How to evade a coevolving brood parasite: egg discrimination versus egg variability as host defences

Arms races between avian brood parasites and their hosts often result in parasitic mimicry of host eggs, to evade rejection. Once egg mimicry has evolved, host defences could escalate in two ways: (i) hosts could improve their level of egg discrimination; and (ii) negative frequency-dependent selection could generate increased variation in egg appearance (polymorphism) among individuals. Proficiency in one defence might reduce selection on the other, while a combination of the two should enable successful rejection of parasitic eggs. We compared three highly variable host species of the Afrotropical cuckoo finch Anomalospiza imberbis, using egg rejection experiments and modelling of avian colour and pattern vision. We show that each differed in their level of polymorphism, in the visual cues they used to reject foreign eggs, and in their degree of discrimination. The most polymorphic host had the crudest discrimination, whereas the least polymorphic was most discriminating. The third species, not currently parasitized, was intermediate for both defences. A model simulating parasitic laying and host rejection behaviour based on the field experiments showed that the two host strategies result in approximately the same fitness advantage to hosts. Thus, neither strategy is superior, but rather they reflect alternative potential evolutionary trajectories.     

Social learning of a brood parasite by its host

Arms races between brood parasites and their hosts provide model systems for studying the evolutionary repercussions of species interactions. However, how naive hosts identify brood parasites as enemies remains poorly understood, despite its ecological and evolutionary significance. Here, we investigate whether young, cuckoo-naive superb fairy-wrens, Malurus cyaneus, can learn to recognize cuckoos as a threat through social transmission of information. Naive individuals were initially unresponsive to a cuckoo specimen, but after observing conspecifics mob a cuckoo, they made more whining and mobbing alarm calls, and spent more time physically mobbing the cuckoo. This is the first direct evidence that naive hosts can learn to identify brood parasites as enemies via social learning.     

Evolution of host egg mimicry in a brood parasite, the great spotted cuckoo

Brood parasitism in birds is one of the best examples of coevolutionary interactions in vertebrates. Coevolution between hosts and parasites is assumed to occur because the parasite imposes strong selection pressures on its hosts, reducing their fitness and thereby favouring counter-adaptations (e.g. egg rejection) which, in turn, select for parasite resistance (e.g. egg mimicry). Great spotted cuckoos ( Clamator glandarius ) are usually considered a brood parasite with eggs almost perfectly mimicking those of their host, the magpie ( Pica pica ). However, Cl. glandarius also exploits South African hosts with very different eggs, both in colour and size, while the Cl. glandarius eggs are similar to those laid in nests of European hosts. Here, we used spectrophotometric techniques for the first time to quantify mimicry of parasitic eggs for eight different host species. We found: (1) non-significant differences in appearance of Cl. glandarius eggs laid in nests of different host species, although eggs laid in South Africa and Europe differed significantly; (2) contrary to the general assumption that Cl. glandarius eggs better mimic those of the main host in Europe ( P. pica ), Cl. glandarius eggs more closely resembled those of the azure-winged magpie ( Cyanopica cyana ), a potential host in which there is no evidence of recent parasitism; (3) the appearance of Cl. glandarius eggs was not significantly related to the appearance of host eggs. We discuss three possible reasons why Cl. glandarius eggs resemble eggs of some of their hosts. We suggest that colouration of Cl. glandarius eggs is an apomorphic trait, and that variation between eggs laid in South African and European host nests is due to genetic isolation among these populations and not due to variation in colouration of host eggs.  © 2003 The Linnean Society of London, Biological Journal of the Linnean Society , 2003, 79 , 551–563.     

