Phylogenomics resolves the invasion history of Acacia auriculiformis in Florida

Authors: MCCULLOCH, GRAHAM - University Of Otago; Madeira, Paul; MAKINSON, JEFFREY - Australian Biological Control Laboratory, ARS; DUTOIT, LUDOVIC - University Of Otago; BLAIR, ZIZAH - Former ARS Employee; WALTER, GIMME - University Of Queensland; NAWAZ, MUHAMMAD - University Of Queensland; PURCELL, MATTHEW - Australian Biological Control Laboratory, ARS

Submitted to: Journal of Biogeography
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 7/17/2020
Publication Date: 9/30/2020
Citation: Mcculloch, G., Madeira, P.T., Makinson, J., Dutoit, L., Blair, Z., Walter, G., Nawaz, M., Purcell, M. 2020. Phylogenomics resolves the invasion history of Acacia auriculiformis in Florida. Journal of Biogeography. 48(2):453-464. https://doi.org/10.1111/jbi.14013.
DOI: https://doi.org/10.1111/jbi.14013

Interpretive Summary: Acacia auriculiformis (Earleaf acacia) is a fast-growing tree with a wide but scattered distribution across northern Australia and Papua New Guinea which has become a serious environmental weed in Florida. Land managers would like to help control populations of this tree with biological control. It is generally believed that the most efficacious biocontrol agents can be found at the geographic origin of the weed. We have set out to identify this geographic origin for the Florida populations. We sampled Earleaf Acacia from across its entire native range and from its invasive range in Florida and used Genotyping-by-sequencing (GBS), a powerful next generation sequencing tool with producing many genetic markers called SNPs, to assess population structuring. The results indicated significant differences among samples from Papua New Guinea, the Northern Territory, and north Queensland. Florida samples also formed a distinct grouping but were most closely related to samples from the Northern Territory, Australia. Results indicate the original introductions likely took place in south Florida. The uniqueness of the Florida samples perhaps is a result of descending from agro-forestry plants whose origins were mostly from the Northern Territory. Another contributor to their uniqueness may be a genetic bottleneck, where small population size at introduction limits the diversity of the underlying genes. There is also evidence of genes changing in the Florida population, probably as adaptations to success in a new environment. Finally, in identifying the origins of the Florida population we can geographically direct the search for biological control agents.

Technical Abstract: Acacia auriculiformis is a fast-growing tree with a wide (but disjunct) distribution across northern Australia and Papua New Guinea. It has become a serious environmental weed in Florida, USA. Historical records indicate it was introduced to the state before 1932, but the provenance of the invasive lineage is not known. Here we reconstruct the invasion history of A. auriculiformis in Florida, to help direct the search for potential biological control agents. We sampled A. auriculiformis from across its entire native distribution and its invasive range in Florida and used Genotyping-by-sequencing (GBS) to assess population structuring. Principal component analysis, based on 9,591 SNPs, indicated significant differentiation among samples from Papua New Guinea, the Northern Territory, and north Queensland. Florida samples also formed a distinct cluster, with these samples most closely related to samples from the Northern Territory, as well as a single sample from Townsville (north Queensland). The Florida population is not structured geographically, although genetic diversity was notably higher in Miami, indicating the original introductions possibly took place in south Florida. Our results indicate the Florida A. auriculiformis lineage most likely originates from the Northern Territory. Nevertheless, the Florida lineage has a unique genetic make-up not found in the native range, perhaps as a result of a combination of artificial selection (as the invasive lineage likely originated from agroforestry plants), and genetic drift associated with a population genetic bottleneck. We also found evidence of allelic shifts in the Florida population, suggesting rapid adaptation to environmental conditions may contribute the success of the invasive lineage.