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Patterns of genetic, phenotypic, and acoustic variation across a chiffchaff ( Phylloscopus collybita abietinus/tristis ) hybrid zone

View Article: PubMed Central - PubMed

ABSTRACT

Characterizing patterns of evolution of genetic and phenotypic divergence between incipient species is essential to understand how evolution of reproductive isolation proceeds. Hybrid zones are excellent for studying such processes, as they provide opportunities to assess trait variation in individuals with mixed genetic background and to quantify gene flow across different genomic regions. Here, we combine plumage, song, mtDNA and whole‐genome sequence data and analyze variation across a sympatric zone between the European and the Siberian chiffchaff (Phylloscopus collybita abietinus/tristis) to study how gene exchange between the lineages affects trait variation. Our results show that chiffchaff within the sympatric region show more extensive trait variation than allopatric birds, with a large proportion of individuals exhibiting intermediate phenotypic characters. The genomic differentiation between the subspecies is lower in sympatry than in allopatry and sympatric birds have a mix of genetic ancestry indicating extensive ongoing and past gene flow. Patterns of phenotypic and genetic variation also vary between regions within the hybrid zone, potentially reflecting differences in population densities, age of secondary contact, or differences in mate recognition or mate preference. The genomic data support the presence of two distinct genetic clades corresponding to allopatric abietinus and tristis and that genetic admixture is the force underlying trait variation in the sympatric region—the previously described subspecies (“fulvescens”) from the region is therefore not likely a distinct taxon. In addition, we conclude that subspecies identification based on appearance is uncertain as an individual with an apparently distinct phenotype can have a considerable proportion of the genome composed of mixed alleles, or even a major part of the genome introgressed from the other subspecies. Our results provide insights into the dynamics of admixture across subspecies boundaries and have implications for understanding speciation processes and for the identification of specific chiffchaff individuals based on phenotypic characters.

No MeSH data available.


The proportion of diagnostic SNPs in the 20 samples from the sympatric zone that were selected for whole‐genome sequencing. The bars indicate the proportions that are of either abietinus (green) or tristis (yellow) origin. The fraction of heterozygous SNPs in an individual is marked with barred green. Samples are grouped by morphotype, mtDNA haplotype, and song type. Individuals S1–S10 are samples from the southern sympatric region, and individuals N1–N10 are samples from the northern sympatric region
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ece32782-fig-0002: The proportion of diagnostic SNPs in the 20 samples from the sympatric zone that were selected for whole‐genome sequencing. The bars indicate the proportions that are of either abietinus (green) or tristis (yellow) origin. The fraction of heterozygous SNPs in an individual is marked with barred green. Samples are grouped by morphotype, mtDNA haplotype, and song type. Individuals S1–S10 are samples from the southern sympatric region, and individuals N1–N10 are samples from the northern sympatric region

Mentions: To compare the genomic composition of whole‐genome sequenced samples from within the sympatric zone with their phenotypes, we assessed the presence of SNPs found to be fixed (low‐stringency data set, n = 3,555) between allopatric abietinus and tristis. This is summarized in Figure 2. For birds with the tristis morphotype, a majority of the nuclear SNPs were homozygous for diagnostic tristis alleles, while there was much more variation for birds with the abietinus morphotype, and there was a strong association between the proportion of diagnostic SNPs and the mtDNA haplotype. However, morphotype, mtDNA type, and genomic composition did not always match. For example, sample N1 had typical abietinus morphotype, but a very large fraction of tristis diagnostic SNPs and a tristis mtDNA haplotype, and sample S4 had typical tristis morphotype and was homozygous for >95% of diagnostic tristis alleles but actually had abietinus mtDNA (Figure 2). Among the samples from the sympatric zone that were scored for genome‐wide SNP polymorphisms, we had acoustic information for 14. Two performed typical abietinus song and both of these had a large fraction of abietinus diagnostic genetic markers (>95%) and abietinus mtDNA type. Of the 12 individuals with mixed song type, six had tristis morphotype and six had abietinus morphotype. A majority of these individuals (10/12) had a combination with a high fraction of tristis diagnostic SNPs and tristis mtDNA, while one bird (S6) had abietinus mtDNA and a large proportion of abietinus diagnostic SNPs. Another bird (S4 again) had abietinus mtDNA but >95% of diagnostic tristis nuclear SNP alleles (Figure 2).


