Investigating the evolutionary effects of one feature on another: does muscle spread suppress caudal autotomy in lizards?

Hypotheses of secondary evolutionary change, where alteration in a particular feature is thought to result in change in another, can be tested in two main ways. First, phylogenies can be used to identify separate cases where one of the features changes and each case can then be examined to see whether the other change also actually takes place and if the perceived sequence of the alterations is appropriate. Secondly, the mechanism by which change in the second feature is supposed to be effected can be scrutinized and, in some cases, subjected to experimental investigation.
This approach was applied to a recent hypothesis, that backward spread of the caudifemoralis longus muscle in the tail base of lizards was the primary cause of loss of capacity to autotomize the tail. Some 23 to 25 independent cases of total autotomy loss in adult lizards were identified. In all but six of these there was no substantial spread of the muscle. In two of the remainder, the muscle appears to have spread ufiev autotomy loss, and another case cannot be tested properly as information about relationships is equivocal. The final three cases exhibit extension of the caudifemoralis longus before autotomy loss, but the latter is not found in related species that also inherit muscle extension, which suggests that other causal factors may be involved. In about 15 other cases, where autotomy becomes restricted to the tail base, there is no marked spread of the caudifemoralis longus. The proposed functional link between muscle extension and autotomy loss is also discussed and discounted     

Patterns of caudal-autotomy evolution in lizards

Using comparative techniques to account for phylogenetic effects, I examined patterns of evolution of caudal autotomy and foraging in 39 lizard species to test the hypothesis that caudal autotomy has co-evolved with morphology, locomotor performance, and foraging behaviour. There were significant positive associations between evolution of the point on the tail (distance from cloaca) at which tail loss occurs (an indirect measure of caudal autotomy) and evolution of each of the following: tail length, caudifemoralis longus (CFL) muscle length, and jump distance. The correlation with the evolution of sprint speed approached significance. These relationships primarily were due to the influence of tail-length evolution on autotomy-point evolution. With the effect of tail-length evolution removed, autotomy-point evolution was negatively correlated with the evolution of tail-loss frequency. The CFL restricts tail loss to portions of the tail posterior to the most distal point of its insertion in the tail. In addition, with the effect of tail-length evolution removed, CFL length co-evolved with sprint speed. These results indicate that tail morphology has co-evolved with caudal autotomy such that the evolution of the CFL has reduced caudal autotomy in certain groups of lizards.
Ambush foraging, the ability to lose the tail, intermediate CFL length, and low locomotor performance (i.e. slow sprint speed and short jump distance) are hypothesized to be the ancestral conditions in lizards using outgroup rooting. The diversification of lizard taxa has resulted in some lineages moving away from ancestral character states (i.e. family Teiidae, superfamily Varanoidea), while others are very similar or identical to their ancestors (i.e. superfamily Iguania).     

Energetic and locomotor costs of tail loss in the Chinese skink, Eumeces chinensis

Caudal autotomy is a defense mechanism used by numerous lizards to evade predators, but this entails costs. We collected 294 adult Chinese skinks (Eumeces chinensis) from a population in Lishui (eastern China) to evaluate energetic and locomotor costs of tail loss. Of the 294 skinks, 214 (c. 73%) had previously experienced caudal autotomy. Neither the proportion of individuals with regenerated tails nor the frequency distribution of locations of the tail break differed between sexes. We successively removed four tail segments from each of the 20 experimental skinks (adult males) initially having intact tails. Lipid content in each removed tail segment was measured, and locomotor performance (sprint speed, the maximal length traveled without stopping and the number of stops in the racetrack) was measured for each skink before and after each tail-removing treatment. Another independent sample of 20 adult males with intact tails was measured for locomotor performance to serve as controls for successive measurements taken for the experimental lizards. Caudal lipids were disproportionately stored along the length of the tail, with most lipids being aggregated in its proximal portion. Tail loss significantly affected sprint speed, but not the maximal length of, or the number of stops during the sprint. However, the adverse influence of tail loss on sprint speed was not significant until more than 51% of the tail (in length) was lost. Our data show that partial tail loss due to predatory encounters or other factors may not severely affect energy stores or locomotor performance in E. chinensis. As tail breaks occurred more frequently in the proximal portion of the tail in skinks collected from the field, we conclude that caudal autotomy occurring in nature often incurs substantial energetic and locomotor costs in E. chinensis.     

