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Ancient Hybridization Fuels Rapid Cichlid Fish Adaptive Radiations


Ancient Hybridization Fuels Rapid Cichlid Fish Adaptive Radiations

Joana I Meier et al. Nat Commun.


Understanding why some evolutionary lineages generate exceptionally high species diversity is an important goal in evolutionary biology. Haplochromine cichlid fishes of Africa's Lake Victoria region encompass >700 diverse species that all evolved in the last 150,000 years. How this 'Lake Victoria Region Superflock' could evolve on such rapid timescales is an enduring question. Here, we demonstrate that hybridization between two divergent lineages facilitated this process by providing genetic variation that subsequently became recombined and sorted into many new species. Notably, the hybridization event generated exceptional allelic variation at an opsin gene known to be involved in adaptation and speciation. More generally, differentiation between new species is accentuated around variants that were fixed differences between the parental lineages, and that now appear in many new combinations in the radiation species. We conclude that hybridization between divergent lineages, when coincident with ecological opportunity, may facilitate rapid and extensive adaptive radiation.

Conflict of interest statement

The authors declare no competing financial interests.


Figure 1
Figure 1. Phylogenetic context of the Lake Victoria Region cichlid radiation.
(a) Maximum likelihood phylogeny built from concatenated RADtag sequences of Lake Victoria Region Superflock (LVRS) cichlids and relatives including all known lineages of haplochromine cichlids (n=156). Radiations are indicated as grey triangles in the phylogenetic tree and multiple samples of a lineage are visually collapsed to a single terminal branch (full tree in Supplementary Fig. 1). Members of the LVRS (including Haplochromis sp. ‘Nyangara' from the Rusizi River and Haplochromis spp. Egypt, see Supplementary Discussion) are indicated with orange stars both in the tree and in the sampling map (b) and are labelled by lake (L) or river (R) they were sampled in. ‘Congolese lineage' LVRS relatives are highlighted with red triangles, members of the ‘Upper Nile lineage' with blue triangles, those from Eastern rivers with dark blue squares, and all other more distantly related lineages with black circles. (b) Sampling map. River drainage systems that we sampled are shown as coloured polygons. The radiation ancestor's closest living relatives are shown in images: ‘Haplochromis' gracilior/Thoracochromis pharyngalis from the Upper Nile lineage and Astatotilapia sp. ‘Yaekama'/A. stappersi from the Congolese lineage. The Lake Victoria cichlids shown in the grey triangle on the right represent some of the many and varied species that arose from the hybrid swarm (Photo credits: Ole Seehausen, Salome Mwaiko, Frans Witte, ‘Teleos', Uli Schliewen, Adrian Indermaur, Oliver Selz; map adapted from
Figure 2
Figure 2. Evidence for Congo-Nilotic hybridization in the ancestry of the LVRS.
(a) Schematic genealogy with taxa used for D statistics (n=73 individuals, see Supplementary Data 2). Abbreviations used in other panels are given in parentheses and the color scheme is the same as in Figure 1. The inferred gene flow edge is shown with an arrow (Note the directionality of gene flow is inferred with the five-population test not shown in this figure). (b) D statistics to test for potential gene flow between each Eastern and Upper Nile taxon (P3) separately (abbreviations given in a) and cichlids from each LVR lake radiation (P1) or the Congolese taxon A. stappersi (P2). Vertical bars correspond to three standard errors. Positive D values indicate gene flow between P1 (LVR lake radiation) and P3 (Eastern or Upper Nile taxon), whereas negative D values indicate gene flow between P2 (A. stappersi) and P3 (Eastern or Upper Nile taxon) as illustrated in (c). Exact values and more test results are given in Supplementary Table 2.
Figure 3
Figure 3. Congo-Nilotic ancestry blocks in LVRS genomes.
