Molecular phylogeny of the Kosciuscola grasshoppers endemic to the Australian alpine and montane regions
N. J. Tatarnic A B E , K. D. L. Umbers A C E F and H. Song D
+ Author Affiliations
- Author Affiliations
A Department of Biological Sciences, Macquarie University, Sydney, NSW 2109, Australia.
B Evolution & Ecology Research Centre, University of New South Wales, Sydney, NSW 2052, Australia.
C Research School of Biology, Australian National University, Canberra, ACT 0200, Australia.
D Department of Biology, University of Central Florida, Orlando, Florida 32816-2368, USA.
E These authors contributed equally to this study.
F Corresponding author. Email: kate.umbers@mq.edu.au
Invertebrate Systematics 27(3) 307-316 https://doi.org/10.1071/IS12072
Submitted: 13 September 2012 Accepted: 20 March 2013 Published: 25 June 2013
Abstract
Diversity and speciation in Australia’s alpine biota are poorly understood. Here we present a molecular phylogeny of the Australian alpine grasshopper genus Kosciuscola (Sjösted) that currently includes five described species. These grasshoppers are of interest not only because of their alpine distribution but also for the extraordinary colour change exhibited by the species K. tristis, whose males turn turquoise when their body temperature exceeds 25°C. We reconstructed the phylogeny with two fragments of the mitochondrial genome using parsimony, maximum likelihood and Bayesian analyses and our data support the current taxonomy. Further, our data show little geographic structuring within some clades, which is puzzling since members of Kosciuscola are brachypterous. Finally, our data coupled with our observations on colouration provide evidence for a genetically distinct clade of K. tristis in the Victorian Alps. This is among the first molecular studies of an alpine invertebrate and one of a few on non-endangered, widespread Australian alpine species. More phylogenetic studies in the Australian Alps are required if we are to understand the evolution of alpine fauna and establish baseline data to monitor their response to climate change.
References
Baker, C. H., Graham, G. C., Scott, K. D., Cameron, S. L., Yeates, D. K., and Merritt, D. J. (2008). Distribution and phylogenetic relationships of Australian glow-worms Arachnocampa (Diptera, Keroplatidae). Molecular Phylogenetics and Evolution 48, 506–514.| Distribution and phylogenetic relationships of Australian glow-worms Arachnocampa (Diptera, Keroplatidae).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXptVOiurg%3D&md5=2fc02302778ee988ae09f0a96fd5c5b5CAS | 18583158PubMed |
Bensasson, D., Zhang, D.-X., Hartl, D. L., and Hewitt, G. M. (2001). Mitochondrial pseudogenes: evolution’s misplaced witnesses. Trends in Ecology & Evolution 16, 314–321.
| Mitochondrial pseudogenes: evolution’s misplaced witnesses.Crossref | GoogleScholarGoogle Scholar |
Berthold, G. (1980). Microtubules in the epidermal cells of Carausius morosus, their pattern and relation to pigment migration. Journal of Insect Physiology 26, 421–425.
| Microtubules in the epidermal cells of Carausius morosus, their pattern and relation to pigment migration.Crossref | GoogleScholarGoogle Scholar |
Brower, A. V. (1994). Rapid morphological radiation and convergence among races of the butterfly Heliconius erato inferred from patterns of mitochondrial DNA evolution. Proceedings of the National Academy of Sciences of the United States of America 91, 6491–6495.
| Rapid morphological radiation and convergence among races of the butterfly Heliconius erato inferred from patterns of mitochondrial DNA evolution.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2cXmt1KrsLw%3D&md5=3a675438e37adf915de3540209eb32c6CAS | 8022810PubMed |
Campbell, N. A., and Dearn, J. M. (1980). Altitudinal variation in and morphological divergence between three related species of grasshopper Praxibulus sp., Kosciuscola cognatus and Kosciuscola usitatus (Orthoptera: Acrididae). Australian Journal of Zoology 28, 103–118.
| Altitudinal variation in and morphological divergence between three related species of grasshopper Praxibulus sp., Kosciuscola cognatus and Kosciuscola usitatus (Orthoptera: Acrididae).Crossref | GoogleScholarGoogle Scholar |
Chapple, D. G., Keogh, J. S., and Hutchinson, M. N. (2005). Substantial genetic substructuring in southeastern and alpine Australia revealed by molecular phylogeography of the Egernia whitii (Lacertilia: Scincidae) species group. Molecular Ecology 14, 1279–1292.
| Substantial genetic substructuring in southeastern and alpine Australia revealed by molecular phylogeography of the Egernia whitii (Lacertilia: Scincidae) species group.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXktleqs7o%3D&md5=3d1ed674794d88f1e68dded2b44ee13eCAS | 15813770PubMed |
Dubey, S., Keogh, J. S., and Shine, R. (2010). Plio-pleistocene diversification and connectivity between mainland and Tasmanian populations of Australian snakes (Drysdalia, Elapidae, Serpentes). Molecular Phylogenetics and Evolution 56, 1119–1125.
