Habitat-dependent call divergence in the common cuckoo: is it a potential signal for assortative mating?

The common cuckoo (Cuculus canorus) is an obligate brood parasite that mimics the eggs of its hosts. The host-specific egg pattern is thought to be inherited matrilinearly, creating female-only host-specific races. Males are thought not to be adapted to their host and they maintain the species by mating arbitrarily with respect to host specialization of females. However, recent results suggest that male cuckoos may also show host-specific adaptations and these may require assortative mating with respect to host. The calls males produce on the breeding grounds could provide a potential mechanism for assortative mating. We tested whether male cuckoo calls differ more between nearby populations that parasitize different hosts than between distant populations that parasitize the same host. We recorded the calls of geographically distant pairs of populations in Hungary, with each pair consisting of a forest population and a nearby reed bed population. Each habitat is characterized by one main host species for the common cuckoo. Our results show that calls of distant cuckoo populations from the same habitat type are more similar to each other than they are to those of nearby populations from a different habitat. These results suggest that cuckoo calls differ sufficiently to allow recognition of habitat-specific individuals.     

Modelling the evolution of common cuckoo host‐races: speciation or genetic swamping?

Co‐evolutionary arms races have provided clear evidence for evolutionary change, especially in host–parasite systems. The evolution of host‐specific races in the common cuckoo (Cuculus canorus), however, is also an example where sexual conflict influences the outcome. Cuckoo females benefit from better adaptation to overcome host defences, whereas cuckoo males face a trade‐off between the benefits of better adaptation to a host and the benefits of multiple mating with females from other host‐races. The outcome of this trade‐off might be genetic differentiation or prevention of it by genetic swamping. We use a simulation model to test which outcome is more likely with three sympatric cuckoo host‐races. We assume a cost for cuckoo chicks that express a host adaptation allele not suited to their foster host species and that cuckoo males that switch to another host‐race experience either a fitness benefit or cost. Over most of the parameter space, cuckoo male host‐race fidelity increases significantly with time, and gene flow between host‐races ceases within a few thousand to a hundred thousand generations. Our results hence support the idea that common cuckoo host‐races might be in the incipient stages of speciation.     

Analysis of molecular differentiation in a hybrid zone between chromosomally distinct races of the common shrew Sorex araneus (Insectivora: Soricidae) suggests their common ancestry

During postglacial colonization, populations that diverged in different refugia produced a patchwork of genomes, often delimited with sharp hybrid zones. The outcome of hybridization following the secondary contact of two genetically distinct populations is hard to predict. In this context, the present study investigated the genetic structure of the hybrid zone between the Drnholec and Białowieża chromosome races of the common shrew ( Sorex araneus ) in Poland using biparentally inherited (seven autosomal microsatellites) and uniparentally inherited (Y-linked microsatellite and mtDNA) molecular markers. On the basis of diagnostic chromosomes, the Drnholec and Białowieża races were classified to different karyotypic groups, which were believed to have independent glacial histories. It was found that genetic differentiation between the Drnholec and Białowieża races was weak and nonsignificant with respect to all molecular markers. However, these results are in contrast with the chromosomal structure of this hybrid zone. The very sharp frequency clines of the diagnostic chromosomes strongly suggest that gene flow between the Drnholec and Białowieża races was reduced. Nonsignificant correlations between genetic differentiation and both the presence of an environmental barrier and geographical distance reveal that only differences in karyotypes might be a reason for limited gene exchange between the races. It is assumed that a lack of molecular differences between the Drnholec and Białowieża races results from a shared ancestral variation.  © 2006 The Linnean Society of London, Biological Journal of the Linnean Society , 2006, 89 , 79–90.     

