Mitochondrial genome characterization and mitogenome phylogenetics in the central Mexican Stenopelmatus talpa complex (Orthoptera: Stenopelmatidae: Stenopelmatini)
DOI:
https://doi.org/10.22201/ib.20078706e.2023.94.5094Keywords:
Trans-Mexican Volcanic Belt, Ensifera, Mesoamerica, DNA barcodingAbstract
The Stenopelmatus talpa species-group (Stenopelmatidae) comprises cricket-like orthopterans distributed across the Trans-Mexican Volcanic Belt (TMVB) morphotectonic province and adjacent areas in central Mexico. Despite recent efforts, the taxonomy and evolutionary relationships for members of this complex still are far from completely known. Here we generated and characterized the mitochondrial (mt) genome of 14 specimens of the S. talpa species-group and evaluated its species limits with the cox1 barcoding locus. Moreover, based on the mt genome DNA
sequence data, we also reconstructed its phylogenetic relationships and made inferences about its biogeographic history based on a relaxed molecular clock analysis. A total of 9 species were delimited using a 2% pairwise distance criterion, which were consistent with our best estimate of phylogeny. The relationships recovered for the S. talpa species-group were similar although with more recent divergence time estimates than those obtained in a previous phylogenetic study, suggesting that its origin and subsequent diversification in the TMVB followed an east-central pattern, with its earliest divergence occurring during the late Pliocene to early Pleistocene.
References
Avise, J. C., Arnold, J., Ball, R. M., Bermingham, E., Lamb, T., Neigel, J. E. et al. (1987). Intraspecific phylogeography: the mitochondrial DNA bridge between population genetics and systematics. Annual Review of Ecology and Systematics, 18, 489–522.
Bae, J. S., Kim, I., Sohn, H. D., & Jin, B. R. (2004). The mitochondrial genome of the firefly, Pyrocoelia rufa: complete DNA sequence, genome organization, and phylogenetic analysis with other insects. Molecular Phylogenetics and Evolution, 32, 978–985. https://doi.org/10.1016/j.ympev.2004.03.009
Ballard, J. W. O., & Pichaud, N. (2014). Mitochondrial DNA: more than an evolutionary bystander. Functional Ecology, 28, 218–231. https://doi.org/10.1111/1365-2435.12177
Ballard, J. W. O., & Rand, D. M. (2005). The population biology of mitochondrial DNA and its phylogenetic implications. Annual Review of Ecology, Evolution, and Systematics, 36, 621–642. https://doi.org/10.1146/annurev.ecolsys.36.091704.175513
Bernt, M., Donath, A., Jühling, F., Externbrink, F., Florentz, C., Fritzsch, G. et al. (2013). MITOS: improved de novo metazoan mitochondrial genome annotation. Molecular Phylogenetics and Evolution, 69, 313–319. https://doi.org/10.1016/j.ympev.2012.08.023
Boore, J. L. (1999). Animal mitochondrial genomes. Nucleic Acids Research, 27, 1767–1780. https://doi.org/10.1093/nar/27.8.1767
Boore, J. L., Collins, T. M., Stanton, D., Daehler, L. L., & Brown, W. M. (1995). Deducing the pattern of arthropod phylogeny from mitochondrial DNA rearrangements. Nature, 376, 163–165. https://doi.org/10.1038/376163a0
Boore, J. L., Lavrov, D. V., & Brown, W. M. (1998). Gene translocation links insects and crustaceans. Nature, 392, 667–668. https://doi.org/10.1038/33577
Bouckaert, R., Heled, J., Kühnert, D., Vaughan, T., Wu, C. H., Xie, D. et al. (2014). BEAST 2: a software platform for Bayesian evolutionary analysis. Plos Computational Biology, 10, e1003537. https://doi.org/10.1371/journal.pcbi.1003537
Cameron, S. L. (2014). Insect mitochondrial genomics: implications for evolution and phylogeny. Annual Review of Entomology, 59, 95–117. https://doi.org/10.1146/annurev-ento-011613-162007
