Landscape genomics and species range limit evolution of the invasive cane toad (Rhinella marina) in Australia

The cane toad (Rhinella [Bufo] marina) is one of only three amphibians to be named one of the top 100 world's worst invasive species by the International Union for Conservation of Nature. This large, Neotropical toad has been introduced and become invasive in over 40 countries in tropical and subtropical ecosystems around the world. The largest and arguably most damaging invasion site is in Australia. Originally introduced in 1935 as a biocontrol agent to control sugar cane beetle pests, the toad has since expanded its Australian range across nearly 20% of the continent's landmass. It is still expanding its range in northwest Australia, while range edges in eastern and southern Australia are relatively stable. Species invasions, although unfortunate, provide unique opportunities to study the evolutionary and ecological causes for species' geographic range limits. This field has had an abundance of theoretical development over the last few decades, but fewer empirical studies. Understanding species' range limits in natural systems has become an urgent priority because global warming, exotic species invasions, and habitat alteration are currently changing the distributions of many species around the world. We used the cane toad invasion of Australia as a model system to study the ecological and evolutionary causes for species' geographic range limits in a landscape genomics framework. Using next generation sequencing we developed approximately 28,000 genomic markers (single nucleotide polymorphisms) for population and landscape genomic analyses. We first investigated general patterns of genomic diversity and differentiation across the cane toad's Australian range in the context of species' range limits. We found that the 'central marginal hypothesis' for species' range limits is supported. We then used genetic differentiation outliers and genotype environment association analyses to detect genomic regions under selection. We found strong evidence for rapid evolution at the expanding invasion front, at even higher levels than stable range edges in eastern and southern Australia. Finally, we performed a common garden laboratory experiment and found phenotypic evidence of local adaptation to breeding pond temperatures at an arid inland edge, but not at a cold southern edge, of the cane toad's Australian range.