Repeatability of Host Female and Male Aggression Towards a Brood Parasite

Current research on behavioural consistency showed that various types of animal behaviour are highly repeatable in the context of mate choice, exploration and parental care, including nest protection. However, the repeatability of aggressive nest defence has not yet been studied in hosts of brood parasites, although host aggression against adult parasites represents a crucial line of antiparasitic defences. Here, we investigated the between‐season repeatability of the great reed warbler (Acrocephalus arundinaceus) aggression towards a stuffed dummy of the brood parasitic common cuckoo (Cuculus canorus). We found that under the relatively stable risk of brood parasitism across breeding seasons, female responses to the cuckoo were highly repeatable, whereas male responses were variable. We suggest that the potential explanation for the observed patterns of female and male behaviours may lie in female's prominent roles in offspring care and nest protection, and in her lower renesting potential in comparison with that of males. However, further studies on the relationship between host aggression and other types of behaviours (host personality) and their fitness consequences under the fluctuating parasitism pressures are required to clarify the adaptive significance of aggressive behaviour observed in hosts of brood parasites.     

Egg Eviction Imposes a Recoverable Cost of Virulence in Chicks of a Brood Parasite

Background

Chicks of virulent brood parasitic birds eliminate their nestmates and avoid costly competition for foster parental care. Yet, efforts to evict nest contents by the blind and naked common cuckoo Cuculus canorus hatchling are counterintuitive as both adult parasites and large older cuckoo chicks appear to be better suited to tossing the eggs and young of the foster parents.

Methodology/Principal Findings

Here we show experimentally that egg tossing imposed a recoverable growth cost of mass gain in common cuckoo chicks during the nestling period in nests of great reed warbler Acrocephalus arundinaceus hosts. Growth rates of skeletal traits and morphological variables involved in the solicitation of foster parental care remained similar between evictor and non-evictor chicks throughout development. We also detected no increase in predation rates for evicting nests, suggesting that egg tossing behavior by common cuckoo hatchlings does not increase the conspicuousness of nests.

Conclusion

The temporary growth cost of egg eviction by common cuckoo hatchlings is the result of constraints imposed by rejecter host adults and competitive nestmates on the timing and mechanism of parasite virulence.     

The Value of Artificial Stimuli in Behavioral Research: Making the Case for Egg Rejection Studies in Avian Brood Parasitism

Experimentation is at the heart of classical and modern behavioral ecology research. The manipulation of natural cues allows us to establish causation between aspects of the environment, both internal and external to organisms, and their effects on animals' behaviors. In recognition systems research, including the quest to understand the coevolution of sensory cues and decision rules underlying the rejection of foreign eggs by hosts of avian brood parasites, artificial stimuli have been used extensively, but not without controversy. In response to repeated criticism about the value of artificial stimuli, we describe four potential benefits of using them in egg recognition research, two each at the proximate and ultimate levels of analysis: (1) the standardization of stimuli for developmental studies and (2) the disassociation of correlated traits of egg phenotypes used for sensory discrimination, as well as (3) the estimation of the strength of selection on parasitic egg mimicry and (4) the establishment of the evolved limits of sensory and cognitive plasticity. We also highlight constraints of the artificial stimulus approach and provide a specific test of whether responses to artificial cues can accurately predict responses to natural cues. Artificial stimuli have a general value in ethological research beyond research in brood parasitism and may be especially critical in field studies involving the manipulation of a single parameter, where other, confounding variables are difficult or impossible to control experimentally or statistically.     

