Evidence for Mito-Nuclear and Sex-Linked Reproductive Barriers between the Hybrid Italian Sparrow and Its Parent Species (original) (raw)
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Hybrid speciation through sorting of parental incompatibilities in Italian sparrows
Molecular Ecology, 2014
Speciation by hybridization is emerging as a significant contributor to biological diversification. Yet, little is known about the relative contributions of (i) evolutionary novelty and (ii) sorting of preexisting parental incompatibilities to the build-up of reproductive isolation under this mode of speciation. Few studies have addressed empirically whether hybrid animal taxa are intrinsically isolated from their parents, and no study has so far investigated by which of the two aforementioned routes intrinsic barriers evolve. Here, we show that sorting of preexisting parental incompatibilities contributes to intrinsic isolation of a hybrid animal taxon. Using a genomic cline framework, we demonstrate that the sex-linked and mito-nuclear incompatibilities isolating the homoploid hybrid Italian sparrow at its two geographically separated hybrid-parent boundaries represent a subset of those contributing to reproductive isolation between its parent species, house and Spanish sparrows.
Hybrid speciation in sparrows II: a role for sex chromosomes?
Molecular Ecology, 2011
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.
Resolution of conflict between parental genomes in a hybrid species
bioRxiv (Cold Spring Harbor Laboratory), 2017
The development of reproductive barriers against parent species is crucial during hybrid speciation, and post-zygotic isolation can be important in this process. Genetic incompatibilities that normally isolate the parent species can become sorted in hybrids to form reproductive barriers towards either parent. However, the extent to which this sorting process is systematically biased and therefore predictable in which loci are involved and which alleles are favored is largely unknown. Theoretically, reduced fitness in hybrids due to the mixing of differentiated genomes can be resolved through rapid evolution towards allelic combinations ancestral to lineage-splitting of the parent species, as these alleles have successfully coexisted in the past. However, for each locus, this effect may be influenced by its chromosomal location, function, and interactions with other loci. We use the Italian sparrow, a homoploid hybrid species that has developed post-zygotic barriers against its parent species, to investigate this prediction. We show significant bias towards fixation of the ancestral allele among 57 nuclear intragenic SNPs, particularly those with a mitochondrial function whose ancestral allele came from the same parent species as the mitochondria. Consistent with increased pleiotropy leading to stronger fitness effects, genes with more protein-protein interactions were more biased in favor of the ancestral allele. Furthermore, the number of protein-protein interactions was especially low among candidate incompatibilities still segregating within Italian sparrows, suggesting that low pleiotropy allows steep intraspecific clines in allele frequencies to form. Finally, we report evidence for pervasive epistatic interactions within one Italian sparrow population, particularly involving loci isolating the two parent species but not hybrid and parent. However there was a lack of classic incompatibilities and no admixture linkage disequilibrium. This suggests that parental genome
Journal of Ornithology, 2005
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.
Journal of Evolutionary Biology, 2001
Mating pattern and gene¯ow were studied in the contact zone between two morphologically very similar Chiffchaff taxa (Phylloscopus collybita, P. brehmii) in SW France and northern Spain. Mating was assortative in brehmii, but not in collybita. Mixed matings were strongly asymmetric (excess of collybita male´brehmii female pairs), but did produce viable offspring in some cases. Sequence divergence of the mitochondrial cytochrome b gene was 4.6%. Haplotypes segregated signi®cantly with phenotype (only ®ve`mismatches' among 94 individuals), demonstrating that mitochondrial gene¯ow was very restricted. The estimated proportion of F 1 hybrids in the reproductive population was signi®cantly lower than expected under a closed population model, indicating strong selection against hybrids. Genetic typing of 101 individuals at four microsatellite loci also showed signi®cant population differentiation, but nuclear gene¯ow was estimated to be 75 times higher than mitochondrial gene¯ow. This strong discrepancy is probably due to unisexual hybrid sterility (Haldane's rule). Thus, there is a strong, but incomplete, reproductive barrier between these taxa.
Journal of Evolutionary Biology, 2015
Bird plumage clines and hybrid speciation Main text word count: 7077 2 Tables, 4 Figures. Homoploid hybrid speciation (HHS) requires reproductive barriers between hybrid and parent species, despite incomplete reproductive isolation (RI) between the parents. Novel secondary sexual trait values in hybrids may cause prezygotic isolation from both parents, while signals inherited by the hybrid from one parent species may cause prezygotic isolation with the other. Here we investigate whether differences in male plumage function as a premating barrier between the hybrid Italian sparrow and one of its parent species, the house sparrow, in a narrow Alpine hybrid zone. Italian sparrow male plumage is a composite mosaic of the parental traits, with its head plumage most similar to its other parent, the Spanish sparrow. We use geographical cline analysis to examine selection on three plumage traits, 75 nuclear SNPs and hybrid indices based on these SNPs. Several SNPs showed evidence of restricted introgression in the Alps, supporting earlier findings. Crown colour exhibited the narrowest plumage cline, representing a 37% (range 4-65%) drop in fitness. The cline was too narrow to be due to neutral introgression. Only crown colour was significantly bimodal in the hybrid zone. Bimodality may be due to RI or a major QTL, although fitness estimates suggest that selection contributes to the pattern. We discuss the implications with respect to HHS and the species status of the Italian sparrow.
Intraspecific genomic variation and local adaptation in a young hybrid species
2019
Hybridization increases genetic variation, hence hybrid species may have a strong evolutionary potential once their admixed genomes have stabilized and incompatibilities have been purged. Yet, little is known about how such hybrid lineages evolve at the genomic level following their formation, in particular the characteristics of their adaptive potential, i.e. constraints and facilitations of diversification. Here we investigate how the Italian sparrow (Passer italiae), a homoploid hybrid species, has evolved and locally adapted to its variable environment. Using restriction site-associated DNA sequencing (RAD-seq) on several populations across the Italian peninsula, we evaluate how genomic constraints and novel genetic variation have influenced population divergence and adaptation. We show that population divergence within this hybrid species has evolved in response to climatic variation. As in non-hybrid species, climatic differences may even reduce gene flow between populations, ...
Mitochondrial heteroplasmy in an avian hybrid form (Passer italiae: Aves, Passeriformes)
Mitochondrial DNA Part B
Mitochondrial heteroplasmy is the result from biparental transmission of mitochondrial DNA (mtDNA) to the offspring. In such rare cases, maternal and paternal mtDNA is present in the same individual. Though recent studies suggested that mtDNA heteroplasmy might be more common than previously anticipated, that phenomenon is still poorly documented and was mostly detected in case studies on hybrid populations. The Italian sparrow, Passer italiae is a homoploid hybrid form that occurs all across the Italian Peninsula mostly under strict absence of either of its parent species, the house sparrow (P. domesticus) and the Spanish sparrow (P. hispaniolensis). In this study, we document a new case of mitochondrial heteroplasmy from two island populations of P. italiae (Ustica and Lipari). Our analysis was based on the mitochondrial NADH dehydrogenase subunit 2 (ND2) that allows for a clear distinction between mitochondrial lineages of the two parental species. We amplified and sequenced the mitochondrial ND2 gene with specifically designed primer combinations for each of the two parental species. In two of our study populations, a single individual carried two different ND2 haplotypes from each of the two parental lineages. These findings contribute to current knowledge on the still poorly documented phenomenon of paternal leakage in vertebrates.