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.

Highly virulent avian brood-parasitic species show elevated embryonic metabolic rates at specific incubation stages compared to less virulent and non-parasitic species.

As the avian embryo grows and develops within the egg, its metabolic rate gradually increases. Obligate avian brood-parasitic birds lay their eggs in the nests of other species to avoid the costs of parental care, and all but one of these brood-parasitic species are altricial at hatching. Yet the chicks of some altricial brood-parasitic species perform the physically demanding task of evicting, stabbing or otherwise killing host progeny within days of hatching. This implies a need for high metabolic rates in the embryo, just as precocial species require. Using flow-through respirometry in situ, we investigated embryonic metabolic rates in diverse avian brood parasite lineages which either kill host offspring (high virulence) or share the nest with host young (low virulence). High-virulence brood parasite embryos exhibited higher overall metabolic rates than both non-parasitic (parental) species and low-virulence parasites. This was driven by significantly elevated metabolic rates around the halfway point of incubation. Additionally, a fine-scale analysis of the embryos of a host-parasitic pair showed faster increases in metabolic rates in the parasite. Together these results suggest that the metabolic patterns of the embryos of high-virulence parasites facilitate their early-life demands.

The evolution of social parasitism in Formica ants revealed by a global phylogeny.

Studying the behavioral and life history transitions from a cooperative, eusocial life history to exploitative social parasitism allows for deciphering the conditions under which changes in behavior and social organization lead to diversification. The Holarctic ant genus Formica is ideally suited for studying the evolution of social parasitism because half of its 172 species are confirmed or suspected social parasites, which includes all three major classes of social parasitism known in ants. However, the life history transitions associated with the evolution of social parasitism in this genus are largely unexplored. To test competing hypotheses regarding the origins and evolution of social parasitism, we reconstructed a global phylogeny of Formica ants. The genus originated in the Old World ∼30 Ma ago and dispersed multiple times to the New World and back. Within Formica, obligate dependent colony-founding behavior arose once from a facultatively polygynous common ancestor practicing independent and facultative dependent colony foundation. Temporary social parasitism likely preceded or arose concurrently with obligate dependent colony founding, and dulotic social parasitism evolved once within the obligate dependent colony-founding clade. Permanent social parasitism evolved twice from temporary social parasitic ancestors that rarely practiced colony budding, demonstrating that obligate social parasitism can originate from a facultative parasitic background in socially polymorphic organisms. In contrast to permanently socially parasitic ants in other genera, the high parasite diversity in Formica likely originated via allopatric speciation, highlighting the diversity of convergent evolutionary trajectories resulting in nearly identical parasitic life history syndromes.

Brood Parasites That Care: Alternative Nesting Tactics in a Subsocial Wasp.

AbstractHosts and brood parasites are a classic example of conflict. Parasites typically provide no offspring care after laying eggs, imposing costs on hosts. Female subsocial wasps (Ammophila pubescens) alternate between initiating their own nests and using an "intruder" tactic of replacing eggs in nests of unrelated conspecifics. Hosts can respond by substituting new eggs of their own, with up to eight reciprocal replacements. Remarkably, intruders usually provision offspring in host nests, often alongside hosts. We used field data to investigate why intruders provision and to understand the basis of interactions. We found that intruders could not increase their fitness payoffs by using the typical brood parasite tactic of not provisioning offspring. Intruders using the typical tactic would benefit when hosts provisioned in their stead, but their offspring would starve when hosts failed to provision. Although some hosts obtained positive payoffs when intruders mistakenly provisioned their offspring, on average utilizing a conspecific nest represents parasitism: hosts pay costs while intruders benefit. Hosts and intruders used the same tactic of egg replacement, but intruders more often laid the final egg. Selection should favor better discrimination of offspring, which could lead to repeated cycles of costly egg replacement.

When perfection isn't enough: host egg signatures are an effective defence against high-fidelity African cuckoo mimicry.

