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Cuckoos, cowbirds and the persistence of brood parasitism.

Brood parasites provide a particularly good opportunity for the study of host-parasite evolution because they directly affect the reproductive success of their hosts. Two parasitic species, the common cuckoo (Cuculus canorus) and the brown-headed cowbird (Molothrus ater), differ widely in their relationships with their hosts, yet share the attribute of having been particularly well studied by biologists. Recent work on the cuckoo and the cowbird has resulted in new answers to the question begged by all brood parasites: why do host species raise parasitic young?

Journal Article↗

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.

Animals↗

Paternity-parasitism trade-offs: a model and test of host-parasite cooperation in an avian conspecific brood parasite.

Efforts to evaluate the evolutionary and ecological dynamics of conspecific brood parasitism in birds and other animals have focused on the fitness costs of parasitism to hosts and fitness benefits to parasites. However, it has been speculated recently that, in species with biparental care, host males might cooperate with parasitic females by allowing access to the host nest in exchange for copulations. We develop a cost-benefit model to explore the conditions under which such host-parasite cooperation might occur. When the brood parasite does not have a nest of her own, the only benefit to the host male is siring some of the parasitic eggs (quasi-parasitism). Cooperation with the parasite is favored when the ratio of host male paternity of his own eggs relative to his paternity of parasitic eggs exceeds the cost of parasitism. When the brood parasite has a nest of her own, a host male can gain additional, potentially more important benefits by siring the high-value, low-cost eggs laid by the parasite in her own nest. Under these conditions, host males should be even more likely to accept parasitic eggs in return for copulations with the parasitic female. We tested these predictions for American coots (Fulica americana), a species with a high frequency of conspecific brood parasitism. Multilocus DNA profiling indicated that host males did not sire any of the parasitic eggs laid in host nests, nor did they sire eggs laid by the parasite in her own nest. We used field estimates of the model parameters from a four-year study of coots to predict the minimum levels of paternity required for the costs of parasitism to be offset by the benefits of mating with brood parasites. Observed levels of paternity were significantly lower than those predicted under a variety of assumptions, and we reject the hypothesis that host males cooperated with parasitic females. Our model clarifies the specific costs and benefits that influence host-parasite cooperation and, more generally, yields precise predictions about expected levels of host male paternity. These predictions will enable a more rigorous assessment of field studies designed to test adaptive hypotheses of host-parasite cooperation.

Animals↗

Imprinting and the origin of parasite-host species associations in brood-parasitic indigobirds, Vidua chalybeata.

Brood-parasitic village indigobirds, Vidua chalybeata, were bred in captivity and foster-reared by their normal host species, the red-billed firefinch, Lagonosticta senegala, or by an experimental foster species, the Bengalese finch, Lonchura striata. Captive-reared female indigobirds were tested as adults for mate choice and for host choice. In tests of mate choice, female indigobirds responded preferentially towards mimicry songs of male indigobirds that were similar to those of the females' own foster parents. Females reared by Bengalese finches responded to male songs that mimicked Bengalese finch song rather than to male songs that mimicked their normal host species, the firefinch. In tests of host choice, females reared by Bengalese finches laid in the nests of Bengalese finches, and females reared by firefinches laid in the nests of firefinches. Wild-caught females showed the same behaviours as captive-bred females reared by firefinches. A female indigobird's social companions (firefinch or Bengalese) following her independence of her foster parents had no effect on her sexual response to male mimicry song or her choice of a host species in brood parasitism. The results support the predictions of a model of imprinting-like behaviour development in which young indigobirds focus their attention on their foster parents, rather than a model of innate bias for songs and nests of their normal host species, or a null model of nonspecific brood parasitism and differential survival. The results provide experimental support for the recent origin of brood parasite-host associations and the significance of imprinting in speciation in these brood parasites. Copyright 2000 The Association for the Study of Animal Behaviour.

Journal Article↗

Dispersal ecology versus host specialization as determinants of ectoparasite distribution in brood parasitic indigobirds and their estrildid finch hosts.

