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Comprehensive phylogenetic analysis of all species of swordtails and platies (Pisces: Genus Xiphophorus) uncovers a hybrid origin of a swordtail fish, Xiphophorus monticolus, and demonstrates that the sexually selected sword originated in the ancestral lineage of the genus, but was lost again secondarily.

Kang JH, Schartl M, Walter RB, Meyer A - BMC Evol. Biol. (2013)

Bottom Line: Based on the phylogeny, the evolutionary history and character state evolution of the sword was reconstructed and found to have originated in the common ancestral lineage of the genus Xiphophorus and that it was lost again secondarily.Previously, we demonstrated that X. clemenciae, another southern swordtail species, arose via hybridization.These findings highlight the potential key role of hybridization in the evolution of this genus and suggest the need for further investigations into how hybridization contributes to speciation more generally.

View Article: PubMed Central - HTML - PubMed

Affiliation: Lehrstuhl für Zoologie und Evolutionsbiologie, Department of Biology, University of Konstanz, Universitätsstraße 10, Konstanz 78457, Germany.

ABSTRACT

Background: Males in some species of the genus Xiphophorus, small freshwater fishes from Meso-America, have an extended caudal fin, or sword - hence their common name "swordtails". Longer swords are preferred by females from both sworded and - surprisingly also, non-sworded (platyfish) species that belong to the same genus. Swordtails have been studied widely as models in research on sexual selection. Specifically, the pre-existing bias hypothesis was interpreted to best explain the observed bias of females in presumed ancestral lineages of swordless species that show a preference for assumed derived males with swords over their conspecific swordless males. However, many of the phylogenetic relationships within this genus still remained unresolved. Here we construct a comprehensive molecular phylogeny of all 26 known Xiphophorus species, including the four recently described species (X. kallmani, X. mayae, X. mixei and X. monticolus). We use two mitochondrial and six new nuclear markers in an effort to increase the understanding of the evolutionary relationships among the species in this genus. Based on the phylogeny, the evolutionary history and character state evolution of the sword was reconstructed and found to have originated in the common ancestral lineage of the genus Xiphophorus and that it was lost again secondarily.

Results: We estimated the evolutionary relationships among all known species of the genus Xiphophorus based on the largest set of DNA markers so far. The phylogeny indicates that one of the newly described swordtail species, Xiphophorus monticolus, is likely to have arisen through hybridization since it is placed with the southern platyfish in the mitochondrial phylogeny, but with the southern swordtails in the nuclear phylogeny. Such discordance between these two types of markers is a strong indication for a hybrid origin. Additionally, by using a maximum likelihood approach the possession of the sexually selected sword trait is shown to be the most likely ancestral state for the genus Xiphophorus. Further, we provide a well supported estimation of the phylogenetic relationships between the previously unresolved northern swordtail groups.

Conclusions: This comprehensive molecular phylogeny of the entire genus Xiphophorus provides evidence that a second swordtail species, X. monticolus, arose through hybridization. Previously, we demonstrated that X. clemenciae, another southern swordtail species, arose via hybridization. These findings highlight the potential key role of hybridization in the evolution of this genus and suggest the need for further investigations into how hybridization contributes to speciation more generally.

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Mitochondrial and nuclear phylogenies of the nine northern swordtail species. The phylogenetic trees were constructed from (a) combined sequences of two mtDNA loci (1235 bp) (complete control region and a segment of the cytochrome b gene), (b) combined sequences of eleven nuclear loci (7073 bp), and (c) combined sequences of two mitochondrial and eleven nuclear loci (8308 bp). Numbers indicate Bayesian posterior probabilities, Maximum-Likelihood, Neighbor-Joining and Maximum-Parsimony bootstrap values, respectively. The values of the branch length that was truncated are 0.115 (a), 0.007 (b) and 0.012 (c). Patterns of the geographical distributions of the nine species in the northern swordtails are shown (d) (map is modified from [2]). Species in the same clades inferred by [21] are shown in same color.
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Figure 3: Mitochondrial and nuclear phylogenies of the nine northern swordtail species. The phylogenetic trees were constructed from (a) combined sequences of two mtDNA loci (1235 bp) (complete control region and a segment of the cytochrome b gene), (b) combined sequences of eleven nuclear loci (7073 bp), and (c) combined sequences of two mitochondrial and eleven nuclear loci (8308 bp). Numbers indicate Bayesian posterior probabilities, Maximum-Likelihood, Neighbor-Joining and Maximum-Parsimony bootstrap values, respectively. The values of the branch length that was truncated are 0.115 (a), 0.007 (b) and 0.012 (c). Patterns of the geographical distributions of the nine species in the northern swordtails are shown (d) (map is modified from [2]). Species in the same clades inferred by [21] are shown in same color.

