Climate variation influences host specificity in avian malaria parasites

Parasites with low host specificity (e.g. infecting a large diversity of host species) are of special interest in disease ecology, as they are likely more capable of circumventing ecological or evolutionary barriers to infect new hosts than are specialist parasites. Yet for many parasites, host specificity is not fixed and can vary in response to environmental conditions. Using data on host associations for avian malaria parasites (Apicomplexa: Haemosporida), we develop a hierarchical model that quantifies this environmental dependency by partitioning host specificity variation into region‐ and parasite‐level effects. Parasites were generally phylogenetic host specialists, infecting phylogenetically clustered subsets of available avian hosts. However, the magnitude of this specialisation varied biogeographically, with parasites exhibiting higher host specificity in regions with more pronounced rainfall seasonality and wetter dry seasons. Recognising the environmental dependency of parasite specialisation can provide useful leverage for improving predictions of infection risk in response to global climate change.     

Egg mimicry by the Pacific koel: mimicry of one host facilitates exploitation of other hosts with similar egg types

When brood parasites exploit multiple host species, egg rejection by hosts may select for the evolution of host‐specific races, where each race mimics a particular host's egg type. However, some brood parasites that exploit multiple hosts with the ability to reject foreign eggs appear to have only a single egg type. In these cases, it is unclear how the parasite egg escapes detection by its hosts. Three possible explanations are: 1) host‐specific races are present, but differences in egg morphology are difficult for the human eye to detect; 2) the brood parasite evolves a single egg type that is intermediate in appearance between the eggs of its hosts; 3) or the parasite evolves mimicry of one of its hosts, which subsequently allows it to exploit other species with similar egg morphology. Here we test these possibilities by quantifying parameters of egg appearance of the brood‐parasitic Pacific koel Eudynamys orientalis and seven of its hosts. Koel eggs laid in the nests of different hosts did not show significant differences in colour or pattern, suggesting that koels have not evolved host‐specific races. Koel eggs were similar in colour, luminance and pattern to the majority of hosts, but were significantly more similar in colour and luminance to one of the major hosts than to two other major hosts, supporting hypothesis 3. Our findings suggest that mimicry of one host can allow a brood parasite to exploit new hosts with similar egg morphologies, which could inhibit the evolution of host defences in naïve hosts.     

The costs of avian brood parasitism explain variation in egg rejection behaviour in hosts

Many bird species can reject foreign eggs from their nests. This behaviour is thought to have evolved in response to brood parasites, birds that lay their eggs in the nest of other species. However, not all hosts of brood parasites evict parasitic eggs. In this study, we collate data from egg rejection experiments on 198 species, and perform comparative analyses to understand the conditions under which egg rejection evolves. We found evidence, we believe for the first time in a large-scale comparative analysis, that (i) non-current host species have rejection rates as high as current hosts, (ii) egg rejection is more likely to evolve when the parasite is relatively large compared with its host and (iii) egg rejection is more likely to evolve when the parasite chick evicts all the host eggs from the nest, such as in cuckoos. Our results suggest that the interactions between brood parasites and their hosts have driven the evolution of egg rejection and that variation in the costs inflicted by parasites is fundamental to explaining why only some host species evolve egg rejection.     

Host switching in cowbird brood parasites: how often does it occur?

Avian obligate brood parasites lay their eggs in nests of host species, which provide all parental care. Brood parasites may be host specialists, if they use one or a few host species, or host generalists, if they parasitize many hosts. Within the latter, strains of host‐specific females might coexist. Although females preferentially parasitize one host, they may occasionally successfully parasitize the nest of another species. These host switching events allow the colonization of new hosts and the expansion of brood parasites into new areas. In this study, we analyse host switching in two parasitic cowbirds, the specialist screaming cowbird (Molothrus rufoaxillaris) and the generalist shiny cowbird (M. bonariensis), and compare the frequency of host switches between these species with different parasitism strategies. Contrary to expected, host switches did not occur more frequently in the generalist than in the specialist brood parasite. We also found that migration between hosts was asymmetrical in most cases and host switches towards one host were more recurrent than backwards, thus differing among hosts within the same species. This might depend on a combination of factors including the rate at which females lay eggs in nests of alternative hosts, fledging success of the chicks in this new host and their subsequent success in parasitizing it.     