Brood parasitic birds offer a unique opportunity to examine the ecological and evolutionary determinants of host associations in avian feather lice (Phthiraptera). Brood parasitic behaviour effectively eliminates vertical transfer of lice between parasitic parents and offspring at the nest, while at the same time providing an opportunity for lice associated with the hosts of brood parasites to colonize the brood parasites as well. Thus, the biology of brood parasitism allows a test of the relative roles of host specialization and dispersal ecology in determining the host-parasite associations of birds and lice. If the opportunity for dispersal is the primary determinant of louse distributions, then brood parasites and their hosts should have similar louse faunas. In contrast, if host-specific adaptations limit colonization ability, lice associated with the hosts of brood parasites may be unable to persist on the brood parasites despite having an opportunity for colonization. We surveyed lice on four brood parasitic finch species (genus Vidua), their estrildid finch host species, and a few ploceid finches. While Brueelia lice were found on both parasitic and estrildid finches, a molecular phylogeny showed that lice infesting the two avian groups belong to two distinct clades within Brueelia. Likewise, distinct louse lineages within the amblyceran genus Myrsidea were found on estrildid finches and the parasitic pin-tailed whydah (Vidua macroura), respectively. Although common on estrildid finches, Myrsidea lice were entirely absent from the brood parasitic indigobirds. The distribution and relationships of louse species on brood parasitic finches and their hosts suggest that host-specific adaptations constrain the ability of lice to colonize new hosts, at least those that are distantly related.

Adaptation, Physiological↗

A single ancient origin of brood parasitism in African finches: implications for host-parasite coevolution.

Robust phylogenies for brood-parasitic birds, their hosts, and nearest nesting relatives provide the framework to address historical questions about host-parasite coevolution and the origins of parasitic behavior. We tested phylogenetic hypotheses for the two genera of African brood-parasitic finches, Anomalospiza and Vidua, using mitochondrial DNA sequence data from 43 passeriform species. Our analyses strongly support a sister relationship between Vidua and Anomalospiza, leading to the conclusion that obligate brood parasitism evolved only once in African finches rather than twice, as has been the conventional view. In addition, the parasitic finches (Viduidae) are not recently derived from either weavers (Ploceidae) or grassfinches (Estrildidae), but represent a third distinct lineage. Among these three groups, the parasitic finches and estrildids, which includes the hosts of all 19 Vidua species, are sister taxa in all analyses of our full dataset. Many characters shared by Vidua and estrildids, including elaborate mouth markings in nestlings, unusual begging behavior, and immaculate white eggs, can therefore be attributed to common ancestry rather than convergent evolution. The host-specificity of mouth mimicry in Vidua species, however, is clearly the product of subsequent host-parasite coevolution. The lineage leading to Anomalospiza switched to parasitizing more distantly related Old World warblers (Sylviidae) and subsequently lost these characteristics. Substantial sequence divergence between Vidua and Anomalospiza indicates that the origin of parasitic behavior in this clade is ancient (approximately 20 million years ago), a striking contrast to the recent radiation of extant Vidua. We suggest that the parasitic finch lineage has experienced repeated cycles of host colonization, speciation, and extinction through their long history as brood parasites and that extant Vidua species represent only the latest iterations of this process. This dynamic process may account for a significantly faster rate of DNA sequence evolution in parasitic finches as compared to estrildids and other passerines. Our study reduces by one the tally of avian lineages in which obligate brood parasitism has evolved and suggests an origin of parasitism that involved relatively closely related species likely to accept and provide appropriate care to parasitic young. Given the ancient origin of parasitism in African finches, ancestral estrildids must have been parasitized well before the diversification of extant Vidua, suggesting a long history of coevolution between these lineages preceding more recent interactions between specific hosts and parasites.

Animals↗

Host-parasite relatedness shown by protein fingerprinting in a brood parasitic bird.

