Tricking Parents: A Review of Mechanisms and Signals of Host Manipulation by Brood-Parasitic Young

Obligate avian brood parasites depend entirely on heterospecific hosts for rearing their offspring. From hatching until independence, the young parasites must deal with the challenge of obtaining sufficient parental care from foster parents that are attuned to provisioning their own offspring. Parent-offspring communication is mediated by complex begging displays in which nestlings and fledglings exhibit visual (e.g., gaping and postures) and vocal (e.g., begging calls) traits that serve as signals to parents to adjust and allocate parental effort. Parasites can manipulate host parental behavior by exploiting these stable parent-offspring communication systems in their favor. During the past 30 years, the study of host exploitation by parasitic chicks has yielded important insights into the function and evolution of manipulative signals in brood parasites. However, despite these major advances, there are still important gaps in our knowledge about how parasitic nestling and fledglings tune into the host’s communication channels and the adaptive value of the visual and acoustic signals they exhibit. Here we review the literature pertaining to host manipulation by parasitic young, focusing on four non-mutually exclusive mechanisms (i.e., host chick mimicry, begging exaggeration, host-attuned begging calls, and sensory exploitation) and the function and evolution of the signals involved, with the aim to summarize and discuss putative adaptations for stimulating parental feeding and escaping host discrimination. Finally, we bring some concluding remarks and suggest directions for future research on the ways in which brood parasites adapt to the communication systems of other birds to exploit the necessary parental care.Fil: Rojas Ripari, Juan Manuel. Consejo Nacional de Investigaciones Científicas y Técnicas. Oficina de Coordinación Administrativa Ciudad Universitaria. Instituto de Ecología, Genética y Evolución de Buenos Aires. Universidad de Buenos Aires. Facultad de Ciencias Exactas y Naturales. Instituto de Ecología, Genética y Evolución de Buenos Aires; ArgentinaFil: Ursino, Cynthia Alejandra. Consejo Nacional de Investigaciones Científicas y Técnicas. Oficina de Coordinación Administrativa Ciudad Universitaria. Instituto de Ecología, Genética y Evolución de Buenos Aires. Universidad de Buenos Aires. Facultad de Ciencias Exactas y Naturales. Instituto de Ecología, Genética y Evolución de Buenos Aires; ArgentinaFil: Reboreda, Juan Carlos. Consejo Nacional de Investigaciones Científicas y Técnicas. Oficina de Coordinación Administrativa Ciudad Universitaria. Instituto de Ecología, Genética y Evolución de Buenos Aires. Universidad de Buenos Aires. Facultad de Ciencias Exactas y Naturales. Instituto de Ecología, Genética y Evolución de Buenos Aires; ArgentinaFil: de Marsico, Maria Cecilia. Consejo Nacional de Investigaciones Científicas y Técnicas. Oficina de Coordinación Administrativa Ciudad Universitaria. Instituto de Ecología, Genética y Evolución de Buenos Aires. Universidad de Buenos Aires. Facultad de Ciencias Exactas y Naturales. Instituto de Ecología, Genética y Evolución de Buenos Aires; Argentin

Yellow Cardinal (Gubernatrix cristata) males respond more strongly to local than to foreign dialects

Bird song is a culturally transmitted behavioural trait strongly tied to territory defence and mate attraction in oscine passerines. Divergent song variations can appear in different populations of the same species as a consequence of multiple factors generating geographically distinct songs also termed dialects. Most studies show that males react more strongly towards local dialects, potentially as a by-product of evolutionary divergence between populations, although other hypotheses have been suggested. In addition, females are hypothesized to show stronger responses to local songs as this may lead to greater reproductive success. In this context, song may become a prezygotic barrier for reproduction. The Yellow Cardinal Gubernatrix cristata is an endangered species of the South American thorny shrubland that has suffered from population fragmentation due to habitat destruction and its capture for the illegal wildlife trade. Genetically different groups that sing their own dialect have been studied in the context of a conservation programme that intends to restore and preserve natural populations by releasing individuals that are recovered from the illegal pet market back into their area of origin. Although dialects have been identified, it remains unknown whether there is vocal recognition between the populations. In this study, we performed playback experiments in two populations and found that male Yellow Cardinals reacted more strongly to the local dialect, although the foreign dialect was still recognized. This information is important as it is not always possible to genetically assign an individual to its geographical origin before release, which could contribute to a secondary contact scenario where dialects play a critical role for settlement and reproduction.Fil: Fracas, Pablo Andrés. Consejo Nacional de Investigaciones Científicas y Técnicas. Oficina de Coordinación Administrativa Ciudad Universitaria. Instituto de Ecología, Genética y Evolución de Buenos Aires. Universidad de Buenos Aires. Facultad de Ciencias Exactas y Naturales. Instituto de Ecología, Genética y Evolución de Buenos Aires; ArgentinaFil: Rojas Ripari, Juan Manuel. Consejo Nacional de Investigaciones Científicas y Técnicas. Oficina de Coordinación Administrativa Ciudad Universitaria. Instituto de Ecología, Genética y Evolución de Buenos Aires. Universidad de Buenos Aires. Facultad de Ciencias Exactas y Naturales. Instituto de Ecología, Genética y Evolución de Buenos Aires; ArgentinaFil: Mahler, Bettina. Consejo Nacional de Investigaciones Científicas y Técnicas. Oficina de Coordinación Administrativa Ciudad Universitaria. Instituto de Ecología, Genética y Evolución de Buenos Aires. Universidad de Buenos Aires. Facultad de Ciencias Exactas y Naturales. Instituto de Ecología, Genética y Evolución de Buenos Aires; ArgentinaFil: Domínguez, Marisol. Universitat Potsdam; Alemani

