Genetic structure of Ponto-Caspian trout populations shows gene flow among river drainages and supports resident Salmo rizeensis as a genetically distinct taxon

Abstract

To assess the genetic structure of Ponto-Caspian brown trout (Salmo trutta complex) populations, we analyzed both mitochondrial DNA sequences and genotypes at 10 microsatellite loci of fish caught in the Black Sea and from nine river catchments in Georgia, flowing into either the Black or Caspian seas. The results show that: (1) there is substantial genetic differentiation among Ponto-Caspian trout populations, both among the populations of different nominal species and within those of the same species; (2) the genetic distance between conspecific populations from the Black and Caspian Sea basins exceeds that among the populations within the same basin. Moreover, within drainages, genetic distance correlates with the geographic distance; (3) the Black Sea itself is not a barrier to gene flow among the watersheds draining into the Black Sea; (4) some populations in the headwaters of the rivers draining into the Black Sea Basin fall out of this pattern and likely form a separate, non-anadromous (resident) taxon, previously described from northeastern Turkey as Salmo rizeensis. This hypothesis is supported by mitochondrial DNA phylogeny. The presence of both anadromous and resident populations in a single river basin calls for a substantial re-thinking of speciation patterns and taxonomy of Eurasian brown trout.

Keywords: Ponto‐Caspian region; Salmo caspius; Salmo labrax; Salmo rizeensis; anadromy; brown trout; isolation by distance; resident forms.

FIGURE 1

Sampling locations of brown trout: Colors show ultimate destination of drainage, red indicates Black Sea, blue indicates Caspian Sea. Population 6, shown in green, indicates the location of fish whose mitochondrial DNA clustered with Salmo rizeensis (Turan et al., 2009).

FIGURE 2

The Bayesian inference tree showing mitochondrial (cytb) haplotype phylogeny in our samples and other published sequences of brown trout. The numbers on the triangles show the numbers of unique sequences from each cluster.

FIGURE 3

Median‐joining network linking the haplotypes of brown trout from the Caspian, Black Sea, and Mediterranean basins. The sampling locations of brown trout from the individual river basins marked with different colors (see the legend on the figure).

FIGURE 4

Ordination of the individual microsatellite genotypes along the first and the second principal component analysis axes. The first axis separates the individuals from the Black and the Caspian Sea basins, the second—individual populations within each of the two basins, including resident populations from Shareula and Chvana, as well as Akavreta and Dolra from the other populations of the Black Sea basin; and, populations from three river drainages independently flowing into the Caspian Sea.

FIGURE 5

The allocation of the studied individuals to the 11 clusters (K) showing the highest delta log likelihood, inferred with STRUCTURE algorithm (considering 1 < K < 14). The non‐rooted tree reflects genetic distances among the inferred clusters (colored numbers) dominating in the locations marked with the black numbers. Colored dots on map are showing the origin of populations grouped in each cluster.

FIGURE 6

Pairwise measures of genetic differentiation for Ponto‐Caspian trout populations. Genetic distances within the same basin are shown with gradation of green and between sea basins with gradation of red. Upper panel—pairwise F _ST values; lower panel—pairwise R _ST values. For the most of the population pairs, F _ST p values < .01. Those where .01 < p < .05 shown in Italics. For insignificant values, red font is used.

FIGURE 7

Neighbor‐joining unrooted tree based on pairwise F _ST of all sampled populations.