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.     

Phylogeny of the cuckoo genus Coccyzus (Aves: Cuculidae): A test of monophyly

Coccyzus comprises nine species of New World cuckoos (Aves: Cuculidae) that breed from southern Canada to central South America. The phylogeny of this genus was reconstructed using 2490 base pairs of the mitochondrial genes cytochrome oxidase II and III, and cytochrome b. Maximum likelihood, maximum parsimony, and Bayesian inference approaches produced similar topologies in which Coccyzus, as currently classified, is polyphyletic. Topological‐constraint analyses demonstrated that trees resulting from this study were significantly better than those derived from conventional classifications. Furthermore, results support paraphyly of Piaya, another genus of New World cuckoos. These conclusions reflect some early classifications of these genera and support the resurrection of Micrococcyx to house the ash‐coloured (Coccyzus cinereus) and dwarf (C. pumilus) cuckoos, and Coccycua for the little cuckoo (Piaya minuta).     

The evolution of egg rejection by cuckoo hosts in Australia and Europe

Exploitation of hosts by brood parasitic cuckoos is expectedto stimulate a coevolutionary arms race of adaptations and counteradaptations.However, some hosts have not evolved defenses against parasitism.One hypothesis to explain a lack of host defenses is that thelife-history strategies of some hosts reduce the cost of parasitismto the extent that accepting parasitic eggs in the nest is evolutionarilystable. Under this hypothesis, it pays hosts to accept cuckooeggs if (1) the energetic cost of raising the cuckoo is low,(2) there is time to renest, and (3) clutch size is small. Weparasitized the nests of host and nonhost species with nonmimeticmodel eggs to test whether the evolution of egg recognitionby cuckoo hosts could be explained by life-history variablesof the host. The most significant factor explaining rates ofrejection of model eggs was whether or not a species was a cuckoohost, with hosts rejecting model eggs at a higher rate thannonhosts. Egg-rejection rates were also explained by visibilitywithin the nest and by cuckoo mass. We found little supportfor the life-history model of egg rejection. Our results suggestthat parasitism is always sufficiently costly to select forhost defenses and that the evolution of defenses may be limitedby proximate constraints such as visibility within the nest.     

Phylogeny, specialization, and brood parasite--host coevolution: some possible pitfalls of parsimony

Coevolutionary hypotheses (COEV) predict that parasitic birdsbecome more specialized in host selection over time as morehost species evolve defenses. A contrasting model, PHYLO, suggeststhat brood parasites exhibit a phylogenetic trajectory towardincreasing generalization because there is a positive correlationbetween present-day numbers of host species and the branchingorder of parasitic cowbird species in a DNA-based phylogeny. However, this apparent phylogenetic pattern does not conflictwith COEV, as some have concluded. Assuming allopatric speciation,which is supported by an area cladogram, COEV predicts a correlationbetween branching order and host number because the potentialhosts of the earliest cowbirds to branch off have had the greatestamount of time to evolve defenses. Although PHYLO is more parsimoniousthan COEV, the difference is trivial, with the latter requiring only one more evolutionary change in the entire cowbird cladeto produce the pattern that exists today. Support for COEVover PHYLO comes from brood parasitic cuckoos, which are muchmore specialized than parasitic cowbirds and represent an olderclade, as shown by new DNA data. Cuckoos also have lower interspecificvariance in host numbers than do cowbirds, which conflicts with PHYLO. Unlike COEV, which assumes that the number of hosts aparasite uses is related at least as much to present ecologicalconditions as to phylogenetic history, PHYLO assumes that currenthost numbers reflect historical character states. However,host number is labile, with as much variation within as betweenspecies. Nor are published host numbers reliable measures ofparasite host selectivity, as they are due in part to researchereffort and range size. Although the comparative approach canprovide insights into evolutionary history, some coevolvedfeatures may be too dynamic to retain a phylogenetic signature,and, in the case of parasitic birds, neither PHYLO nor COEVcan be invalidated, although the latter is more consistentwith available evidence. Strict adherence to parsimony mayoften be inappropriate when assessing coevolved characters.     

Diet specialization and brood parasitism in cuckoo species

1. Brood parasitism is a breeding strategy adopted by many species of cuckoos across the world. This breeding strategy influences the evolution of life histories of brood parasite species.
2. In this study, we tested whether the degree on diet specialization is related to the breeding strategy in cuckoo species, by comparing brood parasite and nonparasite species. We measured the gradient of diet specialization of cuckoos, by calculating the Gini coefficient, an index of inequality, on the multiple traits describing the diet of species. The Gini coefficient is a measure of statistical dispersion on a scale between 0 and 1, reflecting a gradient from low to high specialization, respectively. First, we tested the strength of the phylogenetic signal of diet specialization index among cuckoo species worldwide. Then, we ran phylogenetic generalized least square (PGLS) models to compare diet specialization, distribution range, and body mass of parasitic and nonparasitic cuckoo species, considering the phylogenetic signal of data.
3. After adjusting for the phylogenetic signal of the data and considering both, species distribution range and species body mass, brood parasitic cuckoos were characterized by higher diet specialization than nonbrood parasitic species. Brood parasitic species were also characterized by a larger breeding distribution range than nonparasitic species.
4. The findings of this study provide an additional understanding of the cuckoos’ ecology, relating diet and breeding strategies, information that could be important in conservation ecology.

