van Riemsdijk I et al. (2023), Two transects reveal remarkable variation in ge...

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Heredity (Edinb) 2023 Jul 01;1311:15-24. doi: 10.1038/s41437-023-00617-6.

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Two transects reveal remarkable variation in gene flow on opposite ends of a European toad hybrid zone.

van Riemsdijk I , Arntzen JW , Bucciarelli GM , McCartney-Melstad E , Rafajlović M , Scott PA , Toffelmier E , Shaffer HB , Wielstra B .

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Speciation entails a reduction in gene flow between lineages. The rates at which genomic regions become isolated varies across space and time. Barrier markers are linked to putative genes involved in (processes of) reproductive isolation, and, when observed over two transects, indicate species-wide processes. In contrast, transect-specific putative barrier markers suggest local processes. We studied two widely separated transects along the 900 km hybrid zone between Bufo bufo and B. spinosus, in northern and southern France, for ~1200 RADseq markers. We used genomic and geographic cline analyses to identify barrier markers based on their restricted introgression, and found that some markers are transect-specific, while others are shared between transects. Twenty-six barrier markers were shared across both transects, of which some are clustered in the same chromosomal region, suggesting that their associated genes are involved in reduced gene flow across the entire hybrid zone. Transect-specific barrier markers were twice as numerous in the southern than in the northern transect, suggesting that the overall barrier effect is weaker in northern France. We hypothesize that this is consistent with a longer period of secondary contact in southern France. The smaller number of introgressed genes in the northern transect shows considerably more gene flow towards the southern (B. spinosus) than the northern species (B. bufo). We hypothesize that hybrid zone movement in northern France and hybrid zone stability in southern France explain this pattern. The Bufo hybrid zone provides an excellent opportunity to separate a general barrier effect from localized gene flow-reducing conditions.

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	Fig. 1: Overview of the Bufo hybrid zone and genetic data presented in this study. Maps with (a) the distribution of Bufo bufo and B. spinosus in Europe and North Africa, with small labeled squares indicating the locations of insert map (b) for the northern transect (sample locations 6.N-16.N), and insert map (c) for the southern transect (sample locations 6.S-17.S). The reference populations for B. bufo are 1-5.Bb, and for B. spinosus are 18-22.Bs. The base map for panels b and c was downloaded from mapsland. Bar graphs in panels b and c are the result of Structure with K = 2 on the full 50% missingness dataset, taking a random SNP from each of the 4869 assembled RAD markers. Blue indicates B. bufo ancestry, red bars indicate B. spinosus. Panel d shows the principal component analysis of the same 50% dataset. The reference populations of B. bufo are colored blue and of B. spinosus red. Transect populations are black (“.N” = northern transect, “.S” = southern transect). Ellipses represent the 95% inertia (based on the percentile) of the corresponding group. The bar graph on the right shows the eigenvalues for the first 5 principle components.
	Fig. 2: Markers identified as β or α outlier by Bayesian genomic cline (BGC) analysis, also stand out in their geographic cline when comparing the parameters ‘center’ and ‘width’ (HZAR). Heterozygote deficiency outliers (β > 0) have steep geographic clines, both in the (a) northern transect and (b) southern transect. For markers showing directional introgression (α outliers in BGC), the geographical cline has a shifted center for both the (c) northern transect and (d) southern transect.
	Fig. 3: Geographic cline graphs coloured by Bayesian Genomic Cline (BGC) analysis outlier identification. Geographic clines for barrier markers (β > 0, green) for the (a) northern transect and (b) southern transect; markers showing introgression into B. spinosus (α < 0, orange) for the (c) northern transect and (d) southern transect; and markers showing introgression into B. bufo (α > 0, blue) for the (e) northern transect, and (f) southern transect. In all panels, frequency of the B. spinosus allele on the y-axis and distance along the transect on the x-axis. The gray clines are all other markers (including all outliers of other types). Inward ticks on the top of each graph and notation near inward ticks on the top of the graph (panels a and b only) refers to locations in Fig. 1.
	Fig. 4: Alignment of RAD markers to the B. bufo genome for each transect. Gray lines represent markers which were not identified as outlier by BGC analysis. Above the line are heterozygosity (β) outliers, below the line are directional gene flow outliers (α). Outlier identity is explained in the legend below the figure. Red arrows point to RAD markers which were heterozygote deficiency outliers in both transects.

References [+] :

Abbott, Hybridization and speciation. 2013, Pubmed