Aceptar o eliminar a los compañeros de nido, esa es la cuestión: éxito del Tordo Renegrido (Molothrus bonariensis) en nidos de Músico (Agelaioides badius), en ausencia de pichones del hospedador

Las crías de los parásitos de cría obligados deben obtener recursos de hospedadores de otras especies, adaptadas a los comportamientos de pedido de alimento de su propia progenie. La ausencia de los estímulos apropiados puede llevar a la malnutrición o incluso la muerte de las crías parásitas. Una forma de sortear este desafío es compartir el nido con las crías del hospedador, en tanto los parásitos sean capaces de competir eficientemente por el alimento. Investigamos la capacidad de pichones y juveniles de Tordo Renegrido (Molothrus bonariensis) para estimular el cuidado parental en ausencia de las crías del hospedador en un hospedador capaz de discriminar entre crías propias y parásitas en base a los llamados de pedido de alimento, el Músico (Agelaioides badius). Generamos nidadas experimentales con un único pichón de Tordo Renegrido o de Músico (control), en las que medimos la entrega de alimento, el crecimiento y la supervivencia de los pichones. Encontramos que no hubo diferencias en la tasa de entrega de alimento entre los pichones parásitos y los del hospedador, y que los parámetros de crecimiento fueron similares entre los pichones de Tordo Renegrido criados solos y los reportados para nidadas mixtas. Por lo tanto, los resultados no avalan la hipótesis de que los pichones no miméticos requieran la asistencia de las crías del hospedador para inducir suficiente cuidado parental en el Músico. Más aún, observamos que los juveniles de Tordo Renegrido criados solos continuaron recibiendo cuidado parental luego de dejar el nido, a diferencia de aquellos criados en nidadas mixtas. Esto suma evidencia a la existencia de presiones de selección opuestas actuando sobre la evolución de la aceptación versus eliminación de los pichones del hospedador en los tordos, y sugiere habilidades de discriminación contexto-dependientes en el hospedador que merecen ser investigadas con más detalle.Fil: Rojas Ripari, Juan Manuel. Consejo Nacional de Investigaciones Científicas y Técnicas. Oficina de Coordinación Administrativa Ciudad Universitaria. Instituto de Ecología, Genética y Evolución de Buenos Aires. Universidad de Buenos Aires. Facultad de Ciencias Exactas y Naturales. Instituto de Ecología, Genética y Evolución de Buenos Aires; ArgentinaFil: Segura, Luciano Noel. Universidad Nacional de La Plata. Facultad de Ciencias Naturales y Museo; Argentina. Consejo Nacional de Investigaciones Científicas y Técnicas. Oficina de Coordinación Administrativa Ciudad Universitaria. Instituto de Ecología, Genética y Evolución de Buenos Aires. Universidad de Buenos Aires. Facultad de Ciencias Exactas y Naturales. Instituto de Ecología, Genética y Evolución de Buenos Aires; ArgentinaFil: Reboreda, Juan Carlos. Consejo Nacional de Investigaciones Científicas y Técnicas. Oficina de Coordinación Administrativa Ciudad Universitaria. Instituto de Ecología, Genética y Evolución de Buenos Aires. Universidad de Buenos Aires. Facultad de Ciencias Exactas y Naturales. Instituto de Ecología, Genética y Evolución de Buenos Aires; ArgentinaFil: de Marsico, Maria Cecilia. Consejo Nacional de Investigaciones Científicas y Técnicas. Oficina de Coordinación Administrativa Ciudad Universitaria. Instituto de Ecología, Genética y Evolución de Buenos Aires. Universidad de Buenos Aires. Facultad de Ciencias Exactas y Naturales. Instituto de Ecología, Genética y Evolución de Buenos Aires; ArgentinaXVIII Reunión Argentina de OrnitologíaTandilArgentinaUniversidad Nacional del Centro de la Provincia de Buenos Aires. Facultad de Ciencias Exactas. Instituto Multidisciplinario sobre Ecosistemas y Desarrollo Sustentabl

