The limits of egg recognition: testing acceptance thresholds of American robins in response to decreasingly egg-shaped objects in the nest

Some hosts of avian brood parasites reduce or eliminate the costs of parasitism by removing foreign eggs from the nest (rejecter hosts). In turn, even acceptor hosts typically remove most non-egg-shaped objects from the nest, including broken shells, fallen leaves and other detritus. In search for the evolutionary origins and sensory mechanisms of egg rejection, we assessed where the potential threshold between egg recognition and nest hygiene may lie when it comes to stimulus shape. Most previous studies applied comparisons of egg-sized objects with non-continuous variation in shape. Here, instead, we used two series of three-dimensional-printed objects, designed a priori to increasingly diverge from natural eggs along two axes (width or angularity) of shape variation. As predicted, we detected transitions from mostly acceptance to mostly rejection in the nests of American robins Turdus migratorius along each of the two axes. Our methods parallel previous innovations in egg-rejection studies through the use of continuous variation in egg coloration and maculation contrast, to better understand the sensory limits and thresholds of variation in egg recognition and rejection in diverse hosts of avian brood parasites.

Pre-existing Microfilarial Infections of American Robins (Passeriformes: Turdidae) and Common Grackles (Passeriformes: Icteridae) Have Limited Impact on Enhancing Dissemination of West Nile Virus in Culex pipiens Mosquitoes (Diptera: Culicidae)

Microfilariae (MF) are the immature stages of filarial nematode parasites and inhabit the blood and dermis of all classes of vertebrates, except fish. Concurrent ingestion of MF and arboviruses by mosquitoes can enhance mosquito transmission of virus compared to when virus is ingested alone. Shortly after being ingested, MF penetrate the mosquito’s midgut and may introduce virus into the mosquito’s hemocoel, creating a disseminated viral infection much sooner than normal. This phenomenon is known as microfilarial enhancement. Both American Robins and Common Grackles harbor MF—that is, Eufilaria sp. and Chandlerella quiscali von Linstow (Spirurida: Onchocercidae), respectively. We compared infection and dissemination rates in Culex pipiens L. mosquitoes that fed on birds with and without MF infections that had been infected with West Nile virus (WNV). At moderate viremias, about 107 plaque-forming units (pfu)/ml of blood, there were no differences in infection or dissemination rates among mosquitoes that ingested viremic blood from a bird with or without microfilaremia. At high viremias, >108.5 pfu/ml, mosquitoes feeding on a microfilaremic Grackle with concurrent viremia had significantly higher infection and dissemination rates than mosquitoes fed on viremic Grackles without microfilaremia. Microfilarial enhancement depends on the specific virus, MF, and mosquito species examined. How virus is introduced into the hemocoel by MF differs between the avian/WNV systems described here (i.e., leakage) and various arboviruses with MF of the human filarid, Brugia malayi (Brug) (Spirurida: Onchocercidae) (i.e., cotransport). Additional studies are needed to determine if other avian species and their MF are involved in the microfilarial enhancement of WNV in nature.

Host specialization in microparasites transmitted by generalist vectors: insights into the cellular and immunological mechanisms

ABSTRACTHost specialization is an ecological and evolutionary process by which a pathogen becomes differentially adapted to a subset of hosts, restricting its host range. For parasites transmitted by generalist vectors, host specialization is not expected to evolve because of the decreased survival of those parasites in inadequate hosts. Thus, parasites may develop adaptation strategies, resulting in host specialization. The causative agents of Lyme disease are multiple species of bacteria, Borrelia burgdorferi sensu lato species complex (Bbsl), and are suitable for examining host specialization as birds and rodents were found to carry different species of these bacteria. Debate exists on whether host specialization occurs among these strains within a particular species of Bbsl, such as B. burgdorferi sensu stricto (Bbss). Current evidence supports some Bbss strains are widespread in white-footed mice but others are in non-rodent vertebrates, such as birds. To recapitulate specialization in the laboratory and define the mechanisms for host specialization, we introduced different genotypes of Bbss via tick transmission to American robins and white-footed mice, the Lyme disease reservoirs in North America. Among these strains, we found distinct levels of spirochete presence in the bloodstream and tissues and maintenance by these animals in a host-dependent fashion. We showed that the late stage persistence of these strains largely corresponds to bacterial survival at early infection onsets. We also demonstrated that those early survival phenotypes correspond to spirochete adhesiveness, evasion of complement-mediated killing in sera, and/or not triggering high levels of pro-inflammatory cytokines and antibodies. Our findings thus link host competence to Bbss with spirochete genotypic variation of adhesiveness and inducing/escaping host immune responses, illuminating the potential mechanisms that dictate host specialization. Such information will provide a foundation for further investigation into multi-disciplinary processes driving host specialization of microparasites.AUTHOR SUMMARYHost specialization arises when microparasites adapt to a subset of available hosts, restricting the host ranges they can infect. The mechanisms and selective pressures for the evolution of host specialization remain unclear. The causative agent of Lyme disease (LD), the bacteria species complex of Borrelia burgdorferi sensu lato, is adapted to different vertebrates. However, whether such a differential host adaption also applies to each genotype within the same species is under debate. Further, the mechanisms that drive such host specialization are unclear. We thus introduced three genotypes of one LD bacteria species (B. burgdorferi sensu stricto) individually via tick bite to American robins and white-footed mice, the most common LD reservoirs in North America. We found that these genotypes differed in the persistent maintenance by those reservoirs and occurred in a host-specific fashion. The ability of those bacteria for long-term maintenance was linked with their capability to attach to cells and a lack of induction of high levels of immune responses at early infection onsets. This work demonstrates the potential mechanisms that dictate host specialization of LD bacteria circulating in natural populations. Such information will pave the road to define the molecular, ecological, and evolutionary determinants that drive host-microparasite interactions.

