ECR feature: Elizabeth Joyce on floristic exchange tracks

Elizabeth Joyce is a PhD candidate at the Australian Tropical Herbarium & James Cook University. She is an evolutionary biologist interested in the origins of the northern Australian flora. Here, Lizzy shares her recent work on the routes used by plants to disperse between Australia and Southeast Asia.

Elizabeth Joyce during fieldwork to collect Aglaia elaeagnoidea in the Kimberley, north-western Australia.

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Institute. Australian Tropical Herbarium & James Cook University

Academic life stage. PhD Candidate

Major research themes. Broadly, I am interested in how Earth’s biodiversity has come to be the way it is today. My PhD research has focused on understanding the exchange of flora between the Sunda continental shelf (mainland Asia and parts of Indonesia and the Philippines) and Sahul continental shelf (Australia and New Guinea) across Wallacea throughout the Cenozoic. I have been exploring the drivers of the Sunda-Sahul Floristic Exchange and the effect that it has had on the assembly of the flora throughout Southeast Asia and northern Australia.

Close-up of the fruit of Aglaia elaeagnoidea from the Cape York Peninsula, Australia (Photo by John Elliott, reproduced with permission).

Current study system. I love working across scales and lineages to understand evolution, but the bulk of my research focuses on lineages within the order of flowering plants Sapindales. This is an order of nine families and around 6,550 species, including citrus, mahogany, cashew, mango, pistachio, frankincense, myrrh, lychee and maple, as well as many groups important for medicinal compounds. It’s a fascinating group for studying the dynamics of the Sunda-Sahul Floristic Exchange because of its species richness in the tropics, as well as its morphological and ecological diversity.

Recent paper in JBI. Joyce, E.M., Pannell, C.M., Rossetto, M., Yap, J.‐Y.S., Thiele, K.R., Wilson, P.D. and Crayn, D.M. (2021) Molecular phylogeography reveals two geographically and temporally separated floristic exchange tracks between Southeast Asia and northern Australia. Journal Biogeography, 48(5), 1213-1227. https://doi.org/10.1111/jbi.14072

Distribution map of Aglaia elaeagnoidea; the shaded area represents the known distribution of A. elaeagnoidea, and the dots represent the 129 A. elaeagnoidea specimens sampled for this study. The Kimberley and Cape York Peninsula of northern Australia are outlined (Image taken from the article published in Journal of Biogeography).

Motivation behind this paper. When considering the migration of Southeast Asian plant lineages into northern Australia, it was previously assumed that exchange has only occurred between New Guinea and the Cape York Peninsula of north-eastern Australia. However, there is evidence that fauna and humans have also entered Australia from Southeast Asia via north-western Australia (a region called the Kimberley). Additionally, the Kimberley is known to have many plant species in common with Southeast Asia. So we wanted to test: did these plants reach the Kimberley via one exchange track between New Guinea and the Cape York Peninsula prior to spreading across northern Australia, or is there a second floristic exchange track between Southeast Asia and the Kimberley?

Key methodologies. To investigate exchange tracks between Southeast Asia and northern Australia, we conducted a molecular phylogeographic case study on a species of a tropical tree called Aglaia elaeagnoidea (in Meliaceae, the mahogany family), which is distributed from India, throughout Southeast Asia, in the Kimberley and Cape York Peninsula of Australia and out into the Pacific islands. We used Single Nucleotide Polymorphisms (SNPs) obtained using DArT-seq from samples across the range of A. elaeagnoidea and conducted a variety of population genetic analyses. In conjunction with this, we did some Environmental Niche Modelling of the Last Glacial Maximum when sea levels were lowest between Southeast Asia and Australia to understand where suitable tracks of environment for A. elaeagnoidea might have been at that time. A particularly nifty thing about this study is that we obtained most of our samples from herbarium specimens, including a specimen collected by Robert Wight almost 200 years ago!

Dr. Caroline Pannell (the monographer of Aglaia; left) and Elizabeth Joyce (right) looking through the Aglaia collection at Kew Herbarium in 2019 for sampling (Photo by Marija Joyce, reproduced with permission).

