Resolution of conflict between parental genomes in a hybrid species

AbstractThe 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 admixture can continue to constrain evolution and prevent genome stabilization long after incompatibilities have been purged.</jats:p

Evidence for Mito-Nuclear and Sex-Linked Reproductive Barriers between the Hybrid Italian Sparrow and Its Parent Species

Studies of reproductive isolation between homoploid hybrid species and their parent species have rarely been carried out. Here we investigate reproductive barriers between a recently recognized hybrid bird species, the Italian sparrow Passer italiae and its parent species, the house sparrow P. domesticus and Spanish sparrow P. hispaniolensis. Reproductive barriers can be difficult to study in hybrid species due to lack of geographical contact between taxa. However, the Italian sparrow lives parapatrically with the house sparrow and both sympatrically and parapatrically with the Spanish sparrow. Through whole-transcriptome sequencing of six individuals of each of the two parent species we identified a set of putatively parent species-diagnostic single nucleotide polymorphism (SNP) markers. After filtering for coverage, genotyping success (>97%) and multiple SNPs per gene, we retained 86 species-informative, genic, nuclear and mitochondrial SNP markers from 84 genes for analysis of 612 male individuals. We show that a disproportionately large number of sex-linked genes, as well as the mitochondria and nuclear genes with mitochondrial function, exhibit sharp clines at the boundaries between the hybrid and the parent species, suggesting a role for mito-nuclear and sex-linked incompatibilities in forming reproductive barriers. We suggest that genomic conflict via interactions between mitochondria and sex-linked genes with mitochondrial function ("mother's curse") at one boundary and centromeric drive at the other may best explain our findings. Hybrid speciation in the Italian sparrow may therefore be influenced by mechanisms similar to those involved in non-hybrid speciation, but with the formation of two geographically separated species boundaries instead of one. Spanish sparrow alleles at some loci have spread north to form reproductive barriers with house sparrows, while house sparrow alleles at different loci, including some on the same chromosome, have spread in the opposite direction to form barriers against Spanish sparrows

Data from: Strong selection on male plumage in a hybrid zone between a hybrid bird species and one of its parents

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, whereas 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 single nucleotide polymorphisms (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

AlpsSparrowdata

All individual-level SNP and plumage data used in cline-fitting. This includes: genotypes of 75 SNPs; plumage trait values (discriminant axis scores for multivariate traits) for crown colour, cheek colour and eyebrow colour; a molecular hybrid index based on 75 SNPs; a molecular hybrid index based on 4 SNPs. See publication for more details

Test for gene exchange in sympatry.

<p>FST values between Gargano peninsula populations of Spanish sparrows and sympatric (Lesina) and nearby allopatric Italian sparrows.</p><p>indicates highly significant genotypic divergence, <i>P</i><0.0001.</p

Candidate RI genes revealed by genomic cline analysis.

<p>(A–B) Markers are ordered along chromosomes as in <a href="http://www.plosgenetics.org/article/info:doi/10.1371/journal.pgen.1004075#pgen.1004075.s008" target="_blank">Table S3</a>. (A) <i>BGC</i> run 2 estimates of genomic cline center (α) with 95% credibility intervals for all 86 SNP markers. Red dots indicate markers with significant excess house sparrow ancestry, blue dots indicate markers with significant excess Spanish sparrow ancestry, grey dots indicate markers with either significant house or Spanish excess ancestry but where the difference in allele frequency between the parent species are below 0.5, and black dots indicate markers that do not differ from neutral expectations. (B) <i>BGC</i> run 2 estimates of genomic cline rate (β) with 95% credibility intervals for all 86 SNP markers. Orange dots indicate markers with clines significantly steeper than neutral expectations, white dots indicate markers with significantly shallower clines than neutral expectations, grey dots indicate markers with either significantly steeper or shallower clines than neutral expectations but where the difference in allele frequency between the parent species is below 0.5, and black dots indicate markers that do not differ from neutral expectations. (C) Genomic cline center (α) plotted against genomic cline rate (β). Red dots indicate markers that exhibit significant excess house sparrow (<i>P. d.</i>) ancestry, clines steeper than neutral expectations and where the difference in allele frequency between the parent species is greater than 0.5. The red dots that are encircled and named shift at the Italian-Spanish boundary and are hence candidate RI genes. Blue dots indicate markers that exhibit significant excess Spanish sparrow (<i>P. h.</i>) ancestry, clines steeper than neutral expectations and where the difference in allele frequency between the parent species is greater than 0.5. The blue dots that are encircled and named shift at the Italian-house boundary and are hence candidate RI genes. Green dots indicate markers that have allele frequency differences between the parent species greater than 0.5 and clines steeper than neutral expectations but do not exhibit excess house or Spanish sparrow ancestry. These markers are candidates for being incompatibilities within the Italian sparrow. Grey dots indicate markers in which the allele frequency difference between the parent species is less than 0.5. (D). Examples of <i>BGC</i> genomic clines representative of the marker categories described in panel (C). For illustrations of all clines, see <a href="http://www.plosgenetics.org/article/info:doi/10.1371/journal.pgen.1004075#pgen.1004075.s002" target="_blank">Figure S2</a>.</p

