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Semi-permeable species boundaries in Iberian barbels (Barbus and Luciobarbus, Cyprinidae).

Gante HF, Doadrio I, Alves MJ, Dowling TE - BMC Evol. Biol. (2015)

Bottom Line: Additionally, extent of introgression decreases with increasing genetic divergence in hybridizing species pairs.Our results support a speciation-with-gene-flow scenario with heterogeneous barriers to gene flow across the genome, strengthening with genetic divergence.In spite of the homogenizing effects of ongoing gene flow, species can still be discriminated using a combination of morphological and molecular markers.

View Article: PubMed Central - PubMed

Affiliation: School of Life Sciences, Arizona State University, 85287-4601, Tempe, AZ, USA. hugo.gante@asu.edu.

ABSTRACT

Background: The evolution of species boundaries and the relative impact of selection and gene flow on genomic divergence are best studied in populations and species pairs exhibiting various levels of divergence along the speciation continuum. We studied species boundaries in Iberian barbels, Barbus and Luciobarbus, a system of populations and species spanning a wide degree of genetic relatedness, as well as geographic distribution and range overlap. We jointly analyze multiple types of molecular markers and morphological traits to gain a comprehensive perspective on the nature of species boundaries in these cyprinid fishes.

Results: Intraspecific molecular and morphological differentiation is visible among many populations. Genomes of all sympatric species studied are porous to gene flow, even if they are not sister species. Compared to their allopatric counterparts, sympatric representatives of different species share alleles and show an increase in all measures of nucleotide polymorphism (S, Hd, K, π and θ). High molecular diversity is particularly striking in L. steindachneri from the Tejo and Guadiana rivers, which co-varies with other sympatric species. Interestingly, different nuclear markers introgress across species boundaries at various levels, with distinct impacts on population trees. As such, some loci exhibit limited introgression and population trees resemble the presumed species tree, while alleles at other loci introgress more freely and population trees reflect geographic affinities and interspecific gene flow. Additionally, extent of introgression decreases with increasing genetic divergence in hybridizing species pairs.

Conclusions: We show that reproductive isolation in Iberian Barbus and Luciobarbus is not complete and species boundaries are semi-permeable to (some) gene flow, as different species (including non-sister) are exchanging genes in areas of sympatry. Our results support a speciation-with-gene-flow scenario with heterogeneous barriers to gene flow across the genome, strengthening with genetic divergence. This is consistent with observations coming from other systems and supports the notion that speciation is not instantaneous but a gradual process, during which different species are still able to exchange some genes, while selection prevents gene flow at other loci. We also provide evidence for a hybrid origin of a barbel ecotype, L. steindachneri, suggesting that ecology plays a key role in species coexistence and hybridization in Iberian barbels. This ecotype with intermediate, yet variable, molecular, morphological, trophic and ecological characteristics is the local product of introgressive hybridization of L. comizo with up to three different species (with L. bocagei in the Tejo, with L. microcephalus and L. sclateri in the Guadiana). In spite of the homogenizing effects of ongoing gene flow, species can still be discriminated using a combination of morphological and molecular markers. Iberian barbels are thus an ideal system for the study of species boundaries, since they span a wide range of genetic divergences, with diverse ecologies and degrees of sympatry.

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Bayesian analysis of population structure. Split-and-reanalyze strategy implemented in structure. The entire dataset was initially split into Atlantic- and Mediterranean-draining basins (top left and top right, respectively). The first dataset also includes a population of L. sclateri from a Mediterranean-draining basin (Segura R.) as an allopatric counterpart to L. sclateri from Guadiana R.. The Atlantic-draining dataset was subsequently split into west- and south-draining basins (bottom). Using a combination of changes in consecutive LnP(D) values and Evanno’s [48] ΔK, we determined the most likely number of clusters in each dataset. These analyses indicate that an overall K = 10 populations is the most biologically meaningful genetic structuring of the nuclear dataset. In Additional file 3 we present an alternative strategy to estimate K, using the run with highest likelihood value for each K. The results are very similar, with the detection of additional differentiation within L. bocagei (K = 11)
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Fig8: Bayesian analysis of population structure. Split-and-reanalyze strategy implemented in structure. The entire dataset was initially split into Atlantic- and Mediterranean-draining basins (top left and top right, respectively). The first dataset also includes a population of L. sclateri from a Mediterranean-draining basin (Segura R.) as an allopatric counterpart to L. sclateri from Guadiana R.. The Atlantic-draining dataset was subsequently split into west- and south-draining basins (bottom). Using a combination of changes in consecutive LnP(D) values and Evanno’s [48] ΔK, we determined the most likely number of clusters in each dataset. These analyses indicate that an overall K = 10 populations is the most biologically meaningful genetic structuring of the nuclear dataset. In Additional file 3 we present an alternative strategy to estimate K, using the run with highest likelihood value for each K. The results are very similar, with the detection of additional differentiation within L. bocagei (K = 11)

