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Non-equilibrium estimates of gene flow inferred from nuclear genealogies suggest that Iberian and North African wall lizards (Podarcis spp.) are an assemblage of incipient species.

Pinho C, Harris DJ, Ferrand N - BMC Evol. Biol. (2008)

Bottom Line: To discriminate between the effects of incomplete lineage sorting and gene flow in setting this pattern, we estimated migration rates among species using both FST-based estimators of gene flow, which assume migration-drift equilibrium, and a coalescent approach based on a model of divergence with gene flow.These results corroborate most forms of Iberian and North African Podarcis as differentiated, although incipient, species, supporting a gradual view of speciation, according to which species may persist as distinct despite some permeability to genetic exchange and without having clearly definable genetic boundaries.Additionally, this study constitutes a warning against the misuse of equilibrium estimates of migration among recently-diverged groups.

View Article: PubMed Central - HTML - PubMed

Affiliation: CIBIO, Centro de Investigação em Biodiversidade e Recursos Genéticos, Campus Agrário de Vairão, 4485-661 Vairão, Portugal. catarina@mail.icav.up.pt

ABSTRACT

Background: The study of recently-diverged species offers significant challenges both in the definition of evolutionary entities and in the estimation of gene flow among them. Iberian and North African wall lizards (Podarcis) constitute a cryptic species complex for which previous assessments of mitochondrial DNA (mtDNA) and allozyme variation are concordant in describing the existence of several highly differentiated evolutionary units. However, these studies report important differences suggesting the occurrence of gene flow among forms. Here we study sequence variation in two nuclear introns, beta-fibint7 and 6-Pgdint7, to further investigate overall evolutionary dynamics and test hypotheses related to species delimitation within this complex.

Results: Both nuclear gene genealogies fail to define species as monophyletic. To discriminate between the effects of incomplete lineage sorting and gene flow in setting this pattern, we estimated migration rates among species using both FST-based estimators of gene flow, which assume migration-drift equilibrium, and a coalescent approach based on a model of divergence with gene flow. Equilibrium estimates of gene flow suggest widespread introgression between species, but coalescent estimates describe virtually zero admixture between most (but not all) species pairs. This suggests that although gene flow among forms may have occurred the main cause for species polyphyly is incomplete lineage sorting, implying that most forms have been isolated since their divergence. This observation is therefore in accordance with previous reports of strong differentiation based on mtDNA and allozyme data.

Conclusion: These results corroborate most forms of Iberian and North African Podarcis as differentiated, although incipient, species, supporting a gradual view of speciation, according to which species may persist as distinct despite some permeability to genetic exchange and without having clearly definable genetic boundaries. Additionally, this study constitutes a warning against the misuse of equilibrium estimates of migration among recently-diverged groups.

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Relationship between allele ancestrality and trans-specific proximity for locus β-fibint7. Ancestrality was measured as the distance, in number of mutations, to haplotype BR25, while trans-species allele proximity was measured as the distance to the closest-related allele found in a different species. The area of each circle is proportional to the allele frequency. Alleles belonging to P. muralis (including the supposedly introgressed allele found in P. hispanica type 3) were excluded. Other putatively introgressed alleles are highlighted.
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Figure 3: Relationship between allele ancestrality and trans-specific proximity for locus β-fibint7. Ancestrality was measured as the distance, in number of mutations, to haplotype BR25, while trans-species allele proximity was measured as the distance to the closest-related allele found in a different species. The area of each circle is proportional to the allele frequency. Alleles belonging to P. muralis (including the supposedly introgressed allele found in P. hispanica type 3) were excluded. Other putatively introgressed alleles are highlighted.

Mentions: A second line of evidence suggesting a major role for incomplete lineage sorting relies on the simple observation of patterns of allele relationships, particularly on the β-fibint7 data set. If gene flow was the main cause for the observed species polyphyly, we would expect that both ancestral (alleles that have a central position in the haplotype network) and derived alleles were transpecific or closely related to alleles found in other species. However, we do not detect this pattern; instead, we find that putatively older alleles are more widespread among species than alleles placed as tips, which are likely to have arisen after the species were separated. In order to visualize this trend, we plotted for the β-fibint7 data set the number of mutations separating a given haplotype from haplotype BR25, placed in the centre of the network, against the number of mutations separating that particular haplotype from the nearest haplotype found in another species (Fig. 3). The ancestral nature of haplotype BR25 was confirmed using an alternative method of haplotype network construction [34], which pinpoints the haplotype that is most probably the ancestral within a network. Although Figure 3 is a very rough representation, it clearly illustrates the relationship between allele "ancestrality" and trans-species proximity. Exceptions to this "rule" therefore constitute the most obvious cases of gene flow, as documented by the outlier position of the haplotypes BR62 and BR66 (putatively introgressed from P. hispanica Galera type into P. hispanica sensu stricto). The results are not as clear for 6-Pgdint7, both because a central haplotype cannot be pinpointed with confidence and because this gene shows more segregation between species groups. Nevertheless, there is still a positive correlation between both measures (results not shown).