Coinfecting parasites can modify fluctuating selection dynamics in host–parasite coevolution

Genetically specific interactions between hosts and parasites can lead to coevolutionary fluctuations in their genotype frequencies over time. Such fluctuating selection dynamics are, however, expected to occur only under specific circumstances (e.g., high fitness costs of infection to the hosts). The outcomes of host–parasite interactions are typically affected by environmental/ecological factors, which could modify coevolutionary dynamics. For instance, individual hosts are often infected with more than one parasite species and interactions between them can alter host and parasite performance. We examined the potential effects of coinfections by genetically specific (i.e., coevolving) and nonspecific (i.e., generalist) parasite species on fluctuating selection dynamics using numerical simulations. We modeled coevolution (a) when hosts are exposed to a single parasite species that must genetically match the host to infect, (b) when hosts are also exposed to a generalist parasite that increases fitness costs to the hosts, and (c) when coinfecting parasites compete for the shared host resources. Our results show that coinfections can enhance fluctuating selection dynamics when they increase fitness costs to the hosts. Under resource competition, coinfections can either enhance or suppress fluctuating selection dynamics, depending on the characteristics (i.e., fecundity, fitness costs induced to the hosts) of the interacting parasites.     

Superinfection and the coevolution of parasite virulence and host recovery

Parasite strategies of host exploitation may be affected by host defence strategies and multiple infections. In particular, within‐host competition between multiple parasite strains has been shown to select for higher virulence. However, little is known on how multiple infections could affect the coevolution between host recovery and parasite virulence. Here, we extend a coevolutionary model introduced by van Baalen (Proc. R. Soc. B, 265, 1998, 317) to account for superinfection. When the susceptibility to superinfection is low, we recover van Baalen's results and show that there are two potential evolutionary endpoints: one with avirulent parasites and poorly defended hosts, and another one with high virulence and high recovery. However, when the susceptibility to superinfection is above a threshold, the only possible evolutionary outcome is one with high virulence and high investment into defence. We also show that within‐host competition may select for lower host recovery, as a consequence of selection for more virulent strains. We discuss how different parasite and host strategies (superinfection facilitation, competitive exclusion) as well as demographic and environmental parameters, such as host fecundity or various costs of defence, may affect the interplay between multiple infections and host–parasite coevolution. Our model shows the interplay between coevolutionary dynamics and multiple infections may be affected by crucial mechanistic or ecological details.     

Evidence for aggressive mimicry in an adult brood parasitic bird,and generalized defences in its host

Mimicry of a harmless model (aggressive mimicry) is used by egg, chick and fledgling brood parasites that resemble the host''s own eggs, chicks and fledglings. However, aggressive mimicry may also evolve in adult brood parasites, to avoid attack from hosts and/or manipulate their perception of parasitism risk. We tested the hypothesis that female cuckoo finches (Anomalospiza imberbis) are aggressive mimics of female Euplectes weavers, such as the harmless, abundant and sympatric southern red bishop (Euplectes orix). We show that female cuckoo finch plumage colour and pattern more closely resembled those of Euplectes weavers (putative models) than Vidua finches (closest relatives); that their tawny-flanked prinia (Prinia subflava) hosts were equally aggressive towards female cuckoo finches and southern red bishops, and more aggressive to both than to their male counterparts; and that prinias were equally likely to reject an egg after seeing a female cuckoo finch or bishop, and more likely to do so than after seeing a male bishop near their nest. This is, to our knowledge, the first quantitative evidence for aggressive mimicry in an adult bird, and suggests that host–parasite coevolution can select for aggressive mimicry by avian brood parasites, and counter-defences by hosts, at all stages of the reproductive cycle.     

Specialization and local adaptation of a fungal parasite on two host plant species as revealed by two fitness traits

We investigate the geographic pattern of adaptation of a fungal parasite, Colletotrichum lindemuthianum, on two host species, Phaseolus vulgaris and P. coccineus for two parasite fitness traits: infectivity (ability to attack a host individual) and aggressivity (degree of sporulation and leaf surface damage). Using a cross-inoculation experiment, we show specialization of the fungus on its host species of origin for both traits even when fungi, which originated from hosts growing in sympatry, were tested on sympatric host populations. Within the two host species, we compared infectivity and aggressivity on local versus allopatric plant-fungus combinations. We found evidence for local adaptation for the two traits on P. vulgaris but not on P. coccineus. There was no significant correlation between the degrees of local adaptation for infectivity and aggressivity, indicating that the genetic basis and the effect of selection may differ between these two traits. For the two fitness traits, a positive correlation between the degree of specialization and the degree of local adaptation was found, suggesting that specialization can be reinforced by local adaptation.     