Sexual differences in caudal morphology and its relation to tail autotomy in lacertid lizards

We hypothesized that the presence of the forked hemipenes, and associated musculature, at the base of the tail in male lizards should constrain the capacity to autotomize the tail. Thus, this hypothesis predicts that the non-autotomous base of the tail should be longer in male than in female lizards. We tested this hypothesis in four species oflacertid lizards. Males have on average one to two non-autotomous vertebrae more than females, and the sexual difference in length of the non-autotomous tail base remains constant over the entire body size range. In addition, the first functional autotomy plane in males is usually located on, or is distal to, the vertebrae from which two hemipenial muscles take origin. These observations support the view that functional demands of the male intromittent organs impose constraints on the abilities of tail autotomy. In a natural population of Lacerta vivipara , the proportion of tail breaks that occurred at very short distances from the base was highest in females, indicating that the small sexual difference in length of the non-autotomous tail part is of functional significance. Total length of the tail was largest in males. This can be interpreted as a compensation for the decline in autotomy capacities at the tail base, such that the length of the autotomous part remains similar in both sexes.     

On caudal prehensility and phylogenetic constraint in lizards: The influence of ancestral anatomy on function in Corucia and Furcifer

We examined caudal anatomy in two species of prehensile‐tailed lizards, Furcifer pardalis and Corucia zebrata. Although both species use their tails to grasp, each relies on a strikingly different anatomy to do so. The underlying anatomies appear to reflect phylogenetic constraints on the consequent functional mechanisms. Caudal autotomy is presumably the ancestral condition for lizards and is allowed by a complex system of interdigitating muscle segments. The immediate ancestor of chameleons was nonautotomous and did not possess this specialized anatomy; consequently, the derived arrangement in the chameleon tail is unique among lizards. The limb functions as an articulated linkage system with long tendinous bands originating from longitudinal muscles to directly manipulate vertebrae. Corucia is incapable of autotomy, but it is immediately derived from autotomous ancestors. As such, it has evolved a biomechanical system for prehension quite different from that of chameleons. The caudal anatomy in Corucia is very similar to that of lizards with autotomous tails, yet distinct differences in the ancestral pattern and its relationship to the subdermal tunic are derived. Instead of the functional unit being individual autotomy segments, the interdigitating prongs of muscle have become fused with an emphasis on longitudinal stacks of muscular cones. The muscles originate from the vertebral column and a subdermal collagenous tunic and insert within the adjacent cone. However, there is remarkably little direct connection with the bones. The muscles have origins more associated with the tunic and muscular septa. Like the axial musculature of some fish, the tail of Corucia utilizes a design in which these collagenous elements serve as an integral skeletal component. This arrangement provides Corucia with an elegantly designed system capable of a remarkable variety of bending movements not evident in chameleon tails. J. Morphol. 239:143–155, 1999. © 1999 Wiley‐Liss, Inc.     

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.     

Partial tail loss has no severe effects on energy stores and locomotor performance in a lacertid lizard, <Emphasis Type="Italic">Takydromus septentrionalis</Emphasis>

Many species of lizards use caudal autotomy as a defense strategy to avoid predation, but tail loss entails costs. These topics were studied experimentally in the northern grass lizard, Takydromus septentrionalis. We measured lipids in the three-tail segments removed from each of the 20 experimental lizards (adult females) initially having intact tails to evaluate the effect of tail loss on energy stores; we obtained data on locomotor performance (sprint speed, the maximal length traveled without stopping and the number of stops in the racetrack) for these lizards before and after the tail-removing treatments to evaluate the effect of tail loss on locomotor performance. An independent sample of 20 adult females that retained intact tails was measured for locomotor performance to serve as controls for successive measurements taken for the experimental lizards. The lipids stored in the removed tail was positively correlated with tailbase width when holding the tail length constant, indicating that thicker tails contained more lipids than did thinner tails of the same overall length. Most of the lipids stored in the tail were concentrated in the proximal portion of the tail. Locomotor performance was almost unaffected by tail loss until at least more than 71% of the tail (in length) was lost. Our data show that partial tail loss due to predatory encounters or other factors may not severely affect energy stores and locomotor performance in T. septentrionalis.     

