Microsatellite resources for Passeridae species: a predicted microsatellite map of the house sparrow Passer domesticus

We identified microsatellite sequences of potential utility in the house sparrow (Passer domesticus) and assigned their predicted genome locations. These sequences included newly isolated house sparrow loci, which we fully characterized. Many of the newly isolated loci were polymorphic in two other species of Passeridae: Berthelot's pipit Anthus berthelotii and zebra finch Taeniopygia guttata. In total, we identified 179 microsatellite markers that were either isolated directly from, or are of known utility in, the house sparrow. Sixty-seven of these markers were designed from unique sequences that we isolated from a house sparrow genomic library. These new markers were combined with 36 house sparrow markers isolated by other studies and 76 markers isolated from other passerine species but known to be polymorphic in the house sparrow. We utilized sequence homology to assign chromosomal locations for these loci in the assembled zebra finch genome. One hundred and thirty-four loci were assigned to 25 different autosomes and eight loci to the Z chromosome. Examination of the genotypes of known-sex house sparrows for 37 of the new loci revealed a W-linked locus and an additional Z-linked locus. Locus Pdoμ2, previously reported as autosomal, was found to be Z-linked. These loci enable the creation of powerful and cost-effective house sparrow multiplex primer sets for population and parentage studies. They can be used to create a house sparrow linkage map and will aid the identification of quantitative trait loci in passerine species.     

Hybrid speciation in sparrows I: phenotypic intermediacy,genetic admixture and barriers to gene flow

Homoploid hybrid speciation is thought to require unusual circumstances to yield reproductive isolation from the parental species, and few examples are known from nature. Here, we present genetic evidence for this mode of speciation in birds. Using Bayesian assignment analyses of 751 individuals genotyped for 14 unlinked, nuclear microsatellite loci, we show that the phenotypically intermediate Italian sparrow (Passer italiae) does not form a cluster of its own, but instead exhibits clear admixture (over its entire breeding range) between its putative parental species, the house sparrow (P. domesticus) and the Spanish sparrow (P. hispaniolensis). Further, the Italian sparrow possesses mitochondrial (mt) DNA haplotypes identical to both putative parental species (although mostly of house sparrow type), indicating a recent hybrid origin. Today, the Italian sparrow has a largely allopatric distribution on the Italian peninsula and some Mediterranean islands separated from its suggested parental species by the Alps and the Mediterranean Sea, but co‐occurs with the Spanish sparrow on the Gargano peninsula in southeast Italy. No evidence of interbreeding was found in this sympatric population. However, the Italian sparrow hybridizes with the house sparrow in a sparsely populated contact zone in the Alps. Yet, the contact zone is characterized by steep clines in species‐specific male plumage traits, suggesting that partial reproductive isolation may also have developed between these two taxa. Thus, geographic and reproductive barriers restrict gene flow into the nascent hybrid species. We propose that an origin of hybrid species where the hybrid lineage gets geographically isolated from its parental species, as seems to have happened in this system, might be more common in nature than previously assumed.     

New polymorphic microsatellite loci in the house sparrow, Passer domesticus

We developed 13 new polymorphic microsatellite loci in the house sparrow (Passer domesticus), which exhibited from 2 to 15 alleles. Observed and expected heterozygosities ranged from 0.17 to 0.77 and from 0.35 to 0.85, respectively. We detected no linkage disequilibrium between loci. Allele frequencies supported Hardy-Weinberg equilibrium for 8 loci out of 13 after Bonferroni correction. Combined with loci previously isolated in the house sparrow, these new microsatellite markers provide valuable tools to study population genetics of this species.     

Hybrid speciation in sparrows II: a role for sex chromosomes?