Experimental Manipulation of Intraclutch Variation in the Great Reed Warbler Shows No Effect on Rejection of Parasitic Eggs

In the continuing arms race between hosts and brood parasites, hosts are expected to reduce variation in the appearance of their own eggs within clutches, as it facilitates recognition of parasitic eggs. At the same time, by increasing interclutch variation, hosts should make it more difficult for parasites to evolve perfectly mimetic eggs. In this study, we experimentally manipulated intraclutch variation in the great reed warbler, Acrocephalus arundinaceus, in Hungary, where this species is heavily (c. 64%) parasitized by the common cuckoo, Cuculus canorus. We placed artificial cuckoo eggs, which appeared moderately mimetic to humans, in two groups of nests; in one group we increased variability of egg appearance within clutches by exchanging host eggs among nests. These clutches showed a significantly higher intraclutch variability than natural clutches, which we used as a control group. Our results indicate that it has no effect on rejection behaviour in this species, neither when variation was increased experimentally, nor within the natural range of variation displayed by our population. We suggest that when parasitism is high, selection for reduced intraclutch variation may be less important than frequency‐dependent selection for increased variation between individuals within a host population.     

Do Egg Carrying and Protracted Copulation Affect Mobility in the Golden Egg Bug?

Golden egg bug Phyllomorpha laciniata (Heteroptera, Coreidae) females oviposit on male and female conspecifics that carry ova until they hatch. Embryos benefit from being carried because of diminished risks of predation. Female carriers are never the parents of carried eggs, and males are only rarely the fathers of any carried eggs. Eggs develop and hatch without being carried in the laboratory. Egg carriers may be viewed as victims, exploited by females that encumber them with eggs. The intensity of selection favouring resistance to egg carrying should be proportional to the costs of this behaviour. One possible cost could be a reduction in mobility caused by carried eggs. We compare movement rates among encumbered and unencumbered golden egg bugs of both sexes. Protracted copulations (often exceeding 20 h) typical of this species and mating may also cause reduction in bugs mobility. Therefore, we also evaluate rates of movement of coupled pairs of bugs. Our results indicate that egg loads do not affect the mobility and speed of either males or females. However, copulating pairs are significantly slowed as compared to single bugs. Thus protracted copulations have a clear cost in rates of movement and possibly risks of predation, but there are no apparent mobility costs for egg carrying.     

MHC-I Affects Infection Intensity but Not Infection Status with a Frequent Avian Malaria Parasite in Blue Tits

Host resistance against parasites depends on three aspects: the ability to prevent, control and clear infections. In vertebrates the immune system consists of innate and adaptive immunity. Innate immunity is particularly important for preventing infection and eradicating established infections at an early stage while adaptive immunity is slow, but powerful, and essential for controlling infection intensities and eventually clearing infections. Major Histocompatibility Complex (MHC) molecules are central in adaptive immunity, and studies on parasite resistance and MHC in wild animals have found effects on both infection intensity (parasite load) and infection status (infected or not). It seems MHC can affect both the ability to control infection intensities and the ability to clear infections. However, these two aspects have rarely been considered simultaneously, and their relative importance in natural populations is therefore unclear. Here we investigate if MHC class I genotype affects infection intensity and infection status with a frequent avian malaria infection Haemoproteus majoris in a natural population of blue tits Cyanistes caeruleus. We found a significant negative association between a single MHC allele and infection intensity but no association with infection status. Blue tits that carry a specific MHC allele seem able to suppress H. majoris infection intensity, while we have no evidence that this allele also has an effect on clearance of the H. majoris infection, a result that is in contrast with some previous studies of MHC and avian malaria. A likely explanation could be that the clearance rate of avian malaria parasites differs between avian malaria lineages and/or between avian hosts.     

Changes in Nest Defense against a Brood Parasite over the Breeding Cycle

We measured the responses of nesting least flycatchers (Empidonax minimus) to a model of the brood-parasitic brown-headed cowbird (Molothrus ater). A greater number of vocalizations, approaches and threat displays were directed toward the cowbird model than toward a control model of a fox sparrow (Passerella iliaca), suggesting that the cowbird was recognized as a threat. Flycatchers were more likely to give threat displays during laying when the consequences of brood parasitism were greatest; however, the intensity of all other defensive behavior did not change over the nesting cycle. We suggest that least flycatchers remained aggressive throughout nesting because cowbirds were also predators on eggs and nestlings.     