Non-equilibrium estimates of gene flow inferred from nuclear genealogies suggest that Iberian and North African wall lizards (Podarcis spp.) are an assemblage of incipient species.

Pinho C, Harris DJ, Ferrand N - BMC Evol. Biol. (2008)

Relationship between allele ancestrality and trans-specific proximity for locus β-fibint7. Ancestrality was measured as the distance, in number of mutations, to haplotype BR25, while trans-species allele proximity was measured as the distance to the closest-related allele found in a different species. The area of each circle is proportional to the allele frequency. Alleles belonging to P. muralis (including the supposedly introgressed allele found in P. hispanica type 3) were excluded. Other putatively introgressed alleles are highlighted.
© Copyright Policy - open-access
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC2277379&req=5

Figure 3: Relationship between allele ancestrality and trans-specific proximity for locus β-fibint7. Ancestrality was measured as the distance, in number of mutations, to haplotype BR25, while trans-species allele proximity was measured as the distance to the closest-related allele found in a different species. The area of each circle is proportional to the allele frequency. Alleles belonging to P. muralis (including the supposedly introgressed allele found in P. hispanica type 3) were excluded. Other putatively introgressed alleles are highlighted.
Mentions: A second line of evidence suggesting a major role for incomplete lineage sorting relies on the simple observation of patterns of allele relationships, particularly on the β-fibint7 data set. If gene flow was the main cause for the observed species polyphyly, we would expect that both ancestral (alleles that have a central position in the haplotype network) and derived alleles were transpecific or closely related to alleles found in other species. However, we do not detect this pattern; instead, we find that putatively older alleles are more widespread among species than alleles placed as tips, which are likely to have arisen after the species were separated. In order to visualize this trend, we plotted for the β-fibint7 data set the number of mutations separating a given haplotype from haplotype BR25, placed in the centre of the network, against the number of mutations separating that particular haplotype from the nearest haplotype found in another species (Fig. 3). The ancestral nature of haplotype BR25 was confirmed using an alternative method of haplotype network construction [34], which pinpoints the haplotype that is most probably the ancestral within a network. Although Figure 3 is a very rough representation, it clearly illustrates the relationship between allele "ancestrality" and trans-species proximity. Exceptions to this "rule" therefore constitute the most obvious cases of gene flow, as documented by the outlier position of the haplotypes BR62 and BR66 (putatively introgressed from P. hispanica Galera type into P. hispanica sensu stricto). The results are not as clear for 6-Pgdint7, both because a central haplotype cannot be pinpointed with confidence and because this gene shows more segregation between species groups. Nevertheless, there is still a positive correlation between both measures (results not shown).

Bottom Line: To discriminate between the effects of incomplete lineage sorting and gene flow in setting this pattern, we estimated migration rates among species using both FST-based estimators of gene flow, which assume migration-drift equilibrium, and a coalescent approach based on a model of divergence with gene flow.These results corroborate most forms of Iberian and North African Podarcis as differentiated, although incipient, species, supporting a gradual view of speciation, according to which species may persist as distinct despite some permeability to genetic exchange and without having clearly definable genetic boundaries.Additionally, this study constitutes a warning against the misuse of equilibrium estimates of migration among recently-diverged groups.

View Article: PubMed Central - HTML - PubMed

Affiliation: CIBIO, Centro de Investigação em Biodiversidade e Recursos Genéticos, Campus Agrário de Vairão, 4485-661 Vairão, Portugal. catarina@mail.icav.up.pt

ABSTRACT

Background: The study of recently-diverged species offers significant challenges both in the definition of evolutionary entities and in the estimation of gene flow among them. Iberian and North African wall lizards (Podarcis) constitute a cryptic species complex for which previous assessments of mitochondrial DNA (mtDNA) and allozyme variation are concordant in describing the existence of several highly differentiated evolutionary units. However, these studies report important differences suggesting the occurrence of gene flow among forms. Here we study sequence variation in two nuclear introns, beta-fibint7 and 6-Pgdint7, to further investigate overall evolutionary dynamics and test hypotheses related to species delimitation within this complex.

Results: Both nuclear gene genealogies fail to define species as monophyletic. To discriminate between the effects of incomplete lineage sorting and gene flow in setting this pattern, we estimated migration rates among species using both FST-based estimators of gene flow, which assume migration-drift equilibrium, and a coalescent approach based on a model of divergence with gene flow. Equilibrium estimates of gene flow suggest widespread introgression between species, but coalescent estimates describe virtually zero admixture between most (but not all) species pairs. This suggests that although gene flow among forms may have occurred the main cause for species polyphyly is incomplete lineage sorting, implying that most forms have been isolated since their divergence. This observation is therefore in accordance with previous reports of strong differentiation based on mtDNA and allozyme data.

Conclusion: These results corroborate most forms of Iberian and North African Podarcis as differentiated, although incipient, species, supporting a gradual view of speciation, according to which species may persist as distinct despite some permeability to genetic exchange and without having clearly definable genetic boundaries. Additionally, this study constitutes a warning against the misuse of equilibrium estimates of migration among recently-diverged groups.

Show MeSH