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.

Eggshell composition and surface properties of avian brood-parasitic species compared with non-parasitic species.

The eggs of avian obligate brood-parasitic species have multiple adaptations to deceive hosts and optimize development in host nests. While the structure and composition of the eggshell in all birds is essential for embryo growth and protection from external threats, parasitic eggs may face specific challenges such as high microbial loads, rapid laying and ejection by the host parents. We set out to assess whether eggshells of avian brood-parasitic species have either (i) specialized structural properties, to meet the demands of a brood-parasitic strategy or (ii) similar structural properties to eggs of their hosts, due to the similar nest environment. We measured the surface topography (roughness), wettability (how well surfaces repel water) and calcium content of eggshells of a phylogenetically and geographically diverse range of brood-parasitic species (representing four of the seven independent lineages of avian brood-parasitic species), their hosts and close relatives of the parasites. These components of the eggshell structure have been demonstrated previously to influence such factors as the risk of microbial infection and overall shell strength. Within a phylogenetically controlled framework, we found no overall significant differences in eggshell roughness, wettability and calcium content between (i) parasitic and non-parasitic species, or (ii) parasitic species and their hosts. Both the wettability and calcium content of the eggs from brood-parasitic species were not more similar to those of their hosts' eggs than expected by chance. By contrast, the mean surface roughness of the eggs of brood-parasitic species was more similar to that of their hosts' eggs than expected by chance, suggesting brood-parasitic species may have evolved to lay eggs that match the host nest environment for this trait. The lack of significant overall differences between parasitic and non-parasitic species, including hosts, in the traits we measured, suggests that phylogenetic signal, as well as general adaptations to the nest environment and for embryo development, outweigh any influence of a parasitic lifestyle on these eggshell properties.

Genetic architecture facilitates then constrains adaptation in a host-parasite coevolutionary arms race.

In coevolutionary arms races, interacting species impose selection on each other, generating reciprocal adaptations and counter adaptations. This process is typically enhanced by genetic recombination and heterozygosity, but these sources of evolutionary novelty may be secondarily lost when uniparental inheritance evolves to ensure the integrity of sex-linked adaptations. We demonstrate that host-specific egg mimicry in the African cuckoo finch Anomalospiza imberbis is maternally inherited, confirming the validity of an almost century-old hypothesis. We further show that maternal inheritance not only underpins the mimicry of different host species but also additional mimetic diversification that approximates the range of polymorphic egg "signatures" that have evolved within host species as an escalated defense against parasitism. Thus, maternal inheritance has enabled the evolution and maintenance of nested levels of mimetic specialization in a single parasitic species. However, maternal inheritance and the lack of sexual recombination likely disadvantage cuckoo finches by stifling further adaptation in the ongoing arms races with their individual hosts, which we show have retained biparental inheritance of egg phenotypes. The inability to generate novel genetic combinations likely prevents cuckoo finches from mimicking certain host phenotypes that are currently favored by selection (e.g., the olive-green colored eggs laid by some tawny-flanked prinia, Prinia subflava, females). This illustrates an important cost of coding coevolved adaptations on the nonrecombining sex chromosome, which may impede further coevolutionary change by effectively reversing the advantages of sexual reproduction in antagonistic coevolution proposed by the Red Queen hypothesis.

Multimodal mimicry of hosts in a radiation of parasitic finches.

Brood parasites use the parental care of others to raise their young and sometimes employ mimicry to dupe their hosts. The brood-parasitic finches of the genus Vidua are a textbook example of the role of imprinting in sympatric speciation. Sympatric speciation is thought to occur in Vidua because their mating traits and host preferences are strongly influenced by their early host environment. However, this alone may not be sufficient to isolate parasite lineages, and divergent ecological adaptations may also be required to prevent hybridization collapsing incipient species. Using pattern recognition software and classification models, we provide quantitative evidence that Vidua exhibit specialist mimicry of their grassfinch hosts, matching the patterns, colors and sounds of their respective host's nestlings. We also provide qualitative evidence of mimicry in postural components of Vidua begging. Quantitative comparisons reveal small discrepancies between parasite and host phenotypes, with parasites sometimes exaggerating their host's traits. Our results support the hypothesis that behavioral imprinting on hosts has not only enabled the origin of new Vidua species, but also set the stage for the evolution of host-specific, ecological adaptations.

The Persistence of Polymorphisms across Species Radiations.