Unexpected challenges. An interesting result (although not entirely unexpected) was that Aglaia elaeagnoidea, as currently circumscribed, actually comprises more than one species. We did anticipate this might be an outcome due to the notoriously difficult-to-wrangle morphological variation of Aglaia. We were able to account for the separate species in our sampling thanks to the previous taxonomic work by Dr. Caroline Pannell and previous phylogenetic work on the genus led by Prof. Alexandra Muellner-Riehl. Therefore we were still able to identify the samples relevant to our question of exchange tracks between Southeast Asia and Australia and continue our work. We are currently in the process of writing up the taxonomic implications of this study in a separate paper. We also learned plenty about using herbarium specimens for a phylogeographic study, particularly about which specimens we could and could not retrieve DNA from – lots of lab-work trial and error was involved! We found that the storage conditions of the specimens, as well as the plant collection method, had a huge impact on the quality and quantity of DNA we were able to extract. It was usually impossible to extract useful DNA from specimens that had been stored in tropical conditions for many years or those that had been collected into alcohol. Interestingly, treatment with mercury or gamma irradiation didn’t seem to have as much of an impact and we could often extract DNA from these sheets suitable for DArT-seq. After sampling hundreds of herbarium specimens we were able to pick which herbarium specimens were going to work by eye. The simple, but effective rule of thumb is: the greener the specimen, the better the DNA.

Image of the Aglaia elaeagnoidea specimen collected by Robert Wight in India in 1835 from which we were able to extract DNA and include in this phylogeographic study (Image courtesy of the C. V. Starr Virtual Herbarium of the New York Botanical Garden, http://sweetgum.nybg.org/science/vh/).

Major results. We found that Aglaia elaeagnoidea has two exchange tracks between northern Australia and Southeast Asia: a contemporary track (with ongoing gene flow) between New Guinea and the Cape York Peninsula of north-eastern Australia, and a historical exchange track (with no ongoing gene flow and relatively high genetic differentiation) between Timor-Leste and the Kimberley of north-western Australia. We also found that the climate fluctuations throughout the Quaternary likely induced repeated expansion-contraction cycles in A. elaeagnoidea throughout its range, which is likely to have caused the high degree of genetic structuring that we observed throughout Southeast Asia. These findings support the idea that the Kimberley, Top End and Cape York Peninsula have had independent evolutionary histories, but not just because the biogeographic barriers across northern Australia prevent gene flow between them, but because they have also had separate incursions of Southeast Asian lineages through these exchange tracks. It also emphasizes the complexity of the phylogeography of Southeast Asia, and suggests that movement across the region has been reticulate and iterative with climate fluctuations (especially in the Quaternary). The genetic structuring this leads to might promote speciation and could have contributed to the diversity of the region.

Next steps for this research. This study has raised so many questions! Firstly, the pattern we observed of multiple exchange tracks needs to be tested on other plant lineages, including lineages that are also present in the Top End (Northern Territory) of Australia to see whether it applies at a floristic scale. Secondly, more work needs to be done to understand fully how these exchange tracks have affected northern Australian phytogeography, and whether there is any signature of this also affecting the phytogeography of southern Australia. Our results support the idea that the Kimberley, Top End and Cape York Peninsula have had independent evolutionary histories, but has there been any relationship between these three northern Australian regions with southern Australia? How often do Southeast Asian lineages get into southern Australia and how do they get there? Investigating the relationship between northern Australian phytogeography and southern Australian phytogeography could give us vital clues for better understanding the timing and nature of the aridification of Australia. Finally, the role of animal dispersers in maintaining the exchange tracks between northern Australia and Southeast Asia – particularly fruit pigeons like the Pied Imperial Pigeon (Ducula bicolor) – also needs to be tested. Fruit pigeons such as these are likely to have played a major role in these exchange tracks – and rainforest phylogeography in the region more generally – yet we know hardly anything about their dispersal ecology!

A pair of Pied Imperial Pigeons, the only known dispersers of Aglaia elaeagnoidea on the Cape York Peninsula (Photo by Elizabeth Joyce).

If you could study any organism on Earth, what would it be? How does anyone answer this question!? I really love comparative studies and think they’re hugely insightful, so studying large groups of organisms like the angiosperm order Sapindales gets me excited and is the focus of my current phylogenomic research. Still, if I had to pick only one organism to study right now, I would switch to ‘the dark side’ of animals and study the Pied Imperial Pigeon. But only for plants’ sake! The influence of these guys as dispersers on the phytogeography and phylogeography of Australian and Southeast Asian rainforests, as well as the Sunda-Sahul Floristic Exchange, is likely to be immense, and we really don’t know enough about them. I would love to study the dispersal ecology of these pigeons and their correlations with plant evolution and biogeography.