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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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Map of the distributions of Xiphophorus species. (a) Geographical distributions of all described 26 species in the genus Xiphophorus including the four newly described species – X. monticolus, X. mixei, X. kallmani and X. mayae (colored in blue) and two species of a putatively hybrid origin, X. monticolus and X. clemenciae (in bold). (b) Geographical distributions of three species in the clemenciae clade (maps are modified from [2,58]).
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Figure 1: Map of the distributions of Xiphophorus species. (a) Geographical distributions of all described 26 species in the genus Xiphophorus including the four newly described species – X. monticolus, X. mixei, X. kallmani and X. mayae (colored in blue) and two species of a putatively hybrid origin, X. monticolus and X. clemenciae (in bold). (b) Geographical distributions of three species in the clemenciae clade (maps are modified from [2,58]).

Mentions: Although the origin and evolution of the sword [7,20,26,53-56] and the role of hybridization in the genus Xiphophorus[2] have been addressed before, some of the phylogenetic relationships in this genus still remained uncertain. Traditionally, the genus Xiphophorus has been suggested to consist of four major lineages based on their geographical distributions and other phenotypic traits (i.e., northern platyfish, northern swordtails, southern platyfish and southern swordtails; Figure 1a) [2,11,21,22]. The monophyly and the relationships among those four lineages are not consistently supported in phylogenetic studies using molecular or combined molecular and morphological traits. For example, it has been difficult to assign X. andersi[57] to any specific lineage and inconsistent phylogenetic placements were found based on morphological characters and molecular based phylogenetic analyses [11,22]. Xiphophorus andersi has some platy as well as some swordtail features – it is an elongated – swordtail-like – species, but lacks the pronounced, colored ventral extension of the caudal fin. Also, geographical distributions of some species are inconsistent with those of other members of the lineages to which they were assigned; for example, a southern platyfish, X. xiphidium occurs further north than the northern swordtails [2] (see Figure 1a).


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)

Map of the distributions of Xiphophorus species. (a) Geographical distributions of all described 26 species in the genus Xiphophorus including the four newly described species – X. monticolus, X. mixei, X. kallmani and X. mayae (colored in blue) and two species of a putatively hybrid origin, X. monticolus and X. clemenciae (in bold). (b) Geographical distributions of three species in the clemenciae clade (maps are modified from [2,58]).
© Copyright Policy - open-access
Related In: Results  -  Collection

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

Figure 1: Map of the distributions of Xiphophorus species. (a) Geographical distributions of all described 26 species in the genus Xiphophorus including the four newly described species – X. monticolus, X. mixei, X. kallmani and X. mayae (colored in blue) and two species of a putatively hybrid origin, X. monticolus and X. clemenciae (in bold). (b) Geographical distributions of three species in the clemenciae clade (maps are modified from [2,58]).
Mentions: Although the origin and evolution of the sword [7,20,26,53-56] and the role of hybridization in the genus Xiphophorus[2] have been addressed before, some of the phylogenetic relationships in this genus still remained uncertain. Traditionally, the genus Xiphophorus has been suggested to consist of four major lineages based on their geographical distributions and other phenotypic traits (i.e., northern platyfish, northern swordtails, southern platyfish and southern swordtails; Figure 1a) [2,11,21,22]. The monophyly and the relationships among those four lineages are not consistently supported in phylogenetic studies using molecular or combined molecular and morphological traits. For example, it has been difficult to assign X. andersi[57] to any specific lineage and inconsistent phylogenetic placements were found based on morphological characters and molecular based phylogenetic analyses [11,22]. Xiphophorus andersi has some platy as well as some swordtail features – it is an elongated – swordtail-like – species, but lacks the pronounced, colored ventral extension of the caudal fin. Also, geographical distributions of some species are inconsistent with those of other members of the lineages to which they were assigned; for example, a southern platyfish, X. xiphidium occurs further north than the northern swordtails [2] (see Figure 1a).

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
Related in: MedlinePlus