Brood parasitism as an alternative female breeding tactic is particularly common in ducks, where hosts often receive eggs laid by parasitic females of the same species and raise their offspring. Herein, we test several aspects of a kin selection explanation for this phenomenon in goldeneye ducks (Bucephala clangula) by using techniques of egg albumen sampling and statistical bandsharing analysis based on resampling. We find that host and primary parasite are indeed often related, with mean r = 0.13, about as high as between first cousins. Relatedness to the host is higher in nests where a parasite lays several eggs than in those where she lays only one. Returning young females parasitize their birth nestmates (social mothers or sisters, which are usually also their genetic mothers and sisters) more often than expected by chance. Such adult relatives are also observed together in the field more often than expected and for longer periods than other females. Relatedness and kin discrimination, which can be achieved by recognition of birth nestmates, therefore play a role in these tactics and probably influence their success.

Animals↗

Egg recognition and counting reduce costs of avian conspecific brood parasitism.

Birds parasitized by interspecific brood parasites often adopt defences based on egg recognition but such behaviours are puzzlingly rare in species parasitized by members of the same species. Here I show that conspecific egg recognition is frequent, accurate and used in three defences that reduce the high costs of conspecific brood parasitism in American coots. Hosts recognized and rejected many parasitic eggs, reducing the fitness costs of parasitism by half. Recognition without rejection also occurred and some hosts banished parasitic eggs to inferior outer incubation positions. Clutch size comparisons revealed that females combine egg recognition and counting to make clutch size decisions--by counting their own eggs, while ignoring distinctive parasitic eggs, females avoid a maladaptive clutch size reduction. This is clear evidence that female birds use visual rather than tactile cues to regulate their clutch sizes, and provides a rare example of the ecological and evolutionary context of counting in animals.

Adaptation, Physiological↗

Effects of brood parasitism on host reproductive success: evidence from larval interactions among dung beetles.

This paper investigates the effect of brood parasitism in a dung beetle assemblage in an arid region of Spain. The study was conducted during the spring season (March-May 1994-1998) using mesh cylinders buried into the ground, filled with sand and with sheep dung on top. We quantified the proportion of nests containing larvae of parasitic beetles and their effect on host larvae survival. Experiments on the effect of parasitic larvae on host-larvae survival were conducted by placing scarab brood masses (raised from captive scarabs in the laboratory) in containers with and without aphodiid larvae. During the spring, dung desiccation is rapid, preventing aphodiids nesting in the dung, and forcing these species to adopt brood parasitism as a nesting strategy. Parasitic aphodiids were found in 12-47% of scarab nests of three species. The incidence of brood parasitization was positively related with the number of brood masses contained in the nests, being also higher in the most abundant species. Field data and experiments showed that brood parasites significantly reduced host larvae survival from 74.8% in non-parasitized nests to 8.8% in parasitized nests. Because different rates of nest parasitization and mortality were caused by parasites, brood parasitism had a differential effect on different host species. Thus, brood parasitism constitutes an important mortality factor reducing the reproductive success of the host species and potentially affecting the beetle abundance in the area.

Animals↗

Brood parasitism by brown-headed cowbirds and the expression of sexual characters in their hosts.

Interspecific brood parasites may use the secondary sexual characters of the hosts to decide which species to parasitize. Hence, species with conspicuous and well-recognisable traits may have higher chances of becoming parasitised. Using North American birds and their frequent brood parasite, the brown-headed cowbird Molothrus ater, we tested the relationship between features of song and plumage coloration of hosts and the frequency of brood parasitism while controlling for several potentially confounding factors. Relying on two sets of analysis, we focused separately on the evolutionary view of the parasite and the host. From the cowbird's perspective, we found that males of heavily parasitized species posit songs with low syllable repertoire size, shorter inter-song interval and have brighter plumage. From the host's perspective, a phylogenetic analysis revealed similar associations for features of song, but not for plumage characteristics that were unrelated to brood parasitism. These comparative findings may imply that brood parasites choose novel hosts based on heterospecific signals; and/or host species working against sexual selection escape from brood parasitism by evolving inconspicuous sexual signals. Although our data do not allow us to distinguish between these two evolutionary scenarios, our results suggest that selection factors mediating cowbird parasitism via host recognition by heterospecific signals may have an important role in the evolutionary relationship between brood parasites and their hosts.