Most mimicry systems involve imperfect mimicry, whereas perfect and high-fidelity mimicry are rare. When the fidelity of mimicry is high, mimics might be expected to have the upper hand against their antagonists. However, in coevolving systems, diversification of model phenotypes may provide an evolutionary escape, because mimics cannot simultaneously match all model individuals in the population. Here we investigate high-fidelity mimicry in a highly specialized, Afrotropical brood parasite-host system: the African cuckoo and fork-tailed drongo. Specifically, we test whether host egg polymorphisms are an effective defence against such mimicry. We show, using a combination of image analysis, field experiments and simulations, that: (1) egg colour and pattern mimicry of fork-tailed drongo eggs by African cuckoos is near-perfect on average; (2) drongos show fine-tuned rejection of foreign eggs, exploiting unpredictable pattern differences between parasitic eggs and their own; and (3) the high degree of interclutch variation (polymorphic egg 'signatures') exhibited by drongos gives them the upper hand in the arms race, with 93.7% of cuckoo eggs predicted to be rejected, despite cuckoos mimicking the full range of drongo egg phenotypes. These results demonstrate that model diversification is a highly effective defence against mimics, even when mimicry is highly accurate.

Aggressive hosts are undeterred by a cuckoo's hawk mimicry, but probably make good foster parents.

Parasites face a trade-off if the highest quality hosts are also most resistant to exploitation. For brood parasites, well-defended host nests may be both harder to parasitize and harder to predate, leading to better survival of parasitic chicks. This trade-off could be accentuated if brood-parasitic adaptations to reduce front-line defences of hosts, such as mimicry of hawks by Cuculus cuckoos, do not deter hosts which aggressively mob raptors. Here we investigate the costs and benefits to the African cuckoo (Cuculus gularis) of specializing on a highly aggressive host species, the fork-tailed drongo (Dicrurus adsimilis). Field experiments showed that drongos strongly attacked and mobbed both cuckoo and hawk models, implying that hawk mimicry does not deter front-line defences against African cuckoos. Attacks on cuckoo and hawk models generally declined after the egg stage but attacks on snake models sharply increased, suggesting drongos may treat hawks more like cuckoos than predators. We suggest that the cost to cuckoos of parasitizing an aggressive host may be alleviated by subsequent benefits to their offspring, since drongo nests survived better than nests of other species with similar nesting ecology. These results are indicative of a trade-off between host quality and susceptibility for a brood parasite.

Imprinting in an interspecific brood parasitic bird.

Many animals learn to recognize conspecifics after an early experience with them through sexual imprinting. For brood parasitic birds, it is not possible to develop conspecific recognition using cues provided by their foster parents. One solution is that a unique species-specific signal triggers the learning of additional aspects of the conspecific's phenotype. It has been proposed that for brood parasitic cowbirds, this signal is an innate vocalization, the chatter. This vocalization might act in a cross-modal learning process through which juveniles that listen to the song learn to recognize the visual characteristics of the song's producer. We trained two groups of juvenile shiny cowbirds (Molothrus bonariensis). In one group, individuals listened to the chatter or a heterospecific call while they observed a stuffed model of the corresponding species. In the other group, individuals listened to the call of one species (cowbird or heterospecific) while they observed the stuffed model of the other species. In the preference test, juveniles chose the model associated with the chatter, regardless of whether the model was a cowbird or a heterospecific. These results show how the auditory system through a species-specific signal can lead to cross-modal learning of visual cues allowing conspecific recognition in brood parasitic cowbirds.

Revealing the roles of egg darkness and nest similarity for a cryptic parasite egg versus host's cognition: an alternate coevolutionary trajectory.

As a text-book example of coevolution, the escalating interactions between egg mimicry by parasitic cuckoos and egg recognition by their hosts constitute a key battlefield for parasitism and anti-parasitism strategies. However, some parasite-host systems have deviated from this coevolutionary trajectory because some cuckoos do not lay mimetic eggs, while the hosts do not recognize them, even under the high costs of parasitism. The cryptic egg hypothesis was proposed to explain this puzzle, but the evidence to date is mixed and the relationship between the two components of egg crypticity, egg darkness (dim egg coloration) and nest similarity (similarity to host nest appearance), remains unknown. Here, we developed a 'field psychophysics' experimental design to dissect these components while controlling for undesired confounding factors. Our results clearly show that both egg darkness and nest similarity of cryptic eggs affect recognition by hosts, and egg darkness plays a more influential role than nest similarity. This study provides unambiguous evidence to resolve the puzzle of absent mimicry and recognition in cuckoo-host systems and explains why some cuckoo eggs were more likely to evolve dim coloration rather than similarity to host eggs or host nests.

Experimental evidence that cuckoos choose host nests following an egg matching strategy.

