Nestling Begging Calls Resemble Maternal Vocal Signatures When Mothers Call Slowly to Embryos.

AbstractVocal production learning (the capacity to learn to produce vocalizations) is a multidimensional trait that involves different learning mechanisms during different temporal and socioecological contexts. Key outstanding questions are whether vocal production learning begins during the embryonic stage and whether mothers play an active role in this through pupil-directed vocalization behaviors. We examined variation in vocal copy similarity (an indicator of learning) in eight species from the songbird family Maluridae, using comparative and experimental approaches. We found that (1) incubating females from all species vocalized inside the nest and produced call types including a signature "B element" that was structurally similar to their nestlings' begging call; (2) in a prenatal playback experiment using superb fairy wrens (Malurus cyaneus), embryos showed a stronger heart rate response to playbacks of the B element than to another call element (A); and (3) mothers that produced slower calls had offspring with greater similarity between their begging call and the mother's B element vocalization. We conclude that malurid mothers display behaviors concordant with pupil-directed vocalizations and may actively influence their offspring's early life through sound learning shaped by maternal call tempo.

Nest architecture influences host use by avian brood parasites and is shaped by coevolutionary dynamics.

Brood (social) parasites and their hosts exhibit a wide range of adaptations and counter-adaptations as part of their ongoing coevolutionary arms races. Obligate avian brood parasites are expected to use potential host species with more easily accessible nests, while potential hosts are expected to evade parasitism by building more concealed nests that are difficult for parasites to enter and in which to lay eggs. We used phylogenetically informed comparative analyses, a global database of the world's brood parasites, their host species, and the design of avian host and non-host nests (approx. 6200 bird species) to examine first, whether parasites preferentially target host species that build open nests and, second, whether host species that build enclosed nests are more likely to be targeted by specialist parasites. We found that species building more accessible nests are more likely to serve as hosts, while host species with some of the more inaccessible nests are targeted by more specialist brood parasites. Furthermore, evolutionary-transition analyses demonstrate that host species building enclosed nests frequently evolve to become non-hosts. We conclude that nest architecture and the accessibility of nests for parasitism represent a critical stage of the ongoing coevolutionary arms race between avian brood parasites and their hosts.

Host avian species and environmental conditions influence the microbial ecology of brood parasitic brown-headed cowbird nestlings: What rules the roost?

The role of species interactions, as well as genetic and environmental factors, all likely contribute to the composition and structure of the gut microbiome; however, disentangling these independent factors under field conditions represents a challenge for a functional understanding of gut microbial ecology. Avian brood parasites provide unique opportunities to investigate these questions, as brood parasitism results in parasite and host nestlings being raised in the same nest, by the same parents. Here we utilized obligate brood parasite brown-headed cowbird nestlings (BHCO; Molothrus ater) raised by several different host passerine species to better understand, via 16S rRNA sequencing, the microbial ecology of brood parasitism. First, we compared faecal microbial communities of prothonotary warbler nestlings (PROW; Protonotaria citrea) that were either parasitized or non-parasitized by BHCO and communities among BHCO nestlings from PROW nests. We found that parasitism by BHCO significantly altered both the community membership and community structure of the PROW nestling microbiota, perhaps due to the stressful nest environment generated by brood parasitism. In a second dataset, we compared faecal microbiotas from BHCO nestlings raised by six different host passerine species. Here, we found that the microbiota of BHCO nestlings was significantly influenced by the parental host species and the presence of an inter-specific nestmate. Thus, early rearing environment is important in determining the microbiota of brood parasite nestlings and their companion nestlings. Future work may aim to understand the functional effects of this microbiota variability on nestling performance and fitness.

Genes, Environments, and Phenotypic Plasticity in Immunology.

For most of its history, immunology has sought to control environmental variation to establish genetic causality. As with all biological traits though, variation among individuals arises by three broad pathways: genetic (G), environmental (E), and the interactive between the two (GxE); and immunity is no different. Here, we review the value of applying the evolutionary frameworks of phenotypic plasticity and reaction norms to immunology. Because standardized laboratory environments are vastly different from the conditions under which populations evolved, we hypothesize that immunology might presently be missing important phenotypic variation and even focusing on dysregulated molecular and cellular processes. Modest adjustments to study designs could make model organism immunology more productive, reproducible, and reflective of human physiology.

