Is the enhanced dispersal rate seen at invasion fronts a behaviourally plastic response to encountering novel ecological conditions?
ABSTRACT: As a population expands into novel areas (as occurs in biological invasions), the range edge becomes dominated by rapidly dispersing individuals-thereby accelerating the rate of population spread. That acceleration has been attributed to evolutionary processes (natural selection and spatial sorting), to which we add a third complementary process: behavioural plasticity. Encountering environmental novelty may directly elicit an increased rate of dispersal. When we reciprocally translocated cane toads (Rhinella marina) among study sites in southern Australia, the transported animals massively increased dispersal rates relative to residents (to an extent similar to the evolved increase between range-core versus invasion-front toad populations in Australia). The responses of these translocated toads show that even range-core toads are capable of the long-distance dispersal rates of invasion-front conspecifics and suggest that rapid dispersal (rather than evolving de novo) has simply been expanded from facultative to constitutive expression.
Project description:As is common in biological invasions, the rate at which cane toads (<i>Rhinella marina</i>) have spread across tropical Australia has accelerated through time. Individuals at the invasion front travel further than range-core conspecifics and exhibit distinctive morphologies that may facilitate rapid dispersal. However, the links between these morphological changes and locomotor performance have not been clearly documented. We used raceway trials and high-speed videography to document locomotor traits (e.g. hop distances, heights, velocities, and angles of take-off and landing) of toads from range-core and invasion-front populations. Locomotor performance varied geographically, and this variation in performance was linked to morphological features that have evolved during the toads' Australian invasion. Geographical variation in morphology and locomotor ability was evident not only in wild-caught animals, but also in individuals that had been raised under standardized conditions in captivity. Our data thus support the hypothesis that the cane toad's invasion across Australia has generated rapid evolutionary shifts in dispersal-relevant performance traits, and that these differences in performance are linked to concurrent shifts in morphological traits.
Project description:As a colonizing species expands its range, individuals at the invasion front experience different evolutionary pressures than do those at the range-core. For example, low densities at the edge of the range mean that males should rarely experience intense sperm competition from rivals; and investment into reproduction may trade-off with adaptations for more rapid dispersal. Both of these processes are predicted to favour a reduction in testis size at the invasion front. To explore effects of invasion stage in Australian cane toads (Rhinella marina), we collected and dissected 214 adult males from three regions: one in the species' range-core (northeastern Australia), and two from invasion fronts (one in northwestern Australia and one in southeastern Australia). Despite the brief duration of separation between toads in these areas (approx. 85 years), testis masses averaged greater than 30% higher (as a proportion of body mass) in range-core males than in conspecifics sampled from either vanguard of the invasion. Previous work has documented low reproductive frequencies in female cane toads at the invasion front also, consistent with the hypothesis that evolutionary and ecological pressures unleashed by an invasion can favour relatively low resource allocation to reproduction in both sexes.
Project description:Individuals at the leading edge of expanding biological invasions often show distinctive phenotypic traits, in ways that enhance their ability to disperse rapidly and to function effectively in novel environments. Cane toads (Rhinella marina) at the invasion front in Australia exhibit shifts in morphology, physiology and behaviour (directionality of dispersal, boldness, risk-taking). We took a common-garden approach, raising toads from range-core and range-edge populations in captivity, to see if the behavioural divergences observed in wild-caught toads are also evident in common-garden offspring. Captive-raised toads from the invasion vanguard population were more exploratory and bolder (more prone to 'risky' behaviours) than toads from the range core, which suggests that these are evolved, genetic traits. Our study highlights the importance of behaviour as being potentially adaptive in invasive populations and adds these behavioural traits to the increasing list of phenotypic traits that have evolved rapidly during the toads' 80-year spread through tropical Australia.
Project description:Biological invasions can induce rapid evolutionary change. As cane toads (Rhinella marina) have spread across tropical Australia over an 80-year period, their rate of invasion has increased from around 15 to 60 km per annum. Toads at the invasion front disperse much faster and further than conspecifics from range-core areas, and their offspring inherit that rapid dispersal rate. We investigated morphological changes that have accompanied this dramatic acceleration, by conducting three-dimensional morphometric analyses of toads from both range-core and invasion-front populations. Morphology of heads, limbs, pectoral girdles and pelvic girdles differed significantly between toads from the two areas, ranging from 0.5% to 16.5% difference in mean bone dimensions between populations, with invasion-front toads exhibiting wider forelimbs, narrower hindlimbs and more compact skulls. Those changes plausibly reflect an increased reliance on bounding (multiple short hops in quick succession) rather than separate large leaps. Within an 80-year period, invasive cane toads have converted the basic anuran body plan - which evolved for occasional large leaps to evade predators - into a morphotype better-suited to sustained long-distance travel.