Homoploid hybrid speciation in animals is poorly understood, mainly because of the scarcity of well‐documented cases. Here, we present the results of a multilocus sequence analysis on the house sparrow (Passer domesticus), Spanish sparrow (P. hispaniolensis) and their proposed hybrid descendant, the Italian sparrow (P. italiae). The Italian sparrow is shown to be genetically intermediate between the house sparrow and Spanish sparrow, exhibiting genealogical discordance and a mosaic pattern of alleles derived from either of the putative parental species. The average variation on the Z chromosome was significantly reduced compared with autosomal variation in the putative parental species, the house sparrow and Spanish sparrow. Additionally, divergence between the two species was elevated on the Z chromosome relative to the autosomes. This pattern of variation and divergence is consistent with reduced introgression of Z‐linked genes and/or a faster‐Z effect (increased rate of adaptive divergence on the Z). F_ST‐outlier tests were consistent with the faster‐Z hypothesis: two of five Z‐linked loci (CHD1Z and PLAA) were identified as candidates for being subject to positive, divergent selection in the putative parental species. Interestingly, the two latter genes showed a mosaic pattern in the (hybrid) Italian sparrow; that is, the Italian sparrow was found to be fixed for Spanish sparrow alleles at CHD1Z and to mainly have house sparrow alleles at PLAA. Preliminary evidence presented in this study thus suggests that sex chromosomes may play a significant role in this case of homoploid hybrid speciation.     

Characterization of microsatellite loci in the house fly,Musca domestica L. (Diptera: Muscidae)

The house fly, Musca domestica L., is a cosmopolitan species with a capacity to transmit human pathogens. Here, we report on the development of polymorphic microsatellite loci for house flies and present preliminary results from four house fly subpopulations from Manhattan, Kansas. Twenty‐four microsatellite loci were isolated and characterized using DNA enriched for repeat sequences. Forty individuals from four locations in Kansas were assayed to identify for polymorphic loci. Eight loci were polymorphic with the number of alleles ranging from three to six.     

North African hybrid sparrows (Passer domesticus,P. hispaniolensis) back from oblivion – ecological segregation and asymmetric mitochondrial introgression between parental species

A stabilized hybrid form of the house sparrow (Passer domesticus) and the Spanish sparrow (P. hispaniolensis) is known as Passer italiae from the Italian Peninsula and a few Mediterranean islands. The growing attention for the Italian hybrid sparrow and increasing knowledge on its biology and genetic constitution greatly contrast the complete lack of knowledge of the long‐known phenotypical hybrid sparrow populations from North Africa. Our study provides new data on the breeding biology and variation of mitochondrial DNA in three Algerian populations of house sparrows, Spanish sparrows, and phenotypical hybrids. In two field seasons, the two species occupied different breeding habitats: Spanish sparrows were only found in rural areas outside the cities and bred in open‐cup nests built in large jujube bushes. In contrast, house sparrows bred only in the town centers and occupied nesting holes in walls of buildings. Phenotypical hybrids were always associated with house sparrow populations. House sparrows and phenotypical hybrids started breeding mid of March, and most pairs had three successive clutches, whereas Spanish sparrows started breeding almost one month later and had only two successive clutches. Mitochondrial introgression is strongly asymmetric because about 75% of the rural Spanish sparrow population carried house sparrow haplotypes. In contrast, populations of the Italian hybrid form, P. italiae, were genetically least diverse among all study populations and showed a near‐fixation of house sparrow haplotypes that elsewhere were extremely rare or that were even unique for the Italian Peninsula. Such differences between mitochondrial gene pools of Italian and North African hybrid sparrow populations provide first evidence that different demographic histories have shaped the extant genetic diversity observed on both continents.     

Development and characterization of 11 microsatellite markers in the rock sparrow,Petronia petronia

Eleven polymorphic microsatellite loci were isolated in the passeriform Petronia petronia using the enrichment protocol FIASCO (fast isolation by AFLP of sequences containing repeats). We detected three to 13 alleles per locus in 25 specimens collected from an Italian population. The level of expected heterozygosity ranged from 0.439 to 0.856. One locus is sex linked to the Z chromosome. The total exclusionary probabilities using these loci for the first and the second parent were 0.978 and 0.999, respectively. These are the first microsatellite loci characterized from the rock sparrow that can be used for estimating population structure and for large‐scale parentage analysis.     