Colonial breeding impacts potentially fitness-relevant cognitive processes in barn swallows.

Many animals breed colonially, often in dense clusters, representing a complex social environment with cognitive demands that could ultimately impact individual fitness. However, the effects of social breeding on the evolution of cognitive processes remain largely unknown. We tested the hypothesis that facultative colonial breeding influences attention and decision-making. Barn swallows (Hirundo rustica) breed in solitary pairs or in a range of colony sizes, up to dozens of pairs. We tested for selective attention to social information with playbacks of conspecific alarm calls and for decision-making with simulated predator intrusions, across a range of colony sizes from 1 to 33 pairs. We also evaluated the adaptive value of both processes by measuring seasonal reproductive success. Swallows breeding in larger colonies were more selective in their attention to social information. Birds breeding in larger colonies were also less risk averse, deciding to return more quickly to their nests after a predator approach paradigm. Finally, birds that showed higher selective attention hatched more eggs and birds that returned to their nests more quickly after a predator intrusion had more nestlings. Although we cannot fully attribute these fitness outcomes to the cognitive measures considered in this study, our results suggest that social breeding plays a role in adaptively shaping both the acquisition of social information and decision-making.

Plumage and eggshell colouration covary with the level of sex-specific parental contributions to nest building in birds.

Interspecific variation in sex-specific contributions to prenatal parental care, including avian nest building, is becoming increasingly better understood as we amass more information on more species. We examined whether sex-specific nest building contributions covary with the colouration of parents and their eggs in 521 species of Western Palearctic birds. Having colourful plumage and laying colourful eggs are costly because of the deposition of pigments in feathers and eggs and/or forming costly nanostructural substrates in feathers, and so it might be expected that those costs covary with the costs of nest building at the level of individuals and/or across species to produce of a suite of codivergent traits. Using a phylogenetically informed approach, we tested the hypothesis that species in which females alone invest energy building nests exhibit less sexual plumage dichromatism. However, we found comparative support for the opposite of this prediction. We then tested that species in which females alone build nests lay more colourful, and costlier, eggs because the dual costs of building nests and laying colourful eggs can only be borne by higher quality individuals. As expected, we found that species in which females build nests alone or together with males are more likely to lay colourfully pigmented eggs relative to species in which only males build nests. Finally, stochastic character mapping provided evidence of the repeated evolution of female-only nest building. Interspecific sex differences in plumage colouration therefore covary in a complex manner with female pre- (nest building) and post-copulatory (egg production) investment in reproduction.

Decision rules for egg-color-based rejection by two cavity-nesting hosts of the brown-headed cowbird.

Hosts of obligate avian brood parasites often evolve defense mechanisms to avoid rearing unrelated young. One common defense is egg rejection, for which hosts often rely on eggshell color. Most research has assumed that hosts respond to perceived color differences between their own eggs and parasite eggs regardless of the particular color; however, recent experiments have found that many hosts respond more strongly to brown foreign eggs than to equally dissimilar blue eggs. Yet, none of these prior studies tested a brown-egg-laying species and, with only one exception, all were conducted in open nests where light levels are considered sufficient for effective color-based egg discrimination. Here, we explored how two cavity-nesting hosts of the parasitic brown-headed cowbird (Molothrus ater) - the blue-egg-laying eastern bluebird (Sialia sialis) and the brown-egg-laying house wren (Troglodytes aedon) - respond to experimental eggs painted six distinct colors ranging from blue to brown. Rejection responses of both hosts were best predicted by perceived differences in color between the model egg and their own eggs. Specifically, we found that house wrens preferentially rejected eggs bluer than their own eggs. However, although we found that bluebirds relied on perceived differences in color for their egg rejection decisions, further tests are needed to determine whether they preferentially rejected brown eggs or simply responded to absolute perceived differences in color. These findings demonstrate that these cavity-nesting birds treat perceived color differences in distinct ways, which has important implications on the coevolutionary arms races and the interpretation of avian-perceived color differences.

Following the feeder: A global synthesis of disturbance-based foraging associations of birds.