Cigliano, M. M., Braun, H., Eades, D. C., & Otte, D. (2022). Orthoptera Species File. Version 5.0/5.0. [6th of November, 2022]. http://Orthoptera.SpeciesFile.org
DeSalle, R., Schierwater, B., & Hadrys, H. (2017). MtDNA: The small workhorse of evolutionary studies. Frontiers in Bioscience, 22, 873–887. https://doi.org/10.2741/4522
Drummond, A. J., Ho, S. Y. W., Phillips, M. J., & Rambaut, A. (2006). Relaxed phylogenetics and dating with confidence. Plos Biology, 4, e88. https://doi.org/10.1371/journal.pbio.0040088
Drummond, A. J., Suchard, M. A., Xie, D., & Rambaut, A. (2012). Bayesian phylogenetics with BEAUti and the BEAST 1.7. Molecular Biology and Evolution, 29, 1969–1973. https://doi.org/10.1093/molbev/mss075
Fenn, J. D., Song, H., Cameron, S. L., & Whiting, M. F. (2008). A preliminary mitochondrial genome phylogeny of Orthoptera (Insecta) and approaches to maximizing phylogenetic signal found within mitochondrial genome data. Molecular Phylogenetics and Evolution, 49, 59–68. https://doi.org/10.1016/j.ympev.2008.07.004
Ferrari, L., Orozco-Esquivel, T., Manea, V., & Manea, M. (2012). The dynamic history of the Trans-Mexican Volcanic Belt and the Mexico subduction zone. Tectonophysics, 522, 122–149. https://doi.org/10.1016/j.tecto.2011.09.018
Glenn, T. C., Nilsen, R. A., Kieran, T. J., Finger, J. W., Pierson, T. W., Bentley, K. E. et al. (2016). Adapterama I: universal stubs and primers for thousands of dual-indexed Illumina libraries (iTru & iNext). PeerJ, 7, e775. https://doi.org/10.7717/peerj.7755
Gómez-Tuena, A., Orozco-Esquivel, M. T., & Ferrari, L. (2007). Igneous petrogenesis of the Trans-Mexican volcanic belt. Geological Society of America Special Papers, 422, 129–181. https://doi.org/10.18268/bsgm2005v57n3a2
Gorochov, A. V. (2021). The Families Stenopelmatidae and Anostostomatidae (Orthoptera). 1. Higher Classification, new and little known taxa. Entomological Review, 100, 1106–1151. https://doi.org/10.1134/S0013873820080084
Gutiérrez-Rodríguez, J., Zaldívar-Riverón, A., Weissman, D. B., & Vandergast, A. G. (2022). Extensive species diversification and marked geographic phylogenetic structure in the Mesoamerican genus Stenopelmatus (Orthoptera: Stenopelmatidae: Stenopelmatinae) revealed by mitochondrial and nuclear 3RAD data. Invertebrate Systematics, 36, 1–21. https://doi.org/10.1071/IS21022
Hajibabaei, M., Singer, G. A., Hebert, P. D., & Hickey, D. A. (2007). DNA barcoding: how it complements taxonomy, molecular phylogenetics and population genetics. Trends in Genetics, 23, 167–172. https://doi.org/10.1016/j.tig.2007.02.001
Hebert, P. D., Ratnasingham, S., & De Waard, J. R. (2003). Barcoding animal life: cytochrome c oxidase subunit 1 divergences among closely related species. Proceedings of the Royal Society of London Series B: Biological Sciences, 270, S96–S99. https://doi.org/10.1098/rsbl.2003.0025
Jin, J. J., Yu, W. B., Yang, J. B., Song, Y., Yi, T. S., & Li, D. Z. (2018). GetOrganelle: a simple and fast pipeline for de novo assembly of a complete circular chloroplast genome using genome skimming data. Genome Biology, 21, 1–31. https://doi.org/10.1186/s13059-020-02154-5
Kalyaanamoorthy, S., Minh, B. Q., Wong, T. K., Von Haeseler, A., & Jermiin, L. S. (2017). ModelFinder: fast model selection for accurate phylogenetic estimates. Nature Methods, 14, 587–589. https://doi.org/10.1038/nmeth.4285
Katoh, K., & Standley, D. M. (2013). MAFFT multiple sequence alignment software version 7: improvements in performance and usability. Molecular Biology and Evolution, 30, 772–780. https://doi.org/10.1093/molbev/mst010
Kearse, M., Moir, R., Wilson, A., Stones-Havas, S., Cheung, M., Sturrock, S. et al. (2012). Geneious Basic: an integrated and extendable desktop software platform for the organization and analysis of sequence data. Bioinformatics, 28, 1647–1649. https://doi.org/10.1093/bioinformatics/bts199