Sex allocation in relation to host races in the brood-parasitic common cuckoo (Cuculus canorus)

Sex allocation theory and empirical evidence both suggest that natural selection should favour maternal control of offspring sex ratio in relation to their ability to invest in the offspring. Generalist parasites constitute a particularly interesting group to test this theory as different females commonly utilize different host species showing large variation in provisioning ability. The common cuckoo (Cuculus canorus) is a generalist brood parasite that lays its eggs in the nest of many different passerine birds, but each female tends to specialize on one particular host species giving rise to highly specialized host races. The different host species show large variation in their ability to invest in the parasitic offspring, presenting an opportunity for female cuckoos to bias offspring sex ratio in relation to host species quality. Here, we investigate host-race specific sex allocation controlling for maternal identity in the common cuckoo. We found no evidence of any significant relationship between host race and sex ratio in one sympatric population harbouring three different host races, or in a total of five geographically separated populations. There was also no significant association between host quality, as determined by species-specific female host body mass, and cuckoo sex ratio. Finally, we found no significant relationship between individual cuckoo maternal quality, as determined by her egg volume, and sex ratio within each host race. We conclude that the generalist brood-parasitic common cuckoo show no significant sex-ratio bias in relation to host race and discuss this finding in light of gene flow and host adaptations.     

Sex-biased gene flow and colonization in the Formosan lesser horseshoe bat: inference from nuclear and mitochondrial markers

Sex-biased behaviours are expected to play an important role in partitioning genetic variance in animal populations. Comparing genetic structure at markers with different modes of inheritance provides a means of detecting these behaviours and their consequences for population genetic structure. In colonially breeding mammals, the common combination of female philopatry and male vagility can promote contrasting patterns of genetic differentiation between the sexes, both via their effects on recurrent gene flow and on colonization. We examined sex differences in gene flow and structure by comparing maternally inherited mitochondrial DNA (mtDNA) and biparentally inherited autosomal loci in the Formosan lesser horseshoe bat Rhinolophus monoceros . We found that genetic partitioning was higher at mtDNA than autosomal markers in both sexes, indicative of female-biased philopatry and male-biased dispersal. Across Taiwan, isolation-by-distance was detected for all sex/marker combinations but was steeper for mtDNA than for nuclear markers. We suggest that isolation-by-distance shown from mtDNA at large scales is likely to reflect the stepwise founding of new breeding colonies by females during colonization. In contrast, no isolation-by-distance was found at smaller distances of up to 100 km, indicating that gene flow and/or recent shared ancestry homogenises genetic structure among nearby sites. Our results highlight the value of an indirect genetic approach to understanding sex-biased behaviours and their consequences in a little-studied species.     

Comparative organization of chloroplast, mitochondrial and nuclear diversity in plant populations

Plants offer excellent models to investigate how gene flow shapes the organization of genetic diversity. Their three genomes can have different modes of transmission and will hence experience varying levels of gene flow. We have compiled studies of genetic structure based on chloroplast DNA (cpDNA), mitochondrial DNA (mtDNA) and nuclear markers in seed plants. Based on a data set of 183 species belonging to 103 genera and 52 families, we show that the precision of estimates of genetic differentiation (G(ST)) used to infer gene flow is mostly constrained by the sampling of populations. Mode of inheritance appears to have a major effect on G(ST). Maternally inherited genomes experience considerably more subdivision (median value of 0.67) than paternally or biparentally inherited genomes (approximately 0.10). G(ST) at cpDNA and mtDNA markers covary narrowly when both genomes are maternally inherited, whereas G(ST) at paternally and biparentally inherited markers also covary positively but more loosely and G(ST) at maternally inherited markers are largely independent of values based on nuclear markers. A model-based gross estimate suggests that, at the rangewide scale, historical levels of pollen flow are generally at least an order of magnitude larger than levels of seed flow (median of the pollen-to-seed migration ratio: 17) and that pollen and seed gene flow vary independently across species. Finally, we show that measures of subdivision that take into account the degree of similarity between haplotypes (N(ST) or R(ST)) make better use of the information inherent in haplotype data than standard measures based on allele frequencies only.     

Unequal contribution of sexes in the origin of dog breeds

Dogs (Canis familiaris) were domesticated from the gray wolf (Canis lupus) at least 14,000 years ago, and there is evidence of dogs with phenotypes similar to those in modern breeds 4000 years ago. However, recent genetic analyses have suggested that modern dog breeds have a much more recent origin, probably <200 years ago. To study the origin of contemporaneous breeds we combined the analysis of paternally inherited Y chromosome markers with maternally inherited mitochondrial DNA and biparentally inherited autosomal microsatellite markers in both domestic dogs and their wild ancestor, the gray wolf. Our results show a sex bias in the origin of breeds, with fewer males than females contributing genetically, which clearly differs from the breeding patterns in wild gray wolf populations where both sexes have similar contributions. Furthermore, a comparison of mitochondrial DNA and Y chromosome diversity in dog groups recognized by the World Canine Organization, as well as in groups defined by the breeds' genetic composition, shows that paternal lineages are more differentiated among groups than maternal lineages. This demonstrates a lower exchange of males than of females between breeds belonging to different groups, which illustrates how breed founders may have been chosen.     

