The ecology and evolution of autotomy

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.     

The effects of tail autotomy on survivorship and body growth of Uta stansburiana under conditions of high mortality

We examined the effects of tail autotomy on survivorship and body growth of both adult and juvenile Uta stansburiana by directly manipulating tail condition. Tail loss decreased neither survivorship nor rate of body growth for individuals in two natural populations. Lack of an influence of tail loss on survivorship in these two populations may be the result of high mortality. Under high mortality any differential effects of tail loss will be lower than in populations facing lower mortality. Growth experiments in the laboratory demonstrated that, under conditions of minimal environmental variation and social interactions, there is no tradeoff between body growth and tail regeneration as has been suggested for other species of lizards. One possible reason for this difference is that U. stansburiana does not use the tail as a storage organ for lipids. The original and regenerated tails are composed mainly of protein. In general, any differential body growth between tailed and tailless individuals may be due to social interactions and not a diversion of limited energy into tail regeneration.     

The evolution of autotomy in leaf-footed bugs

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.     

Dynamics of Mara–Serengeti ungulates in relation to land use changes

Caudal autotomy, the ability to shed the tail, is common in lizards as a response to attempted predation. Since Arnold's substantial review of caudal autotomy as a defence in reptiles 20 years ago, our understanding of the costs associated with tail loss has increased dramatically. In this paper, we review the incidence of caudal autotomy among lizards (Reptilia Sauria) with particular reference to questions posed by Arnold. We examine tail break frequencies and factors that determine occurrence of autotomy in natural populations (including anatomical mechanisms, predation efficiency and intensity, microhabitat preference, sex and ontogenetic differences, as well as intraspecific aggression). We also summarize the costs associated with tail loss in terms of survivorship and reproduction, focusing on potential mechanisms that influence fitness (i.e. locomotion costs, behavioural responses and metabolic costs). Finally, we examine the factors that may influence the facility with which autotomy takes place, including regeneration rate, body form and adaptive behaviour. Taking Arnold's example, we conclude with proposals for future research.     

Caudal autotomy and regeneration in lizards

Caudal autotomy, or the voluntary self-amputation of the tail, is an anti-predation strategy in lizards that depends on a complex array of environmental, individual, and species-specific characteristics. These factors affect both when and how often caudal autotomy is employed, as well as its overall rate of success. The potential costs of autotomy must be weighed against the benefits of this strategy. Many species have evolved specialized behavioral and physiological adaptations to minimize or compensate for any negative consequences. One of the most important steps following a successful autotomous escape involves regeneration of the lost limb. In some species, regeneration occurs rapidly; such swift regeneration illustrates the importance of an intact, functional tail in everyday experience. In lizards and other vertebrates, regeneration is a highly ordered process utilizing initial developmental programs as well as regeneration-specific mechanisms to produce the correct types and pattern of cells required to sufficiently restore the structure and function of the sacrificed tail. In this review, we discuss the behavioral and physiological features of self-amputation, with particular reference to the costs and benefits of autotomy and the basic mechanisms of regeneration. In the process, we identify how these behaviors could be used to explore the neural regulation of complex behavioral responses within a functional context.     

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

Abnormal caudal regeneration, the production of additional tails through regeneration events, occurs in lepidosaurs as a result of incomplete autotomy or sufficient caudal wound. Despite being widely known to occur, documented events generally are limited to opportunistic single observations – hindering the understanding of the ecological importance of caudal regeneration. Here we compiled and reviewed a robust global database of both peer‐reviewed and non‐peer reviewed records of abnormal regeneration events in lepidosaurs published over the last 400 years. Using this database, we qualitatively and quantitatively assessed the occurrence and characteristics of abnormal tail regeneration among individuals, among species, and among populations. We identified 425 observations from 366 records pertaining to 175 species of lepidosaurs across 22 families from 63 different countries. At an individual level, regenerations ranged from bifurcations to hexafurcations; from normal regeneration from the original tail to multiple regenerations arising from a single point; and from growth from the distal third to the proximal third of the tail. Species showing abnormal regenerations included those with intra‐vertebral, inter‐vertebral or no autotomy planes, indicating that abnormal regenerations evidently occur across lepidosaurs regardless of whether the species demonstrates caudal autotomy or not. Within populations, abnormal regenerations were estimated at a mean ± SD of 2.75 ± 3.41% (range 0.1–16.7%). There is a significant lack of experimental studies to understand the potential ecological impacts of regeneration on the fitness and life history of individuals and populations. We hypothesised that abnormal regeneration may affect lepidosaurs via influencing kinematics of locomotion, restrictions in escape mechanisms, anti‐predation tactics, and intra‐ and inter‐specific signalling. Behaviourally testing these hypotheses would be an important future research direction.     