Polyrhachis lama, a parasitic ant with an exceptional mode of social integration

Social parasitism is a common phenomenon amongst ants that occurs in manifold variations with differing levels of parasite–host integration. Particularly, high levels of social integration occur amongst closely related species (Emery’s rule), which form mixed colonies with their hosts and comprise the vast majority of social parasites. Considerable lower levels of integration are typically found amongst unrelated species that live in clearly separated colonies. The formicine ant Polyrhachis lama, however, parasitises a phylogenetically distant host species, Diacamma sp. of the subfamily Ponerinae, but lives spatially mixed with the host colonies. Studies on integration and communication have indicated that P. lama shows a high degree of host integration. However, the allocation of brood care behaviour, a central aspect of parasite integration, has not been studied. Because all known ant social parasites that are fully mixed with their host colonies are also true brood parasites, we investigated the integration of P. lama brood. Our results demonstrate that the parasite brood has a high degree of spatial integration, although it remains functionally separated regarding nutritive brood care. This can be attributed to behavioural and morphological differences between the phylogenetically distant species. The observed spatial confinement of parasite brood, however, is most likely due to an unusual method of chemical host integration. The parasite brood remains accepted in the Diacamma colonies only under the presence of adult parasites. Altogether, this suggests an active mechanism of chemical integration based on the acceptance allomones originating from P. lama workers. Electronic supplementary material  The online version of this article (doi:) contains supplementary material, which is available to authorized users.     

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.     

When will rejection of parasite nestlings by hosts of nonevicting avian brood parasites be favored? A misimprinting-equilibrium model

It has been suggested that discrimination and rejection of thenestlings of avian brood parasites are most likely to evolvewhen the parasite nestling is raised alongside the host nestlings,for example, many cowbird-host systems. Under these circumstances,the benefits of discrimination are high because the host parentsmay save most of their brood. However, there is a general absenceof nestling rejection behavior among hosts of nonevicting parasites.In a cost-benefit equilibrium model, based on the premise thathost species learn to recognize their offspring through imprintingon first breeding, we show that nestling recognition can beadaptive for hosts of cowbirds, but only under strict conditions.Namely, when host nestling survival alongside the parasite islow, rates of parasitism are high and the average clutch sizeis large. All of these conditions are seldom simultaneouslyachieved in real systems. Most importantly, the parasite nestling,on average, does not sufficiently depress host nestling survivalto outweigh the costs of nestling recognition and rejectionerrors. Thus, we argue that nestling acceptance behaviors byhosts of nonevicting brood parasites may be explained as anevolutionary equilibrium in which recognition costs act as astabilizing selection pressure against rejection when most ofthe host's offspring survive parasitism.     

Nestling sex predicts susceptibility to parasitism and influences parasite population size within avian broods

Vertebrate hosts differ in their level of parasite susceptibility and infestation. In avian broods, variation in susceptibility of nestlings to ectoparasites may be associated with non‐uniform distributions of parasites among brood mates, with parasites concentrating feeding on the most vulnerable hosts. The presence of a highly susceptible nestling in a brood can benefit the remaining young by reducing the parasite pressure they experience; however, from a parasite’s perspective, broods with fewer susceptible hosts may provide effectively fewer resources than broods of the same size containing a greater abundance of susceptible hosts, and this could limit the number of parasites that a host brood can sustain. To test whether variation in number of susceptible hosts affects the number of parasites in bird nests, we first examined the role of host sex and induced immunity (via methionine supplementation) on susceptibility of mountain bluebirds Sialia currucoides to parasitism by blow flies Protocalliphora spp. We then assessed the effect of variation in number of susceptible hosts on the number of parasites inhabiting the nest. Only females showed a benefit of methionine supplementation, gaining mass more rapidly following supplementation compared to males. This suggests that females are more susceptible to parasites in this system; this was further supported by parasite feeding trials, in which parasites extracted larger blood meals from female than male hosts. Finally, the abundance of parasites in nests was predicted by brood sex ratio: broods containing more female young harboured more parasites. Hence, within‐brood variation in host susceptibility to parasites can not only influence the costs of parasitism for individual nestlings, but may also have consequences for the size of parasite populations within nests. If patterns of maternal investment affect the abundance of nest‐dwelling parasites, these interactions may be important for understanding fitness consequences of maternal resource allocation in many vertebrate hosts.     