The arms race between brood parasites and their hosts provides a classic model to study coevolution. Hosts often reject the parasitic egg, and brood parasites should therefore select host nests in which the colour of the eggs best matches that of their own. Although this hypothesis has received some support, direct experimental evidence is still lacking. Here, we report on a study of Daurian redstarts, which show a distinct egg-colour dimorphism, with females laying either blue or pink eggs. Redstarts are often parasitized by common cuckoos, which lay light blue eggs. First, we showed that cuckoo eggs were more similar in spectral reflectance to the blue than to the pink redstart egg morph. Second, we report that the natural parasitism rate was higher in blue than in pink host clutches. Third, we performed a field experiment in which we presented a dummy clutch of each colour morph adjacent to active redstart nests. In this set-up, cuckoos almost always chose to parasitize a blue clutch. Our results demonstrate that cuckoos actively choose redstart nests in which the egg colour matches the colour of their own eggs. Our study thus provides direct experimental evidence in support of the egg matching hypothesis.

Lack of host specialization despite selective host use in brood parasitic cuckoo catfish.

Host-parasite dynamics involve coevolutionary arms races, which may lead to host specialization and ensuing diversification. Our general understanding of the evolution of host specialization in brood parasites is compromised by a restricted focus on bird and insect lineages. The cuckoo catfish (Synodontis multipunctatus) is an obligate parasite of parental care of mouthbrooding cichlids in Lake Tanganyika. Given the ecological and taxonomic diversity of mouthbrooding cichlids in the lake, we hypothesized the existence of sympatric host-specific lineages in the cuckoo catfish. In a sample of 779 broods from 20 cichlid species, we found four species parasitized by cuckoo catfish (with prevalence of parasitism of 2%-18%). All parasitized cichlids were from the tribe Tropheini, maternal mouthbrooders that spawn over a substrate (rather than in open water). Phylogenetic analysis based on genomic (ddRAD sequencing) and mitochondrial (Dloop) data from cuckoo catfish embryos showed an absence of host-specific lineages. This was corroborated by analyses of genetic structure and co-ancestry matrix. Within host species, parasitism was not associated with any individual characteristic we recorded (parent size, water depth), but was costly as parasitized parents carried smaller clutches of their own offspring. We conclude that the cuckoo catfish is an intermediate generalist and discuss costs, benefits and constraints of host specialization in this species and brood parasites in general.

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.

Eggshell spots are an important cue for the egg retrieval behavior in two tit species.

It is a common occurrence for incubating female ground- or cavity-nesting birds to accidentally roll their own eggs out of the nest cup. To correctly roll eggs that are not in the nest cup back to the nest, birds must be able to discriminate between their eggs and things around their nests that could be easily confused for their eggs (e.g., egg-shaped stones or other birds' eggs). Moreover, there may be a strong interaction between egg retrieval and egg rejection behaviors in the context of avian brood parasitism where recognition and rejection of alien eggs is an effective means for hosts to defend against cuckoo parasitism. It has been shown that green-backed tits (Parus monticolus) and Japanese tits (P. minor) in China have strong egg recognition ability and are able to reject nonmimetic eggs in the nest. Eggshell spots play an essential role in the egg rejection behavior of these two tit hosts. This study investigated the egg retrieval behavior of green-backed tits and Japanese tits by adding one experimental egg to the nest corner to explore whether eggshell spots also play a role in the process of egg retrieval. The results revealed significant differences in the retrieval rates of white-rumped munia (Lonchura striata) eggs painted with spots, Japanese tits' own true eggs, and unpainted, pure white-white-rumped munia eggs. The retrieval rate of white-white-rumped munia eggs was significantly lower than that of spotted white-rumped munia eggs and Japanese tits' own spotted eggs. For green-backed tits, the retrieval rate of spotted white-rumped munia eggs in the nest corner was significantly higher than that of pure white-white-rumped munia eggs, while the rejection rate of spotted white-rumped munia eggs was significantly lower than that of pure white-white-rumped munia eggs. These findings indicate that eggshell spots play a key role in the egg retrieval of green-backed tits and Japanese tits.

Co-parasitism in the face of predation: Effects of natural enemies on a neotropical mockingbird.