Locomotor performance of sand lizards (Lacerta agilis): effects of predatory pressure and parasite load

Locomotor performance affects foraging efficiency, predator avoidance and consequently fitness. Agility and speed determine the animal's social status and reflect its condition. In this study, we test how predatory pressure and parasite load influences locomotor performance of wild specimens of the sand lizard Lacerta agilis. Animals were chased on a 2-metre racetrack. Lizards with autotomy ran significantly faster than lizards with an intact tail, but there was no significant difference in running speed between individuals with fresh caudal autotomy and regenerated tails. Parasite presence and load, age and sex had no significant effect on speed. Our results indicate that autotomy either alters locomotory behaviour or that individuals with autotomised tails were those that previously survived contact with predators, and therefore represented a subgroup of the fastest individuals. Therefore, in general, predatory pressure but not parasites affected locomotor performance in lizards.     

Effects of tail loss on the movement patterns of the lizard, Psammodromus algirus

1. Many lizards use caudal autotomy as a defensive strategy. However, subsequent costs related to the alteration of locomotor abilities might decrease the fitness of individuals. In this paper, the movement patterns of spontaneously moving Psammodromus algirus lizards and their escape performance running at high speed were compared before and after tail loss. A control tailed group was also studied to assess the repeatability of locomotor patterns between trials.
2. Tail loss had a significant effect on spontaneous movement patterns. Tailless individuals moved at significantly slower speeds during bursts of locomotion, and distances moved within bursts were significantly reduced. The overall time spent pausing increased, and, as a result, overall speeds decreased to an even greater extent than burst speeds. However, mean durations of individual locomotor bursts and mean pause durations did not change significantly after tail loss.
3. Loss of the tail decreased mean stride length, although the positive relation between stride length and speed was retained.
4. Escape performance was also greatly affected; loss of the tail resulted in substantially reduced attained, maximal and overall escape speeds. These changes resulted in shorter escape distances (the time of the first pause after the initiation of the escape response) because the mean duration of escape responses did not change.
5. The relevance of these alterations for the ecology of this species, and how individuals may compensate for the costs of tail loss, favouring autotomy as an escape strategy, are discussed.     

Is partial tail loss the key to a complete understanding of caudal autotomy?

Autotomy, the self‐amputation of limbs or appendages, is a dramatic anti‐predator tactic that has repeatedly evolved in a range of invertebrate and vertebrate groups. In lizards, caudal autotomy enables the individual to break away from the predator's grasp, with the post‐autotomy thrashing of the tail distracting the attacker while the lizard makes its escape. This drastic defensive strategy should be selectively advantageous when the benefit (i.e. survival) exceeds the subsequent costs associated with tail loss. Here, we highlight how the position of autotomy along the length of the tail may influence the costs and benefits of the tactic, and thus the adaptive advantage of the strategy. We argue that most studies of caudal autotomy in lizards have focused on complete tail loss and failed to consider variation in the amount of tail shed, and, therefore, our understanding of this anti‐predator behaviour is more limited than previously thought. We suggest that future research should investigate how partial tail loss influences the likelihood of surviving encounters with a predator, and both the severity and duration of costs associated with caudal autotomy. Investigation of partial autotomy may also enhance our understanding of this defensive strategy in other vertebrate and invertebrate groups.     

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.     

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.     

Functional morphology and evolution of tail autotomy in salamanders

Basal tail constriction occurs in about two-thirds of the species of plethodontid salamanders. The constriction, which marks the site of tail autotomy, is a result of a reduction in length and diameter of the first caudal segment. Gross and microscopic anatomical studies reveal that many structural specializations are associated with basal constriction, and these are considered in detail. Areas of weakness in the skin at the posterior end of the first caudal segment, at the attachment of the musculature to the intermyotomal septum at the anterior end of the same segment, and between the last caudosacral and first caudal vertebrae precisely define the route of tail breakage. During autotomy the entire tail is shed, and a cylinder of skin one segment long closes over the wound at the end of the body. It is suggested that specializations described in this paper have evolved independently in three different groups of salamanders. Experiments and field observations reveal that, contrary to expectations, frequency of tail breakage is less in species with apparent provisions for tail autotomy than in less specialized species. The tail is a very important, highly functional organ in salamanders and it is suggested that selection has been for behavioral and structural adaptations for control of tail loss, rather than for tail loss per se.     