Animals↗

A brood parasitic catfish of mouthbrooding cichlid fishes in Lake Tanganyika.

Brood parasitism, where a brood of the parasitic species is fostered by the parents of another species, is well known among birds. In most cases, such offspring show a complete reliance upon their host parents for food, protection and warmth until their independence. In other vertebrate groups, however, such total dependence upon a host species is unknown. I report here the first example of true brood parasitic behaviour discovered among fishes. In Lake Tanganyika, an endemic mochokid catfish, Synodontis multipunctatus Boulenger, is a brood parasite of mouthbrooding fishes of the family Cichlidae. The eggs of the catfish are incubated in the mouths of any of several host species together with the host's eggs, but hatch earlier. Following absorption of their yolk sacs, the catfish fry feed upon the fry of the host while still in its mouth. Thus the early stages of development of this catfish not only depend upon their hosts for food and protection, but exploit almost their entire parental investment.

Animals↗

Tests of landscape influence: nest predation and brood parasitism in fragmented ecosystems.

The effects of landscape fragmentation on nest predation and brood parasitism, the two primary causes of avian reproductive failure, have been difficult to generalize across landscapes, yet few studies have clearly considered the context and spatial scale of fragmentation. Working in two river systems fragmented by agricultural and rural-housing development, we tracked nesting success and brood parasitism in > 2500 bird nests in 38 patches of deciduous riparian woodland. Patches on both river systems were embedded in one of two local contexts (buffered from agriculture by coniferous forest, or adjacent to agriculture), but the abundance of agriculture and human habitation within 1 km of each patch was highly variable. We examined evidence for three models of landscape effects on nest predation based on (1) the relative importance of generalist agricultural nest predators, (2) predators associated with the natural habitats typically removed by agricultural development, or (3) an additive combination of these two predator communities. We found strong support for an additive predation model in which landscape features affect nest predation differently at different spatial scales. Riparian habitat with forest buffers had higher nest predation rates than sites adjacent to agriculture, but nest predation also increased with increasing agriculture in the larger landscape surrounding each site. These results suggest that predators living in remnant woodland buffers, as well as generalist nest predators associated with agriculture, affect nest predation rates, but they appear to respond at different spatial scales. Brood parasitism, in contrast, was unrelated to agricultural abundance on the landscape, but showed a strong nonlinear relationship with farm and house density, indicating a critical point at which increased human habitat causes increased brood parasitism. Accurate predictions regarding landscape effects on nest predation and brood parasitism will require an increased appreciation of the multiple scales at which landscape components influence predator and parasite behavior.

Agriculture↗

Do avian brood parasites eavesdrop on heterospecific sexual signals revealing host quality? A review of the evidence.

Eavesdropping can be defined as the extraction of information from the interactions between other individuals. It provides a relatively cheap way of gathering relevant information for fitness enhancement. Here, we propose that obligate avian brood parasites, which always lay their eggs in foreign nests of individuals of other species, may eavesdrop on their host sexual signals to locate nests of high quality individuals in which to lay their parasitic eggs. Sexual signal variation can honestly signal parental quality. Thus, by eavesdropping on sexual signals, parasites may select high quality foster parents for their own offspring. Such a use of sexual signals within host populations by brood parasites differs from signal exploitation theory that proposes that parasite only use signals to locate potential host independently from signaller quality. Here, we review the avian literature concerning host choice within a host species by obligate avian brood parasites and find evidence for host selection within individuals of a host species on the basis of cues potentially functioning as sexually selected traits, or at least revealing parental abilities. We have also found support for the existence of benefits linked to host selection by avian brood parasites. Finally, one study reported on the attenuation of a sexual ornament in host populations under strong pressure by brood parasites. Most of these findings have been interpreted as evidence for host selection by avian brood parasites based on the conspicuousness of sexual signals. We suggest, however, that these findings may in fact reveal eavesdropping on host signalling performance by brood parasites which would use the information extracted to choose the better individuals among conspecifics of a given host. This provides a new perspective for the study of host selection in obligate brood parasites, and raises interesting questions for the study of animal cognition that would deserve experimental studies.