     

Change in host rejection behavior mediated by the predatory behavior of its brood parasite

Passerine hosts of parasitic cuckoos usually vary in their abilityto discriminate and reject cuckoo eggs. Costs of discriminationand rejection errors have been invoked to explain the maintenanceof this within-population variability. Recently, enforcementof acceptance by parasites has been identified as a rejectioncost in the magpie (Pica pica) and its brood parasite, the greatspotted cuckoo (Clamator glandarius). Previous experimentalwork has shown that rejecter magpies suffer from increased nestpredation by the great spotted cuckoo. Cuckoo predatory behavioris supposed to confer a selective advantage to the parasitebecause magpies experiencing a reproductive failure may providea second opportunity for the cuckoo to parasitize a replacementclutch. This hypothesis implicitly assumes that magpies modulatetheir propensity to reject parasite eggs as a function of previousexperience. We tested this hypothesis in a magpie populationbreeding in study plots varying in parasitism rate. Magpie pairs thatwere experimentally parasitized and had their nests depredated,after their rejection behavior had been assessed, changed theirbehavior from rejection to acceptance. The change in host behaviorwas prominent in study plots with high levels of parasitism,but not in plots with rare or no cuckoo parasitism. We discussthree possible explanations for these differences, concludingthat in study plots with a high density of cuckoos, the probability fora rejecter magpie nest of being revisited and depredated bya cuckoo is high, particularly for replacement clutches, and,therefore, the cost for magpies of rejecting a cuckoo egg ina replacement clutch is increased. Moreover, in areas with highlevels of host defense (low parasitism rate), the probabilityof parasitism and predation of rejecter-magpie nests by thecuckoo is reduced in both first and replacement clutches. Therefore,rejecter magpies in such areas should not change their rejectionbehavior in replacement clutches.     

The spatial habitat structure of host populations explains the pattern of rejection behavior in hosts and parasitic adaptations in cuckoos

In this article we present tentative support for predictionsderived from a spatial habitat structure hypothesis arguingthat common cuckoos Cuculus canorus, the most common obligatebrood parasite in Europe, only breed in areas where they haveaccess to vantage points in trees. Thus, species in which somepopulations breed near trees while other populations breed farther from trees have a different cuckoo—host population dynamicthan species in which all populations always breed in the vicinityof trees. Parasitism rate, mimicry of brood parasite eggs withthose of the hosts, and rejection behavior of hosts varieswith the host breeding habitat. Cuckoos are best adapted toexploit species in which some populations breed near trees while other populations breed in open areas because such hosts arenot always accessible to cuckoos, and thus gene flow amongunparasitized and parasitized populations delays the evolutionof host adaptations. Adaptive behavior in cuckoos as well asin their hosts can be predicted from the spatial habitat structurehypothesis.     

Reduced parasitism by retaliatory cuckoos selects for hosts that rear cuckoo nestlings

We present a model to investigate why some bird species rearthe nestlings of brood parasites in spite of suffering largereductions in their own immediate fitness. Of particular interestis the case in which hosts rear only the parasite's young, allof their own offspring having been ejected or destroyed by theparasite. We investigate the conditions for the evolution ofretaliation by brood parasites against hosts that eject theiryoung, as well as the evolution of nonejection by hosts. Retaliationby cuckoos can evolve, despite potentially benefiting otherbrood parasites, if rates of ejection by hosts are neither toohigh nor too low, and if depredated nests are reparasitizedat a high rate by the depredating cuckoo. The presence of aretaliatory cuckoo then eases the conditions for the evolutionof hosts to accept and rear cuckoo offspring. A key conditionfavoring the evolution of non-ejection is that nonejectors enjoylower rates of parasitism in later clutches compared to ejectors.This requires that cuckoos reparasitize the clutches of ejectorsat relatively high rates and that nonejectors can rear a clutchof their own following the rearing of a cuckoo nestling. Ifthese conditions are not met, it pays hosts to eject cuckoonestlings even if the cuckoo retaliates. The model can explainwhy nonejection is relatively easy to evolve in cases in whichthe host young are reared alongside those of the cuckoo, suchas in cowbirds, and shows how hosts can resist invasion by parasiticcuckoos. The model predicts that retaliatory brood parasitessuch as the cuckoo have good memory for the location and statusof nests in their territory. Hosts of retaliatory cuckoos whosenestlings destroy the host clutch are predicted to have longbreeding seasons or the ability to attempt more than one clutchper season. Our model of retaliation may have wider applicationsto host-parasite relationships, virulence, and immunity.     

Antagonistic antiparasite defenses: nest defense and egg rejection in the magpie host of the great spotted cuckoo

Brood parasites dramatically reduce the reproductive successof their hosts, which therefore have developed defenses againstbrood parasites. The first line of defense is protecting thenest against adult parasites. When the parasite has successfullyparasitized a host nest, some hosts are able to recognize andreject the eggs of the brood parasite, which constitutes the secondline of defense. Both defense tactics are costly and would be counteractedby brood parasites. While a failure in nest defense implies successfulparasitism and therefore great reduction of reproductive successof hosts, a host that recognizes parasitic eggs has the opportunityto reduce the effect of parasitism by removing the parasiticegg. We hypothesized that, when nest defense is counteractedby the brood parasite, hosts that recognize cuckoo eggs shoulddefend their nests at a lower level than nonrecognizers becausethe former also recognize adult cuckoos. Magpie (Pica pica) hoststhat rejected model eggs of the brood parasitic great spottedcuckoo (Clamator glandarius) showed lower levels of nest defensewhen exposed to a great spotted cuckoo than when exposed toa nest predator (a carrion crow Corvus corone). Moreover, magpiesrejecting cuckoo eggs showed lower levels of nest defense againstgreat spotted cuckoos than nonrecognizer magpies, whereas differencesin levels of defense disappeared when exposed to a carrion crow.These results suggest that hosts specialize in antiparasitedefense and that different kinds of defense are antagonistically expressed.We suggest that nest-defense mechanisms are ancestral, whereasegg recognition and rejection is a subsequent stage in the coevolutionaryprocess. However, host recognition ability will not be expressedwhen brood parasites break this second line of defense.