Genetic population structure of sympatric and allopatric populations of Baltic ciscoes (Coregonus albula complex, Teleostei, Coregonidae)

Abstract

Background: Teleost fishes of the Coregonidae are good model systems for studying postglacial evolution, adaptive radiation and ecological speciation. Of particular interest is whether the repeated occurrence of sympatric species pairs results from in-situ divergence from a single lineage or from multiple invasions of one or more different lineages. Here, we analysed the genetic structure of Baltic ciscoes (Coregonus albula complex), examining 271 individuals from 8 lakes in northern Germany using 1244 polymorphic AFLP loci. Six lakes had only one population of C. albula while the remaining two lakes had C. albula as well as a sympatric species (C. lucinensis or C. fontanae).

Results: AFLP demonstrated a significant population structure (Bayesian thetaB = 0.22). Lower differentiation between allopatric (thetaB = 0.028) than sympatric (0.063-0.083) populations contradicts the hypothesis of a sympatric origin of taxa, and there was little evidence for stocking or ongoing hybridization. Genome scans found only three loci that appeared to be under selection in both sympatric population pairs, suggesting a low probability of similar mechanisms of ecological segregation. However, removal of all non-neutral loci decreased the genetic distance between sympatric pairs, suggesting recent adaptive divergence at a few loci. Sympatric pairs in the two lakes were genetically distinct from the six other C. albula populations, suggesting introgression from another lineage may have influenced these two lakes. This was supported by an analysis of isolation-by-distance, where the drift-gene flow equilibrium observed among allopatric populations was disrupted when the sympatric pairs were included.

Conclusions: While the population genetic data alone can not unambiguously uncover the mode of speciation, our data indicate that multiple lineages may be responsible for the complex patterns typically observed in Coregonus. Relative differences within and among lakes raises the possibility that multiple lineages may be present in northern Germany, thus understanding the postglacial evolution and speciation in the C. albula complex requires a large-scale phylogenetic analysis of several potential founder lineages.

Figure 1

Geographical map of sampling locations. Geographical map showing the location of the 8 lakes in which the 10 populations were sampled (inset). Lakes with sympatric population are indicated in grey, and lakes with allopatric populations are indicated in white. The numbers refer to the population numbers in Table 1.

Figure 2

Tree of genetic distances between Coregonus populations. Unrooted neighbor-joining tree of Nei's genetic distances between 10 populations of the Coregonus albula complex. Allopatric populations consist exclusively of C. albula and are named according to the lake of origin (indicated by white colour). Sympatric populations are named by lake origin and the lake-specific species names (indicated by grey colour). Bootstrap support (%) from 100,000 iterations is provided for each node. Values in parentheses report support after removal of outlier loci.

Figure 3

Admixture analysis of hybridization for Lakes Stechlin and Breiter Luzin. Results of the admixture analysis with limited prior probability of hybridization by STRUCTURE for the two sympatric population pairs, Stechlin Coregonus albula (a), Stechlin C. fontanae (b), Breiter Luzin C. albula (c) and Breiter Luzin C. lucinensis (d). Probability of admixture was estimated for the sympatric populations in each lake, and for Lakes Arend and Tollense as potential stocking sources. Hybrids refer either to the first (F1) or the second and older (F2) parental generations.

Figure 4

Scatter plots of AFLP loci putatively under selection. Explorative genome scans comparing differentiation of AFLP loci to the expected neutral distribution under p > 0.99 and p > 0.95 for Lake Stechlin (a) and Lake Breiter Luzin (b). Loci positively exceeding expected neutral F_STs are indicated by white diamonds (p > 0.995) or black diamonds (p > 0.975). Loci shared from both lakes are numbered and indicated by black crosses. Lines indicate the median (solid), the 97.5% quantile (dashed) and the 99.5% quantile (dotted). Some symbols represent multiple loci with almost identical coordinates.