Cryptic gentes revealed in pallid cuckoos Cuculus pallidus using reflectance spectrophotometry

Many cuckoo species lay eggs that match those of their hosts, which can significantly reduce rejection of their eggs by the host species. However, egg mimicry is problematic for generalist cuckoos that parasitize several host species with different egg types. Some generalist cuckoos have overcome this problem by evolving several host-specific races (gentes), each with its own, host-specific egg type. It is unknown how generalist cuckoos lacking gentes are able to avoid egg rejection by hosts. Here we use reflectance spectrophotometry (300-700 nm) on museum egg collections to test for host-specific egg types in an Australian generalist cuckoo reported to have a single egg type. We show that the colour of pallid cuckoo (Cuculus pallidus) eggs differed between four host species, and that their eggs closely mimicked the eggs of the host they parasitized. These results reveal that pallid cuckoos have host-specific egg types that have not been detected by human observation, and indicate that gentes could be more common than previously realized.     

Host-related genetic differentiation in the anther smut fungus Microbotryum violaceum in sympatric, parapatric and allopatric populations of two host species Silene latifolia and S. dioica

We investigated genetic diversity in West European populations of the fungal pathogen Microbotryum violaceum in sympatric, parapatric and allopatric populations of the host species Silene latifolia and S. dioica, using four polymorphic microsatellite loci. In allopatric host populations, the fungus was highly differentiated by host species, exhibiting high values of F(ST) and R(ST), and revealed clear and distinct host races. In sympatric and parapatric populations we found significant population differentiation as well, except for one sympatric population in which the two host species grew truly intermingled. The mean number of alleles per locus for isolates from each of the host species was significantly higher in sympatric/parapatric than in allopatric populations. This suggests that either gene flow between host races in sympatry, or in case of less neutral loci, selection in a more heterogeneous host environment can increase the level of genetic variation in each of the demes. The observed pattern of host-related genetic differentiation among these geographically spread populations suggest a long-term divergence between these host races. In sympatric host populations, both host races presumably come in secondary contact, and host-specific alleles are exchanged depending on the amount of fungal gene flow.     

High gene flow on a continental scale in the polyandrous Kentish plover Charadrius alexandrinus

Gene flow promotes genetic homogeneity of species in time and space. Gene flow can be modulated by sex‐biased dispersal that links population genetics to mating systems. We investigated the phylogeography of the widely distributed Kentish plover Charadrius alexandrinus. This small shorebird has a large breeding range spanning from Western Europe to Japan and exhibits an unusually flexible mating system with high female breeding dispersal. We analysed genetic structure and gene flow using a 427‐bp fragment of the mitochondrial (mtDNA) control region, 21 autosomal microsatellite markers and a Z microsatellite marker in 397 unrelated individuals from 21 locations. We found no structure or isolation‐by‐distance over the continental range. However, island populations had low genetic diversity and were moderately differentiated from mainland locations. Genetic differentiation based on autosomal markers was positively correlated with distance between mainland and each island. Comparisons of uniparentally and biparentally inherited markers were consistent with female‐biased gene flow. Maternally inherited mtDNA was less structured, whereas the Z‐chromosomal marker was more structured than autosomal microsatellites. Adult males were more related than females within genetic clusters. Taken together, our results suggest a prominent role for polyandrous females in maintaining genetic homogeneity across large geographic distances.     

