Purifying selection and genetic drift shaped Pleistocene evolution of the mitochondrial genome in an endangered Australian freshwater fish

Alexandra Pavlova, H. M. Gan, Y. P. Lee, C. M. Austin, Dean M. Gilligan, M. Lintermans, Paul Sunnucks

    Research output: Contribution to journalArticle

    12 Citations (Scopus)

    Abstract

    Genetic variation in mitochondrial genes could underlie metabolic adaptations because mitochondrially encoded proteins are directly involved in a pathway supplying energy to metabolism. Macquarie perch from river basins exposed to different climates differ in size and growth rate, suggesting potential presence of adaptive metabolic differences. We used complete mitochondrial genome sequences to build a phylogeny, estimate lineage divergence times and identify signatures of purifying and positive selection acting on mitochondrial genes for 25 Macquarie perch from three basins: Murray-Darling Basin (MDB), Hawkesbury-Nepean Basin (HNB) and Shoalhaven Basin (SB). Phylogenetic analysis resolved basin-level clades, supporting incipient speciation previously inferred from differentiation in allozymes, microsatellites and mitochondrial control region. The estimated time of lineage divergence suggested an early-to mid-Pleistocene split between SB and the common ancestor of HNB+MDB, followed by mid-To-late Pleistocene splitting between HNB and MDB. These divergence estimates are more recent than previous ones. Our analyses suggested that evolutionary drivers differed between inland MDB and coastal HNB. In the cooler and more climatically variable MDB, mitogenomes evolved under strong purifying selection, whereas in the warmer and more climatically stable HNB, purifying selection was relaxed. Evidence for relaxed selection in the HNB includes elevated transfer RNA and 16S ribosomal RNA polymorphism, presence of potentially mildly deleterious mutations and a codon (ATP6 113) displaying signatures of positive selection (ratio of nonsynonymous to synonymous substitution rates (dN/dS) >1, radical change of an amino-Acid property and phylogenetic conservation across the Percichthyidae). In addition, the difference could be because of stronger genetic drift in the smaller and historically more subdivided HNB with low per-population effective population sizes.

    Original languageEnglish
    Pages (from-to)466-476
    Number of pages11
    JournalHeredity
    Volume118
    Issue number5
    DOIs
    Publication statusPublished - 1 May 2017

    Fingerprint

    Perches
    Genetic Drift
    Mitochondrial Genome
    Mitochondrial Genes
    Fresh Water
    Fishes
    16S Ribosomal RNA
    Phylogeny
    Population Density
    Transfer RNA
    Climate
    Rivers
    Codon
    Microsatellite Repeats
    Energy Metabolism
    Isoenzymes
    Amino Acids
    Mutation
    Growth
    Population

    Cite this

    Pavlova, Alexandra ; Gan, H. M. ; Lee, Y. P. ; Austin, C. M. ; Gilligan, Dean M. ; Lintermans, M. ; Sunnucks, Paul. / Purifying selection and genetic drift shaped Pleistocene evolution of the mitochondrial genome in an endangered Australian freshwater fish. In: Heredity. 2017 ; Vol. 118, No. 5. pp. 466-476.
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    abstract = "Genetic variation in mitochondrial genes could underlie metabolic adaptations because mitochondrially encoded proteins are directly involved in a pathway supplying energy to metabolism. Macquarie perch from river basins exposed to different climates differ in size and growth rate, suggesting potential presence of adaptive metabolic differences. We used complete mitochondrial genome sequences to build a phylogeny, estimate lineage divergence times and identify signatures of purifying and positive selection acting on mitochondrial genes for 25 Macquarie perch from three basins: Murray-Darling Basin (MDB), Hawkesbury-Nepean Basin (HNB) and Shoalhaven Basin (SB). Phylogenetic analysis resolved basin-level clades, supporting incipient speciation previously inferred from differentiation in allozymes, microsatellites and mitochondrial control region. The estimated time of lineage divergence suggested an early-to mid-Pleistocene split between SB and the common ancestor of HNB+MDB, followed by mid-To-late Pleistocene splitting between HNB and MDB. These divergence estimates are more recent than previous ones. Our analyses suggested that evolutionary drivers differed between inland MDB and coastal HNB. In the cooler and more climatically variable MDB, mitogenomes evolved under strong purifying selection, whereas in the warmer and more climatically stable HNB, purifying selection was relaxed. Evidence for relaxed selection in the HNB includes elevated transfer RNA and 16S ribosomal RNA polymorphism, presence of potentially mildly deleterious mutations and a codon (ATP6 113) displaying signatures of positive selection (ratio of nonsynonymous to synonymous substitution rates (dN/dS) >1, radical change of an amino-Acid property and phylogenetic conservation across the Percichthyidae). In addition, the difference could be because of stronger genetic drift in the smaller and historically more subdivided HNB with low per-population effective population sizes.",
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    Purifying selection and genetic drift shaped Pleistocene evolution of the mitochondrial genome in an endangered Australian freshwater fish. / Pavlova, Alexandra; Gan, H. M.; Lee, Y. P.; Austin, C. M.; Gilligan, Dean M.; Lintermans, M.; Sunnucks, Paul.

    In: Heredity, Vol. 118, No. 5, 01.05.2017, p. 466-476.

    Research output: Contribution to journalArticle

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    AU - Gilligan, Dean M.

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