Cane toads (Bufo marinus) are large anurans (weighing up to 2 kg) that were introduced to Australia 70 years ago to control insect pests in sugar-cane fields. But the result has been disastrous because the toads are toxic and highly invasive. Here we show that the annual rate of progress of the toad invasion front has increased about fivefold since the toads first arrived; we find that toads with longer legs can not only move faster and are the first to arrive in new areas, but also that those at the front have longer legs than toads in older (long-established) populations. The disaster looks set to turn into an ecological nightmare because of the negative effects invasive species can have on native ecosystems; over many generations, rates of invasion will be accelerated owing to rapid adaptive change in the invader, with continual 'spatial selection' at the expanding front favouring traits that increase the toads' dispersal.

In classical evolutionary theory, traits evolve because they facilitate organismal survival and/or reproduction. We discuss a different type of evolutionary mechanism that relies upon differential dispersal. Traits that enhance rates of dispersal inevitably accumulate at expanding range edges, and assortative mating between fast-dispersing individuals at the invasion front results in an evolutionary increase in dispersal rates in successive generations. This cumulative process (which we dub "spatial sorting") generates novel phenotypes that are adept at rapid dispersal, irrespective of how the underlying genes affect an organism's survival or its reproductive success. Although the concept is not original with us, its revolutionary implications for evolutionary theory have been overlooked. A range of biological phenomena (e.g., acceleration of invasion fronts, insular flightlessness, preadaptation) may have evolved via spatial sorting as well as (or rather than) by natural selection, and this evolutionary mechanism warrants further study.colonization | evolution | spatial disequilibrium | nonadaptive evolution I n 1859, Charles Darwin proposed a mechanism to explain the process by which organisms become well matched to local conditions. That mechanism was natural selection (1). At its heart lies the concept of differential lifetime reproductive success (LRS). Significant extensions to the paradigm since Darwin's work-such as multiple levels of selection (2, 3)-all rely upon the basic principle that, through time, some genes leave more copies of themselves than do others (4). Here we describe an additional mechanism whereby traits evolve because genes are differentially successful through space rather than time. This idea is not new; the process was described long ago (5), has been explored in several spatially explicit models of nonequilibrial populations (6-8), and is widely recognized by researchers who work with range-edge dynamics (9). The basis of the idea is that on expanding range edges evolutionary change can arise from differential dispersal rates (spatial sorting) as well as from differential survival or reproductive success. Spatial sorting and classical natural selection both require heritable variation, and both result in deterministic shifts in phenotypic attributes, but the two evolutionary processes rely on fundamentally different mechanisms (spatial filtering versus temporal filtering). Mainstream biology has failed to recognize that evolutionary change can be caused by spatial sorting as well as by conventional natural selection. Spatial SortingImagine a species expanding its range into hitherto unoccupied territory and with a genetic basis to variation among individuals in dispersal rates (6-8). For example, continuously distributed variation may occur in dispersal-relevant morphological traits [e.g., seed shape (5), flight musculature and wing size (7, 10), leg length (11), foot size (12)], behavior [movement patterns (13)], and physiology [locomotor endurance (14)]. Alleles that confer the hi...

Most evolutionary theory does not deal with populations expanding or contracting in space. Invasive species, climate change, epidemics, and the breakdown of dispersal barriers, however, all create populations in this kind of spatial disequilibrium. Importantly, spatial disequilibrium can have important ecological and evolutionary outcomes. During continuous range expansion, for example, populations on the expanding front experience novel evolutionary pressures because frontal populations are assorted by dispersal ability and have a lower density of conspecifics than do core populations. These conditions favor the evolution of traits that increase rates of dispersal and reproduction. Additionally, lowered density on the expanding front eventually frees populations on the expanding edge from specialist, coevolved enemies, permitting higher investment into traits associated with dispersal and reproduction rather than defense against pathogens. As a result, the process of range expansion drives rapid life-history evolution, and this seems to occur despite ongoing serial founder events that have complex effects on genetic diversity at the expanding front. Traits evolving on the expanding edge are smeared across the landscape as the front moves through, leaving an ephemeral signature of range expansion in the life-history traits of a species across its newly colonized range. Recent studies suggest that such nonequilibrium processes during recent population history may have contributed to many patterns usually ascribed to evolutionary forces acting in populations at spatial equilibrium.

Current approaches to modeling range advance assume that the distribution describing dispersal distances in the population (the "dispersal kernel") is a static entity. We argue here that dispersal kernels are in fact highly dynamic during periods of range advance because density effects and spatial assortment by dispersal ability ("spatial selection") drive the evolution of increased dispersal on the expanding front. Using a spatially explicit individual-based model, we demonstrate this effect under a wide variety of population growth rates and dispersal costs. We then test the possibility of an evolved shift in dispersal kernels by measuring dispersal rates in individual cane toads (Bufo marinus) from invasive populations in Australia (historically, toads advanced their range at 10 km/year, but now they achieve >55 km/year in the northern part of their range). Under a common-garden design, we found a steady increase in dispersal tendency with distance from the invasion origin. Dispersal kernels on the invading front were less kurtotic and less skewed than those from origin populations. Thus, toads have increased their rate of range expansion partly through increased dispersal on the expanding front. For accurate long-range forecasts of range advance, we need to take into account the potential for dispersal kernels to be evolutionarily dynamic.

The process of rapid range expansion (as seen in many invasive species, and in taxa responding to climate change) may substantially disrupt host-parasite dynamics. Parasites and pathogens can have strong regulatory effects on their host population and, in doing so, exert selection pressure on host life history. We construct a simple individual-based model of host-parasite dynamics during range expansion. This model shows that the parasites and pathogens of a range-expanding host are likely to be absent from the host's invasion front, because stochastic events (serial founder events) in low-density frontal populations result in local extinctions or transmission failure of the parasite/pathogen and, hence, a preponderance of uninfected hosts in the invasion vanguard. This pattern is true for both density-dependent and density-independent transmission rates, although it is exacerbated in the case of density-dependent transmission because, in this case, transmission rates also decline on the front. Data from field surveys on the prevalence of lungworms (Rhabdias pseudosphaerocephala) in invasive cane toads (Bufo marinus) support these predictions, in showing that toads in newly invaded areas of tropical Australia lack the parasite, which only arrives 1-3 years after the toads themselves. The resultant "honeymoon phase" immediately post-invasion, when individuals in the invasion-front population are virtually pathogen-free, may lead to altered host population dynamics on the invasion front, causing, for example, high densities in invasion-front populations, followed by a decline in numbers as parasites and pathogens arrive and begin to reduce host viability. The honeymoon phase may ultimately impact the evolution of life-history investment strategies in both host and parasite on the invasion vanguard, as hosts are released from immune challenges and parasites continuously expand into a favorable and unoccupied niche.