The Link between Autotomy and CNS Regeneration: Echinoderms as Non-Model Species for Regenerative Biology

Achieving regeneration of the central nervous system (CNS) is a major challenge for regenerative medicine. The inability of mammals to regrow a severed CNS contrasts with the amazing regenerative powers of their deuterostome kin, the echinoderms. Rapid CNS regeneration from a specialized autotomy plane in echinoderms presents a highly tractable and suitable non-model system for regenerative biology and evolution. Starfish arm autotomy triggers mass cell migration and local proliferation, facilitating rapid CNS regeneration. Many regeneration events in nature are preceded by autotomy and there are striking parallels between autotomy and regeneration in starfish and lizards. Comparison of these systems holds promise to provide insight into regeneration deficiency in higher vertebrates and to uncover evolutionarily conserved deuterostome-chordate regenerative processes. This will help identify mechanisms that may be present but inactive in higher vertebrates to address the problem of their poor regenerative capacities and the challenge to achieve CNS repair and regrowth.     

Patterns of autotomy and regeneration in Hemigrapsus nudus

Leg autotomy and regeneration can have severe impacts on survival and reproduction, and these impacts may be even more pronounced in animals with multifarious legs, such as decapods. Thus, determining the patterns and frequency of autotomy and regeneration could reveal the effects of these processes on the individual and population level. We investigated whether some legs are lost more often than others and if all legs are equally likely to be regenerated. We sampled nearly 500 purple shore crabs (Hemigrapsus nudus) and showed that (1) most animals are found with at least one injured leg, (2) the patterns of autotomy differ between males and females, and (3) successful claw regeneration is unlikely in both males and females. Future work with H. nudus and other grapsid crabs will elucidate how patterns seen here relate to other developmental and ecological factors.     

Autotomy and arm number increase in Oxycomanthus japonicus (Echinodermata, Crinoidea)

Abstract. We have explored the process by which crinoids increase arm number as they grow. Two hypotheses have been proposed: (1) arm autotomy with subsequent bifurcation and regeneration of a pair of arms, and (2) growth of a pinnule into an additional arm. We have traced the development of Oxycomanthus japonicus for about a year after fertilization and provide the first confirmation that the number of arms increases by autotomy, bifurcation, and subsequent regeneration of a pair of arms. The next such addition tends to occur at some distance from the previous pair. Thus, increase of arm number takes place in such a manner that the density of the arms remains relatively constant, and an efficient filtration fan for feeding is maintained. Although arm autotomy in crinoids has been considered to occur only as a response to physical or chemical disturbance, the present results suggest that autotomy also occurs as a specific, intrinsically programmed event during normal development.     

The influence of fundamental traits on mechanisms controlling appendage regeneration

One of the most compelling questions in evolutionary biology is why some animals can regenerate injured structures while others cannot. Appendage regeneration appears to be common when viewed across the metazoan phylogeny, yet this ability has been lost in many taxa to varying degrees. Within species, the capacity for regeneration also can vary ontogenetically among individuals. Here we argue that appendage regeneration along the secondary body axis may be constrained by fundamental traits such as body size, aging, life stage, and growth pattern. Studies of the molecular mechanisms affecting regeneration have been conducted primarily with small organisms at early life stages. Such investigations disregard the dramatic shifts in morphology and physiology that organisms undergo as they age, grow, and mature. To help explain interspecific and intraspecific constraints on regeneration, we link particular fundamental traits to specific molecular mechanisms that control regeneration. We present a new synthesis for how these fundamental traits may affect the molecular mechanisms of regeneration at the tissue, cellular, and genomic levels of biological organization. Future studies that explore regeneration in organisms across a broad phylogenetic scale, and within an ontogenetic framework, will help elucidate the proximate mechanisms that modulate regeneration and may reveal new biomedical applications for use in regenerative medicine.     

