Iliana Medina

Brood Parasitism and the Evolution of Cooperative Breeding in Birds

Power in Numbers Avian brood parasites target particular bird species to raise their offspring, sometimes at great cost to the foster family. Feeney et al. (p. 1506; see the Perspective by Spottiswoode) analyzed the global distribution of brood parasitism and found a correlation with the occurrence of cooperative breeders across multiple taxa. For example, Australian fairy wrens breed both singly and in cooperative groups, but the group breeders are better able to resist parasites than lone pairs, indicating that the prevalence of cooperative breeding may be a response to brood parasites. The skewed global distribution of cooperatively breeding birds may result from their coevolution with brood parasites. [Also see Perspective by Spottiswoode] The global distribution of cooperatively breeding birds is highly uneven, with hotspots inAustralasia and sub-Saharan Africa. The ecological drivers of this distribution remain enigmatic yet could yield insights into the evolution and persistence of cooperative breeding. We report that the global distributions of avian obligate brood parasites and cooperatively breeding passerines are tightly correlated and that the uneven phylogenetic distribution of cooperative breeding is associated with the uneven targeting of hosts by brood parasites. With a long-term field study, we show that brood parasites can acquire superior care for their young by targeting cooperative breeders. Conversely, host defenses against brood parasites are strengthened by helpers at the nest. Reciprocally selected interactions between brood parasites and cooperative breeders may therefore explain the close association between these two breeding systems.

Hybridization promotes color polymorphism in the aposematic harlequin poison frog, Oophaga histrionica.

Whether hybridization can be a mechanism that drives phenotypic diversity is a widely debated topic in evolutionary biology. In poison frogs (Dendrobatidae), assortative mating has been invoked to explain how new color morphs persist despite the expected homogenizing effects of natural selection. Here, we tested the complementary hypothesis that new morphs arise through hybridization between different color morphs. Specifically, we (1) reconstructed the phylogenetic relationships among the studied populations of a dart-poison frog to provide an evolutionary framework, (2) tested whether microsatellite allele frequencies of one putative hybrid population of the polymorphic frog O. histrionica are intermediate between O. histrionica and O. lehmanni, and (3) conducted mate-choice experiments to test whether putatively intermediate females prefer homotypic males over males from the other two populations. Our findings are compatible with a hybrid origin for the new morph and emphasize the possibility of hybridization as a mechanism generating variation in polymorphic species. Moreover, because coloration in poison frogs is aposematic and should be heavily constrained, our findings suggest that hybridization can produce phenotypic novelty even in systems where phenotypes are subject to strong stabilizing selection.

The evolution of acceptance and tolerance in hosts of avian brood parasites

Avian brood parasites lay their eggs in the nests of their hosts, which rear the parasites progeny. The costs of parasitism have selected for the evolution of defence strategies in many host species. Most research has focused on resistance strategies, where hosts minimize the number of successful parasitism events using defences such as mobbing of adult brood parasites or rejection of parasite eggs. However, many hosts do not exhibit resistance. Here we explore why some hosts accept parasite eggs in their nests and how this is related to the virulence of the parasite. We also explore the extent to which acceptance of parasites can be explained by the evolution of tolerance; a strategy in which the host accepts the parasite but adjusts its life history or other traits to minimize the costs of parasitism. We review examples of tolerance in hosts of brood parasites (such as modifications to clutch size and multi‐broodedness), and utilize the literature on host–pathogen interactions and plant herbivory to analyse the prevalence of each type of defence (tolerance or resistance) and their evolution. We conclude that (i) the interactions between brood parasites and their hosts provide a highly tractable system for studying the evolution of tolerance, (ii) studies of host defences against brood parasites should investigate both resistance and tolerance, and (iii) tolerance and resistance can lead to contrasting evolutionary scenarios.

Environmental variability and acoustic signals: a multi-level approach in songbirds

Among songbirds, growing evidence suggests that acoustic adaptation of song traits occurs in response to habitat features. Despite extensive study, most research supporting acoustic adaptation has only considered acoustic traits averaged for species or populations, overlooking intraindividual variation of song traits, which may facilitate effective communication in heterogeneous and variable environments. Fewer studies have explicitly incorporated sexual selection, which, if strong, may favour variation across environments. Here, we evaluate the prevalence of acoustic adaptation among 44 species of songbirds by determining how environmental variability and sexual selection intensity are associated with song variability (intraindividual and intraspecific) and short-term song complexity. We show that variability in precipitation can explain short-term song complexity among taxonomically diverse songbirds, and that precipitation seasonality and the intensity of sexual selection are related to intraindividual song variation. Our results link song complexity to environmental variability, something previously found for mockingbirds (Family Mimidae). Perhaps more importantly, our results illustrate that individual variation in song traits may be shaped by both environmental variability and strength of sexual selection.

The costs of avian brood parasitism explain variation in egg rejection behaviour in hosts.

Many bird species can reject foreign eggs from their nests. This behaviour is thought to have evolved in response to brood parasites, birds that lay their eggs in the nest of other species. However, not all hosts of brood parasites evict parasitic eggs. In this study, we collate data from egg rejection experiments on 198 species, and perform comparative analyses to understand the conditions under which egg rejection evolves. We found evidence, we believe for the first time in a large-scale comparative analysis, that (i) non-current host species have rejection rates as high as current hosts, (ii) egg rejection is more likely to evolve when the parasite is relatively large compared with its host and (iii) egg rejection is more likely to evolve when the parasite chick evicts all the host eggs from the nest, such as in cuckoos. Our results suggest that the interactions between brood parasites and their hosts have driven the evolution of egg rejection and that variation in the costs inflicted by parasites is fundamental to explaining why only some host species evolve egg rejection.