Phenotypic and genetic makeup of the hybrid Italian sparrow.

<p>Coloration of the map denotes phenotypic distribution as indicated by the bird drawings to the right of the map (blue: house sparrow, turquoise: Italian-house hybrids, yellow: typical Italian sparrow, orange: Italian sparrows with plumage intermediate between typical Italian and Spanish sparrows, red: Spanish sparrow). Bird drawings indicate species-specific male plumage characteristics of the three taxa <a href="http://www.plosgenetics.org/article/info:doi/10.1371/journal.pgen.1004075#pgen.1004075-SummersSmith1" target="_blank">[16]</a>. Pie charts denote mean hybrid index at sampling localities where white and black color indicate house and Spanish sparrow genetic contribution, respectively. Locations with evidence of recent gene exchange between Spanish and Italian sparrows are indicated by arrows.</p

Genetic incompatibilities between the hybrid Italian sparrow and its parent species.

<p>(A) Representative geographic cline (<i>ND2</i>) for the mitochondrion and Z-linked genes shifting significantly between the Italian and Spanish sparrows of mainland Italy/Sicily and Sardinia. Colors refer to posterior likelihood of belonging to group corresponding to the Italian sparrow (>0.9, no color) relative to the Spanish sparrow (<0.1, red). The numbers refer to three transects through the Italian-house sparrow hybrid zone in the Alps. Black dots denote sampling locations. (B) Genomic location (in zebra finch) of genes inferred to be involved in hybrid-parent reproductive isolation. Blue outlines denote genes shifting significantly between the Italian and house sparrow, and red outlines denote genes shifting significantly between the Italian and Spanish sparrow. Markers highlighted in yellow have significantly steeper clines (significant β) than the neutral expectation according to a <i>BGC</i>-analysis (see main text) in addition to being significantly skewed towards either hybrid-parent species boundary (significant α), and hence represent the strongest candidate RI genes. Markers in white have significant α only. Chromosomal location for the Z-linked and Chr. 4A genes are indicated. (C) Geographic clines along transect 2 for the three genes shifting significantly in the Italian-house sparrow hybrid zone in the Alps. Upper panel shows results from the Z-linked genes <i>CHD1Z</i>/<i>CETN3</i>, lower panel shows results for the autosomal gene <i>RPS4</i>. Colors refer to posterior likelihood of belonging to group corresponding to the house sparrow (>0.9, white) relative to the Italian sparrow (<0.1, red). Black dots denote sampling locations.</p

Hybrid speciation through sorting of parental incompatibilities in Italian sparrows

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 pre-existing 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 pre-existing parental incompatibilities contributes to intrinsic isolation of a hybrid animal taxon. Using a genomic cline framework, we demonstrate that the sex-linked and mitonuclear 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. Should such a sorting mechanism prove to be pervasive, the circumstances promoting homoploid hybrid speciation may be broader than currently thought, and indeed, there may be many cryptic hybrid taxa separated from their parent species by sorted, inherited incompatibilities

bgc input file for house sparrow parental population (reference population) when analysing autosomal loci separately

input file for house sparrow parental population (reference population) when analysing autosomal loci separately in parental sympatr