Abstract
We present the first comprehensive molecular phylogeny of Gryllus field cricket species found in the United States and Canada, select additional named Gryllus species found in Mexico and the Bahamas, plus the European field cricket G. campestris Linnaeus and the Afro-Eurasian cricket G. bimaculatus De Geer. Acheta, Teleogryllus, and Nigrogryllus were used as outgroups. Anchored hybrid enrichment was used to generate 492,531 base pairs of DNA sequence from 563 loci. RAxML analysis of concatenated sequence data and Astral analysis of gene trees gave broadly congruent results, especially for older branches and overall tree structure. The North American Gryllus are monophyletic with respect to the two Old World taxa; certain sub-groups show rapid recent divergence. This is the first Anchored Hybrid Enrichment study of an insect group done for closely related species within a single genus, and the results illustrate the challenges of reconstructing the evolutionary history of young rapidly diverged taxa when both incomplete lineage sorting and probable hybridization are at play. Because Gryllus field crickets have been used extensively as a model system in evolutionary ecology, behavior, neuro-physiology, speciation, and life-history and life-cycle evolution, these results will help inform, interpret, and guide future research in these areas.
References
Alexander, R.D. (1968) Life cycle origins, speciation, and related phenomena in crickets. Quarterly Review of Biology, 43, 1–41.
https://doi.org/10.1086/405628
Alexander, R.D. & Bigelow, R.S. (1960) Allochronic speciation in field crickets, and a new species, Acheta veletis. Evolution, 14, 334–346.
https://doi.org/10.1111/j.1558-5646.1960.tb03095.x
Berdan, E.L., Blankers, T., Waurick, I., Mazzoni, C.J. & Mayer, F. (2016) A genes eye view of ontogeny: de novo assembly and profiling of the Gryllus rubens transcriptome. Molecular Ecology Resources, 16 (6), 1478–1490.
https://doi.org/10.1111/1755-0998.12530
Blankers, T., Hennig, R.M. & Gray, D.A. (2015) Conservation of multivariate female preference functions and preference mechanisms in three species of trilling field crickets. Journal of Evolutionary Biology, 28, 630–641.
https://doi.org/10.1111/jeb.12599
Blankers, T., Gray, D.A. & Hennig, R.M. (2017) Multivariate phenotypic evolution: Divergent acoustic signals and sexual selection in Gryllus field crickets. Evolutionary Biology, 44, 43–55.
https://doi.org/10.1007/s11692-016-9388-1
Blankers, T., Vilaça, S.T., Waurick, I., Gray, D.A., Hennig, R.M., Mazzoni, C.J., Mayer, F. & Berdan, E.L. (2018) Demography and selection shape transcriptomic divergence in field crickets. Evolution, 72, 553–567.
https://doi.org/10.1101/193839
Bouckaert, R., Heled, J., Kühnert, D., Vaughan, T., Wu, C.-H., Xie, D., Suchard, M.A., Rambaut, A. & Drummond, A.J. (2014) BEAST 2: A software platform for Bayesian evolutionary analysis A. Prlic (Ed). PLoS Computational Biology, 10, e1003537.
https://doi.org/10.1371/journal.pcbi.1003537
Cade, W.H. & Otte, D. (2000) Gryllus texensis n. sp.: a widely studied field cricket (Orthoptera; Gryllidae) from the southern United States. Transactions of the American Entomological Society (1890-), 126 (1), 117–123.
Crone, E.J., Zera, A.J., Anand, A.N., Oakeshott, J.G., Sutherland, T.D., Russell, R.J., Harshman, L.G., Hoffmann F.G. & Claudianos, C. (2007) Jhe in Gryllus assimilis: cloning, sequence-activity associations and phylogeny. Insect Biochemistry and Molecular Biology, 37, 1359–1365.
https://doi.org/10.1016/j.ibmb.2007.08.005
Desutter-Grandcolas, L. & Robillard, T. (2003) Phylogeny and the evolution of calling songs in Gryllus (Insecta, Orthoptera, Gryllidae). Zoologica Scripta, 32, 173–183.
https://doi.org/10.1046/j.1463-6409.2003.00107.x
Drummond, A.J. & Bouckaert, R.R. (2014) Bayesian evolutionary analysis with BEAST 2. Cambridge University Press, Cambridge, 260 pp.
https://doi.org/10.1017/CBO9781139095112
Dunbar, N.W. (1999) Cosmogenic 36Cl-determined age of the Carrizozo lava flows, south-central New Mexico. New Mexico Geology, 21, 25–29.