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.     

Collective defence portfolios of ant hosts shift with social parasite pressure

Host defences become increasingly costly as parasites breach successive lines of defence. Because selection favours hosts that successfully resist parasitism at the lowest possible cost, escalating coevolutionary arms races are likely to drive host defence portfolios towards ever more expensive strategies. We investigated the interplay between host defence portfolios and social parasite pressure by comparing 17 populations of two Temnothorax ant species. When successful, collective aggression not only prevents parasitation but also spares host colonies the cost of searching for and moving to a new nest site. However, once parasites breach the host''s nest defence, host colonies should resort to flight as the more beneficial resistance strategy. We show that under low parasite pressure, host colonies more likely responded to an intruding Protomognathus americanus slavemaker with collective aggression, which prevented the slavemaker from escaping and potentially recruiting nest-mates. However, as parasite pressure increased, ant colonies of both host species became more likely to flee rather than to fight. We conclude that host defence portfolios shift consistently with social parasite pressure, which is in accordance with the degeneration of frontline defences and the evolution of subsequent anti-parasite strategies often invoked in hosts of brood parasites.     

Intra‐specific body size variation in Polistes paper wasps as a response to social parasite pressure

1. Like avian brood parasites, obligate insect social parasites exploit the parental care of a host species to rear their brood, causing an evident loss of host reproductive success. This fitness cost imposes selective pressure on the host to reduce the parasite effect. A possible outcome of an evolutionary arms race is the selection of host morphological counter‐adaptations to resist parasite attacks. 2. We studied host–parasite pairs of Polistes wasps in which the fighting equipment of the parasite's body allows it to enter the host colony. 3. We searched for host morphological traits related to fighting ability that could be considered counter‐adaptations. As a host–parasite co‐evolutionary arms race can only occur where the two lineages co‐exist, we compared morphological traits of hosts belonging to populations with or without parasite pressure. We report that host foundresses belonging to populations under strong parasite pressure have a larger body size than those belonging to populations without parasite pressure. 4. Behavioural experiments carried out to test if an increase in host body size is useful to oppose parasite usurpation show that large body size foundresses exhibit a greater ability of nest defence.     

Costs to host defence and the persistence of parasitic cuckoos.

Raising genetically unrelated young is maladaptive, yet brood parasitism is widespread in birds. In several systems, hosts can evolve near-perfect defences against the parasite (discrimination and rejection of unlike eggs), making it difficult to understand how the parasite continues to exist. This study demonstrates costs to host defences (e.g. rejection of one's own eggs) such that once the parasite goes extinct on a particular host species, defence mechanisms are selectively disadvantageous. The consequent loss of host defences, and potential for re-exploitation of the host by the parasite, can explain the continued persistence of avian brood parasites. The results provide one general explanation for coexistence of parasites and their hosts.     

The ghosts of parasitism past: lingering frontline anti-brood parasite defenses in a former host

Coevolutionary arms races between brood parasites and hosts provide tractable systems for understanding antagonistic coevolution in nature; however, little is known about the fate of frontline antiparasite defenses when the host “wins” the coevolutionary arms race. By recreating bygone species interactions, using artificial parasitism experiments, lingering defensive behaviors that evolved in the context of parasitism can be understood and may even be used to identify the unknown agent of parasitism past. Here we present the first study of this type by evaluating lingering “frontline” nest defenses that have evolved to prevent egg laying in a former brood parasite host. The Australian reed warbler Acrocephalus australis is currently not parasitized but is known to exhibit fine-tuned egg discrimination—a defensive behavior indicative of a past brood parasite–host arms race and common in closely related parasitized species. Here, using 3D-printed models of adult brood parasites, we examined whether the Australian reed warbler also exhibits frontline defenses to adult brood parasites, and whether we could use these defenses to identify the warbler’s “ghost of parasitism past.” Our findings provide evidence that the Australian reed warbler readily engages in frontline defenses that are considered adaptive specifically in the context of brood parasitism. However, individuals were unable to discriminate between adults of different brood parasite species at their nest. Overall, our results demonstrate that despite a relaxation in selection, defenses against brood parasitism can be maintained across multiple stages of the host’s nesting cycle, and further suggest that, in accordance with previous findings, that learning may be important for fine-tuning frontline defense.     

