Invasive species as drivers of evolutionary change: cane toads in tropical Australia

Abstract

The arrival of an invasive species can have wide-ranging ecological impacts on native taxa, inducing rapid evolutionary responses in ways that either reduce the invader's impact or exploit the novel opportunity that it provides. The invasion process itself can cause substantial evolutionary shifts in traits that influence the invader's dispersal rate (via both adaptive and non-adaptive mechanisms) and its ability to establish new populations. I briefly review the nature of evolutionary changes likely to be set in train by a biological invasion, with special emphasis on recent results from my own research group on the invasion of cane toads (Rhinella marina) through tropical Australia. The toads' invasion has caused evolutionary changes both in the toads and in native taxa. Many of those changes are adaptive, but others may result from non-adaptive evolutionary processes: for example, the evolved acceleration in toad dispersal rates may be due to spatial sorting of dispersal-enhancing genes, rather than fitness advantages to faster-dispersing individuals. Managers need to incorporate evolutionary dynamics into their conservation planning, because biological invasions can affect both the rates and the trajectories of evolutionary change.

Keywords: adaptation; alien species; ecological impact; spatial sorting.

Figure 1

A schematic view of evolutionary processes at work during biological invasions. Lines linking two taxa show potential pathways by which selective forces may be exerted by one species upon the other. Invaders may be subject to selection or sorting for more rapid dispersal and also for traits that facilitate population establishment and minimize dispersal-reducing effects of pathogens. Invaders also interact with each other, and with native species, via a network of processes that include competition, predation, pathogen transfer, toxic ingestion, and hybridization. Each species can interact with others either directly or via indirect effects (mediated by perturbations to other links). The end result is that invasion can unleash a complex array of ecological and evolutionary pressures, even in relatively simple (stable, species-poor) systems.

Figure 2

In Australia, cane toads at the invasion front now travel much further per night than was the case early in the toad's invasion process (A); this high dispersal rate puts substantial pressure on the toads’ locomotor apparatus, resulting in spinal arthritis (large bony swellings on posterior spine, indicated by arrow (B). Modified from Alford et al. (2009) and Brown et al. (2007).

Figure 3

Radio-tracking of death adders (Acanthophis praelongus) after cane toad invasion showed that a snake's fate in the wild could be predicted from its behavioral responses to cane toads (Rhinella marina) in laboratory tests: snakes that attempted to eat toads in the laboratory also did so in the field after release and were killed by the toads’ toxins (A). This selective force has resulted in adaptive shifts in prey choice in snake species exposed to cane toads. (B) Geographic comparisons in blacksnakes, Pseudechis porphyriacus, show that snakes from toad-infested areas refuse to consume toads when offered them in captivity, whereas toad-naïve snakes readily attack toads (and thus are likely to be fatally poisoned). Modified from Phillips et al. (2010d) and Phillips and Shine (2006).