Intraspecific genetic variation in complex assemblages from mitochondrial metagenomics: comparison with DNA barcodes

Article


Gómez-Rodríguez, C., Timmermans, M., Crampton-Platt, A. and Vogler, A. 2017. Intraspecific genetic variation in complex assemblages from mitochondrial metagenomics: comparison with DNA barcodes. Methods in Ecology and Evolution. 8 (2), pp. 248-256. https://doi.org/10.1111/2041-210X.12667
TypeArticle
TitleIntraspecific genetic variation in complex assemblages from mitochondrial metagenomics: comparison with DNA barcodes
AuthorsGómez-Rodríguez, C., Timmermans, M., Crampton-Platt, A. and Vogler, A.
Abstract

Metagenomic shotgun sequencing, using Illumina technology, and de novo genome assembly of mixed field-collected amples of invertebrates readily produce mitochondrial genome sequences, allowing rapid identification and quantification of species diversity. However, intraspecific genetic variability present in the specimen pools is lost during mitogenome assembly, which limits the utility of ‘mitochondrial metagenomics’ for studies of population diversity.
2. Using 10 natural communities (>2600 individuals) of leaf beetles (Chrysomelidae), DNA variation in the mitochondrial cox1-5’ ‘barcode’ was compared for Sanger sequenced individuals and Illumina shotgun sequenced specimen pools.
3. Generally, only a single mitochondrial contig was assembled per species, even in the presence of intraspecific variation. Ignoring ambiguity from the use of two different assemblers, the cox1 barcode regions from these assemblies were exact nucleotide matches of a Sanger sequenced barcode in 90.7% of cases, which dropped to 76.0% in assemblies from samples with large intra and interspecific variability. Nucleotide differences between barcodes from both data types were almost exclusively in synonymous 3rd codon position, although the number of affected sites was very low, and the greatest discrepancies were correlated with poor quality of Sanger sequences.
4. Unassembled shotgun reads were also used to score single nucleotide polymorphisms and to calculate intraspecific nucleotide diversity (pi) for all available populations at each site. These values correlated with Sanger sequenced cox1 variation but were significantly higher.
5. Overall, the assemblage-focused shotgun sequencing of pooled samples produced nucleotide variation data comparable to the well-established specimen-focused Sanger approach. The findings thus extend the application of mitochondrial metagenomics of complex biodiversity samples to the estimation of diversity below the species level.

KeywordsMitochondrial metagenomics, mito-metagenomics, genome skimming, Chrysomelidae, intraspecific variability, population genetics, DNA barcodes
PublisherWiley
JournalMethods in Ecology and Evolution
ISSN2041-210X
Publication dates
Online17 Nov 2016
Print11 Feb 2017
Publication process dates
Deposited17 Oct 2016
Accepted28 Sep 2016
Output statusPublished
Accepted author manuscript
Copyright Statement

This is the peer reviewed version of the following article: Gómez-Rodríguez, C., Timmermans, M. J. T. N., Crampton-Platt, A. and Vogler, A. P. (2017), Intraspecific genetic variation in complex assemblages from mitochondrial metagenomics: comparison with DNA barcodes. Methods Ecol Evol, 8: 248–256. doi:10.1111/2041-210X.12667, which has been published in final form athttp://doi.org/10.1111/2041-210X.12667. This article may be used for non-commercial purposes in accordance with Wiley Terms and Conditions for Self-Archiving."

Digital Object Identifier (DOI)https://doi.org/10.1111/2041-210X.12667
LanguageEnglish
Permalink -

https://repository.mdx.ac.uk/item/86q84

Download files

  • 55
    total views
  • 8
    total downloads
  • 2
    views this month
  • 0
    downloads this month