Spatial Variation in an Avian Host Community: Implications for Disease Dynamics

Because many pathogens can infect multiple host species within a community, disease dynamics in a focal host species can be affected by the composition of the host community. We examine the extent to which spatial variation in species’ abundances in an avian host community may contribute to geographically varying prevalence of a recently emerged wildlife pathogen. Mycoplasma gallisepticum is a pathogen novel to songbirds that has caused substantial mortality in house finches (Carpodacus mexicanus) in eastern North America. Though the house finch is the primary host species for M. gallisepticum, the American goldfinch (Spinus tristis) and northern cardinal (Cardinalis cardinalis) are alternate hosts, and laboratory experiments have demonstrated M. gallisepticum transmission between house finches and goldfinches. Still unknown is the real world impact on disease dynamics of variation in abundances of the three hosts. We analyzed data from winter-long bird and disease surveys in the northeastern United States. We found that higher disease prevalence in house finches was associated with higher numbers of northern cardinals and American goldfinches, although only the effect of cardinal abundance was statistically significant. Nevertheless, our results indicate that spatial variation in bird communities has the potential to cause geographic variation in disease prevalence in house finches.     

X Chromosome Duplications Affect a Region of the Chromosome They Do Not Duplicate in Caenorhabditis Elegans

X chromosome duplications have been used previously to vary the dose of specific regions of the X chromosome to study dosage compensation and sex determination in Caenorhabditis elegans. We show here that duplications suppress and X-linked hypomorphic mutation and elevate the level of activity of an X-linked enzyme, although these two genes are located in a region of the X chromosome that is not duplicated. The effects do not depend on the region of the X chromosome duplicated and is stronger in strains with two doses of a duplication than in strains with one dose. This is evidence for a general elevation of X-linked gene expression in strains carrying X-chromosome duplications, consistent with the hypothesis that the duplications titrate a repressor acting on many X-linked genes.     

Androgens Increase Persistence But Do Not Affect Neophobia in a Problem‐Solving Context in a Songbird

Gonadal steroid hormones enhance cognitive performance, particularly spatial and vocal learning, in mammals and birds. However, it is unknown whether problem‐solving ability is similarly regulated. We propose that androgens, such as testosterone and 5α‐dihydrotestosterone, play a role in mediating problem‐solving behavior as well. As a test, male white‐crowned sparrows (Zonotrichia leucophrys gambelii) were either castrated and administered a blank (Blank‐castrate) or testosterone‐filled implant (T‐castrate) or were sham operated and were exposed to a novel feeder, which they had to open to receive a food reward, in two trials. Testosterone treatment affected neither a neophobic response nor problem‐solving performance. However, T‐castrates were more persistent in manipulating the feeder than Blank‐castrates or Shams. Furthermore, their persistence correlated positively with circulating levels of both testosterone and 5α‐dihydrotestosterone. We suggest that a positive correlation between sex steroids and persistence in foraging and problem‐solving contexts may lead to an adaptive increase in resource acquisition in the breeding season. Given the overall low success on the problem‐solving test, we cannot confidently conclude that androgens do not play a role in mediating problem‐solving behavior. However, unlike in mammals, it seems these hormones do not significantly influence neophobia in foraging contexts in birds.     

Multiple Lines of Egg Defense in a Neotropical Arachnid with Temporary Brood Desertion

Egg predation is the one of the main costs of brood desertion in many ectothermic animals. When stressful environmental conditions constrain parental activities to only some periods of the day, the combination of physical or chemical defenses may attenuate the costs related to egg loss during periods of temporary parental absence. Females of the harvestman Neosadocus maximus periodically abandon their clutches to shelter or forage. They also cover their eggs with a hygroscopic mucus coat and seem to lose fewer eggs to predation than other syntopic harvestmen whose eggs lack the mucus coat. Using two species of N. maximus egg predators, we demonstrate that eggs whose mucus coat was experimentally removed suffered higher predation rate than eggs whose mucus coat was left intact. We argue that this mucus provides physical protection against egg predators, especially small arthropods. A similar mucus coat has independently evolved in other two clades of Neotropical harvestman in which males care for the eggs and typically leave their clutches unattended for several hours a day. We propose that the presence of multiple lines of egg defense may have evolved as a way of lowering the costs imposed by intra‐ and interspecific egg predation during periods of temporary brood desertion.     

