Benjamin L. Phillips

An evolutionary process that assembles phenotypes through space rather than through time

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 organisms 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.

Life-history evolution in range-shifting populations

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.

Reid's paradox revisited: the evolution of dispersal kernels during range expansion.

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.

Stability of the wMel Wolbachia Infection following Invasion into Aedes aegypti Populations

The wMel infection of Drosophila melanogaster was successfully transferred into Aedes aegypti mosquitoes where it has the potential to suppress dengue and other arboviruses. The infection was subsequently spread into two natural populations at Yorkeys Knob and Gordonvale near Cairns, Queensland in 2011. Here we report on the stability of the infection following introduction and we characterize factors influencing the ongoing dynamics of the infection in these two populations. While the Wolbachia infection always remained high and near fixation in both locations, there was a persistent low frequency of uninfected mosquitoes. These uninfected mosquitoes showed weak spatial structure at both release sites although there was some clustering around two areas in Gordonvale. Infected females from both locations showed perfect maternal transmission consistent with patterns previously established pre-release in laboratory tests. After >2 years under field conditions, the infection continued to show complete cytoplasmic incompatibility across multiple gonotrophic cycles but persistent deleterious fitness effects, suggesting that host effects were stable over time. These results point to the stability of Wolbachia infections and their impact on hosts following local invasion, and also highlight the continued persistence of uninfected individuals at a low frequency most likely due to immigration.

Comparisons through time and space suggest rapid evolution of dispersal behaviour in an invasive species

During a biological invasion, we expect that the expanding front will increasingly become dominated by individuals with better dispersal abilities. Over many generations, selection at the invasion front thus will favour traits that increase dispersal rates. As a result of this process, cane toads (Bufo marinus) are now spreading through tropical Australia about 5-fold faster than in the early years of toad invasion; but how have toads changed to make this happen? Here we present data from radio-tracking of free-ranging cane toads from three populations (spanning a 15-year period of the toads’ Australian invasion, and across 1800 km). Our data reveal dramatic shifts in behavioural traits (proportion of nights when toads move from their existing retreat-site to a new one, and distance between those successive retreat-sites) associated with the rapid acceleration of toad invasion. Over a maximum period of 70 years (~50 generations), cane toads at the invasion front in Australia apparently have evolved such that populations include a higher proportion of individuals that make long, straight moves.

Locomotor performance in an invasive species: cane toads from the invasion front have greater endurance, but not speed, compared to conspecifics from a long-colonised area

Cane toads (Bufo marinus) are now moving about 5 times faster through tropical Australia than they did a half-century ago, during the early phases of toad invasion. Radio-tracking has revealed higher daily rates of displacement by toads at the invasion front compared to those from long-colonised areas: toads from frontal populations follow straighter paths, move more often, and move further per displacement than do toads from older (long-established) populations. Are these higher movement rates of invasion-front toads associated with modified locomotor performance (e.g. speed, endurance)? In an outdoor raceway, toads collected from the invasion front had similar speeds, but threefold greater endurance, compared to conspecifics collected from a long-established population. Thus, increased daily displacement in invasion-front toads does not appear to be driven by changes in locomotor speed. Instead, increased dispersal is associated with higher endurance, suggesting that invasion-front toads tend to spend more time moving than do their less dispersive conspecifics. Whether this increased endurance is a cause or consequence of behavioural shifts associated with rapid dispersal is unclear. Nonetheless, shifts in endurance between frontal and core populations of this invasive species point to the complex panoply of traits affected by selection for increased dispersal ability on expanding population fronts.

Invasion, stress, and spinal arthritis in cane toads

The impact of invasive species on biodiversity has attracted considerable study, but impacts of the invasion process on the invaders themselves remain less clear. Invading species encounter conditions different from those in their ancestral habitats and are subject to intense selection for rapid dispersal. The end result may be significant stress on individual organisms, with consequent health problems. Our studies on invasive cane toads in Australia reveal severe spinal arthritis in ≈10% of large adult toads, associated with the same factors (large body size, frequent movement, and relatively long legs) that have enabled toads to invade so rapidly across the Australian tropics.

Rapid shifts in dispersal behavior on an expanding range edge

Dispersal biology at an invasion front differs from that of populations within the range core, because novel evolutionary and ecological processes come into play in the nonequilibrium conditions at expanding range edges. In a world where species’ range limits are changing rapidly, we need to understand how individuals disperse at an invasion front. We analyzed an extensive dataset from radio-tracking invasive cane toads (Rhinella marina) over the first 8 y since they arrived at a site in tropical Australia. Movement patterns of toads in the invasion vanguard differed from those of individuals in the same area postcolonization. Our model discriminated encamped versus dispersive phases within each toad’s movements and demonstrated that pioneer toads spent longer periods in dispersive mode and displayed longer, more directed movements while they were in dispersive mode. These analyses predict that overall displacement per year is more than twice as far for toads at the invasion front compared with those tracked a few years later at the same site. Studies on established populations (or even those a few years postestablishment) thus may massively underestimate dispersal rates at the leading edge of an expanding population. This, in turn, will cause us to underpredict the rates at which invasive organisms move into new territory and at which native taxa can expand into newly available habitat under climate change.

Evolution of dispersal and life history interact to drive accelerating spread of an invasive species.

Populations on the edge of an expanding range are subject to unique evolutionary pressures acting on their life-history and dispersal traits. Empirical evidence and theory suggest that traits there can evolve rapidly enough to interact with ecological dynamics, potentially giving rise to accelerating spread. Nevertheless, which of several evolutionary mechanisms drive this interaction between evolution and spread remains an open question. We propose an integrated theoretical framework for partitioning the contributions of different evolutionary mechanisms to accelerating spread, and we apply this model to invasive cane toads in northern Australia. In doing so, we identify a previously unrecognised evolutionary process that involves an interaction between life-history and dispersal evolution during range shift. In roughly equal parts, life-history evolution, dispersal evolution and their interaction led to a doubling of distance spread by cane toads in our model, highlighting the potential importance of multiple evolutionary processes in the dynamics of range expansion.

The toad ahead: challenges of modelling the range and spread of an invasive species

An ability to predict the rate at which an organism spreads its range is of growing importance because the process of spread (during invasion by an exotic species) is almost identical to that occurring at the expanding range margins of a native species undergoing range shifts in response to climate change. Thus, the methods used for modelling range spread can also be employed to assess the distributional implications of climate change. Here we review the history of research on the spread of cane toads in Australia and use this case study to broadly examine the benefits and pitfalls of various modelling approaches. We show that the problems of estimating the current range, predicting the future range, and predicting the spread rate are interconnected and inform each other. Generally, we argue that correlative approaches to range-prediction are unsuitable when applied to invasive species and suggest that mechanistic methods are beginning to look promising (despite being more difficult to execute), although robust comparisons of correlative versus mechanistic predictions are lacking. Looking to the future, we argue that mechanistic models of range advance (drawing from both population ecology and environmental variation) are the approaches most likely to yield robust predictions. The complexity of these approaches coupled with the steady rise in computing power means that they have only recently become computationally tractable. Thus, we suggest that the field is only recently in a position to incorporate the complexity necessary to robustly model the rate at which species shift their range.