Export as

Related outputs

Turning the tide: rhythmic aggregation behaviour in Anurida maritima (Collembola) is entrained by inundation
Timmermans, M., King, M., Purchase, D., Dickins, J.A., Dickins, T. and Kett, S. 2024. Turning the tide: rhythmic aggregation behaviour in Anurida maritima (Collembola) is entrained by inundation. Journal of Experimental Marine Biology and Ecology. 581. https://doi.org/10.1016/j.jembe.2024.152062
A study of bacteria producing carbonic anhydrase enzyme for CaCO3 precipitation and soil biocementation
Meandira, W., Mavroulidou, M., Timmermans, M., Gunn, M., Gray, C., Pantoja Munoz, L. and Purchase, D. 2024. A study of bacteria producing carbonic anhydrase enzyme for CaCO3 precipitation and soil biocementation. Environmental Science and Pollution Research. 31 (33), pp. 45818-45833. https://doi.org/10.1007/s11356-024-34077-0
Molding the future: optimization of bioleaching of rare earth elements from electronic waste by Penicillium expansum and insights into its mechanism
Gonzalez Baez, A., Pantoja Munoz, L., Timmermans, M., Garelick, H. and Purchase, D. 2024. Molding the future: optimization of bioleaching of rare earth elements from electronic waste by Penicillium expansum and insights into its mechanism. Bioresource Technology. 402. https://doi.org/10.1016/j.biortech.2024.130750
Wolbachia and Spiroplasma endosymbionts in the Anurida maritima (Collembola) species group
Timmermans, M., Prabha, H. and Kett, S. 2023. Wolbachia and Spiroplasma endosymbionts in the Anurida maritima (Collembola) species group. Evolutionary Journal of the Linnean Society. 2 (1). https://doi.org/10.1093/evolinnean/kzad001
Mitochondrial genome divergence supports an ancient origin of circatidal behaviour in the Anurida maritima (Collembola: Neanuridae) species group
Timmermans, M., Arbea, J., Campbell, G., King, M., Prins, A. and Kett, S. 2022. Mitochondrial genome divergence supports an ancient origin of circatidal behaviour in the Anurida maritima (Collembola: Neanuridae) species group. Organisms Diversity & Evolution. 22 (1), pp. 131-140. https://doi.org/10.1007/s13127-021-00503-1
Mimicry diversification in Papilio dardanus via a genomic inversion in the regulatory region of engrailed – invected
Timmermans, M., Srivathsan, A., Collins, S., Meier, R. and Vogler, A. 2020. Mimicry diversification in Papilio dardanus via a genomic inversion in the regulatory region of engrailed – invected. Proceedings of the Royal Society B: Biological Sciences. 287 (1926). https://doi.org/10.1098/rspb.2020.0443
Phylogeny of the Hawkmoth tribe Ambulycini: mitogenomes from museum specimens resolve major relationships
Timmermans, M., Daghmoumi, S., Glass, D., Hamilton, C., Kawahara, A. and Kitching, I. 2019. Phylogeny of the Hawkmoth tribe Ambulycini: mitogenomes from museum specimens resolve major relationships. Insect Systematics and Diversity. 3 (6). https://doi.org/10.1093/isd/ixz025
Phylogenomics resolves major relationships and reveals significant diversification rate shifts in the evolution of silk moths and relatives
Hamilton, C., St Laurent, R., Dexter, K., Kitching, I., Breinholt, J., Zwick, A., Timmermans, M., Barber, J. and Kawahara, A. 2019. Phylogenomics resolves major relationships and reveals significant diversification rate shifts in the evolution of silk moths and relatives. BMC Evolutionary Biology. 19 (1), pp. 1-13. https://doi.org/10.1186/s12862-019-1505-1
The contribution of mitochondrial metagenomics to large-scale data mining and phylogenetic analysis of Coleoptera
Linard, B., Crampton-Platt, A., Moriniere, J., Timmermans, M., Andújar, C., Arribas, P., Miller, K., Lipecki, J., Favreau, E., Hunter, A., Gómez-Rodríguez, C., Barton, C., Nie, R., Gillett, C., Breeschoten, T., Bocak, L. and Vogler, A. 2018. The contribution of mitochondrial metagenomics to large-scale data mining and phylogenetic analysis of Coleoptera. Molecular Phylogenetics and Evolution. 128, pp. 1-11. https://doi.org/10.1016/j.ympev.2018.07.008