A Large Repertoire of Parasite Epitopes Matched by a Large Repertoire of Host Immune Receptors in an Invertebrate Host/Parasite Model

For many decades, invertebrate immunity was believed to be non-adaptive, poorly specific, relying exclusively on sometimes multiple but germ-line encoded innate receptors and effectors. But recent studies performed in different invertebrate species have shaken this paradigm by providing evidence for various types of somatic adaptations at the level of putative immune receptors leading to an enlarged repertoire of recognition molecules. Fibrinogen Related Proteins (FREPs) from the mollusc Biomphalaria glabrata are an example of these putative immune receptors. They are known to be involved in reactions against trematode parasites. Following not yet well understood somatic mechanisms, the FREP repertoire varies considerably from one snail to another, showing a trend towards an individualization of the putative immune repertoire almost comparable to that described from vertebrate adaptive immune system. Nevertheless, their antigenic targets remain unknown. In this study, we show that a specific set of these highly variable FREPs from B. glabrata forms complexes with similarly highly polymorphic and individually variable mucin molecules from its specific trematode parasite S. mansoni (Schistosoma mansoni Polymorphic Mucins: SmPoMucs). This is the first evidence of the interaction between diversified immune receptors and antigenic variant in an invertebrate host/pathogen model. The same order of magnitude in the diversity of the parasite epitopes and the one of the FREP suggests co-evolutionary dynamics between host and parasite regarding this set of determinants that could explain population features like the compatibility polymorphism observed in B. glabrata/S. mansoni interaction. In addition, we identified a third partner associated with the FREPs/SmPoMucs in the immune complex: a Thioester containing Protein (TEP) belonging to a molecular category that plays a role in phagocytosis or encapsulation following recognition. The presence of this last partner in this immune complex argues in favor of the involvement of the formed complex in parasite recognition and elimination from the host.     

Parasite Diversity in an Endemic Region for Avian Malaria and Identification of a Parasite Causing Penguin Mortality

ABSTRACT Understanding the population structure of Plasmodium parasites is essential for malaria intervention. A survey of parasites in vectors and host infections was conducted in an area of intense mortality due to malaria in a captive penguin ( Spheniscus demersus ) colony, using a novel method for identification of Plasmodium species by amplification of ribosomal sequences in DNA or RNA. Three phylogenetically distinct groups of avian Plasmodium were detected in mosquitoes ( Culex ) collected at the study site (Baltimore Zoo, Baltimore, MD) during a period of high transmission. One of the three clades of Plasmodium was found to be prevalent in penguins monitored through the malaria transmission season and consistent with morphological identification as Plasmodium relictum. This parasite sequence was directly associated with the death of a penguin. Thus, a complete transmission cycle is defined at this site. Phylogenetic comparison of ribosomal sequences to an authenticated reference strain of Plasmodium relictum indicates that this is not the parasite causing death in the penguins, suggesting that different parasites may be morphologically indistinguishable.     

Mutations of Phosphorylation Sites in MSL1 Protein Do Not Affect Dosage Compensation in Drosophila melanogaster

Doklady Biochemistry and Biophysics - Proteins MSL1 and MSL2 form the core of the Drosophila dosage compensation complex, which specifically binds to the X chromosome of males. Phosphorylation of...     