Species interactions link animal behaviour to community structure and macroecological patterns of biodiversity. One common type of trophic species interaction is disturbance foraging-the act of obtaining food at a disturbance created by another organism. Disturbance foraging is widespread across the animal kingdom, especially among birds, yet previous research has been largely anecdotal and we still lack a synthetic understanding of how this behaviour varies geographically, phylogenetically and ecologically. To address these gaps, we conducted a comprehensive literature review to test focal hypotheses about disturbance foraging behaviour in birds. We found that avian disturbance foraging was geographically ubiquitous, occurring in both aquatic and terrestrial habitats across six continents and four oceans. Consistent with predictions based on established species diversity gradients in different habitat types, the majority of terrestrial observations occurred at tropical latitudes, whereas aquatic observations took place most frequently in temperate marine waters. Although disturbance foraging was widespread across the avian phylogeny, contrary to our prediction, the behaviour was also conserved phylogenetically (Pagel's λ = 0.7) and clustered within suboscine landbirds in terrestrial environments and seabirds in aquatic environments. Similarly, although disturbers were taxonomically diverse as we predicted, interactions were unexpectedly dominated by swarm-raiding ants in terrestrial environments and cetaceans in aquatic environments. Diet and body mass were also important predictors of disturbance foraging associations: Responders followed disturbers with similar diets and larger body sizes. Overall, our hypothesis-testing framework provides insight into the importance of geography, phylogeny and ecology as predictors of disturbance foraging behaviour. We anticipate that this comprehensive assessment of disturbance foraging will serve to generate additional hypotheses and spark future research and management considerations about this fascinating but poorly studied suite of species interactions, especially as biotic interactions face unprecedented risks in our rapidly changing world.

What's the rumpus? Resident temperate forest birds approach an unfamiliar neotropical alarm call across three continents.

Alarm signals have evolved to communicate pertinent threats to conspecifics, but heterospecifics may also use alarm calls to obtain social information. In birds, mixed-species flocks are often structured around focal sentinel species, which produce reliable alarm calls that inform eavesdropping heterospecifics about predation risk. Prior research has shown that Neotropical species innately recognize the alarm calls of a Nearctic sentinel species, but it remains unclear how generalizable or consistent such innate signal recognition of alarm-calling species is. We tested for the responses to the alarm calls of a Neotropical sentinel forest bird species, the dusky-throated antshrike (Thamnomanes ardesiacus), by naive resident temperate forest birds across three continents during the winter season. At all three sites, we found that approaches to the Neotropical antshrike alarm calls were similarly frequent to the alarm calls of a local parid sentinel species (positive control), while approaches to the antshrike's songs and to non-threatening columbid calls (negative controls) occurred significantly less often. Although we only tested one sentinel species, our findings indicate that temperate forest birds can recognize and adaptively respond globally to a foreign and unfamiliar tropical alarm call, and suggest that some avian alarm calls transcend phylogenetic histories and individual ecological experiences.

Coloniality and development impact intraclutch consistency of avian eggs: a comparative analysis of the individual repeatability of eggshell size and shape metrics.

In oviparous animals, egg morphology is considered an aspect of the extended phenotype of the laying mother and, thus, can be directly assessed for consistency both within and between individual females. Despite a recently renewed interest in the evolution and mechanics of avian eggshell morphology, we still lack a large-scale, comparative understanding of which egg traits are individually plastic and whether individual consistency is shaped by ecological and life history traits at the species level. Here, we aimed to understand whether intraclutch repeatability per se of different eggshell metrics is an evolving trait that responds to selection pressures from socio-ecological contexts across a diverse group of avian species for which clutch-level eggshell morphology data were available to us. Coloniality, ontogeny, and incubation period had significant impacts on the comparative patterns of relative individual repeatability among two egg metrics (i.e., size and shape), whereas other life history traits (including adult size, clutch size, nest type, migration, breeding latitude, host status of brood parasitism) did not have statistical impacts. Our results also demonstrate that individual consistency has a more widespread phylogenetic distribution than expected by evolutionary contingency across avian diversity. Future analyses should also incorporate the effects of intra- and interspecific covariation in other morphological and physiological traits on the evolution of individual consistency, especially those relevant to egg recognition, including eggshell color and maculation.

