Long-term biogeographical processes dominate patterns of genetic diversity in a wingless grasshopper despite substantial recent habitat fragmentation.
SNP markers
biodiversity
biogeography
invertebrate
population structure
Journal
Molecular ecology
ISSN: 1365-294X
Titre abrégé: Mol Ecol
Pays: England
ID NLM: 9214478
Informations de publication
Date de publication:
06 2023
06 2023
Historique:
revised:
26
02
2023
received:
15
12
2022
accepted:
08
03
2023
medline:
7
6
2023
pubmed:
19
3
2023
entrez:
18
3
2023
Statut:
ppublish
Résumé
Low-vagility species may hold strong genetic signatures of past biogeographical processes but are also vulnerable to habitat loss. Flightless grasshoppers of the morabine group were once widespread in southeastern Australia, including Tasmania, but are becoming restricted to remnant patches of vegetation, with local ranges impacted by agriculture and development as well as management. Habitat fragmentation can generate genetically differentiated "island" populations with low genetic variation. However, following revegetation, populations could be re-established, and gene flow increased. Here we characterize single nucleotide polymorphism-based genetic variation in a widespread chromosomal race of the morabine Vandiemenella viatica (race 19) to investigate the genetic health of remnant populations and to provide guidelines for restoration efforts. We update the distribution of this race to new sites in Victoria and Tasmania, and show that V. viatica populations from northern Tasmania and eastern Victoria have reduced genetic variation compared to other mainland populations. In contrast, there was no effect of habitat fragment size on genetic variation. Tasmanian V. viatica populations fell into two groups, one connected genetically to eastern Victoria and the other connected to southwestern Victoria. Mainland populations showed isolation by distance. These patterns are consistent with expectations from past biogeographical processes rather than local recent population fragmentation and emphasize the importance of small local reserves in preserving genetic variation. The study highlights how genomic analyses can combine information on genetic variability and population structure to identify biogeographical patterns within a species, which in turn can inform decisions on potential source populations for translocations.
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
3150-3164Informations de copyright
© 2023 The Authors. Molecular Ecology published by John Wiley & Sons Ltd.
Références
Adeleye, M. A., Haberle, S. G., McWethy, D., Connor, S. E., & Stevenson, J. (2021). Environmental change during the last glacial on an ancient land bridge of Southeast Australia. Journal of Biogeography, 48(11), 2946-2960.
Baur, B., Coray, A., Lenzin, H., & Schmera, D. (2020). Factors contributing to the decline of an endangered flightless longhorn beetle: A 20-year study. Insect Conservation and Diversity, 13(2), 175-186.
Black, S. H., & Vaughan, M. (2009). Endangered insects. In Encyclopedia of insects (pp. 320-324). Elsevier.
Catchen, J., Hohenlohe, P. A., Bassham, S., Amores, A., & Cresko, W. A. (2013). Stacks: An analysis tool set for population genomics. Molecular Ecology, 22(11), 3124-3140.
Chessel, D., Dufour, A. B., & Thioulouse, J. (2004). The ade4 package-I-one-table methods. R News, 4(1), 5-10.
Danecek, P., Auton, A., Abecasis, G., Albers, C. A., Banks, E., DePristo, M. A., Handsaker, R. E., Lunter, G., Marth, G. T., Sherry, S. T., McVean, G., Durbin, R., & 1000 Genomes Project Analysis Group. (2011). The variant call format and VCFtools. Bioinformatics, 27(15), 2156-2158.
Day, M. F. C., & Rentz, D. C. F. (2004). Kenneth Hedley Lewis Key 1911-2002. Historical Records of Australian Science, 15, 65-76.
Decker, P. (2016). Phylogenetic analysis of the Australian trans-Bass Strait millipede genus Pogonosternum (Carl, 1912)(Diplopoda, Polydesmida, Paradoxosomatidae) indicates multiple glacial refugia in southeastern Australia. ZooKeys, 578, 15-31.
Dray, S., & Dufour, A.-B. (2007). The ade4 package: Implementing the duality diagram for ecologists. Journal of Statistical Software, 22, 1-20.
Fick, S. E., & Hijmans, R. J. (2017). WorldClim 2: New 1-km spatial resolution climate surfaces for global land areas. International Journal of Climatology, 37(12), 4302-4315.
Georges, A., Gruber, B., Pauly, G. B., White, D., Adams, M., Young, M. J., & Unmack, P. J. (2018). Genomewide SNP markers breathe new life into phylogeography and species delimitation for the problematic short-necked turtles (Chelidae: Emydura) of Eastern Australia. Molecular Ecology, 27(24), 5195-5213.