Mentions: Due to the presence of large number of clusters (K) and high levels of differentiation among many populations and species, Structure sometimes converged to different solutions in independent replicates of each K, making determination of the best K challenging. Therefore, we consecutively split the complete dataset into smaller datasets, as recommended by the authors of the program as a strategy to deal with dataset multimodality. To determine the number of clusters we followed changes in LnP(D) values of consecutive K (i.e. when values plateau) and Evanno’s et al. ΔK [48]. We first split the dataset in two, based on geography and phylogenetic relationships. The first dataset is composed of all species from rivers draining to the Atlantic and allopatric populations of those species (in this case only L. sclateri from the Segura River). This analysis converged to K = 5 genetic clusters (Fig. 8, upper left), clearly separating populations inhabiting rivers draining to the western margin of the Iberian Peninsula (Douro, Tejo and Sado rivers) from rivers draining to the southern margin (Guadiana and Segura rivers). Further splitting the first dataset using this geographical discontinuity and patterns of gene exchange allows the identification of further intraspecific genetic structure (K = 3 and K = 4; Fig. 8, bottom). The second dataset is composed of species sympatric in rivers draining to the Mediterranean (Ebro, Júcar, Mijares and Bullent rivers) and closely related species (i.e., L. microcephalus from the Guadiana River). This analysis converged to K = 4 genetic clusters (Fig. 8, upper right), which is concordant with species identification based on morphology. The only discordant samples are L. guiraonis from the Júcar River, which are placed in the same group as B. haasi.Fig. 8


Semi-permeable species boundaries in Iberian barbels (Barbus and Luciobarbus, Cyprinidae).

Gante HF, Doadrio I, Alves MJ, Dowling TE - BMC Evol. Biol. (2015)

Bayesian analysis of population structure. Split-and-reanalyze strategy implemented in structure. The entire dataset was initially split into Atlantic- and Mediterranean-draining basins (top left and top right, respectively). The first dataset also includes a population of L. sclateri from a Mediterranean-draining basin (Segura R.) as an allopatric counterpart to L. sclateri from Guadiana R.. The Atlantic-draining dataset was subsequently split into west- and south-draining basins (bottom). Using a combination of changes in consecutive LnP(D) values and Evanno’s [48] ΔK, we determined the most likely number of clusters in each dataset. These analyses indicate that an overall K = 10 populations is the most biologically meaningful genetic structuring of the nuclear dataset. In Additional file 3 we present an alternative strategy to estimate K, using the run with highest likelihood value for each K. The results are very similar, with the detection of additional differentiation within L. bocagei (K = 11)
© Copyright Policy - open-access
Related In: Results  -  Collection

License 1 - License 2
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getmorefigures.php?uid=PMC4465174&req=5