Two European Cornus L. feeding leafmining moths, Antispila petryi Martini, 1899, sp. rev. and A. treitschkiella (Fischer von Röslerstamm, 1843) (Lepidoptera, Heliozelidae): an unjustified synonymy and overlooked range expansion
van Nieukerken, E., Lees, D., Doorenweerd, C., Koster, S., Bryner, R., Schreurs, A., Timmermans, M. and Sattler, K. 2018. Two European Cornus L. feeding leafmining moths, Antispila petryi Martini, 1899, sp. rev. and A. treitschkiella (Fischer von Röslerstamm, 1843) (Lepidoptera, Heliozelidae): an unjustified synonymy and overlooked range expansion. Nota Lepidopterologica. 41 (1), pp. 39-86. https://doi.org/10.3897/nl.41.22264
Nature read in tooth and fur: non-invasive sampling of the Pygmy Shrew (Sorex minutus Linnaeus, 1766) on Lundy for population genetics
Legall, N., Kett, S. and Timmermans, M. 2016. Nature read in tooth and fur: non-invasive sampling of the Pygmy Shrew (Sorex minutus Linnaeus, 1766) on Lundy for population genetics. Journal of the Lundy Field Society. 5, pp. 101-108.
Black rabbits on Lundy: Tudor treasures or post-war phonies?
Timmermans, M., Elmi, H. and Kett, S. 2018. Black rabbits on Lundy: Tudor treasures or post-war phonies? Journal of the Lundy Field Society. 6, pp. 105-113.
What's on the menu: Drosera rotundifolia diet determination using DNA data
Lekesyte, B., Kett, S. and Timmermans, M. 2018. What's on the menu: Drosera rotundifolia diet determination using DNA data. Journal of the Lundy Field Society. 6, pp. 55-64.
The phylogeny of Galerucinae (Coleoptera: Chrysomelidae) and the performance of mitochondrial genomes in phylogenetic inference compared to nuclear rRNA genes
Nie, R., Breeschoten, T., Timmermans, M., Nadein, K., Xue, H., Bai, M., Huang, Y., Yang, X. and Vogler, A. 2018. The phylogeny of Galerucinae (Coleoptera: Chrysomelidae) and the performance of mitochondrial genomes in phylogenetic inference compared to nuclear rRNA genes. Cladistics. 34 (2), pp. 113-130. https://doi.org/10.1111/cla.12196
Independent evolution of sexual dimorphism and female-limited mimicry in swallowtail butterflies (Papilio dardanus and Papilio phorcas)
Timmermans, M., Thompson, M., Collins, S. and Vogler, A. 2017. Independent evolution of sexual dimorphism and female-limited mimicry in swallowtail butterflies (Papilio dardanus and Papilio phorcas). Molecular Ecology. 26 (5), pp. 1273-1284. https://doi.org/10.1111/mec.14012
Uncovering trophic interactions in arthropod predators through DNA shotgun-sequencing of gut contents
Paula, D., Linard, B., Crampton-Platt, A., Srivathsan, A., Timmermans, M., Sujii, E., Pires, C., Souza, L., Andow, D. and Vogler, A. 2016. Uncovering trophic interactions in arthropod predators through DNA shotgun-sequencing of gut contents. PLoS ONE. 11 (9), pp. 1-14. https://doi.org/10.1371/journal.pone.0161841
Family-level sampling of mitochondrial genomes in coleoptera: compositional heterogeneity and phylogenetics
Timmermans, M., Barton, C., Haran, J., Ahrens, D., Culverwell, C., Ollikainen, A., Dodsworth, S., Foster, P., Bocak, L. and Vogler, A. 2016. Family-level sampling of mitochondrial genomes in coleoptera: compositional heterogeneity and phylogenetics. Genome Biology and Evolution. 8 (1), pp. 161-175. https://doi.org/10.1093/gbe/evv241
Mitogenomics of ‘old world Acraea’ butterflies reveals a highly divergent ‘Bematistes’
Timmermans, M., Lees, D., Thompson, M., Sáfián, S. and Brattström, O. 2016. Mitogenomics of ‘old world Acraea’ butterflies reveals a highly divergent ‘Bematistes’. Molecular Phylogenetics and Evolution. 97, pp. 233-241. https://doi.org/10.1016/j.ympev.2015.12.009
Metagenome skimming of insect specimen pools: potential for comparative genomics
