Mitochondrial genome divergence supports an ancient origin of circatidal behaviour in the Anurida maritima (Collembola: Neanuridae) species group

Article


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
TypeArticle
TitleMitochondrial genome divergence supports an ancient origin of circatidal behaviour in the Anurida maritima (Collembola: Neanuridae) species group
AuthorsTimmermans, M., Arbea, J., Campbell, G., King, M., Prins, A. and Kett, S.
Abstract

Animals of the intertidal zone tolerate substantial environmental fuctuations. Survival under such unstable conditions requires specifc adaptations. Several intertidal species have evolved endogenous mechanisms that follow tidal rhythms permitting behavioural alignment with periodic inundation. For example, aggregation behaviour in the springtail Anurida maritima (Guérin-Méneville, 1836) (Collembola: Neanuridae) is controlled by a free-running clock with a period of~12.4 h.
This cosmopolitan species is found in the upper intertidal zone where it forages during low tide. Before high tide, specimens aggregate in cracks in the substrate or under rocks to survive inundation. Here we report that the closely related intertidal species Anurida bisetosa Bagnall, 1949, displays a similar endogenously controlled circatidal behaviour. To obtain a minimum age estimate for this shared derived trait, we sequenced the full mitochondrial genome of A. bisetosa, which was then used for phylogenetic inference and molecular dating. The mitochondrial genomes of A. maritima and A. bisetosa are highly divergent. This divergence extends throughout the whole mitochondrial genome and is mirrored by a similar pattern in the nuclear internal transcribed spacer 2 (ITS2) region. Dating analyses suggest the species potentially split more than 40 million years ago. Under the assumption that the endogenously-controlled rhythmic behaviour evolved once in an ancestor of the two species, the trait must be of older age. Use of a single genetic marker and a limited number of fossil calibration points constrains accuracy of the age estimate, but nevertheless, it ofers a glimpse at otherwise ‘intangible’ palaeoecological and palaeoethological attributes.

LanguageEnglish
PublisherSpringer
JournalOrganisms Diversity & Evolution
ISSN1439-6092
Electronic1618-1077
Publication dates
Online22 Sep 2021
Print31 Mar 2022
Publication process dates
Deposited05 Oct 2021
Accepted14 Jun 2021
Output statusPublished
Accepted author manuscript
Copyright Statement

This is a post-peer-review, pre-copyedit version of an article published in Organisms Diversity & Evolution. This version of the article has been accepted for publication, after peer review (when applicable) and is subject to Springer Nature’s AM terms of use, but is not the Version of Record and does not reflect post-acceptance improvements, or any corrections. The Version of Record is available online at: http://dx.doi.org/10.1007/s13127-021-00503-1

Digital Object Identifier (DOI)https://doi.org/10.1007/s13127-021-00503-1
Permalink -

https://repository.mdx.ac.uk/item/89801

Download files

  • 45
    total views
  • 5
    total downloads
  • 1
    views this month
  • 0
    downloads this month

Export as

Related outputs

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
The bacterial urban resistome: recent advances
Vassallo, A., Kett, S., Purchase, D. and Marvasi, M. 2022. The bacterial urban resistome: recent advances. Antibiotics. 11 (4), pp. 1-17. https://doi.org/10.3390/antibiotics11040512
Antibiotic-resistant genes and bacteria as evolving contaminants of emerging concerns (e-CEC): is it time to include evolution in risk assessment?
Vassallo, A., Kett, S., Purchase, D. and Marvasi, M. 2021. Antibiotic-resistant genes and bacteria as evolving contaminants of emerging concerns (e-CEC): is it time to include evolution in risk assessment? Antibiotics. 10 (9), pp. 1-11. https://doi.org/10.3390/antibiotics10091066
Antifungals, arthropods and antifungal resistance prevention: lessons from ecological interactions
Kett, S., Pathak, A., Turillazzi, S., Cavalieri, D. and Marvasi, M. 2021. Antifungals, arthropods and antifungal resistance prevention: lessons from ecological interactions. Proceedings of the Royal Society B: Biological Sciences. 288 (1944), pp. 1-7. https://doi.org/10.1098/rspb.2020.2716
Characterization of the complete mitochondrial genome of Diplostomum baeri
Landeryou, T., Ropiquet, A., Kett, S., Wildeboer, D. and Lawton, S. 2020. Characterization of the complete mitochondrial genome of Diplostomum baeri. Parasitology International. 79. https://doi.org/10.1016/j.parint.2020.102166
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
Resisting antimicrobial resistance: lessons from fungus farming ants
Pathak, A., Kett, S. and Marvasi, M. 2019. Resisting antimicrobial resistance: lessons from fungus farming ants. Trends in Ecology & Evolution. 34 (11), pp. 974-976. https://doi.org/10.1016/j.tree.2019.08.007
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
Unravelling the riddle of Radix: DNA barcoding for species identification of freshwater snail intermediate hosts of zoonotic digeneans and estimating their inter-population evolutionary relationships
Lawton, S., Lim, R., Dukes, J., Kett, S., Cook, R., Walker, A. and Kirk, R. 2015. Unravelling the riddle of Radix: DNA barcoding for species identification of freshwater snail intermediate hosts of zoonotic digeneans and estimating their inter-population evolutionary relationships. Infection, Genetics and Evolution. 35, pp. 63-74. https://doi.org/10.1016/j.meegid.2015.07.021
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.
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.
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
Intraspecific genetic variation in complex assemblages from mitochondrial metagenomics: comparison with DNA barcodes
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
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
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
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