Lumley, L. M., & Sperling, F. A. (2010). Integrating morphology and mitochondrial DNA for species delimitation within the spruce budworm (Choristoneura fumiferana) cryptic species complex (Lepidoptera: Tortricidae). Systematic Entomology, 35, 416–428. https://doi.org/10.1111/j.1365-3113.2009.00514.x
Maddock, S. T., Briscoe, A. G., Wilkinson, M., Waeschenbach, A., San Mauro, D., Day, J. J. et al. (2016). Next-generation mitogenomics: a comparison of approaches applied to caecilian amphibian phylogeny. Plos One, 11, e0156757. https://doi.org/10.1371/journal.pone.0156757
Minh, B. Q., Schmidt, H. A., Chernomor, O., Schrempf, D., Woodhams, M. D., Von Haeseler, A. et al. (2020). IQ-TREE 2: new models and efficient methods for phylogenetic inference in the genomic era. Molecular Biology and Evolution, 37, 1530–1534. https://doi.org/10.1093/molbev/msaa015
Molak, M., & Ho, S. Y. (2015). Prolonged decay of molecular rate estimates for metazoan mitochondrial DNA. PeerJ, 3, e821. https://doi.org/10.7717/peerj.821
Nee, S., May, R. M., & Harvey, P. H. (1994). The reconstructed evolutionary process. Philosophical Transactions of the Royal Society of London Series B: Biological Sciences, 344, 305–311. https://doi.org/10.1098/rstb.1994.0068
Papadopoulou, A., Anastasiou, I., & Vogler, A. P. (2010). Revisiting the insect mitochondrial molecular clock: the mid-Aegean trench calibration. Molecular Biology and Evolution, 27, 1659–1672. https://doi.org/10.1093/molbev/msq051
Saitou, N., & Nei, M. (1987). The neighbor-joining method: a new method for reconstructing phylogenetic trees. Molecular Biology and Evolution, 4, 406–425. https://doi.org/10.1093/oxfordjournals.molbev.a040454
Sheffield, N. C., Hiatt, K. D., Valentine, M. C., Song, H., & Whiting, M. F. (2010). Mitochondrial genomics in Orthoptera using MOSAS. Mitochondrial DNA, 21, 87–104. https://doi.org/10.3109/19401736.2010.500812
Song, H., Amédégnato, C., Cigliano, M. M., Desutter-Gandcolas, L., Heads, S. W., Huang, Y. et al. (2015). 300 million years of diversification: elucidating the patterns of orthopteran evolution based on comprehensive taxon and gene sampling. Cladistics, 31, 621–651. https://doi.org/10.1111/cla.12116
Song, H., Moulton, M. J., & Whiting, M. F. (2014). Rampant nuclear insertion of mtDNA across diverse lineages within Orthoptera (Insecta). Plos One, 9, e110508. https://doi.org/10.1371/journal.pone.0110508
Swofford, D. L. (2002). PAUP*. Phylogenetic Analysis Using Parsimony (*and other Methods). Version 4. Sinauer Associates, Sunderland, Mass.
Vandergast, A. G., Weissman, D. B., Wood, D. A., Rentz, D. C., Bazelet, C. S., & Ueshima, N. (2017). Tackling an intractable problem: Can greater taxon sampling help resolve relationships within the Stenopelmatoidea (Orthoptera: Ensifera)? Zootaxa, 4291, 1–33. https://doi.org/10.11646/zootaxa.4291.1.1
Weissman, D. B. (2001). North and Central American Jerusalem crickets (Orthoptera: Stenopelmatidae): taxonomy, distribution, life cycle, ecology and related biology of the American species. In H. Laurence (Ed.), The biology of wetas, king crickets and their allies (pp. 57–72). New York: CAB International. https://doi.org/10.1079/9780851994086.0057
Weissman, D. B. (2005). Jerusalem! cricket? (Orthoptera: Stenopelmatidae: Stenopelmatus); origins of a common name. American Entomology, 51, 138–139. https://doi.org/10.1093/ae/51.3.138
Weissman, D. B., Vandergast, A. G., Song, H., Shin, S., McKenna, D. D., & Ueshima, N. (2021). Generic relationships of New World Jerusalem crickets (Orthoptera: Stenopelmatoidea: Stenopelmatinae), including all known species of Stenopelmatus. Zootaxa, 4917, 1–122. https://doi.org/10.11646/zootaxa.4917.1.1