Does Brood Parasitism Induce Paternal Care in a Polygynous Host?

Red‐winged blackbirds (Agelaius phoeniceus) are a polygynous songbird with facultative biparental care, and a common host for brown‐headed cowbirds (Molothrus ater), an obligate brood parasite. We examined brood parasitism and paternal care in a long‐term study of parental care in red‐winged blackbirds. The presence of a cowbird nestling was associated with a higher likelihood of paternal care by the host male redwing in both naturally and experimentally parasitized nests. This result indicates that it was the presence of the brood parasite that was important and not simply that brood parasites chose hosts where paternal care was more likely. Both male and particularly female redwings increased provisioning to parasitized broods. Our work suggests that brood parasites raise the cost of parental care and push a polygynous host species toward monogamy.     

EVOLUTIONARY ASSOCIATIONS OF BROOD PARASITIC FINCHES (VIDUA) AND THEIR HOST SPECIES: ANALYSES OF MITOCHONDRIAL DNA RESTRICTION SITES

The species-specific associations of the African brood parasitic finches Vidua with their estrildid finch host species may have originated by cospeciation with the host species or by later colonizations of new hosts. Predictions of these alternative models were tested in two species groups of brood parasites (indigobirds, paradise whydahs) and their hosts. Phylogenetic analyses suggested that the brood parasites and their hosts did not speciate in parallel. The parasitic indigobirds share mitochondrial haplotypes with each other, and species limits in both indigobirds and paradise whydahs do not correspond with their gene trees. Different parasite species within a region are more closely related to each other than any is to parasites that are associated with its same host species in other regions of Africa. There is little genetic difference between parasite species D?_i,j < 0.001 in the indigobirds, D?_i,j = 0.01 in the whydahs). Genetic distances D?_i,j between the parasite species are less than the genetic distances between their corresponding host species in all parasite-host comparisons, and average only 7.2% as large in the indigobirds as in their hosts and 42% as large in the paradise whydahs as in their hosts. A phylogenetic model that allows ancestral haplotype polymorphisms to be retained in descendant species was compared to a constraint model of species monophyly requiring all but the one ancestral haplotype to be independently derived within each species. The constraint model increases the length of the indigobird tree by 50% over that of the model of retained ancestral polymorphisms; the difference is statistically significant. Both phylogenetic and distance analyses indicate that the brood parasites have become associated with their host species through host switches and independent colonizations of the hosts, rather than through parallel cospeciation with them. The molecular genetic results are supported by recent discoveries of additional host species that are associated with the indigobirds in the field and by variation in the species-specific song behaviors of the brood parasites.     

Biogeography of avian blood parasites (Leucocytozoon spp.) in two resident hosts across Europe: phylogeographic structuring or the abundance–occupancy relationship?

Relationships between hosts and parasites represent complex co-evolving systems that can vary both temporally and spatially. This variation may result in different phylogeographic outcomes, ranging from highly geographically structured parasite populations comprised of specialist lineages that are locally abundant but have restricted global occupancy to geographically unstructured parasite populations consisting of widespread parasites. Here, we present results from a large biogeographic study of the Leucocytozoon blood parasites of two nonmigrant bird species, conducted at nine sites across Europe. The aim was to determine whether the parasite lineages of the two hosts were phylogeographically structured across Europe. Employing molecular methods, we found a large diversity of parasites, and although overall prevalence varied greatly, the parasites were not genetically structured. Several measures of local parasite abundance were associated with the number of sites that the lineage occurred in, which is consistent with the macroecological phenomenon of the abundance-occupancy relationship. Taken together, our results show that parasite dispersal is somewhat uncoupled to that of the host in this system: we suggest that broad host and/or vector preference may play an important role in determining the distribution of these parasites and in affecting host-parasite coevolution in this system.     