Hafernik, J. E. (1992). Threats to invertebrate biodiversity: Implications for conservation strategies. In Conservation biology (pp. 171-195). Routledge, Chapman & Hall.
Hallmann, C. A., Sorg, M., Jongejans, E., Siepel, H., Hofland, N., Schwan, H., Stenmans, W., Müller, A., Sumser, H., Hörren, T., Goulson, D., & de Kroon, H. (2017). More than 75 percent decline over 27 years in total flying insect biomass in protected areas. PLoS One, 12(10), e0185809.
Harvey, J. A., Tougeron, K., Gols, R., Heinen, R., Abarca, M., Abram, P. K., Basset, Y., Berg, M., Boggs, C., & Brodeur, J. (2022). Scientists' warning on climate change and insects. Ecological Monographs, 93(1), e1553. https://doi.org/10.1002/ecm.1553
Hijmans, R. J., Williams, E., & Vennes, C. (2019). Geosphere: Spherical trigonometry. R Package Version, 1(10).
Hoffmann, A. A., Miller, A. D., & Weeks, A. R. (2021). Genetic mixing for population management: From genetic rescue to provenancing. Evolutionary Applications, 14(3), 634-652.
Hoffmann, A. A., White, V. L., Jasper, M., Yagui, H., Sinclair, S. J., & Kearney, M. R. (2021). An endangered flightless grasshopper with strong genetic structure maintains population genetic variation despite extensive habitat loss. Ecology and Evolution, 11(10), 5364-5380.
Hugall, A., Moritz, C., Moussalli, A., & Stanisic, J. (2002). Reconciling paleodistribution models and comparative phylogeography in the wet tropics rainforest land snail Gnarosophia bellendenkerensis (brazier 1875). Proceedings of the National Academy of Sciences, 99(9), 6112-6117.
Jombart, T. (2008). Adegenet: A R package for the multivariate analysis of genetic markers. Bioinformatics, 24(11), 1403-1405.
Kawakami, T. (2008). Speciation and chromosomal rearrangements in the Australian Morabine grasshopper Vandiemenella viatica species group. UNSW Sydney.
Kawakami, T., Butlin, R., Adams, M., Saint, K., Paull, D., & Cooper, S. (2007). Differential gene flow of mitochondrial and nuclear DNA markers among chromosomal races of Australian morabine grasshoppers (Vandiemenella, viatica species group). Molecular Ecology, 16(23), 5044-5056.
Kawakami, T., Butlin, R. K., Adams, M., Saint, K. M., Paull, D. J., & Cooper, S. J. B. (2009). Re-examination of a proposed case of stasipatric speciation: Phylogeography of the Australian morabine grasshoppers (Vandiemenella viatica species group). Molecular Ecology, 18, 3429-3442.
Kawakami, T., Butlin, R. K., & Cooper, S. J. (2011). Chromosomal speciation revisited: Modes of diversification in Australian morabine grasshoppers (Vandiemenella, viatica species group). Insects, 2(1), 49-61.
Kearney, M., & Blacket, M. J. (2008). The evolution of sexual and parthenogenetic Warramaba: A window onto Plio-Pleistocene diversification processes in an arid biome. Molecular Ecology, 17, 5257-5275.
Kearney, M., Jasper, M. E., White, V. L., Aitkenhead, I. J., Blacket, M. J., Kong, J. D., Chown, S. L., & Hoffmann, A. A. (2022). Parthenogenesis without costs in a grasshopper with hybrid origins. Science, 376(6597), 1110-1114.
Key, K. (1977). The genera and species of the tribe Morabini (orthoptera: Eumastacidae: Morabinae). Australian Journal of Zoology, 25(3), 499-565.
Kilian, A., Wenzl, P., Huttner, E., Carling, J., Xia, L., Blois, H., Caig, V., Heller-Uszynska, K., Jaccoud, D., Hopper, C., & Aschenbrenner-Kilian, M. (2012). Diversity arrays technology: A generic genome profiling technology on open platforms. In Data production and analysis in population genomics (pp. 67-89). Springer.
Leidner, A. K., & Neel, M. C. (2011). Taxonomic and geographic patterns of decline for threatened and endangered species in the United States. Conservation Biology, 25(4), 716-725.
Linck, E., & Battey, C. J. (2019). Minor allele frequency thresholds strongly affect population structure inference with genomic data sets. Molecular Ecology Resources, 19(3), 639-647.