Egg Coloration and Recognition of Conspecific Brood Parasitism in Eastern Bluebirds

Individual eastern bluebird (Sialia sialis) females produce clutches of eggs with unique coloration and older females and females in better body condition lay more pigmented blue‐green eggs. Conspecific brood parasitism in this species is not uncommon and bluebirds occasionally reject what appear to be normal eggs by moving them to the periphery of the nest. I used UV‐visual reflectance spectrometry to objectively measure coloration of eggs and nest material. To estimate the conspicuousness of the trait, I calculated the contrast between eggs and background nest material. I found high achromatic and chromatic contrast between the coloration of eggs and of the nests, suggesting that bluebird eggs are highly conspicuous. To test the hypothesis that expression of blue‐green coloration eggs facilitates recognition of eggs laid by conspecific brood parasites, I cross‐fostered individual eggs into host nests during egg laying and monitored the fate of those eggs. I found no support, however, for the hypothesis that egg coloration facilitates discrimination of parasitic eggs from host eggs.     

Behavior of the Avian Parasite Philornis downsi (Diptera: Muscidae) in and Near Host Nests in the Galapagos Islands

The Avian Vampire Fly, Philornis downsi, has invaded the Galapagos Islands, where it causes high mortality of endemic and native landbird species, including most species of Darwin’s finches. Control methods are under development, but key information is missing about the reproductive biology of P. downsi and the behavior of flies in and near nests of their hosts. We used external and internal nest cameras to record the behavior of P. downsi adults within and outside nests of the Galapagos Flycatcher, Myiarchus magnirostris, throughout all stages of the nesting cycle. These recordings showed that P. downsi visited flycatcher nests throughout the day with higher fly activity during the nestling phase during vespertine hours. The observations also revealed that multiple P. downsi individuals can visit nests concurrently, and that there are some interactions among these flies within the nest. Fly visitation to nests occurred significantly more often while parent birds were away from the nest than in the nest, and this timing appears to be a strategy to avoid predation by parent birds. We report fly mating behavior outside the nest but not in the nest cavity. We discuss the relevance of these findings for the adaptive forces shaping P. downsi life history strategies as well as rearing and control measures.

     

Experimental Evolution of a Trypanosome Parasite of Bumblebees and its Implications for Infection Success and Host Immune Response

Selection on basic growth properties of parasites may have many consequences for parasite traits, infection outcome, or host responses to infection. It is known that genotypes (strains) of the trypanosome parasite of bumblebees Crithidia bombi vary widely in their growth rates in their natural host, Bombus terrestris, as well as when cultured in medium. To test for changes in growth rates and their consequences, we here experimentally evolved six strains of C. bombi for fast and slow growth under controlled conditions in culture medium. Subsequently, we infected the evolved lines in live host and found that lines selected for slow growth attained higher infection intensity in the live bumblebee than those evolved for fast growth, whilst the immune response of the host was the same to both kinds of lines. These results fit the expectation that attenuation through rapid adaptation to a different environment, the culture medium, makes the parasite less successful in its next host. Selection for fast growth therefore does not necessarily lead to higher parasite success or more transmission. Hence, insect trypanosome pathogens can be attenuated by experimental evolution in the culture; this could inform important aspects of host-parasite evolution and perhaps vaccine development.     

Guinea Pig Terminal 5-HT1D Autoreceptors Do Not Display a Circadian Variation in Their Responsiveness to Serotonin

Many of the components involved in the synthesis and release of serotonin (5-HT) display a circadian variation in their activity. Autoreceptors located on nerve terminals were recently suggested to underlie some of these circadian variations. The aim of this study was to examine whether terminal 5-HT_1D autoreceptors in the cerebral cortex of the guinea pig exhibit a circadian variation in their responsiveness. The responsiveness of these autoreceptors was assessed by the ability of exogenously applied 5-HT to inhibit the potassium-evoked release of [³H]5-HT from slices of guinea pig cortex. Identical experiments were conducted at four different, equally spaced time points during the light:dark cycle of the guinea pig. The results presented here demonstrate that terminal 5-HT_1D autoreceptors do not exhibit a circadian variation in their responsiveness. Therefore, terminal 5-HT_1D autoreceptors bear similarity to terminal 5-HT_1B autoreceptors identified in rat brain in being devoid of a significant rhythm in their responsiveness.