Begging call matching between a specialist brood parasite and its host: a comparative approach to detect coevolution

Studies of avian brood parasite systems have typically investigated the mimicry of host eggs by specialist parasites. Yet, several examples of similarity between host and parasite chick appearance or begging calls suggest that the escalation of host–parasite arms races may also lead to visual or vocal mimicry at the nestling stage. Despite this, there have been no large-scale comparative studies of begging calls to test whether the similarity of host and parasite is greater than predicted by chance or phylogenetic distance within a geographically distinct species assemblage. Using a survey of the begging calls of all native forest passerines in New Zealand, we show that the begging call of the host-specialist shining cuckoo ( Chrysococcyx lucidus ) is most similar to that of its grey warbler ( Gerygone igata ) host compared to any of the other species, and that this is unlikely to have occurred by chance. Randomization tests revealed that the incorporation of the shining cuckoo's begging calls into our species-set consistently reduced the phylogenetic signal within cluster trees based on begging call similarity. By contrast, the removal of the grey warbler calls did not reduce the phylogenetic signal in the begging call similarity trees. These two results support a scenario in which coevolution of begging calls has not taken place: the begging call of the host retains its phylogenetic signal, whereas that of the parasite has changed to match that of its host.  © 2009 The Linnean Society of London, Biological Journal of the Linnean Society , 2009, 98 , 208–216.     

Polygenic traits and parasite local adaptation

The extent to which parasites are locally adapted to their hosts has important implications for human health and agriculture. A recently developed conceptual framework--the geographic mosaic theory of coevolution--predicts that local maladaptation should be common and largely determined by the interplay between gene flow and spatially variable reciprocal selection. Previous investigation of this theory has predominately focused on genetic systems of infection and resistance characterized by few genes of major effect and particular forms of epistasis. Here we extend existing theory by analyzing mathematical models of host-parasite interactions in which host resistance to parasites is mediated by quantitative traits with an additive polygenic basis. In contrast to previous theoretical studies predicated upon major gene mechanisms, we find that parasite local maladaptation is quite uncommon and restricted to one specific functional form of host resistance. Furthermore, our results show that local maladaptation should be rare or absent in studies that measure local adaptation using reciprocal transplant designs conducted in natural environments. Our results thus narrow the scope over which the predictions of the geographic mosaic theory are likely to hold and provide novel and readily testable predictions about when and where local maladaptation is expected.     

Dynamic egg color mimicry

Evolutionary hypotheses regarding the function of eggshell phenotypes, from solar protection through mimicry, have implicitly assumed that eggshell appearance remains static throughout the laying and incubation periods. However, recent research demonstrates that egg coloration changes over relatively short, biologically relevant timescales. Here, we provide the first evidence that such changes impact brood parasite–host eggshell color mimicry during the incubation stage. First, we use long‐term data to establish how rapidly the Acrocephalus arundinaceus Linnaeus (great reed warbler) responded to natural parasitic eggs laid by the Cuculus canorus Linnaeus (common cuckoo). Most hosts rejected parasitic eggs just prior to clutch completion, but the host response period extended well into incubation (~10 days after clutch completion). Using reflectance spectrometry and visual modeling, we demonstrate that eggshell coloration in the great reed warbler and its brood parasite, the common cuckoo, changes rapidly, and the extent of eggshell color mimicry shifts dynamically over the host response period. Specifically, 4 days after being laid, the host should notice achromatic color changes to both cuckoo and warbler eggs, while chromatic color changes would be noticeable after 8 days. Furthermore, we demonstrate that the perceived match between host and cuckoo eggshell color worsened over the incubation period. These findings have important implications for parasite–host coevolution dynamics, because host egg discrimination may be aided by disparate temporal color changes in host and parasite eggs.     