Durand, E.Y., Patterson, N., Reich, D. & Slatkin, M. (2011). Testing for ancient admixture between closely related populations. Molecular Biology and Evolution, 28 (8), 2239–2252.
https://doi.org/10.1093/molbev/msr048
Gray, D.A. (2005) Does courtship behavior contribute to species-level reproductive isolation in field crickets? Behavioral Ecology, 16 (1), 201–206.
https://doi.org/10.1093/beheco/arh144
Gray, D.A. & Cade, W.H. (2000) Sexual selection and speciation in field crickets. Proceedings National Academy of Sciences U S A, 97, 14449–14454.
https://doi.org/10.1073/pnas.97.26.14449
Gray, D.A., Gabel, E., Blankers, T. & Hennig, R.M. (2016a) Multivariate female preference tests reveal latent perceptual biases. Proceedings Royal Society, B, 283 (1842). [published online]
https://doi.org/10.1098/rspb.2016.1972
Gray, D.A., Gutierrez, N.J., Chen, T.L., Gonzalez, C., Weissman, D.B. & Cole, J.A. (2016b) Species divergence in field crickets: genetics, song, ecomorphology, and pre- and postzygotic isolation. Biological Journal of the Linnaean Society, 117, 192–205.
https://doi.org/10.1111/bij.12668
Gray, D.A., Weissman, D.B., Cole, J.A., Lemmon, E.M. & Lemmon, A.R. (2019) Multilocus phylogeny of Gryllus field crickets (Orthoptera: Gryllidae: Gryllinae) utilizing anchored hybrid enrichment. Dryad, Dataset. [in press]
Gonzalez-Garcia, J.J., Prawirodirdjo, L., Bock, Y. & Agnew, D. (2003) Guadalupe Island, Mexico as a new constraint for Pacific plate motion. Geophysical Research Letters, 30 (16), 1872.
https://doi.org/10.1029/2003GL017732
Gorochov, A.V. (2019) Preliminary hypothesis on the history of Gryllinae (Orthoptera: Gryllidae) in America and new taxa of both the subtribe Anurogryllina and the genus Megalogryllus. Amurian Zoological Journal, 11 (4), 279–308.
https://doi.org/10.33910/2686-9519-2019-11-4-279-308
Haddad S., Shin, S., Lemmon, A.R., Lemmon, E.M., Svacha, P., Farrell, B., Sìlipinìski, A., Windsor, D. & McKenna, D.D. (2018) Anchored hybrid enrichment provides new insights into the phylogeny and evolution of longhorned beetles (Cerambycidae). Systematic Entomology, 43, 68–89.
https://doi.org/10.1111/syen.12257
Hamilton, C.A., Lemmon, A.R., Moriarty Lemmon, E. & Bond, J.E. (2016) Expanding Anchored Hybrid Enrichment to resolve both deep and shallow relationships within the spider Tree of Life. BMC Evolutionary Biology, 16 (1), 212
https://doi.org/10.1186/s12862-016-0769-y
Harrison, R.G. (1983) Barriers to gene exchange between closely related cricket species. I. Laboratory hybridization studies. Evolution, 37, 245–251.
https://doi.org/10.1111/j.1558-5646.1983.tb05534.x
Harrison, R.G. (1985) Barriers to gene exchange between closely related cricket species. II. Life cycle variation and temporal isolation. Evolution, 39, 244–259.
https://doi.org/10.2307/2408360
Harrison, R.G. & Bogdanowicz, S.M. (1995) Mitochondrial DNA phylogeny of North American field crickets: perspectives on the evolution of life cycles, songs, and habitat associations. Journal of Evolutionary Biology, 8, 209–232.
https://doi.org/10.1046/j.1420-9101.1995.8020209.x
Huang, Y., Ortí, G., Sutherlin, M., Duhachek, A. & Zera, A. (2000) Phylogenetic relationships of North American field crickets inferred from mitochondrial DNA data. Molecular Phylogenetics and Evolution, 17, 48–57.
https://doi.org/10.1006/mpev.2000.0815
Izzo, A.S. & Gray, D.A. (2011) Heterospecific courtship and sequential mate choice in sister species of field crickets. Animal Behaviour, 81 (1), 259–264.
https://doi.org/10.1016/j.anbehav.2010.10.015
Jang, Y., Gerhardt, H.C. & Choe, J.C. (2008) A comparative study of aggressiveness in eastern North American field cricket species (genus Gryllus). Behavioral Ecology and Sociobiology, 62, 1397–1407.
https://doi.org/10.1007/s00265-008-0568-6
Jang, Y., Won, Y.-J. & Choe, J.C. (2009) Convergent and divergent patterns of morphological differentiation provide more evidence for reproductive character displacement in a wood cricket Gryllus fultoni (Orthoptera: Gryllidae). BMC Evolutionary Biology, 9, 27.