Animals↗

Interspecific brood parasitism in blackbirds (Icterinae): a phylogenetic perspective.

An 852-base pair region of the cytochrome-b gene was sequenced for the brood parasitic cowbirds and 20 additional taxa of the New World blackbirds (Icterinae). The goal of the study was to determine (i) whether interspecific brood parasitism is multiply derived within the assemblage and (ii) the nature of the evolutionary transformation between various forms of interspecific brood parasitism. Cladistic analysis of the sequence data indicates that brood parasitism evolved a single time within the Icterinae. The primitive form of interspecific brood parasitism in this assemblage is host-specificity, with host-generality representing the derived condition.

Animals↗

Reconciling genetic expectations from host specificity with historical population dynamics in an avian brood parasite, Horsfield's Bronze-Cuckoo Chalcites basalis of Australia.

Mitochondrial DNA (mtDNA) is being used increasingly to explore the evolution of host specificity in avian brood parasites. A stable coevolutionary equilibrium between multiple phylogenetically unrelated hosts and a brood parasitic species predicts that mtDNA diversity in the parasite should be relatively deep and phylogenetically structured. Also, the different intraspecific clades resulting from parasitism to multiple sympatric hosts should themselves occur sympatrically. However, mtDNA diversity in brood parasites is as susceptible to effects of historical population dynamics as in any species. We demonstrate the relevance of these dynamics to the use of mtDNA in understanding coevolution between an Australian brood-parasite, Horsfield's Bronze-Cuckoo Chalcites basalis and its hosts, Malurus fairy-wrens and Acanthiza thornbills. Previous ecological and behavioural analyses argue that Malurus- and Acanthiza-specific host races exist in C. basalis. Yet mtDNA diversity in C. basalis is low and phylogenetically unstructured (mean sequence divergence 0.15 +/- 0.07%, range 0.00%-0.31%) and tests of mtDNA neutrality and range expansion vs. population stability (Tajima's D, Fu & Li's F* and D*, Fu's F(S), mismatch analyses) all indicate that C. basalis has expanded its range very recently, probably within the last few tens of thousands of years following climatic amelioration after a peak of aridity in the late Pleistocene. The low mtDNA diversity and its lack of phylogenetic structure in C. basalis deny the existence of evolutionarily long-term stable host races in C. basalis but not the possibility of recently evolved ones. They highlight the need for renewed behavioural and ecological study of the relationship between C. basalis and its hosts. Our findings illustrate the need to understand the evolutionary context in which a brood parasite and its hosts have evolved if mtDNA data are to be used in testing hypotheses concerning the origin and maintenance of host specificity. They also add to the growing body of work illustrating the use of mismatch analyses and Fu's F(S) in detecting range expansions.

Animals↗

Genomic resources for comparative analyses of obligate avian brood parasitism.

Examples of convergent evolution, wherein distantly related organisms evolve similar traits, including behaviors, underscore the adaptive power of natural selection. In birds, obligate brood parasitism, and the associated loss of parental care behaviors, has evolved independently in seven different lineages, though little is known about the genetic basis of the complex suite of traits associated with this rare life history strategy. We generated genome assemblies for ten brood parasitic species plus eight species representatives of their parental/nesting outgroups. This includes nine long-read chromosome-level assemblies, with scaffold N50 sizes ranging from 38.1 to 72.6 MB, and gene representation completeness measures >97%. Leveraging this new catalog of avian genomes, we constructed clade-level alignments that reveal variation in chromosomal synteny, provide first-time or improved annotations of protein-coding and non-coding genes, and define cross-species ortholog reference sets. We also refine estimates for the timing of the seven independent origins of brood parasitism, ranging from recent events such as 1.6 to 4.5 million years ago in Molothrus cowbirds to much earlier origins over 30 million years ago in two of the three cuckoo lineages. These genomic resources lay the foundation for investigating the genetic and genomic underpinnings of brood parasitism, including the loss of parental care, shifts in mating systems, perhaps resulting in heightened sperm competition, elevated annual fecundity, improved spatial cognition related to nest-finding, and the diverse adaptations shaped by intense coevolution with host species.

