The evolution of autotomy in leaf‐footed bugs

Abstract

Sacrificing body parts is one of many behaviors that animals use to escape predation. This trait, termed autotomy, is classically associated with lizards. However, several other taxa also autotomize, and this trait has independently evolved multiple times throughout Animalia. Despite having multiple origins and being an iconic antipredatory trait, much remains unknown about the evolution of autotomy. Here, we combine morphological, behavioral, and genomic data to investigate the evolution of autotomy within leaf-footed bugs and allies (Insecta: Hemiptera: Coreidae + Alydidae). We found that the ancestor of leaf-footed bugs autotomized and did so slowly; rapid autotomy (<2 min) then arose multiple times. The ancestor likely used slow autotomy to reduce the cost of injury or to escape nonpredatory entrapment but could not use autotomy to escape predation. This result suggests that autotomy to escape predation is a co-opted benefit (i.e., exaptation), revealing one way that sacrificing a limb to escape predation may arise. In addition to identifying the origins of rapid autotomy, we also show that across species variation in the rates of autotomy can be explained by body size, distance from the equator, and enlargement of the autotomizable appendage. K E Y W O R D S : Autotomy, evolutionary ecology, evolutionary origins, latitudinal gradient, phylogenetic comparative methods, predator-prey.

Leaf‐footed bugs possess multiple hidden contrasting color signals, but only one is associated with increased body size

“…To investigate our hypotheses, we used a subclade of leaf‐footed bugs for which there is an existing phylogenetic hypothesis, body size measurements, and autotomy data (data from Emberts et al., 2020). We specifically selected this subclade because we had access to almost every species that was represented in the phylogeny ( n = 26 species; Figure 2) and our previous knowledge suggested that this clade captures the diversity of flight/defense revealing states observed throughout the larger leaf‐footed bug clade.…”

“…For the purposes of this study, we pruned the 62‐tip leaf‐footed bug phylogeny from Emberts et al. (2020), which was built from a concatenated alignment of 567 loci (Emberts et al., 2020, Figure 2). The phylogenetic reconstruction in Emberts et al.…”

“…The phylogenetic reconstruction in Emberts et al. (2020) was done in a maximum likelihood framework as implemented in RAxML (Stamatakis, 2014), and the tree was dated using penalized likelihood as implemented in treePL (Smith & O’Meara, 2012) with four fossil calibrations. In the same study, the authors reported data on body size and latency to autotomize for each taxon.…”

“…The mean and median latency to autotomize (i.e., two measures for the rate of autotomy) for each species was estimated by collecting autotomy data on up to 84 individuals per species. Autotomy trials were conducted by grasping an individual's hind right leg with constant pressure (i.e., reverse action) forceps, while the individual was in contact with a piece of wood for up to 1 hr (Emberts et al., 2020). Those that did not autotomize within an hour were assigned as taking 3,600 s to autotomize (as opposed to removing them) because evidence suggests that these individuals would have likely autotomized, given more time (see Emberts et al., 2020).…”

“…The strongest example comes from a study that compared differences in the frequency of autotomy between two sympatric gecko species and found that the more aggressive species, which actively fights back against predators, had a lower rate of autotomy (Dial, 1978). Although the ability to autotomize is ubiquitous in leaf‐footed bugs, there is extensive variation in the rate of autotomy such that only a fraction of the species can autotomize quickly enough to escape predation (Emberts et al., 2020). Thus, the second aim of this study is to investigate whether the evolution of hidden contrasting coloration, a secondary defense against predation, is associated with the speed at which species autotomize.…”