Natural and artificial scents do not increase egg rejection rates of model brood parasitic eggs by American robins (Turdus migratorius)

Hosts of obligate avian brood parasites can diminish or eliminate the costs of parasitism by rejecting foreign eggs from the nests. A vast literature demonstrates that visual and/or tactile cues can be used to recognize and reject natural or model eggs from the nests of diverse host species. However, data on olfaction-based potential egg recognition cues are both sparse and equivocal: experimentally-applied, naturally-relevant (heterospecific, including parasitic) scents do not appear to increase egg rejection rates in two host species, whereas unnatural scents (human and tobacco scents) do so in one host species. Here I assessed the predictions that (i) human handling of mimetically-painted model eggs would increase rejection rates, and (ii) applying unnatural or natural scents to mimetically or non-mimetically painted model eggs alters these eggs’ respective rejection rates relative to controls. I studied wild American Robins (Turdus migratorius), a robust rejecter species of the eggs of obligate brood parasitic Brown-headed Cowbirds (Molothrus ater). There was no statistical evidence to support either prediction, whereas poorer color-mimicry was still a predicted cause of greater egg rejection in this data set. Nonetheless, future studies could focus on this and other host species and using these and different methods to apply and maintain the scenting of model eggs to more directly test hosts’ use of potential olfactory cues in the foreign-egg rejection process.

Visual acuity and egg spatial chromatic contrast predict egg rejection behavior of American robins

ABSTRACTColor and spatial vision is critical for recognition and discrimination tasks affecting fitness, including finding food and mates, and recognizing offspring. For example, as a counter defense to avoid the cost of raising the unrelated offspring of obligate interspecific avian brood parasites, many host species routinely view, recognize and remove the foreign egg(s) from their nests. Recent research has shown that host species visually attend to both chromatic and spatial pattern features of eggs; yet how hosts simultaneously integrate these features together when recognizing eggs remains an open question. Here, we tested egg rejection responses of American robins (Turdus migratorius) using a range of 3D-printed model eggs covered with blue and yellow checkered patterns differing in relative square sizes. We predicted that robins would reject a model egg if they could visually resolve the blue and yellow squares as separate features, or accept it if the squares blended together and appeared similar in color to the natural blue–green color of robin eggs as perceived by the avian visual system. As predicted, the probability of robins rejecting a model egg increased with greater sizes of its blue and yellow squares. Our results suggest that chromatic visual acuity and viewing distance have the potential to limit the ability of a bird to recognize a foreign egg in its nest, thus providing a limitation to host egg recognition that obligate interspecific avian brood parasites may exploit.

Bird Species Involved in West Nile Virus Epidemiological Cycle in Southern Québec

Despite many studies on West Nile Virus (WNV) in the US, including the reservoir role of bird species and the summer shifts of the Culex mosquito, feeding from birds to mammals, there have been few equivalent studies in the neighboring regions of Canada where WNV is endemic. Here, a priority list of bird species likely involved in WNV transmission in the greater Montréal area is constructed by combining three sources of data: (i) from WNV surveillance in wild birds (2002–2015); (ii) blood meal analysis of Culex pipiens–restuans (CPR), the primary enzootic vectors of WNV in the region, collected from surveillance in 2008 and 2014; (iii) literature review on the sero-prevalence/host competence of resident birds. Each of these data sources yielded 18, 23 and 53 species, and overall, 67 different bird species were identified as potential WNV amplifiers/reservoirs. Of those identified from CPR blood meals, Common starlings, American robins, Song sparrows and House sparrows ranked the highest and blood meal analysis demonstrated a seasonal shift in feed preference from birds to mammals by CPR. Our study indicates that there are broad similarities in the ecology of WNV between our region and the northeastern US, although the relative importance of bird species varies somewhat between regions.