Non-mimetic shiny cowbird nestlings escape discrimination by baywings in absence of host nest mates

Nestlings of obligate brood parasites must obtain resources from heterospecific hosts that are attuned to the solicitation behaviours of their own progeny. Failing to match the appropriate stimuli may result in suboptimal provisioning or even the starvation of parasite young. Parasitic nestlings could overcome it by sharing the nest with host young, as long as they are able to compete efficiently for parental feedings. Here, we examined if non-mimetic shiny cowbird (Molothrus bonariensis) nestlings reared alone fail to elicit sufficient parental care from the grayish baywing (Agelaioides badius), a host that discriminates between their own and parasitic nestlings based on species-specific begging cues. We manipulated baywing broods to assess the ability of shiny cowbird nestlings to elicit parental provisioning and survive without host nest mates. Host provisioning rates and survival did not differ between shiny cowbirds reared alone and host nestlings in singleton broods. Also, growth patterns of experimental nestlings reared alone were similar to those reported for shiny cowbirds reared alongside baywing young. Hence, we did not find support for the hypothesis that non-mimetic nestlings require the assistance of host nest mates to elicit sufficient parental care from its baywing host. Furthermore, we found that shiny cowbirds that were reared alone continued receiving care from baywings after fledging, unlike shiny cowbirds from mixed broods. Our results add evidence to the idea of opposing selective pressures on the evolution of nest mate acceptance in cowbirds and suggest context-dependent host’s discrimination abilities that deserve further investigation. The evolution of nest mate killing versus tolerance strategies is a long-standing question in the study of brood parasitism. Parasitic nestlings may benefit from sharing the nest with host young if they collectively induce more parental provisioning and the parasite can benefit from it. Host nest mates could also confer protection against discrimination when hosts respond preferentially to stimuli of their own kind. We examined this idea in a generalist brood parasite, the shiny cowbird (Molothrus bonariensis), and a host able to discriminate species-specific begging cues. The results showed that shiny cowbirds reared alone performed well and circumvent host discrimination also after leaving the nest. Our study supports the existence of trade-offs on the evolution of nest mate killing behaviours and adds evidence that context-dependent host’s discrimination abilities similar to those observed towards parasitic eggs can be at play towards parasitic fledglings.Facultad de Ciencias Naturales y Muse

Innate development of acoustic signals for host parent–offspring recognition in the brood-parasitic Screaming Cowbird Molothrus rufoaxillaris