Patterns of genetic, phenotypic, and acoustic variation across a chiffchaff ( Phylloscopus collybita abietinus/tristis ) hybrid zone
The proportion of diagnostic SNPs in the 20 samples from the sympatric zone that were selected for whole‐genome sequencing. The bars indicate the proportions that are of either abietinus (green) or tristis (yellow) origin. The fraction of heterozygous SNPs in an individual is marked with barred green. Samples are grouped by morphotype, mtDNA haplotype, and song type. Individuals S1–S10 are samples from the southern sympatric region, and individuals N1–N10 are samples from the northern sympatric region
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Related In: Results  -  Collection

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ece32782-fig-0002: The proportion of diagnostic SNPs in the 20 samples from the sympatric zone that were selected for whole‐genome sequencing. The bars indicate the proportions that are of either abietinus (green) or tristis (yellow) origin. The fraction of heterozygous SNPs in an individual is marked with barred green. Samples are grouped by morphotype, mtDNA haplotype, and song type. Individuals S1–S10 are samples from the southern sympatric region, and individuals N1–N10 are samples from the northern sympatric region
Mentions: To compare the genomic composition of whole‐genome sequenced samples from within the sympatric zone with their phenotypes, we assessed the presence of SNPs found to be fixed (low‐stringency data set, n = 3,555) between allopatric abietinus and tristis. This is summarized in Figure 2. For birds with the tristis morphotype, a majority of the nuclear SNPs were homozygous for diagnostic tristis alleles, while there was much more variation for birds with the abietinus morphotype, and there was a strong association between the proportion of diagnostic SNPs and the mtDNA haplotype. However, morphotype, mtDNA type, and genomic composition did not always match. For example, sample N1 had typical abietinus morphotype, but a very large fraction of tristis diagnostic SNPs and a tristis mtDNA haplotype, and sample S4 had typical tristis morphotype and was homozygous for >95% of diagnostic tristis alleles but actually had abietinus mtDNA (Figure 2). Among the samples from the sympatric zone that were scored for genome‐wide SNP polymorphisms, we had acoustic information for 14. Two performed typical abietinus song and both of these had a large fraction of abietinus diagnostic genetic markers (>95%) and abietinus mtDNA type. Of the 12 individuals with mixed song type, six had tristis morphotype and six had abietinus morphotype. A majority of these individuals (10/12) had a combination with a high fraction of tristis diagnostic SNPs and tristis mtDNA, while one bird (S6) had abietinus mtDNA and a large proportion of abietinus diagnostic SNPs. Another bird (S4 again) had abietinus mtDNA but >95% of diagnostic tristis nuclear SNP alleles (Figure 2).

View Article: PubMed Central - PubMed

ABSTRACT

Characterizing patterns of evolution of genetic and phenotypic divergence between incipient species is essential to understand how evolution of reproductive isolation proceeds. Hybrid zones are excellent for studying such processes, as they provide opportunities to assess trait variation in individuals with mixed genetic background and to quantify gene flow across different genomic regions. Here, we combine plumage, song, mtDNA and whole‐genome sequence data and analyze variation across a sympatric zone between the European and the Siberian chiffchaff (Phylloscopus collybita abietinus/tristis) to study how gene exchange between the lineages affects trait variation. Our results show that chiffchaff within the sympatric region show more extensive trait variation than allopatric birds, with a large proportion of individuals exhibiting intermediate phenotypic characters. The genomic differentiation between the subspecies is lower in sympatry than in allopatry and sympatric birds have a mix of genetic ancestry indicating extensive ongoing and past gene flow. Patterns of phenotypic and genetic variation also vary between regions within the hybrid zone, potentially reflecting differences in population densities, age of secondary contact, or differences in mate recognition or mate preference. The genomic data support the presence of two distinct genetic clades corresponding to allopatric abietinus and tristis and that genetic admixture is the force underlying trait variation in the sympatric region—the previously described subspecies (“fulvescens”) from the region is therefore not likely a distinct taxon. In addition, we conclude that subspecies identification based on appearance is uncertain as an individual with an apparently distinct phenotype can have a considerable proportion of the genome composed of mixed alleles, or even a major part of the genome introgressed from the other subspecies. Our results provide insights into the dynamics of admixture across subspecies boundaries and have implications for understanding speciation processes and for the identification of specific chiffchaff individuals based on phenotypic characters.

No MeSH data available.