Effect of the degree of autotomy on feeding, growth, and reproductive capacity in the multi-armed sea star Heliaster helianthus

The term autotomy refers to the process by which some species lose limbs or parts of limbs in response to adverse biotic or abiotic conditions, as for example, predation or abnormally high temperatures. The multi-armed sea star Heliaster helianthus is a key predator of the intertidal and the shallow rocky subtidal communities of north-central Chile. Natural populations of this sea star have been found with up to 60% of the individuals showing some degree of autotomy. The present study evaluated the effects of autotomy on feeding rate and growth of juvenile and adult H. helianthus after experimentally induced autotomy of 17% and 33% of their arms, as well as on the energy content of the pyloric caeca and gonads of adults during the reproductive period. Experimental juvenile sea stars were maintained and fed in the laboratory over a period of five months and adult sea stars for one month, Intact individuals were maintained as parallel controls. The results showed that juveniles undergoing 33% autotomy decreased their feeding rates, and as a consequence showed lowered net individual growth. In contrast, adults with 17% and 33% autotomy showed marked reductions in feeding. The results showed that autotomized adults had between five and seven times lower contents of carbohydrates, lipids, and proteins (and thus energetic content) in their pyloric caeca and gonads. The loss of the arms not only decreased the capacity for feeding in sea stars, but also allocated energy away from growth and reproduction into the process of regeneration of arms. This suggests that autotomy reduces the fitness of H. helianthus. Growth was reduced in the juveniles, while adults became limited in their ability to store energy which then limited their reproductive potential. Finally, based on the important effect of autotomy on reducing the feeding capacity of H. helianthus, the role of this sea star as a predator in the environment may be strongly affected.     

Morphological and biochemical analyses of original and regenerated lizard tails reveal variation in protein and lipid composition

Caudal autotomy, or voluntary self-amputation of the tail, is a common and effective predator evasion mechanism used by most lizard species. The tail contributes to a multitude of biological functions such as locomotion, energetics, and social interactions, and thus there are often costs associated with autotomy. Notably, relatively little is known regarding bioenergetic costs of caudal autotomy in lizards, though key morphological differences exist between the original and regenerated tail that could alter the biochemistry and energetics. Therefore, we investigated lizard caudal biochemical content before and after regeneration in three gecko and one skink species. Specifically, we integrated biochemical and morphological analyses to quantify protein and lipid content in original and regenerated tails. All lizards lost significant body mass, mostly protein, due to autotomy and biochemical results indicated that original tails of all species contained a greater proportion of protein than lipid. Morphological analyses of two gecko species revealed interspecific differences in protein and lipid content of regenerated lizard tails. Results of this study contribute to our understanding of the biochemical consequences of a widespread predator evasion mechanism.     

Appendage-restricted gene induction using a heated agarose gel for studying regeneration in metamorphosed Xenopus laevis and Pleurodeles waltl

Amphibians and fish often regenerate lost parts of their appendages (tail, limb, and fin) after amputation. Limb regeneration in adult amphibians provides an excellent model for appendage (limb) regeneration through 3D morphogenesis along the proximodistal, dorsoventral, and anteroposterior axes in mammals, because the limb is a homologous organ among amphibians and mammals. However, manipulating gene expression in specific appendages of adult amphibians remains difficult; this in turn hinders elucidation of the molecular mechanisms underlying appendage regeneration. To address this problem, we devised a system for appendage-specific gene induction using a simplified protocol named the “agarose-embedded heat shock (AeHS) method” involving the combination of a heat-shock-inducible system and insertion of an appendage in a temperature-controlled agarose gel. Gene expression was then induced specifically and ubiquitously in the regenerating limbs of metamorphosed amphibians, including a frog (Xenopus laevis) and newt (Pleurodeles waltl). We also induced gene expression in the regenerating tail of a metamorphosed P. waltl newt using the same method. This method can be applied to adult amphibians with large body sizes. Furthermore, this method enables simultaneous induction of gene expression in multiple individuals; further, the data are obtained in a reproducible manner, enabling the analysis of gene functions in limb and tail regeneration. Therefore, this method will facilitate elucidation of the molecular mechanisms underlying appendage regeneration in amphibians, which can support the development of regenerative therapies for organs, such as the limbs and spinal cord.     