Young birds communicate their need to parents through complex begging displays that include visual and acoustic cues. Nestlings of interspecific brood parasites must ‘tune’ into these communication channels to secure parental care from their hosts. Various studies show that parasitic nestlings can effectively manipulate host parental behaviour through their begging calls, but how these manipulative acoustic signals develop in growing parasites remains poorly understood. We investigated the influence of social experience on begging call development in a host-specialist brood parasite, the Screaming Cowbird Molothrus rufoaxillaris. Screaming Cowbird nestlings look and sound similar to those of the primary host, the Greyish Baywing Agelaioides badius. This resemblance is likely to be adaptive because Baywings discriminate against fledglings unlike their own and provision nests at higher rates in response to Baywing-like begging calls than to non-mimetic begging calls. By means of cross-fostering and playback experiments, we tested whether the acoustic cues that elicit recognition by Baywings develop innately in Screaming Cowbird nestlings or are acquired through social experience with host parents or nest mates. Our results suggest that begging call structure was partially modulated by experience because Baywing-reared Screaming Cowbird and host nestlings were acoustically more similar as age increased, whereas acoustic similarity between cross-fostered and Baywing-reared Screaming Cowbird nestlings decreased from 4–5 to 8–10 days of age. Cross-fostered Screaming Cowbirds developed begging calls of lower minimum frequency and broader bandwidth than those of Baywing-reared Screaming Cowbirds by the age of 8–10 days. Despite the observed differences in begging call structure, however, adult Baywings responded similarly to begging calls of 8- to 10-day-old cross-fostered and Baywing-reared Screaming Cowbirds, suggesting that these were functionally equivalent from the host's perspective. These findings support the idea that, although rearing environment can influence certain begging call parameters, the acoustic cues that serve for offspring recognition by Baywings develop in young Screaming Cowbirds independently of social experience.Fil: Rojas Ripari, Juan Manuel. Consejo Nacional de Investigaciones Científicas y Técnicas. Oficina de Coordinación Administrativa Ciudad Universitaria. Instituto de Ecología, Genética y Evolución de Buenos Aires. Universidad de Buenos Aires. Facultad de Ciencias Exactas y Naturales. Instituto de Ecología, Genética y Evolución de Buenos Aires; ArgentinaFil: Ursino, Cynthia Alejandra. Consejo Nacional de Investigaciones Científicas y Técnicas. Oficina de Coordinación Administrativa Ciudad Universitaria. Instituto de Ecología, Genética y Evolución de Buenos Aires. Universidad de Buenos Aires. Facultad de Ciencias Exactas y Naturales. Instituto de Ecología, Genética y Evolución de Buenos Aires; ArgentinaFil: Reboreda, Juan Carlos. Consejo Nacional de Investigaciones Científicas y Técnicas. Oficina de Coordinación Administrativa Ciudad Universitaria. Instituto de Ecología, Genética y Evolución de Buenos Aires. Universidad de Buenos Aires. Facultad de Ciencias Exactas y Naturales. Instituto de Ecología, Genética y Evolución de Buenos Aires; ArgentinaFil: de Marsico, Maria Cecilia. Consejo Nacional de Investigaciones Científicas y Técnicas. Oficina de Coordinación Administrativa Ciudad Universitaria. Instituto de Ecología, Genética y Evolución de Buenos Aires. Universidad de Buenos Aires. Facultad de Ciencias Exactas y Naturales. Instituto de Ecología, Genética y Evolución de Buenos Aires; Argentin

Non-mimetic shiny cowbird nestlings escape discrimination by baywings in absence of host nest mates

Nestlings of obligate brood parasites must obtain resources from heterospecific hosts that are attuned to the solicitation behaviours of their own progeny. Failing to match the appropriate stimuli may result in suboptimal provisioning or even the starvation of parasite young. Parasitic nestlings could overcome it by sharing the nest with host young, as long as they are able to compete efficiently for parental feedings. Here, we examined if non-mimetic shiny cowbird (Molothrus bonariensis) nestlings reared alone fail to elicit sufficient parental care from the grayish baywing (Agelaioides badius), a host that discriminates between their own and parasitic nestlings based on species-specific begging cues. We manipulated baywing broods to assess the ability of shiny cowbird nestlings to elicit parental provisioning and survive without host nest mates. Host provisioning rates and survival did not differ between shiny cowbirds reared alone and host nestlings in singleton broods. Also, growth patterns of experimental nestlings reared alone were similar to those reported for shiny cowbirds reared alongside baywing young. Hence, we did not find support for the hypothesis that non-mimetic nestlings require the assistance of host nest mates to elicit sufficient parental care from its baywing host. Furthermore, we found that shiny cowbirds that were reared alone continued receiving care from baywings after fledging, unlike shiny cowbirds from mixed broods. Our results add evidence to the idea of opposing selective pressures on the evolution of nest mate acceptance in cowbirds and suggest context-dependent host’s discrimination abilities that deserve further investigation.Fil: Rojas Ripari, Juan Manuel. Consejo Nacional de Investigaciones Científicas y Técnicas. Oficina de Coordinación Administrativa Ciudad Universitaria. Instituto de Ecología, Genética y Evolución de Buenos Aires. Universidad de Buenos Aires. Facultad de Ciencias Exactas y Naturales. Instituto de Ecología, Genética y Evolución de Buenos Aires; ArgentinaFil: Segura, Luciano Noel. Universidad Nacional de La Plata. Facultad de Ciencias Naturales y Museo. División Zoología de Vertebrados. Sección Ornitología; Argentina. Consejo Nacional de Investigaciones Científicas y Técnicas. Centro Científico Tecnológico Conicet - La Plata; ArgentinaFil: Reboreda, Juan Carlos. Consejo Nacional de Investigaciones Científicas y Técnicas. Oficina de Coordinación Administrativa Ciudad Universitaria. Instituto de Ecología, Genética y Evolución de Buenos Aires. Universidad de Buenos Aires. Facultad de Ciencias Exactas y Naturales. Instituto de Ecología, Genética y Evolución de Buenos Aires; ArgentinaFil: de Marsico, Maria Cecilia. Consejo Nacional de Investigaciones Científicas y Técnicas. Oficina de Coordinación Administrativa Ciudad Universitaria. Instituto de Ecología, Genética y Evolución de Buenos Aires. Universidad de Buenos Aires. Facultad de Ciencias Exactas y Naturales. Instituto de Ecología, Genética y Evolución de Buenos Aires; Argentin

