary enigmas, are much more frequent. I discuss these results considering (i) the importance of different host defences at all stages of the breeding cycle, (ii) the role of phenotypic plasticity in long‐term coevolution, and (iii) the evolutionary history of host selection. I suggest that in purely antagonistic coevolutionary interactions, such as those involving brood parasites and their hosts, that although cycles will exist during an intermediate phase of the interactions, the arms race will end with the extinction of the host or with the host acquiring successful resistance. As evolutionary time passes, this resistance will force brood parasites to use previously less suitable host species. Furthermore, I present a model that represents the long‐term trajectories and outcomes of coevolutionary interactions between brood parasites and their hosts with respect to the evolution of egg‐rejection defence. This model suggests that as an increasing number of species acquire successful resistance, other unparasitized host species become more profitable and their parasitism rate and the costs imposed by brood parasitism at the population level will increase, selecting for the evolution of host defences. This means that although acceptance is adaptive when the parasitism rate and the costs of parasitism are very low, this cannot be considered to represent an evolutionary equilibrium, as conventional theory has done to date, because it is not stable.     

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.     

Cost of resistance: relationship between reduced fertility and increased resistance in a snail—schistosome host—parasite system

Natural host populations often exhibit genetic variability in resistance to parasitism. One possible mechanism for maintaining such diversity is a trade-off between fitness costs associated with resistance and fitness costs associated with parasitism. However, little is known about the nature or magnitude of these costs in animal populations. Using artificial selection experiments in a Biomphalaria glabrata–Schistosoma mansoni host–parasite system, we demonstrated that resistance and susceptibility to infection are heritable. We then investigated whether resistance had any associated costs in terms of snail reproductive success. Susceptible-selected snail lines showed significantly higher fertility (number of offspring produced) than resistant-selected or unselected control snail lines, irrespective of current infection status. There were no consistent differences between snail lines in fecundity, proportion of abnormal egg masses produced, or mean number of eggs per egg mass. Mortality rate was higher among infected than uninfected snails. These results are consistent with snails incurring costs of resistance to schistosome infection in the absence of the parasite.     

Reciprocal influences and costs of parasitism on the development of Corcyra cephalonica and its endoparasitoid Venturia canescens

Many endoparasitoids develop successfully within a range of host instars. Parasitoid survival is highest when parasitism is initiated in earlier host instars, due to age-related changes in internal (physiological) host defences. Most studies examining fitness-related costs associated with differences in host instar have concentrated on the parasitoid, ignoring the effects of parasitism on the development of surviving hosts that have encapsulated parasitoid eggs. A laboratory experiment was undertaken examining fitness-related costs associated with encapsulation of Venturia canescens (Hymenoptera: Ichneumonidae) eggs by fifth (L5) instar larvae of Corcyra cephalonica (Lepidoptera: Pyralidae). Growth and development of both host and parasitoid were monitored in C. cephalonica larvae containing 0, 1, 2, or 4 parasitoid eggs. Adult size and fecundity of C. cephalonica did not vary with the number of eggs per host. However, there was a distinct increase in host mortality with egg number, although most parasitoids emerged from hosts containing a single egg. The most dramatic effect on the host was a highly significant increase in development time from parasitism to adult eclosion, with hosts containing 4 parasitoid eggs taking over 2.5 days longer to complete development than unparasitized larvae. The egg-to-adult development time and size of adult V. canescens did not vary with egg number per host, as demonstrated in a previous experiment using a different host (Plodia interpunctella). The results described here show that there are fitness-related costs to the host associated with resistance to parasitism.     

Physiological consequences of immune response by Drosophila melanogaster (Diptera: Drosophilidae) against the parasitoid Asobara tabida (Hymenoptera: Braconidae)

Abstract Parasites can exert a wide range of negative effects on their hosts. Consequently, hosts that can resist infection should have a selective advantage over nonresistant conspecifics. Yet, host populations remain susceptible to some parasites. Could genetic heterogeneity in the host's ability to resist parasites reflect costs of mounting an immune response? Previous work on Drosophila melanogaster establishes that maintaining the ability to mount an immune response decreases larval competitive ability. Moreover, mounting an immune response decreases fitness. I report on the impact of mounting an immune response on fitness of D. melanogaster survived parasitism by Asobara tabida. I used isofemale lines to determine whether genotype influences the costs of immune response. I examined fitness consequences both to larvae and adults. Survivors of parasitism show no measurable decrease in larval fitness (development time) but have decreased adult fitness (population growth rates), probably because of their smaller size.     