https://doi.org/10.1186/1471-2148-9-27
Katoh, K. & Standley, D.M. (2013) MAFFT multiple sequence alignment software version 7: improvements in performance and usability. Molecular Biology and Evolution, 30 (4), 772–780.
https://doi.org/10.1093/molbev/mst010
Kearse, M., Moir, R., Wilson, A., Stones-Havas, S., Cheung, M., Sturrock, S., Buxton, S., Cooper, A., Markowitz, S., Duran, C., Thierer, T., Ashton, B., Meintjes, P. & Drummond, A. (2012) Geneious Basic: an integrated and extendable desktop software platform for the organization and analysis of sequence data. Bioinformatics, 28 (12), 1647–1649.
https://doi.org/10.1093/bioinformatics/bts199
Lanfear, R., Calcott, B., Ho, S.Y.W. & Guindon, S. (2012) PartitionFinder: combined selection of partitioning schemes and substitution models for phylogenetic analyses. Molecular Biology and Evolution, 29, 1695–1701.
https://doi.org/10.1093/molbev/mss020
Lanfear, R., Frandsen, P.B., Wright, A.M., Senfeld, T. & Calcott, B. (2016) PartitionFinder2: new methods for selecting partitioned models of evolution for molecular and morphological phylogenetic analysis. Molecular Biology and Evolution, 34, 772–773.
https://doi.org/10.1093/molbev/msw260
Larson, E.L., Hume, G.L., Andrés, J.A. & Harrison, R.G. (2012) Post-mating prezygotic barriers to gene exchange between hybridizing field crickets. Journal of Evolutionary Biology, 25 (1), 174–186.
https://doi.org/10.1111/j.1420-9101.2011.02415.x
Larson, E.L., Becker, C.G., Bondra, E.R. & Harrison, R.G. (2013) Structure of a mosaic hybrid zone between the field crickets Gryllus firmus and G. pennsylvanicus. Ecology and Evolution, 3 (4), 985–1002.
https://doi.org/10.1002/ece3.514
Larson, E.L., White, T.A., Ross, C.L. & Harrison, R.G. (2014) Gene flow and the maintenance of species boundaries. Molecular Ecology, 23 (7), 1668–1678.
https://doi.org/10.1111/mec.12601
Lemmon, A.R. & Lemmon, E.M. (2012) High-throughput identification of informative nuclear loci for shallow-scale phylogenetics and phylogeography. Systematic Biology, 61, 745–761.
https://doi.org/10.1093/sysbio/sys051
Lemmon, E.M. & Lemmon, A.R. (2013) High-throughput genomic data in systematics and phylogenetics. Annual Review of Ecology, Evolution, and Systematics, 44, 99–121.
https://doi.org/10.1146/annurev-ecolsys-110512-135822
Lemmon, A.R., Emme, S.A. & Lemmon, E.M. (2012) Anchored hybrid enrichment for massively high-throughput phylogenomics. Systematic Biology, 61, 727–744.
https://doi.org/10.1093/sysbio/sys049
Letunic, I. & Bork, P. (2016) Interactive tree of life (iTOL) v3: an online tool for the display and annotation of phylogenetic and other trees. Nucleic Acids Research, 44, W242–W245.
https://doi.org/10.1093/nar/gkw290
Maroja, L.S., Andrés, J.A. & Harrison, R.G. (2009) Genealogical discordance and patterns of introgression and selection across a cricket hybrid zone. Evolution, 63, 2999–3015.
https://doi.org/10.1111/j.1558-5646.2009.00767.x
Maroja, L.S., Larson, E.L., Bogdanowicz, S.M. & Harrison, R.G. (2015) Genes with restricted introgression in a field cricket (Gryllus firmus/Gryllus pennsylvanicus) hybrid zone are concentrated on the X chromosome and a single autosome. G3: Genes, Genomes, Genetics, 5 (11), 2219–2227.
https://doi.org/10.1534/g3.115.021246
Mendelson, T.C. & Shaw, K.L. (2005). Rapid speciation in an arthropod. Nature, 433 (7024), 375–376.
https://doi.org/10.1038/433375a
Miller, M., Pfeiffer, W. & Schwartz, T. (2010) Creating the CIPRES Science Gateway for inference of large phylogenetic trees. In: Gateway Computing Environments Workshop (GCE), 2010. IEEE, New Orleans, Louisiana, pp. 1–8.
