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Independent origins of new sex-linked chromosomes in the melanica and robusta species groups of Drosophila.

Flores SV, Evans AL, McAllister BF - BMC Evol. Biol. (2008)

Bottom Line: Two mitochondrial and two nuclear gene sequences were used to reconstruct phylogenetic relationships of a set of nine ingroup species having fused and unfused sex chromosomes and representing a broad sample of both species groups.An estimate tightly constrained around 8 My was obtained for the age of the rearranged sex chromosomes in the melanica group; however, a more loosely constrained estimate of 10-15 My was obtained for the age of the rearrangement in the robusta group.Our findings indicate that the parallel divergence experienced by newly sex-linked genomic regions in these groups represents an excellent system for studying the tempo of sex chromosome evolution.

View Article: PubMed Central - HTML - PubMed

Affiliation: Department of Biological Sciences & Roy J, Carver Center for Comparative Genomics, 143 Biology Building, University of Iowa, Iowa City, IA 52242, USA. sergio-flores@uiowa.edu <sergio-flores@uiowa.edu>

ABSTRACT

Background: Recent translocations of autosomal regions to the sex chromosomes represent important systems for identifying the evolutionary forces affecting convergent patterns of sex-chromosome heteromorphism. Additions to the sex chromosomes have been reported in the melanica and robusta species groups, two sister clades of Drosophila. The close relationship between these two species groups and the similarity of their rearranged karyotypes motivates this test of alternative hypotheses; the rearranged sex chromosomes in both groups are derived through a common origin, or the rearrangements are derived through at least two independent origins. Here we examine chromosomal arrangement in representatives of the melanica and the robusta species groups and test these alternative hypotheses using a phylogenetic approach.

Results: Two mitochondrial and two nuclear gene sequences were used to reconstruct phylogenetic relationships of a set of nine ingroup species having fused and unfused sex chromosomes and representing a broad sample of both species groups. Different methods of phylogenetic inference, coupled with concurrent cytogenetic analysis, indicate that the hypothesis of independent origins of rearranged sex chromosomes within each species group is significantly more likely than the alternative hypothesis of a single common origin. An estimate tightly constrained around 8 My was obtained for the age of the rearranged sex chromosomes in the melanica group; however, a more loosely constrained estimate of 10-15 My was obtained for the age of the rearrangement in the robusta group.

Conclusion: Independent acquisition of new chromosomal arms by the sex chromosomes in the melanica and robusta species groups represents a case of striking convergence at the karyotypic level. Our findings indicate that the parallel divergence experienced by newly sex-linked genomic regions in these groups represents an excellent system for studying the tempo of sex chromosome evolution.

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Saturation on third codon positions. Comparison between ML distance (X axis) and uncorrected distances for third codon positions (Y axis) estimated from: a) CoI, b) CoII, c) cac, and d) sc sequences. Transitions and transversions distances within ingroup and between ingroup-outgroup are labeled. Dotted lines correspond to regression lines fitted to transitions and solid lines for transversions.
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Figure 3: Saturation on third codon positions. Comparison between ML distance (X axis) and uncorrected distances for third codon positions (Y axis) estimated from: a) CoI, b) CoII, c) cac, and d) sc sequences. Transitions and transversions distances within ingroup and between ingroup-outgroup are labeled. Dotted lines correspond to regression lines fitted to transitions and solid lines for transversions.

Mentions: Sequences from the mitochondrial genes Cytochrome oxidase I (mtCoI) and Cytochrome oxidase II (mtCoII), and from the X-chromosome gene regions cacophony (cac) and scute (sc) were used in the phylogenetic analysis. After excluding regions of scute with many indels among repetitious codons and introns from cacophony, the alignment matrix contained the following sizes: CoI = 645 bp; CoII = 657 bp; cac = 588 bp and sc = 579 bp. The mitochondrial genes (CoI and CoII) showed higher observed frequencies of transversions than transitions, even for short corrected pairwise-distances. This is a common pattern for mitochondrial genes in Drosophila [56], and is apparently due to rapid saturation for transition substitutions. Also, the corrected distances estimated from the mitochondrial sequences failed to separate outgroup from ingroup taxa (Fig. 3). Consequently, third positions of the CoI and CoII codons were removed in the following analyses. The nucleotide composition, substitution rates, transition-transversions ratios and models of nucleotide substitution for alternative partitions of the data are summarized in Table 2. Homogeneity tests showed similar phylogenetic signals for each major data partition, although the two nuclear genes did exhibit marginally non-significant heterogeneity (ILD test, P = 0.056). However, this weak incongruence between nuclear genes was not indicated when outgroups were removed (Table 3); therefore, the full concatenated dataset was used for hypothesis testing.


Independent origins of new sex-linked chromosomes in the melanica and robusta species groups of Drosophila.