Costs of reproduction in male lizards, Sceloporus virgatus

Models of life history evolution typically assume a balance between the benefits of current reproductive activity and the costs to future reproductive success or survivorship, but empirical studies often find positive correlations between such components of fitness in undisturbed animal populations. I examined possible survivorship costs of reproduction in free-ranging male lizards, Sceloporus virgatus , and found that males with low levels of mating success were less likely to survive to the following breeding season. I also investigated two possible indicators of reproductive effort, increase in ectoparasite load and decrease in body weight during the breeding season. Levels of parasitism with trombiculid mites at the end of the breeding season were not associated with any measure of fitness or body condition (mating success, survivorship to the following year, relative weight loss). Yearling males (which have low levels of mating success) usually gained weight during the breeding season, while older males generally lost weight during this period. This suggests that young males may have postponed reproduction in favor of body growth and that seasonal weight loss of older males might reflect reproductive effort. Within the group of older males, individuals with the highest levels of mating success did not have high levels of either weight loss or mortality. Mate guarding behavior, an alternative to the aggressive territorial behavior typical of many lizard species, may allow certain males to obtain mates without expending large amounts of energy or exposing themselves to great mortality risks.     

Leave it all behind: a taxonomic perspective of autotomy in invertebrates

Autotomy is defined herein as the shedding of a body part, where (1) the loss of the body part is defensive (autotomy helps prevent the whole animal from being compromised and is in response to external stimuli); (2) shearing occurs by an intrinsic mechanism along a breakage plane (there has been selection for certain body parts to be pulled off easily); and (3) the loss is controlled - the animal moves away from the trapped limb, the loss is under some form of central control (neural or hormonal), or the body part is detached quickly. Autotomy (under this defensive definition) has evolved independently for a diverse array of body parts in many taxa; we have summarised available information for over 200 invertebrate species. The advantages of autotomy include escape from entrapment, an effective form of attack, expulsion of an infected body part or in limiting wounding. We discuss how the incidence of autotomy may therefore be correlated with various traits such as limb function, sex differences, other defence mechanisms, habitat disturbance, and sociality. There are also costs associated with autotomy. Short-term costs include loss of a specialised appendage or organ, reduced speed and stability, or even death. Long-term costs include compromised foraging and feeding (often leading to reduced growth), altered anti-predator, competitive or reproductive behaviour, and even defective development. Regenerating lost appendages may also incur significant costs for the individual. We examine the costs and benefits of autotomy, and discuss the evolutionary selective pressures that contribute to the prevalence and effectiveness of autotomy in invertebrates.     

Reduced tail regeneration in the Common Lizard, Lacerta vivipara, parasitized by blood parasites

1. Many lizards will lose their tail through autotomy as an antipredator device even though there must be significant costs during tail regeneration.
2. Parasites are energetically costly to the host, and may reduce the rate of cell regeneration. The relation between the presence of haemogregarines (phylum Sporozoa) and the rate of tail regeneration in the Common Lizard Lacerta vivipara (Jacquin) was examined.
3. Experimentally induced autotomy in parasitized lizards resulted in a significantly reduced rate of tail regeneration compared with non-parasitized lizards. On the other hand, tail loss was not associated with an abnormal increase of parasite load, suggesting that the physiological stress (induced by tail loss) did not cause a decrease in parasite defence.     

