The Evolution of Predator Resemblance in Avian Brood Parasites

Predators have profound effects on prey behavior and some adult brood parasites use predator resemblance to exploit the antipredator defenses of their hosts. Clarifying host perception of such stimuli is important for understanding the adaptive significance of adult brood parasite characteristics, and the mechanisms by which they misdirect hosts. Here I review the literature to explore the adaptive basis of predator resemblance in avian brood parasites, and natural variation in host responses to these stimuli. I also provide a framework for the information ecology of predator resemblance, which is based on the principles of signal detection theory and draws from empirical evidence from the common cuckoo, Cuculus canorus, as the most widely studied system. In this species, visual and acoustic hawk-like stimuli are effective in manipulating host defenses. Overall, contrasts across host responses suggest that different modalities of information can have independent effects on hosts, and that predator resemblance takes advantage of multiple sensory and cognitive processes. Host perception of these stimuli and the degree to which they are processed in an integrated manner, and the physiological processes underlying regulation of the responses, present new avenues for brood parasitism research.

Host eyes, brains and their brood parasites

1. Brood parasites interact with their hosts for exploitation of host parental abilities and the associated resources. This results in coevolutionary interactions of hosts and parasites. 2. A prime example of such a common specialist brood parasite is the common cuckoo Cuculus canorus and its host races. Hosts use their cognitive abilities to identify parasites and vice versa for their ability to discriminate among potential hosts. 3. We predicted that parasites with relatively large brains for their body size should be more successful at avoiding their hosts, and that hosts with small brains for their body size should more often be exploited by parasites. We also predicted that hosts with relatively large eyes for their body size would have superior discriminatory abilities allowing for superior discrimination against brood parasites. Finally, we predicted that visual ability of specific cuckoo hosts would have evolved exaggerated visual ability as estimated from the relative size of their optic tectum would have resulted in such hosts being more successful as reflected by their higher rate of parasitism. 4. Interspecific variation in size of brain, eye, optic tectum, telencephalon and cerebellum were consistent with these predictions.

Could diffuse coevolution explain the generic eggshell color of the brown-headed cowbird?

The brown-headed cowbird (hereafter cowbird) is an avian brood parasite that produces an egg dissimilar to those produced by the majority of its diverse host community. The cowbird’s generic egg may result from a Jack-of-all-trades strategy; however, the evolutionary mechanisms that select for their generic eggs are unclear. Here we propose that the cowbird’s eggshell phenotypes have evolved via diffuse coevolution, which results from community-level selective pressures, rather than via pairwise coevolution that occurs between a particular host species and its brood parasite. Under diffuse coevolution the cowbird’s host community, with varying eggshell phenotypes and recognition abilities, would select for a cowbird eggshell phenotype intermediate to those of its host community. This selection is exerted by hosts that reject cowbird eggs, rather than those that accept them; therefore, we expect cowbird eggshell colors can be approximated by both the phenotypes and rejection abilities of their host community. Here we use eggshell reflectance data from 43 host species to demonstrate that the cowbird eggshell phenotypes are reasonably predicted (within 2 just noticeable differences) by the eggshell phenotypes and rejection rates of their hosts. These findings suggest that cowbird eggshell phenotypes, and potentially those of other some generalist parasites, may evolve via diffuse coevolution. Importantly, this research provides insight into the underlying evolutionary processes that explain observed phenotypic variation and provides a framework for studying selection on both specialist and generalist parasites' traits.

A Chromosome-Level Genome Assembly of the Reed Warbler (Acrocephalus scirpaceus)

The reed warbler (Acrocephalus scirpaceus) is a long-distance migrant passerine with a wide distribution across Eurasia. This species has fascinated researchers for decades, especially its role as host of a brood parasite, and its capacity for rapid phenotypic change in the face of climate change. Currently, it is expanding its range northwards in Europe, and is altering its migratory behaviour in certain areas. Thus, there is great potential to discover signs of recent evolution and its impact on the genomic composition of the reed warbler. Here we present a high-quality reference genome for the reed warbler, based on PacBio, 10X and Hi-C sequencing. The genome has an assembly size of 1,075,083,815 bp with a scaffold N50 of 74,438,198 bp and a contig N50 of 12,742,779 bp. BUSCO analysis using aves_odb10 as a model showed that 95.7% of BUSCO genes were complete. We found unequivocal evidence of two separate macrochromosomal fusions in the reed warbler genome, in addition to the previously identified fusion between chromosome Z and a part of chromosome 4A in the Sylvioidea superfamily. We annotated 14,645 protein-coding genes, and a BUSCO analysis of the protein sequences indicated 97.5% completeness. This reference genome will serve as an important resource, and will provide new insights into the genomic effects of evolutionary drivers such as coevolution, range expansion, and adaptations to climate change, as well as chromosomal rearrangements in birds.

