The final frontier: ecological and evolutionary dynamics of a global parasite invasion.

Studying rapid biological changes accompanying the introduction of alien organisms into native ecosystems can provide insights into fundamental ecological and evolutionary theory. While powerful, this quasi-experimental approach is difficult to implement because the timing of invasions and their consequences are hard to predict, meaning that baseline pre-invasion data are often missing. Exceptionally, the eventual arrival of Varroa destructor (hereafter Varroa) in Australia has been predicted for decades. Varroa is a major driver of honeybee declines worldwide, particularly as vectors of diverse RNA viruses. The detection of Varroa in 2022 at over a hundred sites poses a risk of further spread across the continent. At the same time, careful study of Varroa's spread, if it does become established, can provide a wealth of information that can fill knowledge gaps about its effects worldwide. This includes how Varroa affects honeybee populations and pollination. Even more generally, Varroa invasion can serve as a model for evolution, virology and ecological interactions between the parasite, the host and other organisms.

Imperfect mimicry of host begging calls by a brood parasitic cuckoo: a cue for nestling rejection by hosts?

Coevolutionary interactions between avian brood parasites and their hosts often lead to the evolution of discrimination and rejection of parasite eggs or chicks by hosts based on visual cues, and the evolution of visual mimicry of host eggs or chicks by brood parasites. Hosts may also base rejection of brood parasite nestlings on vocal cues, which would in turn select for mimicry of host begging calls in brood parasite chicks. In cuckoos that exploit multiple hosts with different begging calls, call structure may be plastic, allowing nestlings to modify their calls to match those of their various hosts, or fixed, in which case we would predict either imperfect mimicry or divergence of the species into host-specific lineages. In our study of the little bronze-cuckoo (LBC) Chalcites minutillus and its primary host, the large-billed gerygone Gerygone magnirostris, we tested whether: (1) hosts use nestling vocalizations as a cue to discriminate cuckoo chicks; (2) cuckoo nestlings mimic the host begging calls throughout the nestling period; and (3) the cuckoo begging calls are plastic, thereby facilitating mimicry of the calls of different hosts. We found that the begging calls of LBCs are most similar to their gerygone hosts shortly after hatching (when rejection by hosts typically occurs) but become less similar as cuckoo chicks get older. Begging call structure may be used as a cue for rejection by hosts, and these results are consistent with gerygone defenses selecting for age-specific vocal mimicry in cuckoo chicks. We found no evidence that LBC begging calls were plastic.

The coevolutionary biology of brood parasitism: a call for integration.

Obligate brood-parasitic cheats have fascinated natural historians since ancient times. Passing on the costs of parental care to others occurs widely in birds, insects and fish, and often exerts selection pressure on hosts that in turn evolve defences. Brood parasites have therefore provided an illuminating system for researching coevolution. Nevertheless, much remains unknown about how ecology and evolutionary history constrain or facilitate brood parasitism, or the mechanisms that shape or respond to selection. In this special issue, we bring together examples from across the animal kingdom to illustrate the diverse ways in which recent research is addressing these gaps. This special issue also considers how research on brood parasitism may benefit from, and in turn inform, related fields such as social evolution and immunity. Here, we argue that progress in our understanding of coevolution would benefit from the increased integration of ideas across taxonomic boundaries and across Tinbergen's Four Questions: mechanism, ontogeny, function and phylogeny of brood parasitism. We also encourage renewed vigour in uncovering the natural history of the majority of the world's brood parasites that remain little-known. Indeed, it seems very likely that some of nature's brood parasites remain entirely unknown, because otherwise we are left with a puzzle: if parental care is so costly, why is brood parasitism not more common? This article is part of the theme issue 'The coevolutionary biology of brood parasitism: from mechanism to pattern'.

The brood parasite's guide to inclusive fitness theory.

Hamilton's theory of inclusive fitness provides a framework for understanding the evolution of social behaviour between kin, including parental and alloparental care. Brood parasitism is a reproductive tactic in which parasites exploit the care of other individuals of the same species (conspecific parasitism) or different species (interspecific parasitism) to rear their brood. Here, drawing from examples in birds and social insects, we identify two insights into brood parasitism that stem from inclusive fitness theory. First, the kin structure within nests, or between neighbouring nests, can create a niche space favouring the evolution of conspecific parasitism. For example, low average relatedness within social insect nests can increase selection for reproductive cheats. Likewise, high average relatedness between adjacent nests of some birds can increase a female's tolerance of parasitism by her neighbour. Second, intrabrood conflict will be high in parasitized broods, from the perspective of both parasite and host young, relative to unparasitized broods. We also discuss offspring recognition by hosts as an example of discrimination in a kin-selected social behaviour. We conclude that the inclusive fitness framework is instructive for understanding aspects of brood parasite and host evolution. In turn, brood parasites present some unique opportunities to test the predictions of inclusive fitness theory. This article is part of the theme issue 'The coevolutionary biology of brood parasitism: from mechanism to pattern'.