The type of leg lost affects habitat use but not survival in a non‐regenerating arthropod

Finding shelter and surviving encounters with predators are pervasive challenges for animals. These challenges may be exacerbated after individuals experience bodily damage. Certain forms of damage arise voluntarily in animals; for instance, some taxa release appendages (tails, legs, or other body parts) as a defensive strategy (“autotomy”). This behavior, however, may pose long‐term negative consequences for habitat use and survival. Additionally, these putative consequences are expected to vary according to the function of the lost body part. We tested the effects of losing different functional leg types (locomotor or sensory) on future habitat use and survival in a Neotropical species of Prionostemma harvestmen (Arachnida: Opiliones) that undergo frequent autotomy but do not regrow limbs. Daytime surveys revealed that both eight‐legged harvestmen and harvestmen missing legs roosted in similar frequencies across habitats (tree bark, mossy tree, or fern), and perched at similar heights. Mark–recapture data showed that harvestmen that lost sensory legs roosted in tree bark less frequently, but on mossy trees more frequently. On the contrary, we did not observe changes in habitat use for eight‐legged animals or animals that lost locomotor legs. This change might be related to sensory exploration and navigation. Lastly, we found that recapture rates across substrates were not affected by the type of legs lost, suggesting that leg loss does not impact survival. This potential lack of effect might play a role in why a defensive strategy like autotomy is so prevalent in harvestmen despite the lack of regeneration.     

Ceratal autotomy and regeneration in the aeolid nudibranch Phidiana crassicornis and the role of predators

Abstract. Ceratal autotomy by the aeolid nudibranch Phidinna crassicornis is common in the field and was induced in the laboratory by mechanical and predatory stimuli. The ceras detaches from the body wall along an autotomy plane located at its basal constriction. Cerata released copious amounts of mucus during autotomy and exhibited a prolonged writhing response that continued for several hours after detachment. Regeneration of cerata autotomized in the field and in the laboratory was documented. Four days after autotomy, regenerating cerata appeared as small protuberances. By day 24 the regenerates acquired their mature structural organisation and vivid colour. The cerata subsequently increased in length and diameter and were indistin‐guishable from surrounding cerata by 41 to 43 days after autotomy. Regeneration rates of cerata induced to autotomize in the laboratory and regeneration of cerata autotomized in the field were similar, averaging 0.08 and 0.067 mdday, respectively. The sequence of morphological events involved with regeneration following experimental and natural induction of autotomy was identical. The kelp crab Pugettia productn induced autotomy by holding cerata with its chelae. This crab also fed on autotomized cerata and consumed locomotory and ceratal mucus. Ceratal autotomy may be an important mechanism of escape from this predatory crustacean. Other potential predators including hermit crabs and tidepool sculpins did not elicit defensive behaviour in P. crussicornis. Nematocysts were present in the enidosacs and their role in defense was investigated. Fired nematocysts were observed in podia of the asteroid Crossaster papposus following ceratal contact but were not seen in the podia of Pycnopodia helianthoides in a similar trial. For P. crassicornis, the cnidosacs may function primarily as a storage device for safe sequestering of nematoeysts that could pose a threat to the digestive system. They did not play a major defensive role against the predators tested, but may be important in the field against other predators.     

Exploring the role of microRNAs in axolotl regeneration

The axolotl, Ambystoma mexicanum, is used extensively for research in developmental biology, particularly for its ability to regenerate and restore lost organs, including in the nervous system, to full functionality. Regeneration in mammals typically depends on the healing process and scar formation with limited replacement of lost tissue. Other organisms, such as spiny mice (Acomys cahirinus), salamanders, and zebrafish, are able to regenerate some damaged body components. Blastema is a tissue that is formed after tissue injury in such organisms and is composed of progenitor cells or dedifferentiated cells that differentiate into various cell types during regeneration. Thus, identifying the molecules responsible for initiation of blastema formation is an important aspect for understanding regeneration. Introns, a major source of noncoding RNAs (ncRNAs), have characteristic sizes in the axolotl, particularly in genes associated with development. These ncRNAs, particularly microRNAs (miRNAs), exhibit dynamic regulation during regeneration. These miRNAs play an essential role in timing and control of gene expression to order and organize processes necessary for blastema creation. Master keys or molecules that underlie the remarkable regenerative abilities of the axolotl remain to be fully explored and exploited. Further and ongoing research on regeneration promises new knowledge that may allow improved repair and renewal of human tissues.