Project description: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.
Project description:Initial research on the spread of cane toads (Rhinella marina) through tropical Australia reported a high incidence of spinal arthritis (spondylosis) in toads at the invasion front (where toads disperse rapidly), but not in areas colonized earlier (where toads are more sedentary). The idea that spondylosis was a cost of rapid dispersal was challenged by wider spatial sampling which linked rates of spondylosis to hot (tropical) climates rather than to dispersal rates. Here, the authors of these competing interpretations collaborate to reinterpret the data. Our reanalysis supports both previous hypotheses; rates of spondylosis are higher in populations established by fast-dispersing toads, and are higher in tropical than in temperate environments; they are also higher in larger toads. The functional reason for climatic effects is unclear, but might involve effects on the soil-living bacteria involved in the induction of spondylosis; and/or may reflect higher movement (as opposed to dispersal) or more pronounced dry-season aggregation rates of toads in tropical conditions.
Project description:The cane toad (<i>Rhinella marina</i>) has undergone rapid evolution during its invasion of tropical Australia. Toads from invasion front populations (in Western Australia) have been reported to exhibit a stronger baseline phagocytic immune response than do conspecifics from range core populations (in Queensland). To explore this difference, we injected wild-caught toads from both areas with the experimental antigen lipopolysaccharide (LPS, to mimic bacterial infection) and measured whole-blood phagocytosis. Because the hypothalamic-pituitary-adrenal axis is stimulated by infection (and may influence immune responses), we measured glucocorticoid response through urinary corticosterone levels. Relative to injection of a control (phosphate-buffered saline), LPS injection increased both phagocytosis and the proportion of neutrophils in the blood. However, responses were similar in toads from both populations. This null result may reflect the ubiquity of bacterial risks across the toad's invaded range; utilization of this immune pathway may not have altered during the process of invasion. LPS injection also induced a reduction in urinary corticosterone levels, perhaps as a result of chronic stress.
Project description:In Australia, large native predators are fatally poisoned when they ingest invasive cane toads (Rhinella marina). As a result, the spread of cane toads has caused catastrophic population declines in these predators. Immediately prior to the arrival of toads at a floodplain in the Kimberley region, we induced conditioned taste aversion in free-ranging varanid lizards (Varanus panoptes), by offering them small cane toads. By the end of the 18-month study, only one of 31 untrained lizards had survived longer than 110 days, compared to more than half (nine of 16) of trained lizards; the maximum known survival of a trained lizard in the presence of toads was 482 days. In situ aversion training (releasing small toads in advance of the main invasion front) offers a logistically simple and feasible way to buffer the impact of invasive toads on apex predators.
Project description:Invasive species often exhibit rapid evolutionary changes, and can provide powerful insights into the selective forces shaping phenotypic traits that influence dispersal rates and/or sexual interactions. Invasions also may modify sexual dimorphism. We measured relative lengths of forelimbs and hindlimbs of more than 3000 field-caught adult cane toads (Rhinella marina) from 67 sites in Hawai'i and Australia (1-80 years post-colonization), along with 489 captive-bred individuals from multiple Australian sites raised in a 'common garden' (to examine heritability and reduce environmental influences on morphology). As cane toads spread from east to west across Australia, the ancestral condition (long limbs, especially in males) was modified. Limb length relative to body size was first reduced (perhaps owing to natural selection on locomotor ability), but then increased again (perhaps owing to spatial sorting) in the invasion vanguard. In contrast, the sex disparity in relative limb length has progressively decreased during the toads' Australian invasion. Offspring reared in a common environment exhibited similar geographical divergences in morphology as did wild-caught animals, suggesting a genetic basis to the changes. Limb dimensions showed significant heritability (2-17%), consistent with the possibility of an evolved response. Cane toad populations thus have undergone a major shift in sexual dimorphism in relative limb lengths during their brief (81 years) spread through tropical Australia.
Project description:Individuals at the leading edge of a biological invasion experience novel evolutionary pressures on mating systems, due to low population densities coupled with tradeoffs between reproduction and dispersal. Our dissections of >1,200 field-collected cane toads (Rhinella marina) at a site in tropical Australia reveal rapid changes in morphological and reproductive traits over a three-year period after the invaders first arrived. As predicted, individuals with dispersal-enhancing traits (longer legs, narrower heads) had reduced reproductive investment (lower gonad mass). Post-invasion, the population was increasingly dominated by individuals with less dispersive phenotypes and a higher investment into reproduction (including, increased expression of sexually dimorphic traits in males). These rapid shifts in morphology and reproductive biology emphasise the impacts of the invasion process on multiple, interlinked aspects of organismal biology.