Caudal vertebral development and morphology in three salamanders with complex life cycles (Ambystoma jeffersonianum, Hemidactylium scutatum, and Desmognathus ocoee)

We describe caudosacral and caudal vertebral morphology across life history stages in three caudate amphibians: Ambystoma jeffersonianum (Ambystomatidae), Desmognathus ocoee (Plethodontidae: Desmognathinae), and Hemidactylium scutatum (Plethodontidae: Plethodontinae). All three species have aquatic larvae, but adults differ in habitat and predator defense strategy. Predator defense includes tail autotomy in D. ocoee and H. scutatum but not A. jeffersonianum. Of the species that autotomize, H. scutatum has a specialized constriction site at the tail base. We investigated whether aquatic larvae exhibit vertebral features similar to those previously described for aquatic adults and examined the effect of metamorphosis, if any, on vertebral morphology and the ontogeny of specialized vertebral features associated with tail autotomy. Interspecific comparisons of cleared-and-stained specimens indicate that vertebral morphology differs dramatically at hatching and that caudosacral and caudal vertebrae undergo continuous ontogenetic change throughout larval, metamorphic, and juvenile periods. Larvae and juveniles of H. scutatum do not exhibit adult vertebral features associated with constricted-base tail autotomy. The pond-type larvae of A. jeffersonianum and H. scutatum have tapering centrum lengths posterior to the sacrum. This pattern is functionally associated with aquatic locomotion. The stream-type larvae of D. ocoee undergo enhanced regional growth in the anterior tail such that the anterior caudal centra become longer than the preceding caudosacral centra. With the exception of the first two caudal vertebrae, a similar growth pattern occurs in H. scutatum adults. We hypothesize that enhanced growth of the anterior caudal segments is associated with tail elongation and autotomy.     

Sexual dimorphism of tail length in lacertid lizards: test of a morphological constraint hypothesis

Males of many lizard species have longer tails than similarly-sized females. We hypothesized that this dimorphism is induced by a longer non-autotomous tail part in males, which is associated with the presence of the copulatory organs at the tail base, and presumably reduces the males' ability to escape predation by tail shedding. A compensatory mechanism would be an increase of total tail length in males, to achieve equal lengths of the autotomous tail part in both sexes. A critical prediction of this 'morphological constraint' hypothesis is that the extent of dimorphism in total tail length increases with the magnitude of sexual differences in length of the non-autotomous tail base. We tested this prediction through a comparative study in a small clade of lacertid lizards. Within each of nine species, sexual differences in length of the non-autotomous tail base and in total tail length do not change with body size. All species, except one, exhibit a clear male-biased dimorphism in length of the non-breakable tail base. In all species studied, males have longer tails than females. We used the method of phylogenetically independent contrasts to explore the interspecific relation between dimorphism in length of the tail base and sexual differences in total tail length. Contrary to our prediction, we found no evidence for a positive correlation between the extent of dimorphism in both traits. Thus, constraints imposed by the male copulatory organs on tail autotomy do not seem to be a significant factor in the evolution of dimorphism in tail length in this clade of lacertid lizards.     

Distribution of energy reserves in a viviparous skink: Does tail autotomy involve the loss of lipid stores?

Abstract Caudal autotomy is an effective defensive strategy used by many lizards to facilitate escape during predatory encounters. However, it has several potentially severe consequences, including a range of energetic costs that are believed to result from the depletion of caudal lipid reserves during tail loss. In this study we examined the possible effect of caudal autotomy on the energetic reserves of a small viviparous skink, Niveoscincus metallicus (O'Shaughnessy 1874). Animals of each sex were collected on three occasions to assess the distribution of lipid stores. In addition, the frequency and position of naturally occurring tail breaks were determined. Both abdominal and caudal lipid stores are present in N. metallicus; however, caudal fat bodies comprise the majority (55–78%) of these fat reserves. Temporal variation in fat body mass, both abdominal and caudal, was evident. There was a significant relationship between the two fat stores, which was distorted in pregnant females, when relatively more fat was stored in the tail. Examination of the distribution of caudal fat in the tail revealed that the majority (90–95%) occurs within the proximal third of the tail. The remainder is located in the middle portion of the tail, with no reserves in the most distal tail section. During late pregnancy, females store relatively more fat closer to the body. The frequency of tail loss in a natural population of N. metallicus was extremely high (78%). Tail breaks were normally distributed along the length of the tail (i.e. most near the middle and fewer distal and proximal breaks). Thus there was a relatively high chance of some lipid depletion as a result of tail loss, but because 76% of breaks occur in the middle and distal thirds of the tail, there is a high probability that tail loss results in only minimal (i.e. <10%) lipid depletion. This is the first instance where both the energetic ‘value’ of the tail and the likelihood of lipid depletion during tail loss have been determined in a lizard. Overall, the combination of the aggregation of caudal fat reserves and position of naturally occurring tail breaks may enable N. metallicus to combine caudal fat storage and tail autotomy with minimal conflict.     