The evolution of reduced antagonism—A role for host–parasite coevolution

Why do some host–parasite interactions become less antagonistic over evolutionary time? Vertical transmission can select for reduced antagonism. Vertical transmission also promotes coevolution between hosts and parasites. Therefore, we hypothesized that coevolution itself may underlie transitions to reduced antagonism. To test the coevolution hypothesis, we selected for reduced antagonism between the host Caenorhabditis elegans and its parasite Serratia marcescens. This parasite is horizontally transmitted, which allowed us to study coevolution independently of vertical transmission. After 20 generations, we observed a response to selection when coevolution was possible: reduced antagonism evolved in the copassaged treatment. Reduced antagonism, however, did not evolve when hosts or parasites were independently selected without coevolution. In addition, we found strong local adaptation for reduced antagonism between replicate host/parasite lines in the copassaged treatment. Taken together, these results strongly suggest that coevolution was critical to the rapid evolution of reduced antagonism.     

A quantitative trait locus for recognition of foreign eggs in the host of a brood parasite

Avian brood parasites reduce the reproductive output of their hosts and thereby select for defence mechanisms such as ejection of parasitic eggs. Such defence mechanisms simultaneously select for counter-defences in brood parasites, causing a coevolutionary arms race. Although coevolutionary models assume that defences and counter-defences are genetically influenced, this has never been demonstrated for brood parasites. Here, we give strong evidence for genetic differences between ejector and nonejectors, which could allow the study of such host defence at the genetic level, as well as studies of maintenance of genetic variation in defences. Briefly, we found that magpies, that are the main host of the great spotted cuckoo in Europe, have alleles of one microsatellite locus (Ase64) that segregate between accepters and rejecters of experimental parasitic eggs. Furthermore, differences in ejection rate among host populations exploited by the brood parasite covaried significantly with the genetic distance for this locus.     

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.     

Hosts of avian brood parasites have evolved egg signatures with elevated information content

Hosts of brood-parasitic birds must distinguish their own eggs from parasitic mimics, or pay the cost of mistakenly raising a foreign chick. Egg discrimination is easier when different host females of the same species each lay visually distinctive eggs (egg ‘signatures’), which helps to foil mimicry by parasites. Here, we ask whether brood parasitism is associated with lower levels of correlation between different egg traits in hosts, making individual host signatures more distinctive and informative. We used entropy as an index of the potential information content encoded by nine aspects of colour, pattern and luminance of eggs of different species in two African bird families (Cisticolidae parasitized by cuckoo finches Anomalospiza imberbis, and Ploceidae by diederik cuckoos Chrysococcyx caprius). Parasitized species showed consistently higher entropy in egg traits than did related, unparasitized species. Decomposing entropy into two variation components revealed that this was mainly driven by parasitized species having lower levels of correlation between different egg traits, rather than higher overall levels of variation in each individual egg trait. This suggests that irrespective of the constraints that might operate on individual egg traits, hosts can further improve their defensive ‘signatures'' by arranging suites of egg traits into unpredictable combinations.     

Begging and cowbirds: brood parasites make hosts scream louder

Avian brood parasites have evolved striking begging abilitythat often allows them to prevail over the host progeny in competitionfor parental resources. Host young are therefore selected bybrood parasites to evolve behavioral strategies that reducethe cost of parasitism. We tested the prediction that the intensityof nestling begging displays functioning to attract parentalcare increases across species with the frequency of parasitismby the brown-headed cowbird (Molothrus ater). This was expectedbecause host young should try to prevail over highly competitiveparasitic broodmates in scramble interactions, act more selfishlywhen frequency of parasitism is high because brood parasitesoften affect more severely host condition than conspecific broodmates,and discount the kin selection costs of subtracting resourcesto unrelated parasites. Across 31 North American host species,begging loudness positively covaried with parasitism rate inPasserines, and such effect was stronger in species with smallcompared with large clutches. Begging loudness increased withbrood parasitism and nest predation among the most suitablehost species. These results held after controlling for concomitantecological factors and for common ancestry effects. Our resultssupport the hypothesis that avian brood parasitism has playeda role in the evolution of begging behavior of host young.     