Female red-winged blackbirds (Agelaius phoeniceus) do not alter nest site selection, maternal programming, or hormone-mediated maternal effects in response to perceived nest predation or brood parasitism risk.

Predation or brood parasitism risks can change the behaviors and reproductive decisions in many parental animals. For oviparous species, mothers can mitigate their reproductive success in at least three ways: (1) by avoiding nest sites with high predation or parasitism risks, (2) through hormonal maternal effects that developmentally prime offspring for survival in risky environments, or (3) by investing less in reproduction when predation or parasitism risks are high. Here, we tested if perceived predation and parasitism risks can induce any of these behavioral or physiological responses by exposing female red-winged blackbirds (Agelaius phoeniceus) to playbacks of two major nest threats, a predator (Cooper's hawk, Accipiter cooperii) and an obligate brood parasite (brown-headed cowbird; Molothrus ater), as well as two controls (harmless Eastern meadowlark, Sturnella magna; and silence). We found that female blackbirds did not avoid nesting at sites treated with predator or brood parasite playbacks, nor were females more likely to abandon nesting attempts at these sites. Egg size and yolk hormone profiles, which are common proxies for maternal investment in oviparous species, were statistically similar across treatment sites. Instead, we found intraclutch variation in yolk steroid hormone profiles: concentrations of three progestogens (pregnanedione, 17α-hydroxypregnenolone, and deoxycorticosterone) and two androgens (testosterone and androstenedione) were higher in third-laid than first-laid eggs. Our study largely confirms previous findings of consistent intraclutch yolk hormone variation in this species, in birds in general, and in other oviparous lineages, but uniquely reports on several yolk steroid hormones largely overlooked in the literature on hormone-mediated maternal effects.

The overlooked complexity of avian brood parasite-host relationships.

The relationships between avian brood parasites and their hosts are widely recognised as model systems for studying coevolution. However, while most brood parasites are known to parasitise multiple species of host and hosts are often subject to parasitism by multiple brood parasite species, the examination of multispecies interactions remains rare. Here, we compile data on all known brood parasite-host relationships and find that complex brood parasite-host systems, where multiple species of brood parasites and hosts coexist and interact, are globally commonplace. By examining patterns of past research, we outline the disparity between patterns of network complexity and past research emphases and discuss factors that may be associated with these patterns. Drawing on insights gained from other systems that have embraced a multispecies framework, we highlight the potential benefits of considering brood parasite-host interactions as ecological networks and brood parasitism as a model system for studying multispecies interactions. Overall, our results provide new insights into the diversity of these relationships, highlight the stark mismatch between past research efforts and global patterns of network complexity, and draw attention to the opportunities that more complex arrangements offer for examining how species interactions shape global patterns of biodiversity.

Niche construction through a Goldilocks principle maximizes fitness for a nest-sharing brood parasite.

Generalist brood parasites that share nests with host nestlings can optimize resource acquisition from host parents by balancing the benefits that host nest-mates provide, including attracting increased provisions to the nest, against the costs of competing with the same host young over foster parental resources. However, it is unclear how parasitic chicks cope when faced with more nest-mates than are optimal for their survival upon hatching. We suggest that, in the obligate brood parasitic brown-headed cowbird (Molothrus ater), chicks use a niche construction strategy and reduce larger, more competitive host broods to maximize the parasites' survival to fledging. We experimentally altered brood sizes to test for Goldilocks principle patterns (i.e. a 'just right' intermediate brood size) of cowbird survival in nests of prothonotary warbler (Protonotaria citrea) hosts. We found that intermediate brood sizes of two host nestlings maximized cowbird fledging success relative to 0 or 4 host nest-mates at hatching. Specifically, cowbird nestlings lowered host brood sizes towards this optimum when placed in broods with more host nestlings. The results suggest that cowbirds reduce, but do not eliminate, host broods as a niche construction mechanism to improve their own probability of survival.

Pressure for rapid and accurate mate recognition promotes avian-perceived plumage sexual dichromatism in true thrushes (genus: Turdus).