Linard, B., Crampton-Platt, A., Gillett, C., Timmermans, M. and Vogler, A. 2015. Metagenome skimming of insect specimen pools: potential for comparative genomics. Genome Biology and Evolution. https://doi.org/10.1093/gbe/evv086
Rapid assembly of taxonomically validated mitochondrial genomes from historical insect collections
Timmermans, M., Viberg, C., Martin, G., Hopkins, K. and Vogler, A. 2016. Rapid assembly of taxonomically validated mitochondrial genomes from historical insect collections. Biological Journal of the Linnean Society. 117 (1), pp. 83-95. https://doi.org/10.1111/bij.12552
Soup to tree: the phylogeny of beetles inferred by mitochondrial metagenomics of a Bornean rainforest sample
Crampton-Platt, A., Timmermans, M., Gimmel, M., Kutty, S., Cockerill, T., Khen, C. and Vogler, A. 2015. Soup to tree: the phylogeny of beetles inferred by mitochondrial metagenomics of a Bornean rainforest sample. Molecular Biology and Evolution. 32 (9), pp. 2302-2316. https://doi.org/10.1093/molbev/msv111
Bulk de novo mitogenome assembly from pooled total DNA elucidates the phylogeny of weevils (Coleoptera: Curculionoidea)
Gillett, C., Crampton-Platt, A., Timmermans, M., Jordal, B., Emerson, B. and Vogler, A. 2014. Bulk de novo mitogenome assembly from pooled total DNA elucidates the phylogeny of weevils (Coleoptera: Curculionoidea). Molecular Biology and Evolution. 31 (8), pp. 2223-2237. https://doi.org/10.1093/molbev/msu154
Towards a mitogenomic phylogeny of Lepidoptera
Timmermans, M., Lees, D. and Simonsen, T. 2014. Towards a mitogenomic phylogeny of Lepidoptera. Molecular Phylogenetics and Evolution. 79, pp. 169-178. https://doi.org/10.1016/j.ympev.2014.05.031
Comparative genomics of the mimicry switch in Papilio dardanus
Timmermans, M., Baxter, S., Clark, R., Heckel, D., Vogel, H., Collins, S., Papanicolaou, A., Fukova, I., Joron, M., Thompson, M., Jiggins, C., ffrench-Constant, R. and Vogler, A. 2014. Comparative genomics of the mimicry switch in Papilio dardanus. Proceedings of the Royal Society B: Biological Sciences. 281 (1787), pp. 1-8. https://doi.org/10.1098/rspb.2014.0465
Validating the power of mitochondrial metagenomics for community ecology and phylogenetics of complex assemblages
Gómez-Rodríguez, C., Crampton-Platt, A., Timmermans, M., Baselga, A. and Vogler, A. 2015. Validating the power of mitochondrial metagenomics for community ecology and phylogenetics of complex assemblages. Methods in Ecology and Evolution. 6 (8), pp. 883-894. https://doi.org/10.1111/2041-210X.12376
Interplay of robustness and plasticity of life-history traits drives ecotypic differentiation in thermally distinct habitats
Liefting, M., van Grunsven, R., Morrissey, M., Timmermans, M. and Ellers, J. 2015. Interplay of robustness and plasticity of life-history traits drives ecotypic differentiation in thermally distinct habitats. Journal of Evolutionary Biology. 28 (5), pp. 1057-1066. https://doi.org/10.1111/jeb.12629
Phylogenetic community ecology of soil biodiversity using mitochondrial metagenomics
Andújar, C., Arribas, P., Ruzicka, F., Crampton-Platt, A., Timmermans, M. and Vogler, A. 2015. Phylogenetic community ecology of soil biodiversity using mitochondrial metagenomics. Molecular Ecology. 24 (14), pp. 3603-3617. https://doi.org/10.1111/mec.13195
Characterising the phenotypic diversity of Papilio dardanus wing patterns using an extensive museum collection
Thompson, M. and Timmermans, M. 2014. Characterising the phenotypic diversity of Papilio dardanus wing patterns using an extensive museum collection. PLoS ONE. 9 (5), pp. 1-9. https://doi.org/10.1371/journal.pone.0096815
The evolutionary genetics of highly divergent alleles of the mimicry locus in Papilio dardanus
Thompson, M., Timmermans, M., Jiggins, C. and Vogler, A. 2014. The evolutionary genetics of highly divergent alleles of the mimicry locus in Papilio dardanus. BMC Evolutionary Biology. 14. https://doi.org/10.1186/1471-2148-14-140