(a) The size distribution of putative ancestry blocks shows mostly small ancestry blocks and slightly larger Congolese (red) than Upper Nile blocks (blue). The plot shows the counts of ancestry blocks in different size categories summed up for five LVRS radiation species across all scaffolds calculated with 3 kb windows. As most blocks do not span multiple windows of 3 kb and many blocks cannot be clearly allocated to Congolese or Upper Nile ancestry (grey) (Supplementary Fig. 8), the average ancestry block size is likely 3 kb or smaller, consistent with hybridization many thousands of years ago. (b) Correlation of ancestry blocks between whole-genome sequenced LVRS members is high overall but decreases with phylogenetic distance. The boxplots show correlation of fd (ref. 78) in 10 kb windows between single individuals of conspecifics (Pundamilia individuals of the same species), sister species (Pu. pundamilia versus Pu. nyererei), more distantly related Lake Victoria (LVi) species (Paralabidochromis flavus versus Pu. pundamilia and Pu. nyererei), Lake Kivu (LKi) species (Pa. paucidens versus Harpagochromis vittatus) and Lake Victoria against Lake Kivu species. This suggests that all radiation member species share the same hybridization event in their ancient history but vary in how long after that event they remained part of the same recombining population. It also suggests that some of the admixture variation still segregates within individual species (indicated by the deviation from an fd correlation of 1 among conspecifics).
Figure 4
Figure 4. High LWS opsin diversity likely because of the ancient hybridization event.
The two major LWS opsin haplotype classes, I and II, in the LVRS (orange) are each shared exclusively with either the Congolese (A. stappersi and A. sp. ‘Yaekama', red) or the Upper Nile lineage (H. gracilior and T. pharyngalis, blue), respectively (details in Supplementary Fig. 7; Supplementary Data 3). LWS haplotype class I is generally associated with cichlids living in shallow and clear water habitats, whereas class II is associated with deeper and more turbid habitats. Speciation by divergence in habitat type seems to have been accompanied by fixation of alternative LWS haplotypes both at early and at late stages of the adaptive radiation. This is exemplified by near fixation of alternative haplotype classes between ecologically divergent genera such as shallow water rocky shore algae scrapers of Neochromis and Mbipia versus mud bottom detritivores of the genus Enterochromis, and by the young incipient species pair of Pundamilia macrocephala ‘blue' (living very shallow) and ‘yellow' (living deeper) which have predominantly alleles of haplotype class I and II, respectively (Photo credits: Ole Seehausen, Adrian Indermaur, ‘Teleos', Oliver Selz, Uli Schliewen).
Figure 5
Figure 5. Differential sorting of hybridization-derived variation in the LVRS.
(a) Sites fixed for alternative alleles in the Congolese (C) and Upper Nile (N) taxa are enriched for high global FST outlier SNPs in Lake Victoria. Of the 12,890 biallelic SNPs among six sympatric Lake Victoria species (shown in (b)), 340 are outliers of high global FST (LV outliers). We assigned SNPs to five different ancestry categories according to the presence or absence of the two alleles in the Congolese (C) and Upper Nile (N) lineage taxa. The grey bars show the proportion of LV outliers among all SNPs in each ancestry category. Total SNP counts in each category and P-values of two-sided Fisher's exact tests are shown on top. Ancestry category (1) includes all SNPs for which only one of the two LV alleles was found in the Congolese and Upper Nile taxa together (novel LV allele or unsampled in parental lineages), (2) both LV alleles found in the Congolese taxa (polymorphic in LVRS even without Upper Nile hybridization), (3) only one allele found in Congolese but both alleles found in Upper Nile taxa (not available in LVRS without hybridization), and 4) Congolese and Upper Nile taxa each fixed for alternative LV alleles (not available in LVRS without hybridization) potentially including Bateson–Dobzhansky–Muller incompatibilities. Category 5 includes sites with similar initial allele frequency in Lake Victoria (16%) than sites fixed for alternative alleles in the parental lineages (category 4) to test if the enrichment in category 4 could simply be because of high initial allele frequency. (b) Differential sorting of parental alleles between Lake Victoria cichlid species at LV outliers fixed for alternative alleles in the Congolese and Upper Nile lineage taxa (mean global FST among LV species=0.52). Each square represents a SNP coloured according to the allele frequency in that species ranging from red (fixed for Congolese allele) to blue (fixed for Upper Nile allele). All except two sites (2+3 from the right) are located on different scaffolds of the Pundamilia nyererei reference genome. If known, chromosomal positions on the Oreochromis niloticus genome are shown below. At least 10 of the 22 chromosomes are involved in mosaic-like allele sorting between radiation species at loci that were fixed for alternative alleles in the parental lineages of the ancestral hybrid swarm (Photo credits: Oliver Selz, Ole Seehausen, Adrian Indermaur, ‘Teleos', Uli Schliewen).

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