Tradeoffs between dispersal and reproduction at an invasion front of cane toads in tropical Australia

Abstract

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.Any organism has a finite store of resources to allocate among competing demands such as maintenance, growth, and reproduction; and hence, natural selection is expected to fine-tune that allocation in ways that maximise lifetime reproductive success 1 . As a result, levels of investment into reproduction should depend upon competing priorities, with organisms decreasing reproductive output if investment into other functions yields higher benefits in fitness. Such tradeoffs may be especially clear during biological invasions, because of differences in evolutionary forces at the invasion front versus in long-colonised areas 2 . Individuals at an expanding range edge often exhibit unusually high rates of dispersal 3,4 , requiring energy that may decrease allocation of resources to other functions such as immune defence 5-7 and reproduction [8][9][10][11] . The increased allocation to dispersal is exacerbated by the non-adaptive process of spatial sorting; individuals that allocate more energy into dispersal will likely be close to the range edge, even if more rapid dispersal does not enhance fitness 12 .To test these ideas, we need to compare attributes of individuals at an expanding invasion front to conspecifics in longer-colonised areas. We can perform that comparison either through space (monitoring sites with different times since invasion) or through time (monitoring a single site as an invasion passes through). Most available evidence comes from spatial comparisons, which minimise confounding due to temporal (seasonal, annual) variation but introduce confounding factors that vary among sites (e.g. resource levels, predator abundance) 13 . Comparisons through time at a single site avoid those problems, but require longer-term monitoring and introduce confounds associated with temporally variable factors. In the current paper, we describe the results of studies over a three-year period at a single site, beginning soon after the initial arrival of a colonising species.The invasion of cane toads (Rhinella marina, formerly Bufo marinus) through tropical Australia has attracted co...

Stress and immunity: Field comparisons among populations of invasive cane toads in Florida

“…Over 60 years since their release in South Florida, cane toad populations have dispersed up to 450 km north (U.S. Geological Survey, 2020). As they have high invasive potential, cane toads have been used as an ectotherm model in ecoimmunology and invasion biology studies covering a wide diversity of topics including: history and geographical dispersal effects on locomotor and reproductive behavior (Brown, Holden, Shine, & Phillips, 2018; Brown, Kelehear, & Shine, 2011; Gruber, Brown, Whiting, & Shine, 2017; Kelehear & Shine, 2020; Kosmala, Christian, Brown, & Shine, 2017), corticosterone (CORT) immune interactions (Brown, Kelehear, Shilton, Phillips, & Shine, 2015; Brown, Phillips, Dubey, Shine, 2015; Brown, Shilton, & Shine, 2011; Brown, Shilton, Phillips, & Shine, 2007; S. T. Gardner, Assis, Smith, Appel, & Mendonça, 2020; S. Gardner et al, 2018; Graham, Kelehear, Brown, & Shine, 2012; Llewellyn et al, 2012), parasitic load (Phillips et al, 2010), genetic and phenotypic modifications (Rollins, Richardson, & Shine, 2015; Stuart, Shine, & Brown, 2019), and interactions of these invasive toads with native fauna (Brown & Shine, 2014; Mayer et al, 2015).…”

Evolution of life history and dispersal traits during the range expansion of a biological control agent

“…Dispersal traits increased while female weight and fecundity also increased and age at first reproduction decreased at the edge of the range expansion. Other study systems have shown a trade-off between dispersal and reproduction traits at the edge (Hughes et al 2003;Kelehear & Shine 2020). As Bonte & Dahirel (2017) argue, dispersal can be seen as a life-history trait that evolves independently, and that may be the case here.…”

How biological invasions affect animal behaviour: A global, cross‐taxonomic analysis

“…Behavioural traits linked to dispersal were expected to have changed more often in invasive species, as dispersal and spread are part of the invasion process, particularly if a non-native species is to thrive. For example, cane toads were found to move faster and follow straighter paths following selection in their new environment, the open Australian landscape (Brown, Phillips, & Shine, 2014; see also Kelehear & Shine, 2020). Environmental conditions in new habitats can be challenging for invasive species, requiring changes in activity, movements or strategies against dehydration.…”