Family ties in a neotropical cooperative breeder: within-group relatedness and fine-scale genetic structure in the greyish Baywing (Agelaioides badius)

Cooperative breeding is a reproductive system in which one or more adults (helpers) assist others in rearing their offspring. Cooperative breeding occurs in 9% of birds, encompassing remarkable variation in mating systems and patterns of social organization. Understanding how this diversity evolved requires assessing social and genetic relationships across a broad range of cooperative systems. Yet, for some geographical regions like the Neotropics, detailed genetic studies of cooperatively breeding birds are still comparatively scarce. We used double-digest restriction-site associated DNA sequencing to define the genetic relationships within and between cooperative groups in a Neotropical facultative cooperative breeder, the Greyish Baywing Agelaioides badius. Between 2015 and 2018, we banded and sampled adults and nestlings of 41 breeding groups from a population in the Province of Buenos Aires, Argentina. We found that helpers were primarily males, the majority of which were genetically related to the individuals they assisted, either as previous offspring of the breeding pair or as first- or second-order relatives of the breeding male. However, we also observed unrelated male and female helpers. Parentage analysis indicates that reproduction was strongly skewed towards the dominant pair and helpers never gained paternity within and only once outside their social group. This scenario is consistent with helping behaviour being driven primarily by kin selection rather than by direct genetic benefits to helpers. However, the occasional occurrence of helpers unrelated to the breeding pair suggests that non-reproductive direct benefits such as increased access to resources or future breeding opportunities may also influence helping decisions in this species. We found weak evidence consistent with male natal philopatry, and fine-scale genetic structure, as adult males in our population showed higher relatedness at close geographical distances than females. Future studies that further examine the mechanisms behind group formation and the fitness pay-offs of helping behaviour will increase our understanding of the complex cooperative system of the Greyish Baywing.Fil: Rojas Ripari, Juan Manuel. Consejo Nacional de Investigaciones Científicas y Técnicas. Oficina de Coordinación Administrativa Ciudad Universitaria. Instituto de Ecología, Genética y Evolución de Buenos Aires. Universidad de Buenos Aires. Facultad de Ciencias Exactas y Naturales. Instituto de Ecología, Genética y Evolución de Buenos Aires; Argentina. Universidad de Buenos Aires. Facultad de Ciencias Exactas y Naturales. Departamento de Ecología, Genética y Evolución; ArgentinaFil: Campagna, Leonardo. Cornell University; Estados UnidosFil: Mahler, Bettina. Consejo Nacional de Investigaciones Científicas y Técnicas. Oficina de Coordinación Administrativa Ciudad Universitaria. Instituto de Ecología, Genética y Evolución de Buenos Aires. Universidad de Buenos Aires. Facultad de Ciencias Exactas y Naturales. Instituto de Ecología, Genética y Evolución de Buenos Aires; Argentina. Universidad de Buenos Aires. Facultad de Ciencias Exactas y Naturales. Departamento de Ecología, Genética y Evolución; ArgentinaFil: Lovette, Irby. Cornell University; Estados UnidosFil: Reboreda, Juan Carlos. Consejo Nacional de Investigaciones Científicas y Técnicas. Oficina de Coordinación Administrativa Ciudad Universitaria. Instituto de Ecología, Genética y Evolución de Buenos Aires. Universidad de Buenos Aires. Facultad de Ciencias Exactas y Naturales. Instituto de Ecología, Genética y Evolución de Buenos Aires; Argentina. Universidad de Buenos Aires. Facultad de Ciencias Exactas y Naturales. Departamento de Ecología, Genética y Evolución; ArgentinaFil: de Marsico, Maria Cecilia. Consejo Nacional de Investigaciones Científicas y Técnicas. Oficina de Coordinación Administrativa Ciudad Universitaria. Instituto de Ecología, Genética y Evolución de Buenos Aires. Universidad de Buenos Aires. Facultad de Ciencias Exactas y Naturales. Instituto de Ecología, Genética y Evolución de Buenos Aires; Argentina. Universidad de Buenos Aires. Facultad de Ciencias Exactas y Naturales. Departamento de Ecología, Genética y Evolución; Argentin