assemblies↗

Relic behaviours, coevolution and the retention versus loss of host defences after episodes of avian brood parasitism.

Most previous studies of brood parasitism have stressed that host defences, such as egg recognition, are lost in the absence of parasitism. Such losses could result in coevolutionary cycles in which parasites shift away from well-defended hosts only to switch back to them later at a time when these hosts have lost much or all of their defences and the parasite's current hosts have built up effective defences. However, the alternative 'single trajectory' model predicts that parasites rarely switch back to old hosts because ex-hosts retain egg recognition for long periods in the absence of parasitism. If true, egg recognition by the host may be a 'relic behaviour', because in the absence of parasitism its adaptive value is close to neutral. Using artificial nonmimetic eggs, I tested for egg recognition in two populations that are currently unparasitized but that are descended from lineages likely to have been parasitized in the past: the grey catbird, Dumetella carolinensis, on Bermuda and the loggerhead shrike, Lanius ludovicianus, in California. Both of these populations showed long-term retention, ejecting nonmimetic eggs at rates of nearly 100%. Because potential present-day selection pressures, such as conspecific parasitism, do not explain this egg recognition, Bermuda catbirds apparently retain recognition from North American conspecifics that were cowbird hosts before colonizing Bermuda and shrikes retain recognition from Old World congeners that were hosts of cuckoos. Retention is also indicated by passerines in California and the Caribbean that had high rejection rates of nonmimetic eggs before coming into contact with cowbirds. These new data suggest that both the coevolutionary cycles and single trajectory models have importance and that rejection behaviour can have insignificant costs, which is consistent with evolutionary lag explanations for the acceptance of parasitic eggs shown by some cuckoo and many cowbird hosts. Copyright 2001 The Association for the Study of Animal Behaviour.

Journal Article↗

Food availability affects Osmia pumila (Hymenoptera: Megachilidae) foraging, reproduction, and brood parasitism.

Food limitation can reduce reproductive success directly, as well as indirectly, if foraging imposes a risk of predation or parasitism. The solitary bee Osmia pumila suffers brood parasitism by the cleptoparasitic wasp Sapyga centrata, which enters the host nest to oviposit while the female bee is away. I studied foraging and reproduction of O. pumila nesting within cages stocked with rich or sparse floral resources, and the presence or absence of S. centrata to test (1) the response of nesting female O. pumila to food shortages, (2) the response of nesting female O. pumila to the presence of parasites, and (3) whether brood produced under scarce resources are more likely to be parasitized by S. centrata. The rate of brood cell production was significantly lower in cages with sparse floral resources, although females in sparse cages did not produce significantly fewer brood cells overall. Sapyga centrata did not influence the rate of brood cell production, but females exposed to the cleptoparasites had marginally significantly lower reproductive output. Nests in parasite cages had significantly fewer brood cells than those in parasite free cages. The mean duration of foraging bouts made by female O. pumila in sparse cages was not significantly longer than that in rich cages. O. pumila spent less time in the nest between pollen and nectar foraging bouts in sparse cages with S. centrata than those in other cages suggesting that these individuals made more frequent food foraging trips. Despite the weak effects of parasites and bloom density on foraging behavior, O. pumila brood cells experienced a 5-fold higher probability of parasitism by S. centrata in cages with sparse bloom than in those with rich bloom [corrected]. These results support the hypothesis that indirect effects of food scarcity increase O. pumila susceptibility to brood parasitism, although the exact mechanism is not entirely clear yet.

Adaptation, Physiological↗