Co-parasitism is ubiquitous and has important consequences for the ecology and evolution of wild host populations. Studies of parasite co-infections remain limited in scope, with few experimental tests of the fitness consequences of multiple parasites, especially in natural populations. We measured the separate and combined effects of Philornis seguyi nest flies and shiny cowbirds Molothrus bonariensis on the fitness of a shared host, the chalk-browed mockingbird (Mimus saturninus) in Argentina. Using a two-factor experimental approach, we manipulated the presence of nest flies and cowbirds in mockingbird nests and assessed their effects on mockingbird haemoglobin levels, begging and provisioning rates, body size, and fledging success. We also monitored rates of nest predation in relation to parasitism by flies and cowbirds. Nest flies reduced the haemoglobin concentration, body size, and fledging success of mockingbirds, likely because mockingbirds did not compensate for parasitism by begging more or feeding their nestlings more. Cowbirds also reduced the fledging success of mockingbirds, even though they had no detectable effect on haemoglobin or body size. Nests with cowbirds, which beg more than mockingbirds, attracted more nest predators. There was no significant interaction between the effects of flies and cowbirds on any component of mockingbird fitness. The combined effects of nest flies and cowbirds were strictly additive. In summary, we show that nest flies and cowbirds both reduce host fitness, but do not have interactive effects in co-parasitized nests. Our results further suggest that predators exacerbate the effects of nest flies and cowbirds on their hosts. Our study shows that the fitness consequences of co-parasitism are complex, especially in the context of community-level interactions.

El co-parasitismo es ubicuo y tiene consecuencias importantes para la ecología y la evolución de las poblaciones de hospedadores silvestres. Los estudios de coinfecciones por parásitos poseen un alcance limitado, con pocos trabajos experimentales que analicen las consecuencias del parasitismo múltiple sobre la eficacia biológica, especialmente en poblaciones naturales. Medimos los efectos separados y combinados de las moscas de los nidos Philornis seguyi y el tordo renegrido (Molothrus bonariensis) sobre la eficacia biológica de un hospedador compartido, la calandria grande (Mimus saturninus) en Argentina. Utilizando un enfoque experimental de dos factores, manipulamos la presencia de moscas de nido y tordos en los nidos de calandrias y evaluamos sus efectos sobre los niveles de hemoglobina, las tasas de solicitud de alimento y aprovisionamiento, el tamaño corporal y el éxito de supervivencia de los pichones de calandria. También monitoreamos las tasas de depredación de nidos en relación con el parasitismo de moscas y tordos. Las moscas de los nidos redujeron la concentración de hemoglobina, el tamaño corporal y el éxito de supervivencia de los pichones de calandrias, probablemente porque las calandrias no compensaron el parasitismo solicitando más alimento o alimentando más a sus pichones. Los tordos también redujeron el éxito de supervivencia de las calandrias, aunque no tuvieron un efecto detectable sobre la hemoglobina o el tamaño corporal. Los nidos con tordos, quienes solicitaron más alimento más que las calandrias, atrajeron a más depredadores de nidos. El aumento de la depredación de nidos asociado a la alta intensidad de solicitud de alimento puede explicar por qué las calandrias en Argentina no solicitan más alimento en respuesta al parasitismo de las moscas. No hubo una interacción significativa entre los efectos de las moscas y los tordos en ningún componente de la eficacia biológica de las calandrias. Los efectos combinados de las moscas de los nidos y los tordos fueron estrictamente aditivos. En resumen, mostramos que las moscas de los nidos y los tordos reducen la eficacia biológica del hospedador, pero no tienen efectos interactivos en los nidos co-parasitados. Nuestros resultados sugieren además que los depredadores exacerban los efectos de las moscas de los nidos y los tordos sobre sus hospedadores. Nuestro estudio muestra que las consecuencias del co-parasitismo sobre la eficacia biológica son complejas, especialmente en el contexto de las interacciones a nivel comunitario.

Eggshell colour differences in a classic example of coevolved eggshell mimicry.

Avian brood parasitism is a model system for understanding coevolutionary arms races, and the great reed warbler (Acrocephalus arundinaceus, hereafter 'warbler') and its parasite the common cuckoo (Cuculus canorus, hereafter 'cuckoo') are prime examples of this coevolutionary struggle. Here, warblers select for egg colour mimicry by rejecting poorly matched cuckoo eggs. Contrary to long-held assumptions, recent work showed that warblers tend to reject lighter and browner eggs but tended to accept darker and bluer eggs rather than basing rejection decisions solely on perceived colour differences (i.e. the degree of mimicry). This counterintuitive, colour-biased rejection behaviour would select for bluer and darker cuckoo eggs, but would only be adaptive if cuckoos were consistently lighter and browner than warbler eggs. Therefore, we tested whether warbler eggs were consistently bluer and darker than cuckoo eggs. To do so, we re-analysed eggshell reflectance spectra of warblers and the cuckoos that parasitized them in the Czech Republic. As expected, we found that warbler eggs were significantly bluer and darker than the cuckoo eggs at the population level. Thus, we demonstrate imperfect mimicry in a long-coevolved cuckoo host-race and provide insights for exploring the coevolutionary interactions among hosts and their brood parasites.