The role of swarming sites for maintaining gene flow in the brown long-eared bat (Plecotus auritus)

Bat-swarming sites where thousands of individuals meet in late summer were recently proposed as 'hot spots' for gene flow among populations. If, due to female philopatry, nursery colonies are genetically differentiated, and if males and females of different colonies meet at swarming sites, then we would expect lower differentiation of maternally inherited genetic markers among swarming sites and higher genetic diversity within. To test these predictions, we compared genetic variance from three swarming sites to 14 nursery colonies. We analysed biparentally (five nuclear and one sex-linked microsatellite loci) and maternally (mitochondrial D-loop, 550 bp) inherited molecular markers. Three mtDNA D-loop haplolineages that were strictly separated at nursery colonies were mixed at swarming sites. As predicted by the 'extra colony-mating hypothesis', genetic variance among swarming sites (V(ST)) for the D-loop drastically decreased compared to the nursery population genetic variance (V(PT)) (31 and 60%, respectively), and genetic diversity increased at swarming sites. Relatedness was significant at nursery colonies but not at swarming sites, and colony relatedness of juveniles to females was positive but not so to males. This suggests a breakdown of colony borders at swarming sites. Although there is behavioural and physiological evidence for sexual interaction at swarming sites, this does not explain why mating continues throughout the winter. We therefore propose that autumn roaming bats meet at swarming sites across colonies to start mating and, in addition, to renew information about suitable hibernacula.     

SEX-BIASED GENE FLOW IN SPECTACLED EIDERS (ANATIDAE): INFERENCES FROM MOLECULAR MARKERS WITH CONTRASTING MODES OF INHERITANCE

Abstract Genetic markers that differ in mode of inheritance and rate of evolution (a sex‐linked Z‐specific micro‐satellite locus, five biparentally inherited microsatellite loci, and maternally inherited mitochondrial [mtDNA] sequences) were used to evaluate the degree of spatial genetic structuring at macro‐ and microgeographic scales, among breeding regions and local nesting populations within each region, respectively, for a migratory sea duck species, the spectacled eider (Somateria fisheri). Disjunct and declining breeding populations coupled with sex‐specific differences in seasonal migratory patterns and life history provide a series of hypotheses regarding rates and directionality of gene flow among breeding populations from the Indigirka River Delta, Russia, and the North Slope and Yukon‐Kuskokwim Delta, Alaska. The degree of differentiation in mtDNA haplotype frequency among breeding regions and populations within regions was high (φ_CT= 0.189, P < 0.01; φ_SC= 0.059, P < 0.01, respectively). Eleven of 17 mtDNA haplotypes were restricted to a single breeding region. Genetic differences among regions were considerably lower for nuclear DNA loci (sex‐linked: φ_ST= 0.001, P > 0.05; biparentally inherited microsatellites: mean θ= 0.001, P > 0.05) than was observed for mtDNA. Using models explicitly designed for uniparental and biparentally inherited genes, estimates of spatial divergence based on nuclear and mtDNA data together with elements of the species' breeding ecology were used to estimate effective population size and degree of male and female gene flow. Differences in the magnitude and spatial patterns of gene correlations for maternally inherited and nuclear genes revealed that females exhibit greater natal philopatry than do males. Estimates of generational female and male rates of gene flow among breeding regions differed markedly (3.67 × 10^‐4 and 1.28 × 10^‐2, respectively). Effective population size for mtDNA was estimated to be at least three times lower than that for biparental genes (30,671 and 101,528, respectively). Large disparities in population sizes among breeding areas greatly reduces the proportion of total genetic variance captured by dispersal, which may accelerate rates of inbreeding (i.e., promote higher coancestries) within populations due to nonrandom pairing of males with females from the same breeding population.     

The common cuckoo Cuculus canorus is not locally adapted to its reed warbler Acrocephalus scirpaceus host

The obligate avian brood parasitic common cuckoo Cuculus canorus comprises different strains of females that specialize on particular host species by laying eggs of a constant type that often mimics those of the host. Whether cuckoos are locally adapted for mimicking populations of the hosts on which they are specialized has never been investigated. In this study, we first explored the possibility of local adaptation in cuckoo egg mimicry over a geographical mosaic of selection exerted by one of its main European hosts, the reed warbler Acrocephalus scirpaceus. Secondly, we investigated whether cuckoos inhabiting reed warbler populations with a broad number of alternative suitable hosts at hand were less locally adapted. Cuckoo eggs showed different degrees of mimicry to different reed warbler populations. However, cuckoo eggs did not match the egg phenotypes of their local host population better than eggs of other host populations, indicating that cuckoos were not locally adapted for mimicry on reed warblers. Interestingly, cuckoos exploiting reed warblers in populations with a relatively larger number of co-occurring cuckoo gentes showed lower than average levels of local adaptation in egg volume. Our results suggest that cuckoo local adaptation might be prevented when different cuckoo populations exploit more or fewer different host species, with gene flow or frequent host switches breaking down local adaptation where many host races co-occur.     

