Speciation in the mountains: phylogenomics of the alpine grasshopper genus Kosciuscola

A project undertaken at the Western Australian Museum, and supervised by Nikolai Tatarnic

Introduction

Formed over 600 million years, Australia’s alpine landscape exhibits high levels of endemism (e.g. ~25% of Australia’s alpine plants are endemic). Though it is the highest bioregion in Australia, due to its extreme age the Australian Alps have been weathered over millennia, with few peaks exceeding 2000 m. For alpine specialists, these peaks are isolated habitat islands, and in species with low dispersal capability, such as flightless insects, the potential for reproductive isolation and speciation is high. The grasshopper genus Kosciuscola currently includes 5 species, all endemic to the Australian Alps. Our recent research has uncovered a hidden diversity of cryptic species within the genus. Preliminary collecting across the Snowy Mountains have revealed a recurring assemblage of 3-4 Kosciuscola species on multiple peaks, but not necessarily the same species. Though they have historically been considered as such, we believe that multiple suites of species exist across the Alpine region, representing multiple speciation events. This natural replication affords us a unique opportunity to look at broad patterns of speciation mediated by vicariance and climatic specialization, and may help us predict how Alpine communities will respond to continuing climate change.

Background

The grasshopper genus Kosciuscola is unique in many ways. Firstly, K. tristis is the only species known to exhibit temperature-mediated, reversible colour change (Key & Day 1954). Similarly, K. tristis is also the only species of grasshopper to engage in fierce male-male combat (Umbers et al. 2012). And thirdly, the genus is of considerable ecological interest, as all members are restricted to Australia’s Alpine bioregion, with species segregated along an altitudinal gradient. Across their mainland range (K. tasmanicus is restricted to Tasmania), from the peak downwards these species are: K. tristis, K. usitatus, K. cognatus, and K cuneatus, with some sympatry at intermediate elevations. We recently discovered that Kosciuscola harbours multiple cryptic species distributed across the Alps in recurring altitudinally segregated species assemblages, isolated from one another by large, low elevation distances. For example, on Mt Kosciusko we find K. tristis, K. usitatus, K. cognatus, and K cuneatus, while at Mt Buffalo we find a different K. tristis, a different K. cognatus, etc. (Fig. 1). We believe these different assemblages reflect relict populations, which were once contiguous but have since become isolated on alpine habitat islands as the continent warmed and their ranges contracted. We predict that all species within a “species type” will be more closely related to one another than to other species in the genus. We also predict that higher elevation species became isolated first, with lower elevation species and populations showing more recent connectivity. Genomic-level analyses will provide the necessary data for both phylogenetic and population genetic study.

Scientific objectives
  1. Collect fresh specimens from the Kosciuscola assemblage from multiple peaks across the Australian Alpine Region
  2. Using transcriptome-based exon capture, develop custom microarrays to capture target exons from Kosciuscola species
  3. Using genomic data, reconstruct the phylogenetic relationships within Kosciuscola
  4. Estimate divergence times for different species of Kosciuscola and correlate this with the geological history of the Australian Alps
  5. Investigate population genomic structures within Kosciuscola to understand patterns of speciation in relation to altitudinal gradient across mountain ranges
 Key Publications

Badisco, L.., Huybrechts, J., Simonet, G., Verlinden, H., Marchal, E., Huybrechts, R., Schoofs, L., De loof, A., Vanden Broek. J., 2011. Transcriptome analysis of the desert locust central nervous system: Production and annotation of a Schistocerca gregaria EST database. PLoS One 6, e17274.

Bensasson, D., Zhang, D.-X., Hartl, D. L., Hewitt, G. M. 2001. Mitochondrial pseudogenes: evolution's misplaced witnesses. Trends in Ecology and Evolution 16, 314-321.

Bi, K., Vanderpool, D., Singhal, S., Linderoth, T., Moritz, C., Good, J. M. 2012. Transcriptome-based exon capture enables highly cost-effective comparative genomic data collection at moderate evolutionary scales. BMC Genomics 12, 403.

Crabb, P. 2003. Managing the Australian Alps: a history of cooperative management of the Australian Alps national parks, Centre for Resource and Environmental Studies, ANU & the Australian Alps Liaison Committee, Canberra.

Hodges, E., Rooks, M., Xuan, Z., Bhattacharjee, A., Gordon, D. B., Brizuela, L., McCombie, W. R., Hannon, G. J. 2009. Hybrid selection of discrete genomic intervals on custom-designed microarrays for massively parallel sequencing. Nature Protocols 4, 960-974.

Key, K.H.L. & Day, M.F. 1954. A temperature-controlled physiological colour response in the grasshopper Kosciuscola tristis Sjost (Orthoptera: Acrididae). Australian Journal of Zoology, 2, 309-339.

Ma, Z., Yu, J., Kang, L. 2006. LocustDB: a relational database for the transcriptome and biology of the migratory locust (Locusta migratoria). BMC Genomics 7, 11.

Shendure, J., Ji, H. 2008. Next-generation DNA sequencing. Nature Biotechnology 26, 1135-1145.

Tatarnic, N.J., Umbers, K.D.L., and Song, H. 2013. Molecular phylogeny of the Kosciuscola grasshoppers endemic to the Australian alpine and montane regions. Invertebrate Systematics 27, 307-316.

Umbers, K. D. L., Tatarnic, N. J., Holwell, G. I., and Herberstein, M. E. 2012. Ferocious fighting between male grasshoppers. PLoS ONE 7(11): e49600 doi:10.1371/journal.pone.0049600

Figure 1. Males of “Kosciuscola tristis” from three different populations: A) Dead Horse Gap, NSW; B) Mt Baw Baw, Victoria; and C) Mt Buffalo, Victoria.