Mentions: The relationships among the nine northern swordtail species differed more between the mtDNA and nuclear DNA phylogenies (Figure 2). Because species of the northern swordtail lineage are used by several laboratories for behavioral ecological work and as model for study of evolutionary questions, we, therefore, conducted additional analyses on the northern swordtails only - based on the nuclear and mitochondrial data sets separately and also combined both data sets (Figure 3) – in an effort to resolve the phylogenetic relationships among the species in this lineage. For these analyses, two platyfish species (X. evelynae and X. gordoni) were used as outgroups (Figure 3). Aligned nucleotide sequences of the mitochondrial loci contained 151 variable sites and 85 of those were parsimony informative with 0.041 [SE (Standard Error) = 0.003] of average p-distance, whereas the nuclear loci exhibited 245 variable sites and 110 of those were informative with 0.01 (SE = 0.001). The best-fit evolutionary models chosen (jModeltest 0.1.1, [70]) for the mitochondrial and nuclear loci were TPM1uf+I+G and TPM1uf+G, respectively. The combined mitochondrial and nuclear alignments contained 396 variable sites and 195 of these were parsimony informative with 0.015 (SE = 0.001) of average p-distance and TrN+G was determined as the best-fit evolutionary model.


Comprehensive phylogenetic analysis of all species of swordtails and platies (Pisces: Genus Xiphophorus) uncovers a hybrid origin of a swordtail fish, Xiphophorus monticolus, and demonstrates that the sexually selected sword originated in the ancestral lineage of the genus, but was lost again secondarily.

Kang JH, Schartl M, Walter RB, Meyer A - BMC Evol. Biol. (2013)

Mitochondrial and nuclear phylogenies of the nine northern swordtail species. The phylogenetic trees were constructed from (a) combined sequences of two mtDNA loci (1235 bp) (complete control region and a segment of the cytochrome b gene), (b) combined sequences of eleven nuclear loci (7073 bp), and (c) combined sequences of two mitochondrial and eleven nuclear loci (8308 bp). Numbers indicate Bayesian posterior probabilities, Maximum-Likelihood, Neighbor-Joining and Maximum-Parsimony bootstrap values, respectively. The values of the branch length that was truncated are 0.115 (a), 0.007 (b) and 0.012 (c). Patterns of the geographical distributions of the nine species in the northern swordtails are shown (d) (map is modified from [2]). Species in the same clades inferred by [21] are shown in same color.
© Copyright Policy - open-access
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC3585855&req=5