How is host egg mimicry maintained in the cuckoo (Cuculus canorus)?

To investigate the evolutionary mechanism (host specificity vs. random searching) maintaining mimicry between cuckoo egg appearance and that of different European cuckoo Cuculus canorus hosts, we studied the level of mimicry between the appearance of C. canorus eggs and that of their hosts' eggs in different habitats in southern Finland by using ultraviolet-visible reflectance spectrophotometry. In the main habitat used by C. canorus for reproduction, eggs laid in nests of different host species differed in appearance. Host use by C. canorus was not related to the abundance of hosts, and the level of mimicry was not related to host abundance in the habitat. Furthermore, a close match between C. canorus egg appearance and that of host eggs within habitats was detected after removing the potentially confounding effect of host abundance. In the only two suitable host species nesting in trees (namely chaffinch Fringilla coelebs and brambling Fringilla montifringilla ) we detected changes in C. canorus egg appearance that paralleled those of the two host species. Thus our findings suggest the existence of a correlation between the appearance of C. canorus eggs and that of their hosts' eggs within different habitat types, and suggest that mimicry is maintained by strict host preferences by each C. canorus female when laying.  © 2004 The Linnean Society of London, Biological Journal of the Linnean Society , 2004, 82 , 57–68.     

Virulence and age at reproduction: new insights into host–parasite coevolution

We consider an explicit mutation–selection process to investigate the dynamics underlying the coevolution of parasite’s virulence and host’s prereproductive life span in a system with discrete generations. Conforming with earlier models, our model predicts that virulence generally increases with natural mortality of the host, and that a moderate increase in virulence selects for lower ages at reproduction. However, the epidemiological feedback in our model also gives rise to unusual and unexpected patterns. In particular, if virulence is sufficiently high the model can lead to a bifurcation pattern, where two strategies coexist in the host population. The first is to develop rapidly to reproduce before being infected. Individuals following this strategy suffer, however, from reduced fecundity. The second strategy is to develop much more slowly. Because of the high virulence, the effective period of transmission is short, so that a few slowly developing individuals escape infection. These individuals, although choosing a risky strategy, benefit from high fecundity.     

Multiple infections,kin selection and the evolutionary epidemiology of parasite traits

The coinfection of a host by several parasite strains is known to affect selective pressures on parasite strategies of host exploitation. I present a general model of coinfections that ties together kin selection models of virulence evolution and epidemiological models of multiple infections. I derive an analytical expression for the invasion fitness of a rare mutant in a population with an arbitrary distribution of the multiplicity of infection (MOI) across hosts. When a single mutation affects parasite strategies in all MOI classes, I show that the evolutionarily stable level of virulence depends on a demographic average of within‐host relatedness across all host classes. This generalization of previous kin selection results requires that within‐host parasite densities do not vary between hosts. When host exploitation strategies are allowed to vary across classes, I show that the strategy of host exploitation in a focal MOI class depends on the relative magnitudes of parasite reproductive values in the focal class and in the next. Thus, in contrast to previous findings, lower within‐host relatedness in competitive parasite interactions can potentially correspond to either higher or lower levels of virulence.     

Experimental evolution of local parasite maladaptation

Sign and magnitude of local adaptation in host–parasite systems may vary with ecological, epidemiological or genetic parameters. To investigate the role of host genetic background, we established long‐term experimental populations of different genotypes of the protozoan Paramecium caudatum, infected with the bacterial parasite Holospora undulata. We observed the evolution of an overall pattern of parasite local maladaptation for infectivity, indicating a general coevolutionary disadvantage of this parasite. Maladaptation extended to host populations with the same genetic background, similar to extending from the local to a higher regional level in natural populations. Patterns for virulence were qualitatively similar, but with less statistical support. A nonsignificant correlation with levels of (mal)adaptation for infectivity suggests independent evolution of these traits. Our results indicate similar (co)evolutionary trajectories in populations with different genetic backgrounds. Nonetheless, the correlated clines of genetic distance and parasite performance illustrate how genetic background can shape spatial gradients of local adaptation.