Host and brood parasite coevolutionary interactions covary with comparative patterns of the avian visual system

In coevolutionary arms-races, reciprocal ecological interactions and their fitness impacts shape the course of phenotypic evolution. The classic example of avian host–brood parasite interactions selects for host recognition and rejection of increasingly mimetic foreign eggs. An essential component of perceptual mimicry is that parasitic eggs escape detection by host sensory systems, yet there is no direct evidence that the avian visual system covaries with parasitic egg recognition or mimicry. Here, we used eye size measurements collected from preserved museum specimens as a metric of the avian visual system for species involved in host–brood parasite interactions. We discovered that (i) hosts had smaller eyes compared with non-hosts, (ii) parasites had larger eyes compared with hosts before but not after phylogenetic corrections, perhaps owing to the limited number of independent evolutionary origins of obligate brood parasitism, (iii) egg rejection in hosts with non-mimetic parasitic eggs positively correlated with eye size, and (iv) eye size was positively associated with increased avian-perceived host–parasite eggshell similarity. These results imply that both host-use by parasites and anti-parasitic responses by hosts covary with a metric of the visual system across relevant bird species, providing comparative evidence for coevolutionary patterns of host and brood parasite sensory systems.

The neuroethology of avian brood parasitism

ABSTRACT Obligate brood-parasitic birds never build nests, incubate eggs or supply nestlings with food or protection. Instead, they leave their eggs in nests of other species and rely on host parents to raise their offspring, which allows the parasite to continue reproducing throughout the breeding season. Although this may be a clever fitness strategy, it is loaded with a set of dynamic challenges for brood parasites, including recognizing individuals from their own species while growing up constantly surrounded by unrelated individuals, remembering the location of potential host nests for successful reproduction and learning the song of their species while spending time being entirely surrounded by another species during a critical developmental period, a predicament that has been likened to being ‘raised by wolves’. Here, I will describe what we currently know about the neurobiology associated with the challenges of being a brood parasite and what is known about the proximate mechanisms of brood parasite evolution. The neuroethology of five behaviors (mostly social) in brood parasites is discussed, including: (1) parental care (or the lack thereof), (2) species recognition, (3) song learning, (4) spatial memory and (5) pair-bonding and mate choice. This Review highlights how studies of brood parasites can lend a unique perspective to enduring neuroethological questions and describes the ways in which studying brood-parasitic species enhances our understanding of ecologically relevant behaviors.

Referential alarm calling elicits future vigilance in a host of an avian brood parasite

Yellow warblers ( Setophaga petechia ) use referential ‘seet’ calls to warn mates of brood parasitic brown-headed cowbirds ( Molothrus ater ). In response to seet calls during the day, female warblers swiftly move to sit tightly on their nests, which may prevent parasitism by physically blocking female cowbirds from inspecting and laying in the nest. However, cowbirds lay their eggs just prior to sunrise, not during daytime. We experimentally tested whether female warblers, warned by seet calls on one day, extend their anti-parasitic responses into the future by engaging in vigilance at sunrise on the next day, when parasitism may occur. As predicted, daytime seet call playbacks caused female warblers to leave their nests less often on the following morning, relative to playbacks of both their generic anti-predator calls and silent controls. Thus, referential calls do not only convey the identity or the type of threat at present but also elicit vigilance in the future to provide protection from threats during periods of heightened vulnerability.

Multiple parasitism promotes facultative host acceptance of cuckoo eggs and rejection of cuckoo chicks

Many hosts of brood parasitic cuckoos reject foreign eggs from the nest. Yet where nests commonly receive more than one cuckoo egg, hosts might benefit by instead accepting parasite eggs. This is because cuckoos remove an egg from the nest before adding their own, and keeping cuckoo eggs in the nest reduces the odds that further host eggs are removed by subsequent cuckoos. This 'clutch dilution effect' has been proposed as a precondition for the evolution of cuckoo nestling eviction by hosts, but no previous studies have tested this in a host that rejects cuckoo nestlings. We tested the clutch dilution hypothesis in large-billed gerygones (Gerygone magnirostris), which are multiply parasitized by little bronze-cuckoos (Chalcites minutillus). Gerygones evict cuckoo nestlings but accept cuckoo eggs. Consistent with multiple parasitism favouring egg acceptance, we found gerygone egg survival was higher under scenarios of cuckoo egg acceptance than rejection. Yet gerygones were also flexible in their egg acceptance, with 35% abandoning cuckoo-egg-only clutches. This novel demonstration of adaptive clutch dilution suggests that multiple parasitism can favour a facultative response to brood parasite eggs, whereby hosts accept or reject parasite eggs depending on clutch composition.

A Chromosome-level Genome Assembly of the Reed Warbler (Acrocephalus scirpaceus)

The reed warbler (Acrocephalus scirpaceus) is a long-distance migrant passerine with a wide distribution across Eurasia. This species has fascinated researchers for decades, especially its role as host of a brood parasite, and its capacity for rapid phenotypic change in the face of climate change. Currently, it is expanding its range northwards in Europe, and is altering its migratory behaviour in certain areas. Thus, there is great potential to discover signs of recent evolution and its impact on the genomic composition of the reed warbler. Here we present a high-quality reference genome for the reed warbler, based on PacBio, 10X and Hi-C sequencing. The genome has an assembly size of 1,075,083,815 bp with a scaffold N50 of 74,438,198 bp and a contig N50 of 12,742,779 bp. BUSCO analysis using aves_odb10 as a model showed that 95.7% of genes in the assembly were complete. We found unequivocal evidence of two separate macrochromosomal fusions in the reed warbler genome, in addition to the previously identified fusion between chromosome Z and a part of chromosome 4A in the Sylvioidea superfamily. We annotated 14,645 protein-coding genes, of which 97.5% were complete BUSCO orthologs. This reference genome will serve as an important resource, and will provide new insights into the genomic effects of evolutionary drivers such as coevolution, range expansion, and adaptations to climate change, as well as chromosomal rearrangements in birds.