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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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Maximum likelihood phylogeny of S7-2 alleles. Bootstrap and Approximate Likelihood Ratio Test support values (left/right, respectively) are given next to relevant nodes. Each rectangle represents one allele. Colors represent morphological identification of specimens following Almaça [21]
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Fig5: Maximum likelihood phylogeny of S7-2 alleles. Bootstrap and Approximate Likelihood Ratio Test support values (left/right, respectively) are given next to relevant nodes. Each rectangle represents one allele. Colors represent morphological identification of specimens following Almaça [21]

Mentions: Sequence analysis of four nuclear loci yielded 3,792 aligned sites (S7-1, 813 bp; S7-2, 827 bp; Gh-1, 1018 bp; Gh-2, 1134 bp). The Iberian specimens analyzed exhibited 35, 54, 41 and 41 alleles for S7-1, S7-2, Gh-1 and Gh-2, respectively. In general, gene trees are similar to each other (Figs. 4, 5, 6, 7) and are in agreement with relationships previously suggested by mtDNA, allozymes and morphology (e.g. [22–27, 30, 46, 47]). In particular, two main monophyletic lineages corresponding to the two genera, Barbus and Luciobarbus, are recovered. The former lineage is comprised of the Iberian endemic B. haasi and central and eastern European taxa included for phylogenetic context (B. barbus, B. carpathicus and B. prespensis). For S7-1, S7-2 and Gh-2, the Iberian Luciobarbus lineage comprises two monophyletic groups, one composed of L. graellsii, L. guiraonis and L. microcephalus, and another composed of L. bocagei, L. comizo, L. sclateri and L. steindachneri. Gh-1 is the least resolved nuclear marker at the species level, revealing a monophyletic group composed of L. graellsii and L. guiraonis, while L. microcephalus is recovered in a weakly supported group together with other sympatric species. The Iberian Luciobarbus lineages are further diagnosed by particular insertion-deletion variants at S7-1, S7-2 and Gh-2.Fig. 4


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

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

Maximum likelihood phylogeny of S7-2 alleles. Bootstrap and Approximate Likelihood Ratio Test support values (left/right, respectively) are given next to relevant nodes. Each rectangle represents one allele. Colors represent morphological identification of specimens following Almaça [21]
© Copyright Policy - open-access
Related In: Results  -  Collection

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

Fig5: Maximum likelihood phylogeny of S7-2 alleles. Bootstrap and Approximate Likelihood Ratio Test support values (left/right, respectively) are given next to relevant nodes. Each rectangle represents one allele. Colors represent morphological identification of specimens following Almaça [21]
Mentions: Sequence analysis of four nuclear loci yielded 3,792 aligned sites (S7-1, 813 bp; S7-2, 827 bp; Gh-1, 1018 bp; Gh-2, 1134 bp). The Iberian specimens analyzed exhibited 35, 54, 41 and 41 alleles for S7-1, S7-2, Gh-1 and Gh-2, respectively. In general, gene trees are similar to each other (Figs. 4, 5, 6, 7) and are in agreement with relationships previously suggested by mtDNA, allozymes and morphology (e.g. [22–27, 30, 46, 47]). In particular, two main monophyletic lineages corresponding to the two genera, Barbus and Luciobarbus, are recovered. The former lineage is comprised of the Iberian endemic B. haasi and central and eastern European taxa included for phylogenetic context (B. barbus, B. carpathicus and B. prespensis). For S7-1, S7-2 and Gh-2, the Iberian Luciobarbus lineage comprises two monophyletic groups, one composed of L. graellsii, L. guiraonis and L. microcephalus, and another composed of L. bocagei, L. comizo, L. sclateri and L. steindachneri. Gh-1 is the least resolved nuclear marker at the species level, revealing a monophyletic group composed of L. graellsii and L. guiraonis, while L. microcephalus is recovered in a weakly supported group together with other sympatric species. The Iberian Luciobarbus lineages are further diagnosed by particular insertion-deletion variants at S7-1, S7-2 and Gh-2.Fig. 4

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