Locomotor performance of cane toads differs between native-range and invasive populations

Abstract

Invasive species provide a robust opportunity to evaluate how animals deal with novel environmental challenges. Shifts in locomotor performance—and thus the ability to disperse—(and especially, the degree to which it is constrained by thermal and hydric extremes) are of special importance, because they might affect the rate that an invader can spread. We studied cane toads (Rhinella marina) across a broad geographical range: two populations within the species' native range in Brazil, two invasive populations on the island of Hawai'i and eight invasive populations encompassing the eastern, western and southern limits of the toad invasion in Australia. A toad's locomotor performance on a circular raceway was strongly affected by both its temperature and its hydration state, but the nature and magnitude of those constraints differed across populations. In their native range, cane toads exhibited relatively low performance (even under optimal test conditions) and a rapid decrease in performance at lower temperatures and hydration levels. At the other extreme, performance was high in toads from southern Australia, and virtually unaffected by desiccation. Hawai'ian toads broadly resembled their Brazilian conspecifics, plausibly reflecting similar climatic conditions. The invasion of Australia has been accompanied by a dramatic enhancement in the toads' locomotor abilities, and (in some populations) by an ability to maintain locomotor performance even when the animal is cold and/or dehydrated. The geographical divergences in performance among cane toad populations graphically attest to the adaptability of invasive species in the face of novel abiotic challenges.

The thermal dependency of locomotor performance evolves rapidly within an invasive species

“…In a previous study, we showed that locomotor performance of wild‐caught cane toads differed among populations from Brazil, Hawai'i, and four locations within Australia (Kosmala et al., ). However, we were unable to identify the proximate basis for that divergence; it might have been entirely due to toads acclimating to the conditions they experience during ontogeny.…”

“…This protocol is described in more detail by Kosmala et al. (). All procedures were approved by the University of Sydney Animal Care and Ethics Committee (Protocol # 703) and by Charles Darwin University Animal Ethics and Welfare Committee (AEWC) (Protocol # A13016).…”

“…Studies on captive-reared progeny of toads collected in different parts of Australia have confirmed that many of those divergences are heritable (Gruber et al, 2017;Hudson, Brown, et al, 2016;Hudson et al, 2017) and, hence, are likely to be the result of adaptation. In recent work, we documented significant differences in thermal and hydric performance curves between wild-caught cane toads from different parts of Australia, as well as between Australian populations and those from the native range in Brazil, and a stepping-stone population in Hawai'i (Kosmala et al, 2017). To clarify the degree to which such divergences are a result of adaptation rather than plasticity, we raised toads from eastern and Western Australia under standard ("common-garden") conditions and measured their locomotor abilities under a range of thermal and hydric conditions.…”

“…Adjusting performance optima to local conditions may be achieved via thermal plasticity (within‐generation phenotypic plasticity, whereby environmental conditions directly induce shifts in thermal performance curves) or adaptation (across‐generation shifts in the relative frequencies of alleles that optimize performance under the conditions most often encountered) (Beuchat et al., ; Gilbert et al., ; Maron, Elmendorf, & Vilà, ; Maron, Vila, Bommarco, Elmendorf, & Beardsley, ; McCann et al., ; Seiter & Kingsolver, ; Titon et al., ; Wilson, ; Winwood‐Smith et al., ). Studies of wild‐caught individuals can demonstrate phenotypically plastic responses, but cannot unequivocally test the role of adaptive change in generating geographic divergence in thermal performance curves (e.g., Kosmala, Christian, Brown, & Shine, ). To demonstrate that geographic divergence in performance optima is due to across‐generation shifts, we need to measure the performance of offspring from different populations that have been reared under standard (“common‐garden”) conditions (Hoffmann & Merilä, ; Hudson, Brown, & Shine, ; Phillips, Brown, Webb, & Shine, ).…”

Invasion history alters the behavioural consequences of immune system activation in cane toads

“…Any population that expands rapidly into hitherto uncolonised territory is likely to experience powerful new evolutionary pressures. Some of those novel challenges result from encounters with new types of predators, pathogens, prey and competitors (Brown, Kelehear, & Shine, ; Lee & Klasing, ; Sakai et al., ; Strauss, Lau, & Carroll, ), whereas others are driven by novel abiotic conditions (Kosmala, Christian, Brown, & Shine, ) or by the process of range expansion itself (Shine, Brown, & Phillips, ). In response to such demands, many invasive species demonstrate rapid phenotypic changes, via either developmental plasticity or adaptation, that enhance the ability of invasion‐front individuals to deal with those novel challenges (e.g.…”