Fig8: Bayesian analysis of population structure. Split-and-reanalyze strategy implemented in structure. The entire dataset was initially split into Atlantic- and Mediterranean-draining basins (top left and top right, respectively). The first dataset also includes a population of L. sclateri from a Mediterranean-draining basin (Segura R.) as an allopatric counterpart to L. sclateri from Guadiana R.. The Atlantic-draining dataset was subsequently split into west- and south-draining basins (bottom). Using a combination of changes in consecutive LnP(D) values and Evanno’s [48] ΔK, we determined the most likely number of clusters in each dataset. These analyses indicate that an overall K = 10 populations is the most biologically meaningful genetic structuring of the nuclear dataset. In Additional file 3 we present an alternative strategy to estimate K, using the run with highest likelihood value for each K. The results are very similar, with the detection of additional differentiation within L. bocagei (K = 11)
Mentions: Due to the presence of large number of clusters (K) and high levels of differentiation among many populations and species, Structure sometimes converged to different solutions in independent replicates of each K, making determination of the best K challenging. Therefore, we consecutively split the complete dataset into smaller datasets, as recommended by the authors of the program as a strategy to deal with dataset multimodality. To determine the number of clusters we followed changes in LnP(D) values of consecutive K (i.e. when values plateau) and Evanno’s et al. ΔK [48]. We first split the dataset in two, based on geography and phylogenetic relationships. The first dataset is composed of all species from rivers draining to the Atlantic and allopatric populations of those species (in this case only L. sclateri from the Segura River). This analysis converged to K = 5 genetic clusters (Fig. 8, upper left), clearly separating populations inhabiting rivers draining to the western margin of the Iberian Peninsula (Douro, Tejo and Sado rivers) from rivers draining to the southern margin (Guadiana and Segura rivers). Further splitting the first dataset using this geographical discontinuity and patterns of gene exchange allows the identification of further intraspecific genetic structure (K = 3 and K = 4; Fig. 8, bottom). The second dataset is composed of species sympatric in rivers draining to the Mediterranean (Ebro, Júcar, Mijares and Bullent rivers) and closely related species (i.e., L. microcephalus from the Guadiana River). This analysis converged to K = 4 genetic clusters (Fig. 8, upper right), which is concordant with species identification based on morphology. The only discordant samples are L. guiraonis from the Júcar River, which are placed in the same group as B. haasi.Fig. 8

Bottom Line: Additionally, extent of introgression decreases with increasing genetic divergence in hybridizing species pairs.Our results support a speciation-with-gene-flow scenario with heterogeneous barriers to gene flow across the genome, strengthening with genetic divergence.In spite of the homogenizing effects of ongoing gene flow, species can still be discriminated using a combination of morphological and molecular markers.

View Article: PubMed Central - PubMed

Affiliation: School of Life Sciences, Arizona State University, 85287-4601, Tempe, AZ, USA. hugo.gante@asu.edu.

ABSTRACT

Background: The evolution of species boundaries and the relative impact of selection and gene flow on genomic divergence are best studied in populations and species pairs exhibiting various levels of divergence along the speciation continuum. We studied species boundaries in Iberian barbels, Barbus and Luciobarbus, a system of populations and species spanning a wide degree of genetic relatedness, as well as geographic distribution and range overlap. We jointly analyze multiple types of molecular markers and morphological traits to gain a comprehensive perspective on the nature of species boundaries in these cyprinid fishes.

Results: Intraspecific molecular and morphological differentiation is visible among many populations. Genomes of all sympatric species studied are porous to gene flow, even if they are not sister species. Compared to their allopatric counterparts, sympatric representatives of different species share alleles and show an increase in all measures of nucleotide polymorphism (S, Hd, K, π and θ). High molecular diversity is particularly striking in L. steindachneri from the Tejo and Guadiana rivers, which co-varies with other sympatric species. Interestingly, different nuclear markers introgress across species boundaries at various levels, with distinct impacts on population trees. As such, some loci exhibit limited introgression and population trees resemble the presumed species tree, while alleles at other loci introgress more freely and population trees reflect geographic affinities and interspecific gene flow. Additionally, extent of introgression decreases with increasing genetic divergence in hybridizing species pairs.

Conclusions: We show that reproductive isolation in Iberian Barbus and Luciobarbus is not complete and species boundaries are semi-permeable to (some) gene flow, as different species (including non-sister) are exchanging genes in areas of sympatry. Our results support a speciation-with-gene-flow scenario with heterogeneous barriers to gene flow across the genome, strengthening with genetic divergence. This is consistent with observations coming from other systems and supports the notion that speciation is not instantaneous but a gradual process, during which different species are still able to exchange some genes, while selection prevents gene flow at other loci. We also provide evidence for a hybrid origin of a barbel ecotype, L. steindachneri, suggesting that ecology plays a key role in species coexistence and hybridization in Iberian barbels. This ecotype with intermediate, yet variable, molecular, morphological, trophic and ecological characteristics is the local product of introgressive hybridization of L. comizo with up to three different species (with L. bocagei in the Tejo, with L. microcephalus and L. sclateri in the Guadiana). In spite of the homogenizing effects of ongoing gene flow, species can still be discriminated using a combination of morphological and molecular markers. Iberian barbels are thus an ideal system for the study of species boundaries, since they span a wide range of genetic divergences, with diverse ecologies and degrees of sympatry.

Show MeSH
Related in: MedlinePlus