Lindenmayer, D. B., Northrop-Mackie, A. R., Montague-Drake, R., Crane, M., Michael, D., Okada, S., & Gibbons, P. (2012). Not all kinds of revegetation are created equal: Revegetation type influences bird assemblages in threatened Australian woodland ecosystems. PLoS One, 7(4), e34527. https://doi.org/10.1371/journal.pone.0034527
Lunt, I. D. (1991). Management of remnant lowland grasslands and grassy woodlands for nature conservation: A review. Victorian Naturalist, 108(3), 56-66.
Martin, M. (2011). Cutadapt removes adapter sequences from high-throughput sequencing reads. EMBnet. Journal, 17(1), 10-12.
Mesibov, R. (1994). Faunal breaks in Tasmania and their significance for invertebrate conservation. Memoirs of the Queensland Museum. Brisbane, 36(1), 133-136.
Myburgh, A. M., & Daniels, S. R. (2015). Exploring the impact of habitat size on phylogeographic patterning in the Overberg velvet worm Peripatopsis overbergiensis (Onychophora: Peripatopsidae). Journal of Heredity, 106(3), 296-305.
New, T. R., & Samways, M. J. (2014). Insect conservation in the southern temperate zones: An overview. Austral Entomology, 53(1), 26-31. https://doi.org/10.1111/aen.12071
Palacios-Gimenez, O. M., Koelman, J., Palmada-Flores, M., Bradford, T. M., Jones, K. K., Cooper, S. J., Kawakami, T., & Suh, A. (2020). Comparative analysis of morabine grasshopper genomes reveals highly abundant transposable elements and rapidly proliferating satellite DNA repeats. BMC Biology, 18(1), 1-21.
Paradis, E. (2010). Pegas: An R package for population genetics with an integrated-modular approach. Bioinformatics, 26(3), 419-420.
Rochette, N. C., Rivera-Colón, A. G., & Catchen, J. M. (2019). Stacks 2: Analytical methods for paired-end sequencing improve RADseq-based population genomics. Molecular Ecology, 28(21), 4737-4754.
Rowell, A., & Crawford, I. (1995). A survey of the morabine grasshopper Keyacris scurra (Rehn) in the ACT: CSIRO.
Sánchez-Bayo, F., & Wyckhuys, K. A. (2019). Worldwide decline of the entomofauna: A review of its drivers. Biological Conservation, 232, 8-27.
Sands, D. P. (2018). Important issues facing insect conservation in Australia: Now and into the future. Austral Entomology, 57(2), 150-172.
Schmidt, T. L., Jasper, M. E., Weeks, A. R., & Hoffmann, A. A. (2021). Unbiased population heterozygosity estimates from genome-wide sequence data. Methods in Ecology and Evolution, 12(10), 1888-1898.
Smith, A. B. (2022). enmSdm: Tools for modeling niches and distributions of species. Retrieved from http://github.com/adamlilith/enmSdm
Sunnucks, P., Blacket, M. J., Taylor, J. M., Sands, C. J., Ciavaglia, S. A., Garrick, R. C., Tait, N. N., Rowell, D. M., & Pavlova, A. (2006). A tale of two flatties: Different responses of two terrestrial flatworms to past environmental climatic fluctuations at Tallaganda in montane southeastern Australia. Molecular Ecology, 15(14), 4513-4531.
Tamura, K., Stecher, G., & Kumar, S. (2021). MEGA11: Molecular evolutionary genetics analysis version 11. Molecular Biology and Evolution, 38(7), 3022-3027.
Wang, X., Fang, X., Yang, P., Jiang, X., Jiang, F., Zhao, D., Li, B., Cui, F., Wei, J., Ma, C., & Wang, Y. (2014). The locust genome provides insight into swarm formation and long-distance flight. Nature Communications, 5, 2957.
Weeks, A. R., Stoklosa, J., & Hoffmann, A. A. (2016). Conservation of genetic uniqueness of populations may increase extinction likelihood of endangered species: The case of Australian mammals. Frontiers in Zoology, 13(1), 31.
White, M., Blackith, R., Blackith, R., & Cheney, J. (1967). Cytogenetics of the viatica group morabine grasshoppers. I. the coastal species. Australian Journal of Zoology, 15(2), 263-302. https://doi.org/10.1071/ZO9670263
White, M. J. D. (1956). Adaptive chromosomal-polymorphism in an Australian grasshopper. Evolution, 10(3), 298-313. https://doi.org/10.2307/2406014
White, M. J. D., Carson, H. L., & Cheney, J. (1964). Chromosomal races in the Australian grasshopper Moraba viatica in a zone of geographic overlap. Evolution, 18, 417-429.
Willi, Y., Burskirk, J. V., & Hoffmann, A. A. (2006). Limits to the adaptive potential of small populations. Annual Review of Ecology, Evolution, and Systematics, 37, 433-458.