| Plio-pleistocene diversification and connectivity between mainland and Tasmanian populations of Australian snakes (Drysdalia, Elapidae, Serpentes).Crossref | GoogleScholarGoogle Scholar | 20430104PubMed |
Gallagher, S. J., Greenwood, D. R., Taylor, D., Smith, A. J., Wallace, M. W., and Holdgate, G. R. (2003). The Pliocene climatic and environmental evolution of southeastern Australia: Evidence from the marine and terrestrial realm. Palaeogeography, Palaeoclimatology, Palaeoecology 193, 349–382.
| The Pliocene climatic and environmental evolution of southeastern Australia: Evidence from the marine and terrestrial realm.Crossref | GoogleScholarGoogle Scholar |
Green, K., Osborne, M. J. (1994). ‘Wildlife of the Australian Snow-country.’ (Reed Books: Sydney.)
Hennessy, K., Fitzharris, B., Bates, B. C., Harvey, N., Howden, S. M., Hughes, L., Salinger, J., and Warrick R. (2007). Australia and New Zealand. Climate Change 2007: Impacts, Adaptation and Vulnerability. Contribution of Working Group II to the Fourth Assessment Report of the Intergovernmental Panel on Climate Change. (Eds M. L. Parry, O. F. Canziani, J. P. Palutikof, P. J. van der Linden and C. E. Hanson.) pp. 507–540. (Cambridge University Press, Cambridge, UK.)
Ho, S. Y. W., and Lanfear, R. (2012). Mito-communication: callibrating mitochondrial rates in marine invertebrates. Mitochondrial DNA 23, 321.
| Mito-communication: callibrating mitochondrial rates in marine invertebrates.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XpsVSgur8%3D&md5=2e350524f9c9e311a4b8b2173fefe960CAS |
Hollis, D. (1975). A review of the subfamily Oxyniae (Orthoptera: Acridoidea). Bulletin of the British Museum (Natural History) Entomology 31, 189–234.
Huelsenbeck, J. P., and Ronquist, F. (2001). MrBayes: Bayesian inference of phylogenetic trees. Bioinformatics 17, 754–755.
| MrBayes: Bayesian inference of phylogenetic trees.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD3MvotV2isw%3D%3D&md5=05e0e72b0d363640632985f3a1bdf974CAS | 11524383PubMed |
Hutchinson, M. N., and Donnellan, S. C. (1992). Taxonomy and genetic variation in the Australian lizards of the genus Pseudemoia (Scincidae: Lygosominae). Journal of Natural History 26, 215–264.
| Taxonomy and genetic variation in the Australian lizards of the genus Pseudemoia (Scincidae: Lygosominae).Crossref | GoogleScholarGoogle Scholar |
Key, K. H. L. (1970). ‘Orthoptera: Grasshoppers, Locusts and Crickets.’ (CSIRO Publishing: Melbourne.)
Key, K. H. L. (1992). A higher classification of the Australian Acridoidea (Orthoptera). I. General introduction and subfamily Oxyinae. Invertebrate Systematics 6, 547–551.
Key, K. H. L., and Day, M. F. (1954a). The physiological mechanism of colour change in the grasshopper, Kosciuscola tristis Sjöst. (Orthoptera: Acrididae). Australian Journal of Zoology 2, 340–363.
| The physiological mechanism of colour change in the grasshopper, Kosciuscola tristis Sjöst. (Orthoptera: Acrididae).Crossref | GoogleScholarGoogle Scholar |
Key, K. H. L., and Day, M. F. (1954b). A temperature-controlled physiological colour response in the grasshopper, Kosciuscola tristis Sjöst. (Orthoptera: Acrididae). Australian Journal of Zoology 2, 309–339.
| A temperature-controlled physiological colour response in the grasshopper, Kosciuscola tristis Sjöst. (Orthoptera: Acrididae).Crossref | GoogleScholarGoogle Scholar |
Knowles, L. L. (2000). Tests of Pleistocene speciation in montane grasshoppers (genus Melanoplus) from the sky islands of Western North America. Evolution 54, 1337–1348.
| 1:STN:280:DC%2BD3cvltVeitA%3D%3D&md5=8a11c7067a9c0b610834c8d2d2d3c9b3CAS | 11005300PubMed |
Knowles, L. L., and Otte, D. (2000). Phylogenetic analysis of montane grasshoppers from western North America (genus Melanoplus, Acrididae: Melanoplinae). Annals of the Entomological Society of America 93, 421–431.