True recognition of nestlings by hosts selects for mimetic cuckoo chicks.

Brood parasitic cuckoos lay their eggs in other birds' nests, whereafter the young cuckoo hatches, ejects its nest-mates and monopolizes the care of the host parents. Theory predicts that hosts should not evolve to recognize and reject cuckoo chicks via imprinting because of the risk of mistakenly imprinting on a cuckoo chick in their first brood and thereafter always rejecting their own chicks. However, recent studies have revealed that some hosts do reject cuckoo chicks from the nest, indicating that these hosts' recognition systems either do not rely on first brood imprinting, or use cues that are independent of chick phenotype. Here, we investigate the proximate mechanisms of chick rejection behaviour in the large-billed gerygone (Gerygone magnirostris), a host of the little bronze-cuckoo (Chalcites minutillus). We find that gerygones use true template-based recognition based on at least one visual chick trait (the number of hatchling down-feathers), and that this is further mediated by experience of adult cuckoos at the nest during egg-laying. Given the theoretical constraints of acquiring recognition templates via imprinting, gerygones must possess a template of own-chick appearance that is largely innate. This true recognition has facilitated the evolution of very rapid hatchling rejection and, in turn, striking visual mimicry of host young by little bronze-cuckoo chicks.

Cryptic cuckoo eggs hide from competing cuckoos.

Interspecific arms races between cuckoos and their hosts have produced remarkable examples of mimicry, with parasite eggs evolving to match host egg appearance and so evade removal by hosts. Certain bronze-cuckoo species, however, lay eggs that are cryptic rather than mimetic. These eggs are coated in a low luminance pigment that camouflages them within the dark interiors of hosts' nests. We investigated whether cuckoo egg crypsis is likely to have arisen from the same coevolutionary processes known to favour egg mimicry. We added high and low luminance-painted eggs to the nests of large-billed gerygones (Gerygone magnirostris), a host of the little bronze-cuckoo (Chalcites minutillus). Gerygones rarely rejected either egg type, and did not reject natural cuckoo eggs. Cuckoos, by contrast, regularly removed an egg from clutches before laying their own and were five times more likely to remove a high luminance model than its low luminance counterpart. Given that we found one-third of all parasitized nests were exploited by multiple cuckoos, our results suggest that competition between cuckoos has been the key selective agent for egg crypsis. In such intraspecific arms races, crypsis may be favoured over mimicry because it can reduce the risk of egg removal to levels below chance.

A novel method of rejection of brood parasitic eggs reduces parasitism intensity in a cowbird host.

The hosts of brood parasitic birds are under strong selection pressure to recognize and remove foreign eggs from their nests, but parasite eggs may be too large to be grasped whole and too strong to be readily pierced by the host's bill. Such operating constraints on egg removal are proposed to force some hosts to accept parasite eggs, as the costs of deserting parasitized clutches can outweigh the cost of rearing parasites. By fitting microcameras inside nests, we reveal that the Neotropical baywing (Agelaioides badius), a host of the screaming cowbird (Molothrus rufoaxillaris) and shiny cowbird (Molothrus bonariensis), instead circumvents such constraints by kicking parasite eggs out of the nest. To our knowledge, this is the first report of a passerine bird using its feet to remove objects from the nest. Kick-ejection was an all-or-nothing response. Baywings kick-ejected parasite eggs laid before their own first egg and, if heavily parasitized, they ejected entire clutches and began again in the same nest. Few baywings were able to rid their nests of every parasite egg, but their novel ejection method allowed them to reduce the median parasitism intensity by 75 per cent (from four to one cowbird eggs per nest), providing an effective anti-parasite defence.

Brood parasite eggs enhance egg survivorship in a multiply parasitized host.

Despite the costs to avian parents of rearing brood parasitic offspring, many species do not reject foreign eggs from their nests. We show that where multiple parasitism occurs, rejection itself can be costly, by increasing the risk of host egg loss during subsequent parasite attacks. Chalk-browed mockingbirds (Mimus saturninus) are heavily parasitized by shiny cowbirds (Molothrus bonariensis), which also puncture eggs in host nests. Mockingbirds struggle to prevent cowbirds puncturing and laying, but seldom remove cowbird eggs once laid. We filmed cowbird visits to nests with manipulated clutch compositions and found that mockingbird eggs were more likely to escape puncture the more cowbird eggs accompanied them in the clutch. A Monte Carlo simulation of this 'dilution effect', comparing virtual hosts that systematically either reject or accept parasite eggs, shows that acceptors enjoy higher egg survivorship than rejecters in host populations where multiple parasitism occurs. For mockingbirds or other hosts in which host nestlings fare well in parasitized broods, this benefit might be sufficient to offset the fitness cost of rearing parasite chicks, making egg acceptance evolutionarily stable. Thus, counterintuitively, high intensities of parasitism might decrease or even reverse selection pressure for host defence via egg rejection.