Isolation by time and habitat and coexistence of distinct host races of the common cuckoo

Isolation by time occurs when different populations of a single species reproduce at different times and thereby reduce the probability of interbreeding, potentially causing divergent adaptation to timing of reproduction, eventually resulting in ecological species separated by timing of reproduction. We analysed extensive data on timing of reproduction by different host races of the common cuckoo Cuculus canorus that is an obligate brood parasite laying eggs in the nests of many different species of passerine birds. Because different hosts breed at different times, specific host races of cuckoos have adapted to specific hosts by laying eggs when nests of these hosts are available, and such divergence may be further exaggerated by differences in timing of breeding among host races with similar habitat requirements. Host species accounted for a quarter of the variance in timing of breeding by the cuckoo. Common cuckoos reproduced at a similar, but narrower subset of dates as did possible hosts, showing that only a fraction of hosts with specific breeding dates were parasitized. Common cuckoo eggs laid in the 'right' kind of nests, phenotypically matching the eggs of the host, were laid later during the season than cuckoo eggs laid in the 'wrong' kind of nests where the eggs did not mimic those of the host. Pairs of sympatric cuckoo host races differed more in timing of breeding than pairs of allopatric host races, and pairs of cuckoo host races with similar breeding habitat differed more in breeding date than pairs of cuckoo host races with dissimilar habitat, as expected from reproductive character displacement. These findings are consistent with cuckoo host races being isolated by timing of breeding and habitat.     

Evidence from population genetics that the ectomycorrhizal basidiomycete Laccaria amethystina is an actual multihost symbiont

It is commonly assumed that ectomycorrhizal (ECM) fungi associated with temperate forest tree roots are not host-specific. Because this assumption relies on species delineations based on fruitbodies morphology or ribosomal DNA sequences, host-specific, cryptic biological species cannot be ruled out. To demonstrate that Laccaria amethystina has true generalist abilities, we sampled 510 fruitbodies on three French sites situated 150–450 km away from each other. At each site, populations from monospecific stands ( Abies alba , Castanea europea and Fagus sylvatica ) or mixed stands ( F. sylvatica  +  Quercus robur or Q. robur  + Carpinus betulus ) were sampled. Three different sets of markers were used for genotyping: (i) five microsatellite loci plus the ribosomal DNA intergenic spacer, (ii) the mitochondrial large ribosomal DNA subunit, and (iii) direct amplification of length polymorphism (DALP), a new method for fungi providing dominant markers. Evidence for allogamous populations (with possible inbreeding at local scale) and possibly for biparental mitochondrial inheritance was found. All markers congruently demonstrated that L. amethystina populations show little structure at this geographical scale, indicating high gene flow (as many as 50% of founding spores in all populations being of external origin). Our results also showed that host species contributed even less to population differentiation, and there was no evidence for cryptic biological species. This first in situ demonstration of a true multihost ability in an ECM species is discussed in terms of ecology and evolutionary biology.     

THE GENETIC STRUCTURE OF A GYNODIOECIOUS PLANT: NUCLEAR AND CYTOPLASMIC GENES

Sex expression in gynodioecious plants is often determined by an interaction between biparentally and maternally inherited genes. Their relative rates of gene flow should be considered when modeling the evolution of the sex ratio in structured populations. In order to understand patterns of gene flow in Silene vulgaris, a gynodioecious plant, genetic structure was estimated from biparentally inherited genetic markers (allozymes) and a maternally inherited marker (chloroplast DNA) using Wright's F_st. Based on data from 16 local populations, chloroplast DNA showed considerably more genetic structure than did allozymes (F_st values of 0.62 and 0.22, respectively). This suggests that the rate of gene flow is about three times greater for nuclear genes.     

