The ecology and evolution of autotomy

Abstract

Autotomy, the self-induced loss of a body part, occurs throughout Animalia. A lizard dropping its tail to escape predation is an iconic example, however, autotomy occurs in a diversity of other organisms. Octopuses can release their arms, crabs can drop their claws, and bugs can amputate their legs. The diversity of organisms that can autotomize body parts has led to a wealth of research and several taxonomically focused reviews. These reviews have played a crucial role in advancing our understanding of autotomy within their respective groups. However, because of their taxonomic focus, these reviews are constrained in their ability to enhance our understanding of autotomy. Here, we aim to synthesize research on the ecology and evolution of autotomy throughout Animalia, building a unified framework on which future studies can expand. We found that the ability to drop an appendage has evolved multiple times throughout Animalia and that once autotomy has evolved, selection appears to act on the removable appendage to increase the efficacy and/or efficiency of autotomy. This could explain why some autotomizable body parts are so elaborate (e.g. brightly coloured). We also show that there are multiple benefits, and variable costs, associated with autotomy. Given this variation, we generate an economic theory of autotomy (modified from the economic theory of escape) which makes predictions about when an individual should resort to autotomy. Finally, we show that the loss of an autotomizable appendage can have numerous consequences on population and community dynamics. By taking this broad taxonomic approach, we identified patterns of autotomy that transcend specific lineages and highlight clear directions for future research.

When one tail isn't enough: abnormal caudal regeneration in lepidosaurs and its potential ecological impacts

“…The ability to regenerate tissue is often, but not exclusively, coupled with autotomy (Lozito & Tuan, 2017;Alibardi, 2019;Emberts et al, 2019;Barr et al, 2019b). Evolving and being lost multiple times across taxonomic levels, autotomy and regeneration capacity is significantly influenced by both abiotic and biotic factors (Alibardi, 2017(Alibardi, , 2019Emberts et al, 2019).…”

Reproductive and energetic costs of injury in the mangrove tree crab

“…Ecological theory predicts that evolution should yield strategies that move organisms towards optimal performance (Stearns 1989). It has been hypothesized that this should lead to a tradeoff where organisms reproduce less in order to, instead, allocate that energy for regenerating the injured/lost body part (Juanes & Smith 1995, Emberts et al 2019). Theoretical work based on tail autotomy in lizards and salamanders predicts that this tradeoff following limb loss may decrease reproduction to different degrees (Bernardo & Agosta 2005).…”

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

“…Leaf‐footed bugs are also well known for another antipredatory defense, autotomy, which is self‐induced appendage loss (Emberts, St. Mary, Herrington, & Miller, 2018; Emberts, Miller, Kiehl, & St. Mary, 2017; Emberts, St. Mary, & Miller, 2016). Autotomy is a secondary defense (i.e., a defense to evade a pursuant predator; Edmunds, 1974) used by a variety of species to escape predation and has been observed in arthropods, cephalopods, lizards, and amphibians (Emberts, Escalante, & Bateman, 2019). Because sacrificing an appendage is often costly, it is hypothesized that the evolution of other antipredatory defenses should reduce selection for rapid autotomy.…”