Studies on polymorphisms have been foundational to our understanding of evolution. The presence of different phenotypic morphs is sometimes considered a precursor to speciation in which morphs evolve into different species. While speciation should initially reduce genetic variation in daughter versus parental species, a common pattern is the recurrence of the same phenotypic polymorphism in many species of a clade. Despite the ubiquity of these persistent polymorphisms, there is little discussion of their evolutionary origins. How does the genetic variation underpinning such polymorphisms cross speciation boundaries? What selection pressures maintain the morphs in multiple daughter species? Using diverse case studies, we highlight the characteristics of polymorphisms and selection regimes influencing the likelihood of polymorphism retention across species radiations.

Convergent evolution of reduced eggshell conductance in avian brood parasites.

Brood parasitism has evolved independently in several bird lineages, giving rise to strikingly similar behavioural adaptations that suggest convergent evolution. By comparison, convergence of physiological traits that optimize this breeding strategy has received much less attention, yet these species share many similar physiological traits that optimize this breeding strategy. Eggshell structure is important for embryonic development as it controls the flux of metabolic gases, such as O2, CO2 and H2O, into and out of the egg; in particular, water vapour conductance ( GH2O) is an essential process for optimal development of the embryo. Previous work has shown that common cuckoos ( Cuculus canorus) have a lower than expected eggshell GH2O compared with their hosts. Here, we sought to test whether this is a trait found in other independently evolved avian brood parasites, and therefore reflects a general adaptation to a parasitic lifestyle. We analysed GH2O for seven species of brood parasites from four unique lineages as well as for their hosts, and combined this with species from the literature. We found lower than expected GH2O among all our observed brood parasites both compared with hosts (except for brown-headed cowbirds ( Molothrus ater)) and compared with the expected rates given their phylogenetic positions. These findings suggest that a lowered GH2O may be a general adaptation for brood parasitism, perhaps helping the parasite nestling to develop greater aerobic fitness. This article is part of the theme issue 'The coevolutionary biology of brood parasitism: from mechanism to pattern'.

Signals, cues and the nature of mimicry.

'Mimicry' is used in the evolutionary and ecological literature to describe diverse phenomena. Many are textbook examples of natural selection's power to produce stunning adaptations. However, there remains a lack of clarity over how mimetic resemblances are conceptually related to each other. The result is that categories denoting the traditional subdivisions of mimicry are applied inconsistently across studies, hindering attempts at conceptual unification. This review critically examines the logic by which mimicry can be conceptually organized and analysed. It highlights the following three evolutionarily relevant distinctions. (i) Are the model's traits being mimicked signals or cues? (ii) Does the mimic signal a fitness benefit or fitness cost in order to manipulate the receiver's behaviour? (iii) Is the mimic's signal deceptive? The first distinction divides mimicry into two broad categories: 'signal mimicry' and 'cue mimicry'. 'Signal mimicry' occurs when mimic and model share the same receiver, and 'cue mimicry' when mimic and model have different receivers or when there is no receiver for the model's trait. 'Masquerade' fits conceptually within cue mimicry. The second and third distinctions divide both signal and cue mimicry into four types each. These are the three traditional mimicry categories (aggressive, Batesian and Müllerian) and a fourth, often overlooked category for which the term 'rewarding mimicry' is suggested. Rewarding mimicry occurs when the mimic's signal is non-deceptive (as in Müllerian mimicry) but where the mimic signals a fitness benefit to the receiver (as in aggressive mimicry). The existence of rewarding mimicry is a logical extension of the criteria used to differentiate the three well-recognized forms of mimicry. These four forms of mimicry are not discrete, immutable types, but rather help to define important axes along which mimicry can vary.

Coupled range dynamics of brood parasites and their hosts responding to climate and vegetation changes.

As populations shift their ranges in response to global change, local species assemblages can change, setting the stage for new ecological interactions, community equilibria and evolutionary responses. Here, we focus on the range dynamics of four avian brood parasite species and their hosts in southern Africa, in a context of bush encroachment (increase in woody vegetation density in places previously occupied by savanna-grassland mosaics) favouring some species at the expense of others. We first tested whether hosts and parasites constrained each other's ability to expand or maintain their ranges. Secondly, we investigated whether range shifts represented an opportunity for new host-parasite and parasite-parasite interactions. We used multispecies dynamic occupancy models with interactions, fitted to citizen science data, to estimate the contribution of interspecific interactions to range shifts and to quantify the change in species co-occurrence probability over a 25-year period. Parasites were able to track their hosts' range shifts. We detected no deleterious effect of the parasites' presence on either the local population viability of host species or the hosts' ability to colonize newly suitable areas. In the recently diversified indigobird radiation (Vidua spp.), following bush encroachment, the new assemblages presented more potential opportunities for speciation via host switch, but also more potential for hybridization between extant lineages, also via host switch. Multispecies dynamic occupancy models with interactions brought new insights into the feedbacks between range shifts, biotic interactions and local demography: brood parasitism had little detected impact on extinction or colonization processes, but inversely the latter processes affected biotic interactions via the modification of co-occurrence patterns.