The process of total tail autotomy in the South-American rodent, Proechimys

Tail autotomy in Proechimys cuvieri was studied both morphologically and histologically. The rupture always occurs at the base of the external tail, e.g. in the immediate vicinity of its junction with the body. It thus concerns the whole caudal appendage. The distal epiphysis is separated from the fifth caudal vertebra and lost with the rest of the tail. There is no single reason responsible for the constancy of this breaking point, but several morphological factors can act together: these include strong binding of the five first caudal vertebrae to the body, disappearance of the plurisegmental muscles beyond this level, and the great extent and loose structure of the epiphyseal plates. Autotomy is a biological event occurring throughout the life of the animals, but it is of a cumulative nature. Tail loss is much more prevalent in older and heavier animals than in juveniles. Overall, about 9% of wild populations show this loss. Owing to the increasing percentage of occurrence from young to old, tail autotomy seems to enhance the survival chances of its owner, although direct proof of any predation influence are still lacking.     

Unique Structural Features Facilitate Lizard Tail Autotomy

Autotomy refers to the voluntary shedding of a body part; a renowned example is tail loss among lizards as a response to attempted predation. Although many aspects of lizard tail autotomy have been studied, the detailed morphology and mechanism remains unclear. In the present study, we showed that tail shedding by the Tokay gecko (Gekko gecko) and the associated extracellular matrix (ECM) rupture were independent of proteolysis. Instead, lizard caudal autotomy relied on biological adhesion facilitated by surface microstructures. Results based on bio-imaging techniques demonstrated that the tail of Gekko gecko was pre-severed at distinct sites and that its structural integrity depended on the adhesion between these segments.     

Variation of the number of proximal caudal vertebrae with tail reduction in Old World monkeys

Tail length in primates can vary greatly between species or even between local conspecific populations, and the tail is markedly reduced in several lineages. In Old World monkeys, tail length is considered as an important feature reflecting their phylogeny and adaptations. The number of caudal vertebrae is one of the important factors which determine tail length, and it is known that this number varies with tail length. Caudal vertebrae can be divided into two types (proximal and distal), and tail mobility and function are considered to be different in these two regions. Though the number of vertebrae in each region is important for understanding tail length evolution in Old World monkeys, there have been few attempts to investigate this matter. This study focused only on the proximal caudal vertebrae, which are more easily preserved than the distal ones, and tested if there is variation in their number with tail length or phylogenic differences. As a result, two important findings were obtained: (1) the variation of the number of proximal caudal vertebrae was different among the phylogenic groups, and (2) especially in Papionini, there was a great variation in the number of proximal caudal vertebrae, and it correlated strongly with relative tail length [RTL = (tail length/head and body length (sitting height)) × 100 %]. I speculate that these variations in the number of proximal caudal vertebrae were possibly caused by a change of the embryonic developmental mechanism of tail morphogenesis, a common mechanism of morphological evolution. To clarify the mechanisms and evolutionary trends of the variation in the proximal caudal vertebrae, not only morphological approaches but also developmental biological approaches will be necessary in the future.     

Handling-related tail loss in an endangered skink: incidence, correlates and a possible solution

Caudal autotomy (tail loss) during capture and handling is widely reported among several families of lizards. Autotomy causes elevated stress levels in lizards, and imposes a significant fitness cost on autotomized individuals. Despite these detrimental impacts, conservation and ethical issues associated with handling-related tail loss have received little attention. We assessed the incidence and correlates of tail autotomy during capture and handling in an endangered skink, the alpine she-oak skink Cyclodomorphus praealtus . A significant proportion (9.3%) of lizards autotomized their tails during capture and handling. Medium-sized lizards were more likely to lose their tails during handling, and this effect was exacerbated at intermediate body temperatures. Probability of autotomy had a complex relationship with cumulative observer experience, independent of other risk factors. Based on the modelled relationship of autotomy with body temperature, we propose that alpine she-oak skinks be cooled immediately after capture to reduce rates of autotomy during subsequent handling.