Multiscale spatial genetic structure within and between populations of wild cherry trees in nuclear genotypes and chloroplast haplotypes

Spatial genetic structure (SGS) of plants mainly depends on the effective population size and gene dispersal. Maternally inherited loci are expected to have higher genetic differentiation between populations and more intensive SGS within populations than biparentally inherited loci because of smaller effective population sizes and fewer opportunities of gene dispersal in the maternally inherited loci. We investigated biparentally inherited nuclear genotypes and maternally inherited chloroplast haplotypes of microsatellites in 17 tree populations of three wild cherry species under different conditions of tree distribution and seed dispersal. As expected, interpopulation genetic differentiation was 6–9 times higher in chloroplast haplotypes than in nuclear genotypes. This difference indicated that pollen flow 4–7 times exceeded seed flow between populations. However, no difference between nuclear and chloroplast loci was detected in within‐population SGS intensity due to their substantial variation among the populations. The SGS intensity tended to increase as trees became more aggregated, suggesting that tree aggregation biased pollen and seed dispersal distances toward shorter. The loss of effective seed dispersers, Asian black bears, did not affect the SGS intensity probably because of mitigation of the bear loss by other vertebrate dispersers and too few tree generations after the bear loss to alter SGS. The findings suggest that SGS is more variable in smaller spatial scales due to various ecological factors in local populations.     

Socially acquired host-specific mimicry and the evolution of host races in Horsfield's bronze-cuckoo Chalcites basalis

Coevolution between parasites and their hosts typically leads to increasing specialization on host species by the parasite. Where multiple hosts are parasitized, specialization on each host can result in genetic divergence within the parasite population to create host races, and, ultimately, new species. We investigate how host-specific traits arise in Horsfield's bronze-cuckoo Chalcites basalis nestlings. Newly hatched cuckoos evict host young from the nest, yet in the absence of a model they accurately mimic the different begging calls of a primary host (superb fairy-wren, Malurus cyaneus) and a secondary host (buff-rumped thornbill, Acanthiza reguloides). Using cross-fostering experiments, we show that begging calls are modified after parasitism, through experience. Further, we demonstrate the mechanism by which mimetic calls are acquired. All cuckoo nestlings initially produced the call of their primary host. When cross-fostered as eggs to a secondary host, calls increased in variability and were rapidly modified to resemble those of the secondary host through shaping by host parents. We suggest that plasticity in the development of host-specific traits after parasitism is likely to reduce selection for host race formation.     

Habitat structure and the dispersal of male and female bottlenose dolphins (Tursiops truncatus)

Bottlenose dolphins (Tursiops truncatus) are widely distributed and a high degree of morphometric and genetic differentiation has been found among both allopatric and parapatric populations. We analysed 145 samples along a contiguous distributional range from the Black Sea to the eastern North Atlantic for mitochondrial and nuclear genetic diversity, and found population structure with boundaries that coincided with transitions between habitat regions. These regions can be characterized by ocean floor topography, and oceanographic features such as surface salinity, productivity and temperature. At the extremes of this range there was evidence for the directional emigration of females. Bi-parentally inherited markers did not show this directional bias in migration, suggesting a different dispersal strategy for males and females at range margins. However, comparative assessment based on mitochondrial DNA and nuclear markers indicated that neither sex showed a strong bias for greater dispersal on average. These data imply a mechanism for the evolutionary structuring of populations based on local habitat dependence for both males and females.     

A host-race of the cuckoo Cuculus canorus with nestlings attuned to the parental alarm calls of the host species

The common cuckoo has several host-specific races, each with a distinctive egg that tends to match its host's eggs. Here, we show that the host-race specializing on reed warblers also has a host-specific nestling adaptation. In playback experiments, the nestling cuckoos responded specifically to the reed warbler's distinctive 'churr' alarm (given when a predator is near the nest), by reducing begging calls (likely to betray their location) and by displaying their orange-red gape (a preparation for defence). When reed warbler-cuckoos were cross-fostered and raised by two other regular cuckoo hosts (robins or dunnocks), they did not respond to the different alarms of these new foster-parents. Instead, they retained a specific response to reed warbler alarms but, remarkably, increased both calling and gaping. This suggests innate pre-tuning to reed warbler alarms, but with exposure necessary for development of the normal silent gaping response. By contrast, cuckoo chicks of another host-race specializing on redstarts showed no response to either redstart or reed warbler alarms. If host-races are restricted to female cuckoo lineages, then chick-tuning in reed warbler-cuckoos must be under maternal control. Alternatively, some host-races might be cryptic species, not revealed by the neutral genetic markers studied so far.