Genetic admixture despite ecological segregation in a North African sparrow hybrid zone (Aves,Passeriformes, Passer domesticus × Passer hispaniolensis)

Under different environmental conditions, hybridization between the same species might result in different patterns of genetic admixture. Particularly, species pairs with large distribution ranges and long evolutionary history may have experienced several independent hybridization events over time in different zones of overlap. In birds, the diverse hybrid populations of the house sparrow (Passer domesticus) and the Spanish sparrow (Passer hispaniolensis) provide a striking example. Throughout their range of sympatry, these two species do not regularly interbreed; however, a stabilized hybrid form (Passer italiae) exists on the Italian Peninsula and on several Mediterranean islands. The spatial distribution pattern on the Eurasian continent strongly contrasts the situation in North Africa, where house sparrows and Spanish sparrows occur in close vicinity of phenotypically intermediate populations across a broad mosaic hybrid zone. In this study, we investigate patterns of divergence and admixture among the two parental species, stabilized and nonstabilized hybrid populations in Italy and Algeria based on a mitochondrial marker, a sex chromosomal marker, and 12 microsatellite loci. In Algeria, despite strong spatial and temporal separation of urban early‐breeding house sparrows and hybrids and rural late‐breeding Spanish sparrows, we found strong genetic admixture of mitochondrial and nuclear markers across all study populations and phenotypes. That pattern of admixture in the North African hybrid zone is strikingly different from i) the Iberian area of sympatry where we observed only weak asymmetrical introgression of Spanish sparrow nuclear alleles into local house sparrow populations and ii) the very homogenous Italian sparrow population where the mitogenome of one parent (P. domesticus) and the Z‐chromosomal marker of the other parent (P. hispaniolensis) are fixed. The North African sparrow hybrids provide a further example of enhanced hybridization along with recent urbanization and anthropogenic land‐use changes in a mosaic landscape.     

Are house sparrow populations limited by the lack of cavities in urbanized landscapes? An experimental test

Current urban policies are associated with deep changes in urban structures, which may impoverish urban biodiversity. A major concern is the disappearance of nesting sites for wild vertebrate species living in urban areas. New urban structures without any cracks or cavities may especially preclude cavity nesters from breeding in cities and they may cause population declines. In that context, we experimentally investigated this question in an urban exploiter bird species (the house sparrow Passer domesticus), which is dramatically declining in most European cities. To test if the lack of cavities is limiting house sparrow populations in urban areas, we equipped 11 sites along an urbanization gradient with nest boxes and we then evaluated the rate of occupancy of these nest‐boxes. This urbanization gradient was characterized by very rural places (isolated farms) and moderately urbanized areas (town of medium size, i.e. 60 000 inhabitants). Surprisingly, rural nest boxes were more occupied than urban ones, suggesting that cavity availability is probably more constraining in rural areas relative to urban ones. Therefore, our study suggests that urban house sparrow populations are probably not constrained by a lack of nesting sites in medium size cities with urban designs similar to our city of interest (Niort, western France). This hypothesis definitely needs now to be tested in further urban landscapes (e.g. large cities and urban landscapes with other architecture and management policies).     

Single origin of human commensalism in the house sparrow

The current, virtually worldwide distribution of the house sparrow (Passer domesticus) is a result of its commensal relationship with humans. It has been suggested that long before the advent of agriculture, an early glacial advance resulted in two disjunct ranges of ancestral house sparrows - one in the Middle East and another on the Indian subcontinent. Differentiation during this period of isolation resulted in two major groups of subspecies: the domesticus group and the indicus group. According to this hypothesis, commensalism with humans would have evolved independently in the two regions and at least twice. An alternative hypothesis is that morphological differences between the subspecies represent very recent differentiation, following expansions from a single source. To test between these hypotheses, we analysed genetic variation at the mitochondrial DNA control region and at three nuclear loci from several house sparrow populations in Europe, Asia and North Africa. No differentiation between the indicus and domesticus groups was found, supporting the single origin hypothesis. One of the subspecies in the indicus group, P. d. bactrianus, differs ecologically from other house sparrows in being migratory and in preferentially breeding in natural habitat. We suggest that bactrianus represents a relict population of the ancestral, noncommensal house sparrow. When agricultural societies developed in the Middle East about 10 000 years ago, a local house sparrow population of the bactrianus type adapted to the novel environment and eventually became a sedentary, human commensal. As agriculture and human civilizations expanded, house sparrows experienced a correlated and massive expansion in range and numbers. The pattern of genetic variation analysed here is consistent with this scenario.     

