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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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Scatterplot of PC1 and PC2 of meristic traits of all endemic Iberian Barbus and Luciobarbus species. Center of symbol represents morphological identification of specimens following Almaça [21], perimeter of each symbol represents mtDNA lineage defined in Fig. 3. Polygon delimits samples from each population/species
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Fig2: Scatterplot of PC1 and PC2 of meristic traits of all endemic Iberian Barbus and Luciobarbus species. Center of symbol represents morphological identification of specimens following Almaça [21], perimeter of each symbol represents mtDNA lineage defined in Fig. 3. Polygon delimits samples from each population/species

Mentions: Multivariate analysis of meristic traits is effective in separating the Iberian endemic species of Barbus and Luciobarbus. The first two principal components explain 80.1 % of the observed variation, with all variables contributing to both axes, although traits that contribute the most to one axis contribute the least to the other (Table 2). Plotting the two components against each other provides clear visual separation of most of the recognized species (Fig. 2). Barbus haasi is the most morphologically distinct Iberian barbel, with all Luciobarbus analyzed being more similar to each other in meristic morphospace. The first component separates L. comizo, L. bocagei and L. sclateri from L. microcephalus, L. guiraonis and L. graellsii, and these groups from B. haasi, while the second component separates species within the first two groups of Luciobarbus. Therefore, species living in sympatry can be correctly discriminated using a few morphological traits, with the notable exception of L. steindachneri. Specimens of L. steindachneri show substantial variation in meristic traits, some individuals overlapping with either L. comizo or L. bocagei in the Tejo River and with L. comizo or L. sclateri in the Guadiana River. As a whole, L. steindachneri occupies an intermediate position in the morphospace relative to the other Iberian Luciobarbus.Table 2


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

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

Scatterplot of PC1 and PC2 of meristic traits of all endemic Iberian Barbus and Luciobarbus species. Center of symbol represents morphological identification of specimens following Almaça [21], perimeter of each symbol represents mtDNA lineage defined in Fig. 3. Polygon delimits samples from each population/species
© Copyright Policy - open-access
Related In: Results  -  Collection

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

Fig2: Scatterplot of PC1 and PC2 of meristic traits of all endemic Iberian Barbus and Luciobarbus species. Center of symbol represents morphological identification of specimens following Almaça [21], perimeter of each symbol represents mtDNA lineage defined in Fig. 3. Polygon delimits samples from each population/species
Mentions: Multivariate analysis of meristic traits is effective in separating the Iberian endemic species of Barbus and Luciobarbus. The first two principal components explain 80.1 % of the observed variation, with all variables contributing to both axes, although traits that contribute the most to one axis contribute the least to the other (Table 2). Plotting the two components against each other provides clear visual separation of most of the recognized species (Fig. 2). Barbus haasi is the most morphologically distinct Iberian barbel, with all Luciobarbus analyzed being more similar to each other in meristic morphospace. The first component separates L. comizo, L. bocagei and L. sclateri from L. microcephalus, L. guiraonis and L. graellsii, and these groups from B. haasi, while the second component separates species within the first two groups of Luciobarbus. Therefore, species living in sympatry can be correctly discriminated using a few morphological traits, with the notable exception of L. steindachneri. Specimens of L. steindachneri show substantial variation in meristic traits, some individuals overlapping with either L. comizo or L. bocagei in the Tejo River and with L. comizo or L. sclateri in the Guadiana River. As a whole, L. steindachneri occupies an intermediate position in the morphospace relative to the other Iberian Luciobarbus.Table 2

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