Stress and immunity at the invasion front: a comparison across cane toad (Rhinella marina) populations

Abstract

At an invasion front, energetic and physiological trade‐offs may differ from those at the range‐core as a result of selection for enhanced dispersal, combined with a low density of conspecifics (which reduces pathogen transmission and competition for food). We measured traits related to energy stores and immunity in wild cane toads (Rhinella marina) across a 750‐km transect from their invasion front in tropical Australia, back into sites colonized 21 years earlier. Several traits were found to vary with population age; some linearly and others in a curvilinear manner. The relative size of spleens and fat bodies was highest in the oldest and newest populations, where rates of lungworm infection were lowest. Toads from older populations produced more corticosterone in response to a standardized stressor, and had higher lymphocyte counts (but lower basophil counts). The amount of skin swelling elicited by phytohaemagglutinin injection did not vary geographically, although recruitment of leukocytes to the injected tissue was higher in toads from long‐colonized areas. Because this was a field‐based study, we cannot differentiate the effects of population age, toad density or pathogen pressure on our measures of stress and immune responses, nor can we distinguish whether the causation involves hard‐wired adaptive processes or phenotypically plastic responses. Nonetheless, our data demonstrate substantial variation in immune systems among toads at varying distances from an invasion front, showing that a biological invasion imposes strong pressures on physiological systems of the invader.

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

“…Two thousand km eastwards, we also collected 86 toads from two sites (−19.3S, 146.8W; −17.9S, 145.9W) where toads had been present for >70 years. Toads from populations less than 3 years old occur at low density and exhibit low levels of parasite infection compared with older populations (Brown, Kelehear, Shilton, Phillips, & Shine, ; Brown et al., ). Behaviourally, they exhibit higher levels of movement and directionality than toads from older populations (Brown et al., ; Phillips, Brown, Travis, & Shine, ).…”

“…Two thousand km eastwards, we also collected 86 toads from two sites (−19.3S, 146.8W; −17.9S, 145.9W) where toads had been present for >70 years. Toads from populations less than 3 years old occur at low density and exhibit low levels of parasite infection compared with older populations (Brown, Kelehear, Shilton, Phillips, & Shine, 2015;Brown et al, 2013).…”

Immune and environment‐driven gene expression during invasion: An eco‐immunological application of RNA‐Seq

“…Furthermore, loci putatively under selection are involved in tolerance of temperature extremes and dehydration . Traits such as leg length (Hudson et al, 2016), spleen size, and fat body mass (Brown, Kelehear, Shilton, Phillips, & Shine, 2015b) follow a U-shaped (curvilinear) pattern F I G U R E 1 Geographic distribution of the cane toad in Australia (dark gray region). For example, behavioral propensity for exploration increases with distance from the introduction site (Gruber, Brown, Whiting, & Shine, 2017).…”

“…The densities of many invasive populations follow a "traveling wave," in which population density is low at recently colonized areas (e.g., the invasion front), high in areas that have been colonized for several years (e.g., intermediate areas), and low at longcolonized areas (e.g., the range core; Hilker, Lewis, Seno, Langlais, & Malchow, 2005;Simberloff & Gibbons, 2004). This parasitic lungworm is absent from toads at the invasion front and is most prevalent in toads from intermediate areas (Brown, Kelehear, et al, 2015b;Phillips et al, 2010). This parasitic lungworm is absent from toads at the invasion front and is most prevalent in toads from intermediate areas (Brown, Kelehear, et al, 2015b;Phillips et al, 2010).…”

Differences in standard metabolic rate at the range edge versus the center of an expanding invasive population of Xenopus laevis in the West of France

“…Range expansions and range shifts are closely related to the capacity of an organism to reproduce, disperse, and survive (Burton, Phillips & Travis, 2010). Theoretical and empirical studies have highlighted the differential allocation of resources to these life-history traits between individuals living at the edge, and those living at the core of the range of expanding populations (Burton et al, 2010;Hughes, Hill & Dytham, 2003;Karlsson & Johansson, 2008;Llewelyn et al, 2011;Bonte et al, 2012;Brown et al, 2015;Hudson et al, 2015;Chuang & Peterson, 2016). For example, a preferential allocation of resources toward dispersal and associated phenotypic traits (e.g.…”