Brood Parasitism Is Linked to Egg Pattern Diversity within and among Species of Australian Passerines

Bird eggs show striking diversity in color and pattern. One explanation for this is that interactions between avian brood parasites and their hosts drive egg phenotype evolution. Brood parasites lay their eggs in the nests of other species, their hosts. Many hosts defend their nests against parasitism by rejecting foreign eggs, which selects for parasite eggs that mimic those of the host. In theory, this may in turn select for changes in host egg phenotypes over time to facilitate discrimination of parasite eggs. Here, we test for the first time whether parasitism by brood parasites has led to increased divergence in egg phenotype among host species. Using Australian host and nonhost species and objective measures of egg color and pattern, we show that (i) hosts of brood parasites have higher within-species variation in egg pattern than nonhosts, supporting previous findings in other systems, and (ii) host species have diverged more in their egg patterns than nonhost species after controlling for divergence time. Overall, our results suggest that brood parasitism has played a significant role in the evolution of egg diversity and that these effects are evident, not only within species, but also among species.

Coevolution is linked with phenotypic diversification but not speciation in avian brood parasites

Coevolution is often invoked as an engine of biological diversity. Avian brood parasites and their hosts provide one of the best-known examples of coevolution. Brood parasites lay their eggs in the nests of other species, selecting for host defences and reciprocal counteradaptations in parasites. In theory, this arms race should promote increased rates of speciation and phenotypic evolution. Here, we use recently developed methods to test whether the three largest avian brood parasitic lineages show changes in rates of phenotypic diversity and speciation relative to non-parasitic lineages. Our results challenge the accepted paradigm, and show that there is little consistent evidence that lineages of brood parasites have higher speciation or extinction rates than non-parasitic species. However, we provide the first evidence that the evolution of brood parasitic behaviour may affect rates of evolution in morphological traits associated with parasitism. Specifically, egg size and the colour and pattern of plumage have evolved up to nine times faster in parasitic than in non-parasitic cuckoos. Moreover, cuckoo clades of parasitic species that are sympatric (and share similar host genera) exhibit higher rates of phenotypic evolution. This supports the idea that competition for hosts may be linked to the high phenotypic diversity found in parasitic cuckoos.

Batten down the thatches: front-line defences in an apparently defenceless cuckoo host

Avian brood parasites lay their eggs in the nests of other species, imposing high costs on their hosts. In theory, this should select for the evolution of defences against parasitism in hosts, yet eviction of parasite eggs or chicks is absent in many host species. One such host is the yellow-rumped thornbill, Acanthiza chrysorrhoa, the primary host of the shining bronze-cuckoo, Chalcites lucidus, in Australia. Here we tested whether the lack of egg and chick rejection in yellow-rumped thornbills has led to the evolution of alternative defences against brood parasitism. We provide evidence that this host has evolved two types of frontline defences. First, yellow-rumped thornbills responded to the presence of a cuckoo mount near the nest with mobbing behaviour and by occupying their dome-shaped nests, potentially as a means of blocking the small entrance hole. Second, we show that brood parasitism imposes directional selection for early breeding on the yellow-rumped thornbill and that yellow-rumped thornbills show a concomitant shift in their breeding phenology, breeding earlier than both congeneric and sympatric species. Our results highlight the importance of studying apparently defenceless hosts in order to identify alternative defence strategies.

The evolution of host specialisation in avian brood parasites

Traditional ecological theory predicts that specialisation can promote speciation; hence, recently derived species are specialists. However, an alternative view is that new species have broad niches, which become narrower and specialised over time. Here, we test these hypotheses using avian brood parasites and three different measures of host specialisation. Brood parasites provide an ideal system in which to investigate the evolution of specialisation, because some exploit more than 40 host species and others specialise on only one. We find that young brood parasite species are smaller and specialise on a narrower range of host sizes, as expected, if specialisation is linked with the generation of new species. Moreover, we show that highly virulent parasites are more specialised, supporting findings in other host-parasite systems. Finally, we demonstrate that different measures of specialisation can lead to different conclusions, and specialisation indices should be designed taking into account the biology of each system.

The Evolution of Clutch Size in Hosts of Avian Brood Parasites

Coevolution with avian brood parasites shapes a range of traits in their hosts, including morphology, behavior, and breeding systems. Here we explore whether brood parasitism is also associated with the evolution of host clutch size. Several studies have proposed that hosts of highly virulent parasites could decrease the costs of parasitism by evolving a smaller clutch size, because hosts with smaller clutches will lose fewer progeny when their clutch is parasitized. We describe a model of the evolution of clutch size, which challenges this logic and shows instead that an increase in clutch size (or no change) should evolve in hosts. We test this prediction using a broad-scale comparative analysis to ask whether there are differences in clutch size within hosts and between hosts and nonhosts. Consistent with our model, this analysis revealed that host species do not have smaller clutches and that hosts that incur larger costs from raising a parasite lay larger clutches. We suggest that brood parasitism might be an influential factor in clutch-size evolution and could potentially select for the evolution of larger clutches in host species.