Dataset Information

Comparative Phylogenomic Assessment of Mitochondrial Introgression among Several Species of Chipmunks (Tamias).

ABSTRACT: Many species are not completely reproductively isolated, resulting in hybridization and genetic introgression. Organellar genomes, such as those derived from mitochondria (mtDNA) and chloroplasts, introgress frequently in natural systems; however, the forces shaping patterns of introgression are not always clear. Here, we investigate extensive mtDNA introgression in western chipmunks, focusing on species in the Tamias quadrivittatus group from the central and southern Rocky Mountains. Specifically, we investigate the role of selection in driving patterns of introgression. We sequenced 51 mtDNA genomes from six species and combine these sequences with other published genomic data to yield annotated mitochondrial reference genomes for nine species of chipmunks. Genomic characterization was performed using a series of molecular evolutionary and phylogenetic analyses to test protein-coding genes for positive selection. We fit a series of maximum likelihood models using a model-averaging approach, assessed deviations from neutral expectations, and performed additional tests to search for codons under the influence of selection. We found no evidence for positive selection among these genomes, suggesting that selection has not been the driving force of introgression in these species. Thus, extensive mtDNA introgression among several species of chipmunks likely reflects genetic drift of introgressed alleles in historically fluctuating populations.

SUBMITTER: Sarver BA

PROVIDER: S-EPMC5381575 | biostudies-literature | 2017 Jan

REPOSITORIES: biostudies-literature

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Comparative Phylogenomic Assessment of Mitochondrial Introgression among Several Species of Chipmunks (Tamias).

Sarver Brice A J BA Demboski John R JR Good Jeffrey M JM Forshee Nicholas N Hunter Samuel S SS Sullivan Jack J

Genome biology and evolution 20170101 1

Many species are not completely reproductively isolated, resulting in hybridization and genetic introgression. Organellar genomes, such as those derived from mitochondria (mtDNA) and chloroplasts, introgress frequently in natural systems; however, the forces shaping patterns of introgression are not always clear. Here, we investigate extensive mtDNA introgression in western chipmunks, focusing on species in the Tamias quadrivittatus group from the central and southern Rocky Mountains. Specifical ...[more]

PMID: 28172670

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Project description:Evidence from natural systems suggests that hybridization between animal species is more common than traditionally thought, but the overall contribution of introgression to standing genetic variation within species remains unclear for most animal systems. Here, we use targeted exon capture to sequence thousands of nuclear loci and complete mitochondrial genomes from closely related chipmunk species in the Tamias quadrivittatus group that are distributed across the Great Basin and the central and southern Rocky Mountains of North America. This recent radiation includes six overlapping, ecologically distinct species (Tamias canipes, Tamias cinereicollis, Tamias dorsalis, T. quadrivittatus, Tamias rufus, and Tamias umbrinus) that show evidence for widespread introgression across species boundaries. Such evidence has historically been derived from a handful of markers, typically focused on mitochondrial loci, to describe patterns of introgression; consequently, the extent of introgression of nuclear genes is less well characterized. We conducted a series of phylogenomic and species-tree analyses to resolve the phylogeny of six species in this group. In addition, we performed several population-genomic analyses to characterize nuclear genomes and infer coancestry among individuals. Furthermore, we used emerging quartets-based approaches to simultaneously infer the species tree (SVDquartets) and identify introgression (HyDe). We found that, in spite of rampant introgression of mitochondrial genomes between some species pairs (and sometimes involving up to three species), there appears to be little to no evidence for nuclear introgression. These findings mirror other genomic results where complete mitochondrial capture has occurred between chipmunk species in the absence of appreciable nuclear gene flow. The underlying causes of recurrent massive cytonuclear discordance remain unresolved in this group but mitochondrial DNA appears highly misleading of population histories as a whole. Collectively, it appears that chipmunk species boundaries are largely impermeable to nuclear gene flow and that hybridization, while pervasive with respect to mtDNA, has likely played a relatively minor role in the evolutionary history of this group. [Cytonuclear discordance; hyridization; introgression, phylogenomics; SVDquartets; Tamias.].

Project description:BACKGROUND: Nucleotide sequences and the gene arrangements of mitochondrial genomes are effective tools for resolving phylogenetic problems. Hemipteroid insects are known to possess highly reorganized mitochondrial genomes, but in the suborder Heteroptera (Insecta: Hemiptera), there was only one complete mitochondrial genome sequenced without gene rearrangement and the phylogeny of infraorder Pentatomomorpha in Heteroptera was still uncertain. RESULTS: Fifteen mitochondrial genomes of the suborder Heteroptera were sequenced. Gene rearrangements were found as follows: 1) tRNA-I and tRNA-Q switched positions in Aradidae, 2) tRNA-T and tRNA-P switched positions in Largidae and Pyrrhocoridae. Two recombination events were found in Alydidae and Malcidae. The other mt-genomes were organized in the same way as observed in Drosophila yakuba. The phylogenetic analyses of infraorder Pentatomomorpha based on the nucleotide sequence raised the hypothesis of (Aradoidea + (Pentatomoidea + (Pyrrhocoroidea + (Lygaeoidea + Coreoidea)))). The rearrangement of tRNA-T and tRNA-P also linked Largidae and Pyrrhocoridae together. Furthermore, the conserved sequence block in the unusual intergenic spacers between tRNA-H and ND4 favored the monophyly of Lygaeoidea. Tetranucleotide ATCA was inferred to be the initiation codon of ND2 in Cydnidae. No correlation was found between the rates of nucleotide substitution and gene rearrangement. CG content was significantly correlated with the nucleotide substitution rate of each gene. For ND1, there was a positive correlation (P < 0.01) between amino acids variations and hydrophobicity, but a negative correlation (P < 0.01) for ND6. No conserved sequence was found among the control regions and these regions were not always the most AT-rich region of the mt-genome. CONCLUSION: Heteropteran insects are extremely complex groups worthy of further study because of the unusual tetranucleotide initiation codon and their great mt-genomic diversity, including gene rearrangements and recombinations. The mt-genome is a powerful molecular marker for resolving phylogeny at the level of the superfamily and family. Gene rearrangements were not correlated with nucleotide substitution rates. CG content variation caused the different evolutionary patterns among genes. For ND1, in many polar or nonpolar regions the specific identity of the amino acid residues might be more important than maintaining the polarity of these regions, while the opposite is true for ND6. Most sequences of the control regions did not appear to be important for regulatory functions. Finally, we suggest that the term "AT-rich regions" should not be used.

Dataset Information

Comparative Phylogenomic Assessment of Mitochondrial Introgression among Several Species of Chipmunks (Tamias).

Publications

Comparative Phylogenomic Assessment of Mitochondrial Introgression among Several Species of Chipmunks (Tamias).

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