Costs of resistance and infection by a generalist pathogen

Pathogen infection is typically costly to hosts, resulting in reduced fitness. However, pathogen exposure may also come at a cost even if the host does not become infected. These fitness reductions, referred to as “resistance costs”, are inducible physiological costs expressed as a result of a trade‐off between resistance to a pathogen and aspects of host fitness (e.g., reproduction). Here, we examine resistance and infection costs of a generalist fungal pathogen (Metschnikowia bicuspidata) capable of infecting a number of host species. Costs were quantified as reductions in host lifespan, total reproduction, and mean clutch size as a function of pathogen exposure (resistance cost) or infection (infection cost). We provide empirical support for infection costs and modest support for resistance costs for five Daphnia host species. Specifically, only one host species examined incurred a significant cost of resistance. This species was the least susceptible to infection, suggesting the possibility that host susceptibility to infection is associated with the detectability and size of resistance cost. Host age at the time of pathogen exposure did not influence the magnitude of resistance or infection cost. Lastly, resistant hosts had fitness values intermediate between unexposed control hosts and infected hosts. Although not statistically significant, this could suggest that pathogen exposure does come at some marginal cost. Taken together, our findings suggest that infection is costly, resistance costs may simply be difficult to detect, and the magnitude of resistance cost may vary among host species as a result of host life history or susceptibility.     

Differences in parasite susceptibility and costs of resistance between naturally exposed and unexposed host populations

It is generally assumed that resistance to parasitism entails costs. Consequently, hosts evolving in the absence of parasites are predicted to invest less in costly resistance mechanisms than hosts consistently exposed to parasites. This prediction has, however, rarely been tested in natural populations. We studied the susceptibility of three naïve, three parasitized and one recently isolated Asellus aquaticus isopod populations to an acanthocephalan parasite. We found that parasitized populations, with the exception of the isopod population sympatric with the parasite strain used, were less susceptible to the parasite than the naïve populations. Exposed but uninfected (resistant) isopods from naïve populations, but not from parasitized populations, exhibited greater mortality than controls, implying that resistance entails survival costs primarily for naïve isopods. These results suggest that parasites can drive the evolution of host resistance in the wild, and that co‐existence with parasites may increase the cost‐effectiveness of defence mechanisms.     

Condition and fecundity of the damselfly,Enallagma ebrium (Hagen): the importance of ectoparasites

Summary The extent, magnitude, and cause of natural covariation between degree of parasitism and other variables known or suspected of influencing host fitness (such as host age or body size) has been understudied. We demonstrate that degree of parasitism by larval water mites (Arrenurus spp.) was associated with reduced condition of males and with lowered fecundity of young females of the damselfly, Enallagma ebrium (Hagen) (Odonata: Coenagrionidae). We also demonstrate that degree of parasitism can covary with both age and size of host damselflies. We explain the putative causes of such natural covariation, and we suggest that degree of parasitism, host age, and host size can all interact to determine damselfly fitness. We expect that natural covariation between the host's phenotype and degree of parasitism will be frequently observed. Studies of such natural covariation will help researchers to assess better the importance of several variables on host reproductive success and to understand better the dynamics of host-parasite interactions.     