| Phylogenetic analysis of montane grasshoppers from western North America (genus Melanoplus, Acrididae: Melanoplinae).Crossref | GoogleScholarGoogle Scholar |
Koumoundouros, T., Sumner, J., Clemann, N., and Stuart-Fox, D. (2009). Current genetic isolation and fragmentation contrasts with historical connectivity in an alpine lizard (Cyclodomorphus praealtus) threatened by climate change. Biological Conservation 142, 992–1002.
| Current genetic isolation and fragmentation contrasts with historical connectivity in an alpine lizard (Cyclodomorphus praealtus) threatened by climate change.Crossref | GoogleScholarGoogle Scholar |
Lanfear, R., and Ho, S. Y. W. (2012). Mito-communication: mitochondrial mutation rates in the water flea Daphnia pulex. Mitochodrial DNA 23, 154.
| Mito-communication: mitochondrial mutation rates in the water flea Daphnia pulex.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XkvFSisr4%3D&md5=148448072487b6eb8e367068054d97a9CAS |
Maddison, W. P., and Knowles, L. L. (2006). Inferring phylogeny despite incomplete lineage sorting. Systematic Biology 55, 21–30.
| Inferring phylogeny despite incomplete lineage sorting.Crossref | GoogleScholarGoogle Scholar | 16507521PubMed |
Mitrovski, P., Heinze, D. A., Broome, L., Hoffmann, A. A., and Weeks, A. R. (2007). High levels of variation despite genetic fragmentation in populations of the endangered mountain pygmy-possum, Burramys parvus, in alpine Australia. Molecular Ecology 16, 75–87.
| High levels of variation despite genetic fragmentation in populations of the endangered mountain pygmy-possum, Burramys parvus, in alpine Australia.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXit1Cltb8%3D&md5=cc2d3a647435e9ee2990e27527b92d32CAS | 17181722PubMed |
Morgan, M. J., Hunter, D., Pietsch, R., Osborne, W., and Keogh, J. S. (2008). Assessment of genetic diversity in the critically endangered Australian corroboree frogs, Pseudophryne corroboree and Pseudophryne pengilleyi, identifies four evolutionarily significant units for conservation. Molecular Ecology 17, 3448–3463.
| 19160475PubMed |
Moulton, M. J., Song, H., and Whiting, M. F. (2010). Assessing the effects of primer specificity on eliminating numt coamplification in DNA barcoding: a case study from Orthoptera (Arthropoda: Insecta). Molecular Ecology Resources 10, 615–627.
| Assessing the effects of primer specificity on eliminating numt coamplification in DNA barcoding: a case study from Orthoptera (Arthropoda: Insecta).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXpsFSltrw%3D&md5=45e951af2ef30a1655272f371f8a5688CAS | 21565066PubMed |
O’Farrell, A. F. (1964). On physiological colour change in some Australian Odonata. Journal of the Entomological Society of Australia (New South Wales) 1, 5–12.
Osborne, M. J., Norman, J. A., Christidis, L., and Murray, N. D. (2000). Genetic distinctness of isolated populations of an endangered marsupial, the mountain pygmy-possum, Burramys parvus. Molecular Ecology 9, 609–613.
| Genetic distinctness of isolated populations of an endangered marsupial, the mountain pygmy-possum, Burramys parvus.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD3c3lt12msw%3D%3D&md5=ad7ff33b55c9e26c5fc6ca31ba0be820CAS | 10792703PubMed |
Posada, D. (2008). jModelTest: Phylogenetic model averaging. Molecular Biology and Evolution 25, 1253–1256.
| jModelTest: Phylogenetic model averaging.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXotlKgsb4%3D&md5=8761d5f1a58540f62fc8afb3f3b08888CAS | 18397919PubMed |
Rehn, J. A. G. (1957). ‘The Grasshoppers and Locusts (Acridoidea) of Australia. Family Acrididae: Subfamily Cyrtacanthacrldinae tribes Oxyini. Spathosternini. and Praxibulini.’ (CSIRO: Melbourne.)
Song, H. (2010). Grasshopper systematics: past, present and future. Journal of Orthoptera Research 19, 57–68.
| Grasshopper systematics: past, present and future.Crossref | GoogleScholarGoogle Scholar |
Song, H., Buhay, J. E., Whiting, M. F., and Crandall, K. A. (2008). Many species in one: DNA barcoding overestimates the number of species when nuclear mitochondrial pseudogenes are coamplified. Proceedings of the National Academy of Sciences of the United States of America 105, 13486–13491.
| Many species in one: DNA barcoding overestimates the number of species when nuclear mitochondrial pseudogenes are coamplified.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXhtFChs7vP&md5=616c57ecc032736406f8b1664d3d763cCAS | 18757756PubMed |
Stamatakis, A. (2006). RAxML-VI-HPC: maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models. Bioinformatics 22, 2688–2690.