Host plant preference and performance of the sibling species of butterflies <Emphasis Type="Italic">Leptidea sinapis</Emphasis> and <Emphasis Type="Italic">Leptidea reali</Emphasis>: a test of the trade-off hypothesis for food specialisation

A large proportion of phytophagous insect species are specialised on one or a few host plants, and female host plant preference is predicted to be tightly linked to high larval survival and performance on the preferred plant(s). Specialisation is likely favoured by selection under stable circumstances, since different host plant species are likely to differ in suitability—a pattern usually explained by the “trade-off hypothesis”, which posits that increased performance on a given plant comes at a cost of decreased performance on other plants. Host plant specialisation is also ascribed an important role in host shift speciation, where different incipient species specialise on different host plants. Hence, it is important to determine the role of host plants when studying species divergence and niche partitioning between closely related species, such as the butterfly species pair Leptidea sinapis and Leptidea reali. In Sweden, Leptidea sinapis is a habitat generalist, appearing in both forests and meadows, whereas Leptidea reali is specialised on meadows. Here, we study the female preference and larval survival and performance in terms of growth rate, pupal weight and development time on the seven most-utilised host plants. Both species showed similar host plant rank orders, and larvae survived and performed equally well on most plants with the exceptions of two rarely utilised forest plants. We therefore conclude that differences in preference or performance on plants from the two habitats do not drive, or maintain, niche separation, and we argue that the results of this study do not support the trade-off hypothesis for host plant specialisation, since the host plant generalist Leptidea sinapis survived and performed as well on the most preferred meadow host plant Lathyrus pratensis as did Leptidea reali although the generalist species also includes other plants in its host range. Electronic supplementary material  The online version of this article (doi:) contains supplementary material, which is available to authorized users.     

Host and brood parasite coevolutionary interactions covary with comparative patterns of the avian visual system

In coevolutionary arms-races, reciprocal ecological interactions and their fitness impacts shape the course of phenotypic evolution. The classic example of avian host–brood parasite interactions selects for host recognition and rejection of increasingly mimetic foreign eggs. An essential component of perceptual mimicry is that parasitic eggs escape detection by host sensory systems, yet there is no direct evidence that the avian visual system covaries with parasitic egg recognition or mimicry. Here, we used eye size measurements collected from preserved museum specimens as a metric of the avian visual system for species involved in host–brood parasite interactions. We discovered that (i) hosts had smaller eyes compared with non-hosts, (ii) parasites had larger eyes compared with hosts before but not after phylogenetic corrections, perhaps owing to the limited number of independent evolutionary origins of obligate brood parasitism, (iii) egg rejection in hosts with non-mimetic parasitic eggs positively correlated with eye size, and (iv) eye size was positively associated with increased avian-perceived host–parasite eggshell similarity. These results imply that both host-use by parasites and anti-parasitic responses by hosts covary with a metric of the visual system across relevant bird species, providing comparative evidence for coevolutionary patterns of host and brood parasite sensory systems.     

Coevolution of daily activity timing in a host–parasite system

Coevolutionary theories applied in the study of host–parasite systems indicate that lineages exhibit progressive trends in response to reciprocal selective pressures. Avian brood parasites have generated intense interest as models for coevolutionary processes. Similar to avian cuckoos, Polistes wasp social parasites usurp a nest and exploit the parental care of a congeneric species to rear their own brood. In the present study, we show a coevolutionary arms race in the daily activity pattern in a Polistes host–parasite pair. We measured the daily activity rate, in constant laboratory conditions, of both host and parasite females during the period in which nest usurpations occur. The parasites showed a hyperkinesis in the middle of the day. As the field observations suggested, this mid-day activity is used to perform host nest usurpation attempts. Timing the usurpations allows the parasite to maximize its usurpation attempts during daytime when the host defence is lower. A field comparison of host presence on the nest in two populations with different parasitism rates showed that populations under strong parasitic pressure exhibit timing counteradaptations to optimize nest defence. This study provides the first example of a mutual coadaptation in timing activity in a parasite–host system.  © 2009 The Linnean Society of London, Biological Journal of the Linnean Society , 2009, 96 , 399–405.