GENETICS OF BRASSICA RAPA. 3. COSTS OF DISEASE RESISTANCE TO THREE FUNGAL PATHOGENS

Genetic costs of resistance to pathogens may be an important factor maintaining heritable variation for resistance in natural populations. Pleiotropic fitness trade-offs occur when genetic resistance causes reduction in other components of fitness. Although costs of resistance have an important influence on plant-pathogen interactions, few previous studies have detected pleiotropic costs of resistance in the absence of confounding effects of linkage disequilibrium. To avoid this potential problem, we performed artificial selection experiments on resistance to two fungal pathogens, Leptosphaeria maculans, and Peronospora parasitica, and compared growth rates of resistant and susceptible genotypes of Brassica rapa in the absence of pathogens. Leptosphaeria resistance had no effect on growth rate, indicating cost-free defense. In contrast, Peronospora-resistant genotypes grow 6% slower than Peronospora-susceptible genotypes in pathogen-free environments, indicating a significant genetic fitness cost to Peronospora resistance. Such genetic trade-offs could maintain genetic variation in the wild. Another factor that might explain heritable variation for resistance is ecological trade-offs, in which genetic resistance to one species causes susceptibility to another. Such ecological trade-offs do not exist for the pathogens studied in this system.     

COSTS AND BENEFITS OF MOSQUITO REFRACTORINESS TO MALARIA PARASITES: IMPLICATIONS FOR GENETIC VARIABILITY OF MOSQUITOES AND GENETIC CONTROL OF MALARIA

The problem of fitness costs associated with host resistance to parasitism is related to the evolution of parasite virulence, population genetic diversity and the dynamics of host-parasite relationships, and proposed strategies for disease control through the genetic manipulation of mosquito vectors. Two Aedes aegypti populations, refractory and susceptible to Plasmodium gallinaceum, were previously selected from the Moyo-In-Dry strain (MOYO) through inbreeding (F = 0.5). Reproductive success and survivorship of the two populations were compared, and the influence of the parasite on mosquito fitness also was evaluated. Fitness components studied include fecundity, adult survivorship and egg-to-adult developmental time, blood-meal size, and adult body size. The refractory population has a significantly shorter egg-to-adult developmental time and a smaller body size, takes a smaller blood meal, and subsequently lays fewer eggs than the susceptible population. The mean longevity of the refractory population is significantly shorter than the susceptible population. Exposure to the parasite exhibited little effect on the survivorship and fecundity of either population. Several factors may contribute to the lower fitness of the refractory population, including founder effect, inbreeding depression, the effect of other uncharacterized genes linked to genes conferring refractoriness, and pleiotropic effects associated with these genes. The results are discussed in relation to the genetic diversity of natural mosquito populations and their implications for the genetic control of malaria.     

The relationship among host plant species,egg clutch size,and level of parasitism for the sharpshooter Tapajosa rubromarginata

The sharpshooter Tapajosa rubromarginata (Signoret) (Hemiptera: Cicadellidae, Proconiini), a vector of the bacterium Xylella fastidiosa Wells et al. (Xanthomonadaceae) that causes citrus variegated chlorosis, has more than 30 reported host plant species. The fitness of a phytophagous insect is determined by the host plant suitability, plant resistance, and the natural enemies. The aim of this study was to: (1) identify plant species utilized as oviposition substrate by T. rubromarginata in the field; (2) establish the relationship between plants and clutch size; (3) establish the relationship among host plants, clutch size, and level of parasitism; and (4) establish variations in parasitoid composition and abundance in the various host plants. Egg masses of the sharpshooter were surveyed on plants reported as hosts, or those that were abundant in the study site. The number of eggs of the sharpshooter and emerged parasitoids were recorded for all the collected masses. We found egg masses of T. rubromarginata on 12 out of 21 plant species sampled. The size of the egg masses was greatly influenced by the type of leaf venation and to a lesser extent by the plant species. Parasitism rates were influenced by both leaf venation and host plant. Trichogrammatidae species were mostly associated with egg masses in plants with parallel-veined leaves, whereas Mymaridae attacked masses laid in reticular-veined leaves. The choice between a good host plant, but heavily attacked by parasitoids, and the host plants that are less suitable for nymphs but less frequently attacked by natural enemies, was a trade-off for T. rubromarginata females to increase their fitness. We conclude that the host plant utilization by T. rubromarginata females in the field could be influenced by leaf structure and the strategy to avoid parasitism by selecting plants that were less attractive for parasitoids.