| 1:CAS:528:DC%2BD28XhtFKlsbfI&md5=b75cb342275b0257cdc9a3a5e1c1c37bCAS | 16928733PubMed |
Sunnucks, P., and Hales, D. F. (1996). Numerous transposed sequences of mitochondrial cytochrome oxidase I–II in aphids of the genus Sitobion (Hemiptera: Aphididae). Molecular Biology and Evolution 13, 510–524.
| Numerous transposed sequences of mitochondrial cytochrome oxidase I–II in aphids of the genus Sitobion (Hemiptera: Aphididae).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK28Xht1Kgurk%3D&md5=5552febd7b53d0c63f77daf2fa5e9ba9CAS | 8742640PubMed |
Swofford, D. L. (2002). PAUP*. Phylogenetic Analysis Using Parsimony (*and Other Methods). Version 4. Sinauer Associates, Sunderland, MA, USA.
Sword, G. A., Senior, L. B., Gaskin, J. F., and Joern, A. (2007). Double trouble for grasshopper molecular systematics: intra-individual heterogeneity of both mitochondrial 12S-valine-16S and nuclear internal transcribed spacer ribosomal DNA sequences in Hesperotettix viridis (Orthoptera: Acridae). Systematic Entomology 32, 420–428.
| Double trouble for grasshopper molecular systematics: intra-individual heterogeneity of both mitochondrial 12S-valine-16S and nuclear internal transcribed spacer ribosomal DNA sequences in Hesperotettix viridis (Orthoptera: Acridae).Crossref | GoogleScholarGoogle Scholar |
Thomas, J. A., Welch, J. J., Woolfit, M., and Bromham, L. (2006). There is no universal molecular clock for invertebrates, but rate variation does not scale with body size. Proceedings of the National Academy of Sciences of the United States of America 103, 7366–7371.
| There is no universal molecular clock for invertebrates, but rate variation does not scale with body size.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XkslOrsL0%3D&md5=48940b16ddf445850488d04f35c00548CAS | 16651532PubMed |
Tichy, H., and Loftus, R. (1987). Response characteristics of a cold receptor in the stick insect Carausius morosus. Journal of Comparative Physiology. A, Neuroethology, Sensory, Neural, and Behavioral Physiology 160, 33–42.
| Response characteristics of a cold receptor in the stick insect Carausius morosus.Crossref | GoogleScholarGoogle Scholar |
Umbers, K. D. L. (2011). Turn the temperature to turquoise: cues for colour change in the male chameleon grasshopper (Kosciuscola tristis) (Orthoptera: Acrididae). Journal of Insect Physiology 57, 1198–1204.
| Turn the temperature to turquoise: cues for colour change in the male chameleon grasshopper (Kosciuscola tristis) (Orthoptera: Acrididae).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXhtFarsrbK&md5=29c3c2184e55376064991d8424d6993fCAS |
Umbers, K. D. L., Dennison, S., Manahan, C. A., Blondin, L., Pagés, C., Risterucci, A.-M., and Chapuis, M.-P. (2012). Microsatellite markers for the chameleon grasshopper (Kosciuscola tristis) (Orthoptera: Acrididae), an Australian alpine specialist. International Journal of Molecular Sciences 13, 12094–12099.
| Microsatellite markers for the chameleon grasshopper (Kosciuscola tristis) (Orthoptera: Acrididae), an Australian alpine specialist.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XhvVaqtbvM&md5=b67406bc05d92b714306dd832516fcf6CAS |
Umbers, K. D. L., Herberstein, M. E., and Madin, J. S. (2013a). Colour in insect thermoregulation: empirical and theoretical tests in the colour-changing grasshopper, Kosciuscola tristis. Journal of Insect Physiology 59, 81–90.
| Colour in insect thermoregulation: empirical and theoretical tests in the colour-changing grasshopper, Kosciuscola tristis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XhslymtL%2FK&md5=323ee18d0a39d77e4ad64fabdf0e93bdCAS |
Umbers, K. D. L., Tatarnic, N. J., Holwell, G. I., and Herberstein, M. E. (2013b). Bright turquoise as an intraspecific signal in the chameleon grasshopper (Kosciuscola tristis). Behavioral Ecology and Sociobiology 67, 439–447.
| Bright turquoise as an intraspecific signal in the chameleon grasshopper (Kosciuscola tristis).Crossref | GoogleScholarGoogle Scholar |
Veron, J. E. N., O’Farrell, A. F., and Dixon, B. (1974). The fine structure of Odonata chromatophores. Tissue & Cell 6, 613–626.
| The fine structure of Odonata chromatophores.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaE2M7ktFCjuw%3D%3D&md5=4243f525ee9e7622a64c744446f57c55CAS |