Mirarab, S. & Warnow, T. (2015) ASTRAL-II: coalescent-based species tree estimation with many hundreds of taxa and thousands of genes. Bioinformatics, 31 (12), i44–i52.
https://doi.org/10.1093/bioinformatics/btv234
Misof, B., Liu, S., Meusemann, K., Peters, R.S., Donath, A., Mayer, C., Frandsen, P.B., Ware, J., Flouri, T., Beutel, R.G., Niehuis, O., Petersen, M., Izquierdo-Carrasco, F., Wappler, T., Rust, J., Aberer, A.J., Aspöck, U., Aspöck, H., Bartel, D., Blanke, A., Berger, S., Böhm, A., Buckley, T.R., Calcott, B., Chen, J., Friedrich, F., Fukui, M., Fujita, M., Greve, C., Grobe, P., Gu, S., Huang, Y., Jermiin, L.S., Kawahara, A.Y., Krogmann, L., Kubiak, M., Lanfear, R., Letsch, H., Li, Y., Li, Z., Li, J., Lu, H., Machida, R., Mashimo, Y., Kapli, P., McKenna, D.D., Meng, G., Nakagaki, Y., Navarrete-Heredia, J.L., Ott, M., Ou, Y., Pass, G., Podsiadlowski, L., Pohl, H., Von Reumont, B.M., Schütte, K., Sekiya, K., Shimizu, S., Slipinski, A., Stamatakis, A., Song, W., Su, X., Szucsich, N.U., Tan, M., Tan, X., Tang, M., Tang, J., Timelthaler, G., Tomizuka, S., Trautwein, M., Tong, X., Uchifune, T., Walzl, M.G., Wiegmann, B.M., Wilbrandt, J., Wipfler, B., Wong, T.K.F., Wu, Q., Wu, G., Xie, Y., Yang, S., Yang, Q., Yeates, D.K., Yoshizawa, K., Zhang, Q., Zhang, R., Zhang, W., Zhang, Y., Zhao, J., Zhou, C., Zhou, L., Ziesmann, T., Zou, S., Li, Y., Xu, X., Zhang, Y., Yang, H., Wang, J., Wang, J., Kjer, K.M. & Zhou, X. (2014) Phylogenomics resolves the timing and pattern of insect evolution. Science, 346 (6210), 763–767.
https://doi.org/10.1126/science.1257570
Prum, R.O., Berv, J.S., Dornburg, A., Field, D.J., Townsend, J.P., Lemmon, E.M. & Lemmon, A.R. (2015) A fully resolved, comprehensive phylogeny of birds (Aves) using targeted next generation DNA sequencing. Nature, 526, 569–573.
https://doi.org/10.1038/nature15697
Rambaut, A. (2009) FigTree. Version 1.3.1. Available from: http://tree.bio.ed.ac.uk/software/figtree/ (accessed 12 January 2020)
Rambaut, A. & Drummond, A.J. (2013) Tracer. Version 1.6. Available from: http://tree.bio.ed.ac.uk.software/tracer/ (accessed 12 January 2020)
Rambaut, A. & Drummond, A.J. (2014) TreeAnnotator v. 2.1.2. Available from: https://code.google.com/p/beast-mcmc/ (accessed 12 January 2020)
Rehn, J.A.G. & Hebard, M. (1915) The genus Gryllus (Orthoptera) as found in America. Proceedings of the Academy of Natural Sciences Philadelphia, 67, 293–322.
Rokyta, D.R., Lemmon, A.R., Margres, M.J. & Arnow, K. (2012) The venom-gland transcriptome of the eastern diamondback rattlesnake (Crotalus adamanteus). BMC Genomics, 13, 312.
https://doi.org/10.1186/1471-2164-13-312
Scudder, S.H. (1901) The species of Gryllus on the Pacific coast. Psyche, 9, 267–270.
https://doi.org/10.1155/1901/239671
Scudder, S.H. (1902) The species of Gryllus found in the United States east of the Sierra Nevadas. Psyche, 9, 291–296.
https://doi.org/10.1155/1902/35962
Stamatakis, A. (2006) RAxML-VI-HPC: maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models. Bioinformatics, 22 (21), 2688–2690.
https://doi.org/10.1093/bioinformatics/btl446
Veen, T., Faulks, J., Tyler, F., Lloyd, J. & Tregenza, T. (2013) Diverse reproductive barriers in hybridising crickets suggests extensive variation in the evolution and maintenance of isolation. Evolutionary Ecology, 27, 993–1015.
https://doi.org/10.1007/s10682-012-9610-2
Weissman, D.B. & Gray, D.A. (2019) Crickets of the genus Gryllus in the United States (Orthoptera: Gryllidae: Gryllinae). Zootaxa, 4705 (1), 001–277.
https://doi.org/10.11646/zootaxa.4705.1.1
Weissman, D.B., Walker, T.J. & Gray, D.A. (2009) The Jamaican field cricket Gryllus assimilis and two new sister species (Orthoptera: Gryllidae). Annals of the Entomological Society of America, 102, 367–380.
https://doi.org/10.1603/008.102.0304