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Admixture between old lineages facilitated contemporary ecological speciation in Lake Constance stickleback.

ABSTRACT: Ecological speciation can sometimes rapidly generate reproductively isolated populations coexisting in sympatry, but the origin of genetic variation permitting this is rarely known. We previously explored the genomics of very recent ecological speciation into lake and stream ecotypes in stickleback from Lake Constance. Here, we reconstruct the origin of alleles underlying ecological speciation by combining demographic modelling on genome-wide single nucleotide polymorphisms, phenotypic data and mitochondrial sequence data in the wider European biogeographical context. We find that parallel differentiation between lake and stream ecotypes across replicate lake-stream ecotones resulted from recent secondary contact and admixture between old East and West European lineages. Unexpectedly, West European alleles that introgressed across the hybrid zone at the western end of the lake, were recruited to genomic islands of differentiation between ecotypes at the eastern end of the lake. Our results highlight an overlooked outcome of secondary contact: ecological speciation facilitated by admixture variation.

SUBMITTER: Marques DA

PROVIDER: S-EPMC6751218 | biostudies-literature | 2019 Sep

REPOSITORIES: biostudies-literature

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Admixture between old lineages facilitated contemporary ecological speciation in Lake Constance stickleback.

Marques David A DA Lucek Kay K Sousa Vitor C VC Excoffier Laurent L Seehausen Ole O

Nature communications 20190918 1

Ecological speciation can sometimes rapidly generate reproductively isolated populations coexisting in sympatry, but the origin of genetic variation permitting this is rarely known. We previously explored the genomics of very recent ecological speciation into lake and stream ecotypes in stickleback from Lake Constance. Here, we reconstruct the origin of alleles underlying ecological speciation by combining demographic modelling on genome-wide single nucleotide polymorphisms, phenotypic data and ...[more]

PMID: 31534121

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Project description:The formation of species in the absence of geographic barriers (i.e. sympatric speciation) remains one of the most controversial topics in evolutionary biology. While theoretical models have shown that this most extreme case of primary divergence-with-gene-flow is possible, only a handful of accepted empirical examples exist. And even for the most convincing examples uncertainties remain; complex histories of isolation and secondary contact can make species falsely appear to have originated by sympatric speciation. This alternative scenario is notoriously difficult to rule out. Midas cichlids inhabiting small and remote crater lakes in Nicaragua are traditionally considered to be one of the best examples of sympatric speciation and lend themselves to test the different evolutionary scenarios that could lead to apparent sympatric speciation since the system is relatively small and the source populations known. Here we reconstruct the evolutionary history of two small-scale radiations of Midas cichlids inhabiting crater lakes Apoyo and Xiloá through a comprehensive genomic data set. We find no signs of differential admixture of any of the sympatric species in the respective radiations. Together with coalescent simulations of different demographic models our results support a scenario of speciation that was initiated in sympatry and does not result from secondary contact of already partly diverged populations. Furthermore, several species seem to have diverged simultaneously, making Midas cichlids an empirical example of multispecies outcomes of sympatric speciation. Importantly, however, the demographic models strongly support an admixture event from the source population into both crater lakes shortly before the onset of the radiations within the lakes. This opens the possibility that the formation of reproductive barriers involved in sympatric speciation was facilitated by genetic variants that evolved in a period of isolation between the initial founding population and the secondary migrants that came from the same source population. Thus, the exact mechanisms by which these species arose might be different from what had been thought before.

Project description:Active sulfate-reducing microorganisms (SRM) in freshwater sediments are under-examined, despite the well-documented cryptic sulfur cycle occurring in these low-sulfate habitats. In Lake Constance sediment, sulfate reduction rates of up to 1,800 nmol cm-3 day-1 were previously measured. To characterize its SRM community, we used a tripartite amplicon sequencing approach based on 16S rRNA genes, 16S rRNA, and dsrB transcripts (encoding the beta subunit of dissimilatory sulfite reductase). We followed the respective amplicon dynamics in four anoxic microcosm setups supplemented either with (i) chitin and sulfate, (ii) sulfate only, (iii) chitin only, or (iv) no amendment. Chitin was used as a general substrate for the whole carbon degradation chain. Sulfate turnover in sulfate-supplemented microcosms ranged from 38 to 955 nmol day-1 (g sediment f. wt.)-1 and was paralleled by a decrease of 90-100% in methanogenesis as compared to the respective methanogenic controls. In the initial sediment, relative abundances of recognized SRM lineages accounted for 3.1 and 4.4% of all bacterial 16S rRNA gene and 16S rRNA sequences, respectively. When normalized against the 1.4 × 108 total prokaryotic 16S rRNA gene copies as determined by qPCR and taking multiple rrn operons per genome into account, this resulted in approximately 105-106 SRM cells (g sediment f. wt.)-1. The three amplicon approaches jointly identified Desulfobacteraceae and Syntrophobacteraceae as the numerically dominant and transcriptionally most active SRM in the initial sediment. This was corroborated in the time course analyses of sulfate-consuming sediment microcosms irrespective of chitin amendment. Uncultured dsrAB family-level lineages constituted in sum only 1.9% of all dsrB transcripts, with uncultured lineage 5 and 6 being transcriptionally most active. Our study is the first holistic molecular approach to quantify and characterize active SRM including uncultured dsrAB lineages not only in Lake Constance but for lake sediments in general.

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Admixture between old lineages facilitated contemporary ecological speciation in Lake Constance stickleback.

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Admixture between old lineages facilitated contemporary ecological speciation in Lake Constance stickleback.

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