Fitness consequences of hybridization between house sparrows (Passer domesticus) and tree sparrows (P. montanus)

Gene transfer may occur following hybridization between closely related species if hybrids are viable and able to breed with individuals of one or both of the parental species. House (Passer domesticus) and tree sparrows (P. montanus) occasionally hybridize and produce viable offspring. Previously, we concluded that male tree × house sparrow hybrids are most probably fertile based on the observation of a male F1 hybrid feeding the nestlings with a female house sparrow in two consecutive clutches. However, recent DNA analyses based on blood samples revealed that all nestlings (4) in the first clutch were sired by a neighbouring house sparrow male, whereas nestlings in the second clutch (2) were not blood sampled and most probably died before fledging. This indicates that extensive extra-pair fertilization confounded our previous conclusion, and indicates that social partnership and attending behaviour can be imprecise measures of paternity.     

Proportions of mammalian-type and reptilian-type nephrons in the kidneys of two passerine birds

We compared the proportions of mammalian-type and reptilian-type nephrons in the kidneys of two species of passerine birds. The desert house sparrow (Passer domesticus) is relatively well adapted for water conservation, whereas the white-crowned sparrow (Zonotrichia leucophrys) is more mesic adapted. The two species do not differ in body mass, but the kidneys of P. domesticus are significantly smaller than those of Z. leucophrys. Associated with its smaller size, the house sparrow kidney has significantly fewer glomeruli (35,700 per kidney) than does the white-crowned sparrow kidney (53,000 per kidney). The medullary cones, which contain the loops of Henle of the mammalian-type nephrons, are significantly longer in house sparrows than in white-crowned sparrows (2.2 vs. 1.9 mm). The number of medullary cones, the number of nephrons per medullary cone, and, hence, the number of mammalian-type nephrons do not differ between the two species. The smaller number of nephrons in the kidney of the house sparrow therefore represents a smaller number of reptilian-type nephrons. Desert house sparrows have 18% mammalian-type nephrons, whereas white-crowned sparrows have 10% mammaliantype nephrons. The relative reduction of reptilian-type nephrons in P. domesticus may reduce the flow of dilute urine through the collecting ducts, thereby permitting a greater concentration gradient to be established along the length of the medullary cones.     

Contrasting adaptive immune defenses and blood parasite prevalence in closely related Passer sparrows

Immune system components differ in their functions and costs, and immune defense profiles are likely to vary among species with differing ecologies. We compared adaptive immune defenses in two closely related species that have contrasting inflammatory immune responses, the widespread and abundant house sparrow (Passer domesticus) and the less abundant tree sparrow (Passer montanus). We found that the house sparrow, which we have previously shown mounts weaker inflammatory responses, exhibits stronger adaptive immune defenses, including antibody responses, natural antibody titers, and specific T-cell memory, than the tree sparrow. Conversely, tree sparrows, which mount strong inflammatory responses, also mount stronger nonspecific inflammatory T-cell responses but weaker specific adaptive responses. Prevalence of avian malaria parasite infections, which are controlled by adaptive immune defenses, was higher in the geographically restricted tree sparrow than in the ubiquitous house sparrow. Together these data describe distinct immune defense profiles between two closely related species that differ greatly in numbers and distributions. We suggest that these immunological differences could affect fitness in ways that contribute to the contrasting abundances of the two species in North American and Western Europe.     

House sparrow (Passer domesticus) habitat use in urbanized landscapes

The house sparrow (Passer domesticus) is showing population declines in many parts of Europe, with recent declines being particularly severe in urban areas. To date, relatively little is known about the species’ habitat associations within urbanized landscapes. We report here an investigation of the habitat associations of house sparrows using a survey of 1223 stratified randomly selected 500 × 500-m squares within urbanized landscapes of the UK, defined as at least 25% ‘human cover’. The densities of chirping male house sparrows and of all house sparrows were analysed separately to obtain insights into breeding habitat requirements and general habitat associations, respectively. Multi-model inference showed that residential areas (houses, flats), allotments (areas used for small-scale horticulture) and farm buildings were key predictors of house sparrow density and chirping male density. Separate analyses on landscapes of differing human cover showed similar results. Within residential areas, the increase of house sparrow density with habitat area (on a log scale) was approximately threefold greater when private gardens were present than when they were absent. The model predicted a rapid decline in house sparrow abundance when only a small area of private gardens is converted to continuous housing. Allotments and residential areas with gardens are likely to be under pressure due to increased demand for housing, specifically from the infilling of green space within urban areas. It would seem to be imperative that any action plan to protect urban house sparrow populations should include specific protection of such key habitats. Electronic supplementary material The online version of this article (doi:) contains supplementary material, which is available to authorized users.     