Female behaviour drives expression and evolution of gustatory receptors in butterflies.

Secondary plant compounds are strong deterrents of insect oviposition and feeding, but may also be attractants for specialist herbivores. These insect-plant interactions are mediated by insect gustatory receptors (Grs) and olfactory receptors (Ors). An analysis of the reference genome of the butterfly Heliconius melpomene, which feeds on passion-flower vines (Passiflora spp.), together with whole-genome sequencing within the species and across the Heliconius phylogeny has permitted an unprecedented opportunity to study the patterns of gene duplication and copy-number variation (CNV) among these key sensory genes. We report in silico gene predictions of 73 Gr genes in the H. melpomene reference genome, including putative CO2, sugar, sugar alcohol, fructose, and bitter receptors. The majority of these Grs are the result of gene duplications since Heliconius shared a common ancestor with the monarch butterfly or the silkmoth. Among Grs but not Ors, CNVs are more common within species in those gene lineages that have also duplicated over this evolutionary time-scale, suggesting ongoing rapid gene family evolution. Deep sequencing (∼1 billion reads) of transcriptomes from proboscis and labial palps, antennae, and legs of adult H. melpomene males and females indicates that 67 of the predicted 73 Gr genes and 67 of the 70 predicted Or genes are expressed in these three tissues. Intriguingly, we find that one-third of all Grs show female-biased gene expression (n = 26) and nearly all of these (n = 21) are Heliconius-specific Grs. In fact, a significant excess of Grs that are expressed in female legs but not male legs are the result of recent gene duplication. This difference in Gr gene expression diversity between the sexes is accompanied by a striking sexual dimorphism in the abundance of gustatory sensilla on the forelegs of H. melpomene, suggesting that female oviposition behaviour drives the evolution of new gustatory receptors in butterfly genomes.

Fine-scale spatiotemporal patterns of genetic variation reflect budding dispersal coupled with strong natal philopatry in a cooperatively breeding mammal.

The relatedness structure of animal populations is thought to be a critically important factor underlying the evolution of mating systems and social behaviours. While previous work has shown that population structure is shaped by many biological processes, few studies have investigated how these factors vary over time. Consequently, we explored the fine-scale spatiotemporal genetic structure of an intensively studied population of cooperatively breeding banded mongooses (Mungos mungo) over a 10-year period. Overall population structure was strong (average F(ST)  = 0.129) but groups with spatially overlapping territories were not more genetically similar to one another than noncontiguous groups. Instead, genetic differentiation was associated with historical group-fission (budding) events, with new groups diverging from their parent groups over time. Within groups, relatedness was high within but not between the sexes, although the latter increased over time since group formation due to group founders being replaced by philopatric young. This trend was not mirrored by a decrease in average offspring heterozygosity over time, suggesting that close inbreeding may often be avoided, even when immigration into established groups is virtually absent and opportunities for extra-group matings are rare. Fine-scale spatiotemporal population structure could have important implications in social species, where relatedness between interacting individuals is a vital component in the evolution of patterns of inbreeding avoidance, reproductive skew and kin-selected helping and harming.

RAF gene fusion breakpoints in pediatric brain tumors are characterized by significant enrichment of sequence microhomology.

Gene fusions involving members of the RAF family of protein kinases have recently been identified as characteristic aberrations of low-grade astrocytomas, the most common tumors of the central nervous system in children. While it has been shown that these fusions cause constitutive activation of the ERK/MAPK pathway, very little is known about their formation. Here, we present a detailed analysis of RAF gene fusion breakpoints from a well-characterized cohort of 43 low-grade astrocytomas. Our findings show that the rearrangements that generate these RAF gene fusions may be simple or complex and that both inserted nucleotides and microhomology are common at the DNA breakpoints. Furthermore, we identify novel enrichment of microhomologous sequences in the regions immediately flanking the breakpoints. We thus provide evidence that the tandem duplications responsible for these fusions are generated by microhomology-mediated break-induced replication (MMBIR). Although MMBIR has previously been implicated in the pathogenesis of other diseases and the evolution of eukaryotic genomes, we demonstrate here that the proposed details of MMBIR are consistent with a recurrent rearrangement in cancer. Our analysis of repetitive elements, Z-DNA and sequence motifs in the fusion partners identified significant enrichment of the human minisatellite conserved sequence/χ-like element at one side of the breakpoint. Therefore, in addition to furthering our understanding of low-grade astrocytomas, this study provides insights into the molecular mechanistic details of MMBIR and the sequence of events that occur in the formation of genomic rearrangements.