Combined measures of mimetic fidelity explain imperfect mimicry in a brood parasite-host system.

The persistence of imperfect mimicry in nature presents a challenge to mimicry theory. Some hypotheses for the existence of imperfect mimicry make differing predictions depending on how mimetic fidelity is measured. Here, we measure mimetic fidelity in a brood parasite-host system using both trait-based and response-based measures of mimetic fidelity. Cuckoo finches Anomalospiza imberbis lay imperfectly mimetic eggs that lack the fine scribbling characteristic of eggs of the tawny-flanked prinia Prinia subflava, a common host species. A trait-based discriminant analysis based on Minkowski functionals-that use geometric and topological morphometric methods related to egg pattern shape and coverage-reflects this consistent difference between host and parasite eggs. These methods could be applied to quantify other phenotypes including stripes and waved patterns. Furthermore, by painting scribbles onto cuckoo finch eggs and testing their rate of rejection compared to control eggs (i.e. a response-based approach to quantify mimetic fidelity), we show that prinias do not discriminate between eggs based on the absence of scribbles. Overall, our results support relaxed selection on cuckoo finches to mimic scribbles, since prinias do not respond differently to eggs with and without scribbles, despite the existence of this consistent trait difference.

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.

Extreme offspring ornamentation in American coots is favored by selection within families, not benefits to conspecific brood parasites.

Offspring ornamentation typically occurs in taxa with parental care, suggesting that selection arising from social interactions between parents and offspring may underlie signal evolution. American coot babies are among the most ornamented offspring found in nature, sporting vividly orange-red natal plumage, a bright red beak, and other red parts around the face and pate. Previous plumage manipulation experiments showed that ornamented plumage is favored by strong parental choice for chicks with more extreme ornamentation but left unresolved the question as to why parents show the preference. Here we explore natural patterns of variation in coot chick plumage color, both within and between families, to understand the context of parental preference and to determine whose fitness interests are served by the ornamentation. Conspecific brood parasitism is common in coots and brood parasitic chicks could manipulate hosts by tapping into parental choice for ornamented chicks. However, counter to expectation, parasitic chicks were duller (less red) than nonparasitic chicks. This pattern is explained by color variation within families: Chick coloration increases with position in the egg-laying order, but parasitic eggs are usually the first eggs a female lays. Maternal effects influence chick coloration, but coot females do not use this mechanism to benefit the chicks they lay as parasites. However, within families, chick coloration predicts whether chicks become "favorites" when parents begin control over food distribution, implicating a role for the chick ornamentation in the parental life-history strategy, perhaps as a reliable signal of a chick's size or age.

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.

Visual complexity of egg patterns predicts egg rejection according to Weber's law.

Visual complexity is ubiquitous in nature. Drivers of complexity include selection in coevolutionary arms races between antagonists. However, the causes and consequences of biological complexity and its perception are largely understudied, partly because complexity is difficult to quantify. Here, we address this by studying egg pattern complexity and its perception in hosts (tawny-flanked prinia Prinia subflava), which visually recognize and reject mimetic eggs of their virulent brood parasite (cuckoo finch Anomalospiza imberbis). Using field data and an optimization algorithm, we compute a complexity metric which predicts rejection of experimentally placed conspecific eggs in prinia nests. Real cuckoo finch eggs exhibit significantly lower pattern complexity than prinia eggs, suggesting that high complexity benefits hosts because it distinguishes host eggs from parasitic eggs. We show that prinias perceive complexity differences according to Weber's law of proportional processing (i.e. relative, rather than absolute, differences between stimuli are processed in discrimination, such that two eggs with simple patterns are more easily discriminable than two with complex patterns). This may influence coevolutionary trajectories of hosts and parasites. The new methods presented for quantifying complexity and its perception can help us to understand selection pressures driving the evolution of complexity and its consequences for species interactions.

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.