Contrasting levels of extra-pair paternity in mainland and island populations of the house sparrow (Passer domesticus): is there an 'island effect'?

Despite the many studies that have investigated the genetic mating system of socially monogamous birds, very little is known about the underlying causes of extra-pair paternity and few studies have attempted to test those hypotheses which have been suggested. This study describes die analysis of die genetic mating system of two populations of the house sparrow [Passer domesticus) , and uses the results from four other populations to test existing hypodieses using an intra-specific comparative approach. The parentage analysis was conducted using a combination of published and newly presented microsatellite loci isolated from the house sparrow. One population in Kentucky, U.S.A. was found to contain what may be considered to be a typical level of extra-pair paternity for mis species (10.5%, 19/185 offspring). The second, a population on the island of Lundy, UK, exhibited a very low level (1.3%, 4/305 offspring), significandy lower dian that in all the other populations studied so far. The finding of such diverse rates of extra-pair paternity, along with the existing estimates from ofher populations, has allowed us to test the effects of breeding density and genetic variation on die level of extra-pair paternity. We found no effect of either factor on the frequency of extra-pair paternity in the house sparrow, leaving the cause of this variation open to fresh ideas.     

Occurrence of keratinophilic fungi on Indian birds

Keratinophilic fungi were isolated from feathers of most common Indian birds,viz. domestic chicken (Gallus domesticus), domestic pigeon (Columba livia), house sparrow (Passer domesticus), house crow (Corvus splendens), duck (Anas sp.), rose-ringed parakeet (Psittacula krameri). Out of 87 birds, 58 yielded 4 keratinophilic fungal genera representing 13 fungal species and one sterile mycelium. The isolated fungi were cultured on Sabouraud's dextrose agar at 28±2°C.Chrysosporium species were isolated on most of the birds.Chrysosporium lucknowense andChrysosporium tropicum were the most common fungal species associated with these Indian birds. Maximum occurrence of fungi (47%) was recorded on domestic chickens and the least number of keratinophilic fungi was isolated from the domestic pigeon and duck. The average number of fungi per bird was found to be the 0.44.     

Does the house sparrow Passer domesticus represent a global model species for egg rejection behavior?

Conspecific brood parasitism (CP) is a facultative breeding tactic whereby females lay their eggs in the nests of conspecifics. In some species, potential hosts have evolved the ability to identify and reject foreign eggs from their nest. Previous studies suggest that the ubiquitous house sparrow Passer domesticus in Spain and South Africa employs both CP and egg rejection, while a population in China does not. Given the species’ invasive range expansions, the house sparrow represents a potentially excellent global model system for parasitic egg rejection across variable ecological conditions. We examined the responses of house sparrows to experimental parasitism at three geographically distinct locations (in Israel, North America, and New Zealand) to provide a robust test of how general the findings of the previous studies are. In all three geographic regions egg rejection rates were negligible and not statistically different from background rates of disappearance of control eggs, suggesting that the house sparrow is not a suitable model species for egg rejection experiments on a global scale.     

A genome‐wide linkage map for the house sparrow (Passer domesticus) provides insights into the evolutionary history of the avian genome

The house sparrow is an important model species for studying physiological, ecological and evolutionary processes in wild populations. Here, we present a medium density, genome wide linkage map for house sparrow (Passer domesticus) that has aided the assembly of the house sparrow reference genome, and that will provide an important resource for ongoing mapping of genes controlling important traits in the ecology and evolution of this species. Using a custom house sparrow 10 K iSelect Illumina SNP chip we have assigned 6,498 SNPs to 29 autosomal linkage groups, based on a mean of 430 informative meioses per SNP. The map was constructed by combining the information from linkage with that of the physical position of SNPs within scaffold sequences in an iterative process. Averaged between the sexes; the linkage map had a total length of 2,004 cM, with a longer map for females (2,240 cM) than males (1,801 cM). Additionally, recombination rates also varied along the chromosomes. Comparison of the linkage map to the reference genomes of zebra finch, collared flycatcher and chicken, showed a chromosome fusion of the two avian chromosomes 8 and 4A in house sparrow. Lastly, information from the linkage map was utilized to conduct analysis of linkage disequilibrium (LD) in eight populations with different effective population sizes (N_e) in order to quantify the background level LD. Together, these results aid the design of future association studies, facilitate the development of new genomic tools and support the body of research that describes the evolution of the avian genome.