Bottleneck revisited: increased adaptive variation despite reduced overall genetic diversity in a rapidly adapting invader

Abstract

Invasive species often exhibit rapid evolution in their introduced ranges despite the genetic bottlenecks that are thought to accompany the translocation of small numbers of founders; however, some invasions may not fit this "genetic paradox." The invasive cane toad (Rhinella marina) displays high phenotypic variation across its environmentally heterogeneous introduced Australian range. Here, we used three genome-wide datasets to characterize population structure and genetic diversity in invasive toads: RNA-Seq data generated from spleens sampled from the toads native range in French Guiana, the introduced population in Hawaii that was the source of Australian founders, and Australia; RNA-Seq data generated from brains sampled more extensively in Hawaii and Australia; and previously published RADSeq data from transects across Australia. We found that toads form three genetic clusters: (1) native range toads, (2) toads from the source population in Hawaii and long-established areas near introduction sites in Australia, and (3) toads from more recently established northern Australian sites. In addition to strong divergence between native and invasive populations, we find evidence for a reduction in genetic diversity after introduction. However, we do not see this reduction in loci putatively under selection, suggesting that genetic diversity may have been maintained at ecologically relevant traits, or that mutation rates were high enough to maintain adaptive potential. Nonetheless, cane toads encounter novel environmental challenges in Australia and appear to respond to selection across environmental breaks; the transition between genetic clusters occurs at a point along the invasion transect where temperature rises and rainfall decreases. We identify loci known to be involved in resistance to heat and dehydration that show evidence of selection in Australian toads. Despite well-known predictions regarding genetic drift and spatial sorting during invasion, this study highlights that natural selection occurs rapidly and plays a vital role in shaping the structure of invasive populations. Author SummaryDespite longstanding evidence for the link between genetic diversity and population viability, the "genetic paradox" concept reflects the observation that invasive populations are successful in novel environments despite a putative reduction in genetic diversity. However, some recent studies have suggested that successful invasions may often occur due to an absence of obstacles such as genetic diversity loss or novel adaptive challenges. The recent emergence of genome-wide technologies provides us with the tools to study this question comprehensively by assessing both overall genetic diversity, and diversity of loci that underlie ecologically relevant traits. The invasive cane toad is a useful model because there is abundant phenotypic evidence of rapid adaptation during invasion. Our results suggest strong genetic divergence between native and invasive populations, and a reduction in overall genetic diversity; however, we do not see this reduction when solely assessing ecologically relevant loci. This could be for reasons that support or refute the genetic paradox. Further studies may provide perspectives from other systems, allowing us to explore how variables such as propagule size affect the fit of an invasion to the model of the paradox. Studying invasive species remains important due to their largely negative impacts on the environment and economy.