Ecological conditions limiting the time to find a compatible mate or increasing the difficulty in doing so likely promote the evolution of traits used for species and mate recognition. In addition to interspecific character displacement signalling species identity, intraspecific traits that signal an individual's sex and breeding status reduce the challenge of identifying a compatible conspecific mate and should be more common in migratory rather than sedentary species, species with shorter breeding seasons and species breeding under high sympatry with many closely related heterospecifics. Here, we tested this recognition hypothesis for promoting plumage sexual dichromatism in the true thrushes (Turdus spp.), a large and diverse genus of passerine birds. We used receptor-noise limited models of avian vision to quantify avian-perceived chromatic and achromatic visual contrasts between male and female plumage patches and tested the influence of breeding season length, spatial distribution and sympatry with other Turdus species on plumage dichromatism. As predicted, we found that (1) true thrush species with migratory behaviour have greater plumage sexual dichromatism than non-migratory species, (2) species with longer breeding seasons have less plumage sexual dichromatism, and (3) greater numbers of Turdus thrush species breeding in sympatry is associated with more plumage sexual dichromatism. These results suggest that social recognition systems, including species and mate recognition, play a prominent role in the evolution of plumage sexual dichromatism in true thrushes.

Non-invasive elevation of circulating corticosterone increases the rejection of foreign eggs in female American robins (Turdus migratorius).

Avian obligate brood parasites rely on other species to raise their offspring. In turn, many brood parasite hosts have evolved defensive behaviors to reduce the costs of brood parasitism, yet the proximate bases underlying these defenses remain poorly understood. Recent studies regarding the potential endocrine mechanisms of foreign-egg rejection have implicated corticosterone as a physiological mediator of anti-parasitic defenses. For example, corticosterone is elevated in response to non-mimetic eggs in an egg rejecter thrush, the Eurasian blackbird (Turdus merula) and this hormone's suppression reduces egg rejection rates in the congeneric American robin (T. migratorius). American robins are also among the few host species of obligate brood parasitic brown-headed cowbirds (Molothrus ater) that readily reject foreign eggs from their nests. We non-invasively elevated corticosterone levels in incubating female robins by dissolving it in DMSO gel which was then applied onto eggs already in the clutch. Relative to controls treated with pure DMSO gel, corticosterone-treated female robins were more likely to reject a non-mimetic, cowbird-sized foreign egg (72 %) than control females (50 %) when accounting for the known effect of lower clutch sizes on greater egg rejection. Future studies are needed to assess the sensory and cognitive impact(s) of corticosterone, as well as other hormones essential for parental care, in this and other hosts' defense behaviors against avian brood parasitism.

Eggshell texture but not odor treatment affects model egg rejection in American robins (Turdus migratorius).

To curb fitness costs associated with obligate avian brood parasitism, some hosts have evolved to reject foreign eggs in the nest. American robins (Turdus migratorius) are among the few hosts of the brown-headed cowbird (Molothrus ater) that mostly remove parasitic eggs from their nests. With the parasite's eggs looking nothing like their own, American robins likely rely most on visual cues when making rejection decisions. However, we still know little about the roles that tactile and olfactory cues play in robin's or other rejecter hosts' rejection decisions. Here, we conducted a set of experiments to test for the use of tactile or olfactory cues in egg rejection by robins. For the tactile experiment, we found that robins were more likely to reject rough rather than smooth eggs. However, our tactile model egg design was not able to fully discriminate between tactile and visual sensory modalities. In the olfaction experiment, we did not find a significant effect of egg scent treatment on rejection rates. Accordingly, future studies on egg rejection should attempt to fully distinguish between tactile and visual cues, as well as examine olfactory cues in other egg rejecter host species.

Host community-wide patterns of post-fledging behavior and survival of obligate brood parasitic brown-headed cowbirds.

The antagonistic arms races between obligate brood parasites and their hosts provide critical insights into coevolutionary processes and constraints on the evolution of life history strategies. In avian brood parasites-a model system for examining host-parasite dynamics-research has primarily focused on the egg and nestling stage, while far less is known about the behavior and ecology of fledgling and juvenile brood parasites. To provide greater insights into the post-fledging period of generalist brood parasites, we used handheld and automated telemetry systems to examine the behavior and survival of fledgling brown-headed cowbirds (Molothrus ater). Our host community-wide analysis (data on cowbirds fledged from different host species were pooled) shows that fledgling cowbirds' follow patterns of movement and survival found across the post-fledging literature on parental passerine species. Cowbird fledgling survival was lowest during the first 3 days post-fledging, whereas daily rates of survival neared 100% after about 16 days post-fledging. Cowbird daytime post-fledging activity rates, perch heights, and distance from the natal area all increased with fledging age and young generally gained independence from host parents at 3-4 weeks post-fledging, with approximately the same latency as has been observed in studies on fledglings of cowbird host species. Our research demonstrates how automated telemetry systems can overcome past methodological limitations in post-fledging research and provides an important foundation for future studies examining adaptations that cowbirds and other brood parasites use to exploit hosts during the post-fledging period.