Figure 3: Mitochondrial and nuclear phylogenies of the nine northern swordtail species. The phylogenetic trees were constructed from (a) combined sequences of two mtDNA loci (1235 bp) (complete control region and a segment of the cytochrome b gene), (b) combined sequences of eleven nuclear loci (7073 bp), and (c) combined sequences of two mitochondrial and eleven nuclear loci (8308 bp). Numbers indicate Bayesian posterior probabilities, Maximum-Likelihood, Neighbor-Joining and Maximum-Parsimony bootstrap values, respectively. The values of the branch length that was truncated are 0.115 (a), 0.007 (b) and 0.012 (c). Patterns of the geographical distributions of the nine species in the northern swordtails are shown (d) (map is modified from [2]). Species in the same clades inferred by [21] are shown in same color.
Mentions: The relationships among the nine northern swordtail species differed more between the mtDNA and nuclear DNA phylogenies (Figure 2). Because species of the northern swordtail lineage are used by several laboratories for behavioral ecological work and as model for study of evolutionary questions, we, therefore, conducted additional analyses on the northern swordtails only - based on the nuclear and mitochondrial data sets separately and also combined both data sets (Figure 3) – in an effort to resolve the phylogenetic relationships among the species in this lineage. For these analyses, two platyfish species (X. evelynae and X. gordoni) were used as outgroups (Figure 3). Aligned nucleotide sequences of the mitochondrial loci contained 151 variable sites and 85 of those were parsimony informative with 0.041 [SE (Standard Error) = 0.003] of average p-distance, whereas the nuclear loci exhibited 245 variable sites and 110 of those were informative with 0.01 (SE = 0.001). The best-fit evolutionary models chosen (jModeltest 0.1.1, [70]) for the mitochondrial and nuclear loci were TPM1uf+I+G and TPM1uf+G, respectively. The combined mitochondrial and nuclear alignments contained 396 variable sites and 195 of these were parsimony informative with 0.015 (SE = 0.001) of average p-distance and TrN+G was determined as the best-fit evolutionary model.

Bottom Line: Based on the phylogeny, the evolutionary history and character state evolution of the sword was reconstructed and found to have originated in the common ancestral lineage of the genus Xiphophorus and that it was lost again secondarily.Previously, we demonstrated that X. clemenciae, another southern swordtail species, arose via hybridization.These findings highlight the potential key role of hybridization in the evolution of this genus and suggest the need for further investigations into how hybridization contributes to speciation more generally.

View Article: PubMed Central - HTML - PubMed

Affiliation: Lehrstuhl für Zoologie und Evolutionsbiologie, Department of Biology, University of Konstanz, Universitätsstraße 10, Konstanz 78457, Germany.

ABSTRACT

Background: Males in some species of the genus Xiphophorus, small freshwater fishes from Meso-America, have an extended caudal fin, or sword - hence their common name "swordtails". Longer swords are preferred by females from both sworded and - surprisingly also, non-sworded (platyfish) species that belong to the same genus. Swordtails have been studied widely as models in research on sexual selection. Specifically, the pre-existing bias hypothesis was interpreted to best explain the observed bias of females in presumed ancestral lineages of swordless species that show a preference for assumed derived males with swords over their conspecific swordless males. However, many of the phylogenetic relationships within this genus still remained unresolved. Here we construct a comprehensive molecular phylogeny of all 26 known Xiphophorus species, including the four recently described species (X. kallmani, X. mayae, X. mixei and X. monticolus). We use two mitochondrial and six new nuclear markers in an effort to increase the understanding of the evolutionary relationships among the species in this genus. Based on the phylogeny, the evolutionary history and character state evolution of the sword was reconstructed and found to have originated in the common ancestral lineage of the genus Xiphophorus and that it was lost again secondarily.

Results: We estimated the evolutionary relationships among all known species of the genus Xiphophorus based on the largest set of DNA markers so far. The phylogeny indicates that one of the newly described swordtail species, Xiphophorus monticolus, is likely to have arisen through hybridization since it is placed with the southern platyfish in the mitochondrial phylogeny, but with the southern swordtails in the nuclear phylogeny. Such discordance between these two types of markers is a strong indication for a hybrid origin. Additionally, by using a maximum likelihood approach the possession of the sexually selected sword trait is shown to be the most likely ancestral state for the genus Xiphophorus. Further, we provide a well supported estimation of the phylogenetic relationships between the previously unresolved northern swordtail groups.

Conclusions: This comprehensive molecular phylogeny of the entire genus Xiphophorus provides evidence that a second swordtail species, X. monticolus, arose through hybridization. Previously, we demonstrated that X. clemenciae, another southern swordtail species, arose via hybridization. These findings highlight the potential key role of hybridization in the evolution of this genus and suggest the need for further investigations into how hybridization contributes to speciation more generally.

Show MeSH