Flores SV, Evans AL, McAllister BF - BMC Evol. Biol. (2008)

Saturation on third codon positions. Comparison between ML distance (X axis) and uncorrected distances for third codon positions (Y axis) estimated from: a) CoI, b) CoII, c) cac, and d) sc sequences. Transitions and transversions distances within ingroup and between ingroup-outgroup are labeled. Dotted lines correspond to regression lines fitted to transitions and solid lines for transversions.
© Copyright Policy - open-access
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC2268673&req=5

Figure 3: Saturation on third codon positions. Comparison between ML distance (X axis) and uncorrected distances for third codon positions (Y axis) estimated from: a) CoI, b) CoII, c) cac, and d) sc sequences. Transitions and transversions distances within ingroup and between ingroup-outgroup are labeled. Dotted lines correspond to regression lines fitted to transitions and solid lines for transversions.
Mentions: Sequences from the mitochondrial genes Cytochrome oxidase I (mtCoI) and Cytochrome oxidase II (mtCoII), and from the X-chromosome gene regions cacophony (cac) and scute (sc) were used in the phylogenetic analysis. After excluding regions of scute with many indels among repetitious codons and introns from cacophony, the alignment matrix contained the following sizes: CoI = 645 bp; CoII = 657 bp; cac = 588 bp and sc = 579 bp. The mitochondrial genes (CoI and CoII) showed higher observed frequencies of transversions than transitions, even for short corrected pairwise-distances. This is a common pattern for mitochondrial genes in Drosophila [56], and is apparently due to rapid saturation for transition substitutions. Also, the corrected distances estimated from the mitochondrial sequences failed to separate outgroup from ingroup taxa (Fig. 3). Consequently, third positions of the CoI and CoII codons were removed in the following analyses. The nucleotide composition, substitution rates, transition-transversions ratios and models of nucleotide substitution for alternative partitions of the data are summarized in Table 2. Homogeneity tests showed similar phylogenetic signals for each major data partition, although the two nuclear genes did exhibit marginally non-significant heterogeneity (ILD test, P = 0.056). However, this weak incongruence between nuclear genes was not indicated when outgroups were removed (Table 3); therefore, the full concatenated dataset was used for hypothesis testing.

Bottom Line: Two mitochondrial and two nuclear gene sequences were used to reconstruct phylogenetic relationships of a set of nine ingroup species having fused and unfused sex chromosomes and representing a broad sample of both species groups.An estimate tightly constrained around 8 My was obtained for the age of the rearranged sex chromosomes in the melanica group; however, a more loosely constrained estimate of 10-15 My was obtained for the age of the rearrangement in the robusta group.Our findings indicate that the parallel divergence experienced by newly sex-linked genomic regions in these groups represents an excellent system for studying the tempo of sex chromosome evolution.

View Article: PubMed Central - HTML - PubMed

Affiliation: Department of Biological Sciences & Roy J, Carver Center for Comparative Genomics, 143 Biology Building, University of Iowa, Iowa City, IA 52242, USA. sergio-flores@uiowa.edu <sergio-flores@uiowa.edu>

ABSTRACT

Background: Recent translocations of autosomal regions to the sex chromosomes represent important systems for identifying the evolutionary forces affecting convergent patterns of sex-chromosome heteromorphism. Additions to the sex chromosomes have been reported in the melanica and robusta species groups, two sister clades of Drosophila. The close relationship between these two species groups and the similarity of their rearranged karyotypes motivates this test of alternative hypotheses; the rearranged sex chromosomes in both groups are derived through a common origin, or the rearrangements are derived through at least two independent origins. Here we examine chromosomal arrangement in representatives of the melanica and the robusta species groups and test these alternative hypotheses using a phylogenetic approach.

Results: Two mitochondrial and two nuclear gene sequences were used to reconstruct phylogenetic relationships of a set of nine ingroup species having fused and unfused sex chromosomes and representing a broad sample of both species groups. Different methods of phylogenetic inference, coupled with concurrent cytogenetic analysis, indicate that the hypothesis of independent origins of rearranged sex chromosomes within each species group is significantly more likely than the alternative hypothesis of a single common origin. An estimate tightly constrained around 8 My was obtained for the age of the rearranged sex chromosomes in the melanica group; however, a more loosely constrained estimate of 10-15 My was obtained for the age of the rearrangement in the robusta group.

Conclusion: Independent acquisition of new chromosomal arms by the sex chromosomes in the melanica and robusta species groups represents a case of striking convergence at the karyotypic level. Our findings indicate that the parallel divergence experienced by newly sex-linked genomic regions in these groups represents an excellent system for studying the tempo of sex chromosome evolution.

Show MeSH
Related in: MedlinePlus