Embryo movement is more frequent in avian brood parasites than birds with parental reproductive strategies.

Movement of the embryo is essential for musculoskeletal development in vertebrates, yet little is known about whether, and why, species vary. Avian brood parasites exhibit feats of strength in early life as adaptations to exploit the hosts that rear them. We hypothesized that an increase in embryonic movement could allow brood parasites to develop the required musculature for these demands. We measured embryo movement across incubation for multiple brood-parasitic and non-parasitic bird species. Using a phylogenetically controlled analysis, we found that brood parasites exhibited significantly increased muscular movement during incubation compared to non-parasites. This suggests that increased embryo movement may facilitate the development of the stronger musculoskeletal system required for the demanding tasks undertaken by young brood parasites.

Nest substrate and tool shape significantly affect the mechanics and energy requirements of avian eggshell puncture.

Some host species of avian obligate brood parasites reject parasitic eggs from their nest whereas others accept them, even though they recognize them as foreign. One hypothesis to explain this seemingly maladaptive behavior is that acceptors are unable to pierce and remove the parasitic eggshell. Previous studies reporting on the force and energy required to break brood parasites' eggshells were typically static tests performed against hard substrate surfaces. Here, we considered host nest as a substrate to simulate this potentially critical aspect of the natural context for egg puncture while testing the energy required to break avian eggshells. Specifically, as a proof of concept, we punctured domestic chicken eggs under a series of conditions: varying tool shape (sharp versus blunt), tool dynamics (static versus dynamic) and the presence of natural bird nests (of three host species). The results show a complex set of statistically significant interactions between tool shapes, puncture dynamics and nest substrates. Specifically, the energy required to break eggs was greater for the static tests than for the dynamic tests, but only when using a nest substrate and a blunt tool. In turn, in the static tests, the addition of a nest significantly increased energy requirements for both tool types, whereas during dynamic tests, the increase in energy associated with the nest presence was significant only when using the sharp tool. Characterizing the process of eggshell puncture in increasingly naturalistic contexts will help in understanding whether and how hosts of brood parasites evolve to reject foreign eggs.

How to build a puncture- and breakage-resistant eggshell? Mechanical and structural analyses of avian brood parasites and their hosts.

Evolved eggshell strength is greater in several lineages of obligate avian brood parasites (birds that lay their eggs in other species' nests) than in their hosts. Greater strength is typically indirectly implied by eggshell thickness comparisons between parasites and hosts. Nevertheless, there is strong evidence that the eggshell structural organization differentially influences its mechanical properties. Using instrumental puncture tests and SEM/EBSD and XRD techniques, we studied the most relevant eggshell mechanical, textural, ultrastructural and microstructural features between several host species and their parasitic cowbirds (Molothrus spp.). These parasitic species display different egg-destructive behaviors, reducing host reproductive fitness, including the more frequently host-egg puncturing M. rufoaxillaris and M. bonariensis, and the host egg-removing M. ater. The results, analyzed using a phylogenetic comparative approach, showed interspecific patterns in the mechanical and structural features. Overall, the eggshells of the two egg-puncturing parasites (but not of M. ater) were stronger, stiffer and required greater stress to produce a fracture than the respective hosts' eggs. These features were affected by eggshell microstructure and ultrastructure, related to the increase in the intercrystalline boundary network acting in cooperation with the increase in palisade layer thickness. Both structural features generate more options and greater lengths of intercrystalline paths, increasing the energy consumed in crack or fissure propagation. The reported patterns of all these diverse eggshell features support a new set of interpretations, confirming several hypotheses regarding the impact of the two reproductive strategies (parasitic versus parental) and parasitic egg destruction behaviors (more versus less frequently puncturing).