It is lonely at the front: contrasting evolutionary trajectories in male and female invaders

Abstract

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.

May the (selective) force be with you: Spatial sorting and natural selection exert opposing forces on limb length in an invasive amphibian

“…Our results support the hypothesis that the elongation of forelimbs in invasion‐front toads (Hudson, Brown, et al., ) evolved for enhanced rates of dispersal despite a cost in male–male competition. In the population that we studied (which was 10–20 years behind the expanding invasion front), more force was required to displace amplexing male toads with relatively short arms than to displace those with long forearms.…”

“…In natural populations, a male's body size may be the most important predictor of his success in male–male bouts. In cane toads, limb length relative to body length does not change markedly as the animal grows larger (Hudson, Brown, et al., ), indicating that a male is likely to be relatively short‐armed or long‐armed throughout his life. If mean body sizes are similar between individuals with different arm lengths, the variance in relative arm length may be a target of significant selection.…”

“…This scenario implies that, in the case of forearm length, natural selection in high‐density populations behind the invasion front may operate in the opposite direction to spatial sorting. Offspring of toads from these disparate populations exhibit similar morphological traits as their parents, even when raised under standard conditions (Hudson, Brown, et al., ). Thus, clines in forelimb length reflect a heritable trait, rather than a phenotypically plastic response to local conditions (Figure ).…”

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

“…The curvilinearity in expression of many of our differentially expressed genes resembles that of other phenotypic traits affected by spatial sorting, such as leg length (Hudson et al, 2016). The curvilinearity in expression of many of our differentially expressed genes resembles that of other phenotypic traits affected by spatial sorting, such as leg length (Hudson et al, 2016).…”

“…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).…”