Evolutionary aspects of tail shedding in lizards and their relatives

Arnold, E. N.

doi:10.1080/00222938400770131

Cited by 292 publications

(390 citation statements)

References 51 publications

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“…Although many animals capable of agametic reproduction have extraordinary regenerative abilities (21), and asexual and regenerative developmental processes can overlap substantially (1,11,25), naidines clearly demonstrate that regeneration is far from universal among agametically reproducing species, even in species, such as naidines, in which agametic reproduction is derived from regeneration (26). Furthermore, naidines join the small but growing list of examples showing that loss of regenerative abilities is not necessarily accompanied by large-scale changes in morphological complexity (2,4,5,12). Naidines all share a similar body plan, and species that cannot regenerate do not differ in any consistent way from fully regenerating species.…”

Section: Discussionmentioning

confidence: 99%

“…Large groups such as nematodes, birds, mammals, and leeches, for example, are largely or entirely incapable of regenerating any body part, indicating relatively old losses of regeneration. Many other, more recent losses of regeneration have also occurred, for example, among annelids, arthropods, planarians, fishes, and lizards (2)(3)(4)(5)(6). Despite longstanding interest in the process of animal regeneration (7,8), over a century of speculation on the root causes of variation in this feature (1,4,9), and recent advances in understanding its developmental and molecular basis (10,11), we still know little about the evolutionary and developmental processes involved in regeneration loss.…”

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confidence: 99%

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Latent regeneration abilities persist following recent evolutionary loss in asexual annelids

Bely

Sikes

2009

Proc. Natl. Acad. Sci. U.S.A.

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Regeneration abilities have been repeatedly lost in many animal phyla. However, because regeneration research has focused almost exclusively on highly regenerative taxa or on comparisons between regenerating and nonregenerating taxa that are deeply diverged, virtually nothing is known about how regeneration loss occurs. Here, we show that, following a recent evolutionary loss of regeneration, regenerative abilities can remain latent and still be elicited. Using comparative regeneration experiments and a molecular phylogeny, we show that ancestral head regeneration abilities have been lost three times among naidine annelids, a group of small aquatic worms that typically reproduce asexually by fission. In all three lineages incapable of head regeneration, worms consistently seal the wound but fail to progress to the first stage of tissue replacement. However, despite this coarse-level convergence in regeneration loss, further investigation of two of these lineages reveals marked differences in how much of the regeneration machinery has been abolished. Most notably, in a species representing one of these two lineages, but not in a representative of the other, amputation within a narrow proliferative region that forms during fission can still elicit regeneration of an essentially normal head. Thus, the presence at the wound site of elements characteristic of actively growing tissues, such as activated stem cells or growth factors, may permit blocks to regeneration to be circumvented, allowing latent regeneration abilities to be manifested. regeneration loss | Annelida | asexual reproduction | evolution

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Section: Discussionmentioning

confidence: 99%

mentioning

confidence: 99%

Latent regeneration abilities persist following recent evolutionary loss in asexual annelids

Bely

Sikes

2009

Proc. Natl. Acad. Sci. U.S.A.

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“…Many amphibians (Scadding 1980), reptiles (Arnold 1984;Bellairs & Bryant 1985), fishes ( Wagner & Misof 1992) and arthropods (Needham 1953;Needham 1965;Bulliere & Bulliere 1985;Vollrath 1990) have the ability to regenerate lost legs or tails, and these appendages can comprise up to 40% of an individual's biomass. Since appendage regeneration requires the allocation of resources, this process can have profound consequences.…”

Section: Introductionmentioning

confidence: 99%

Leg regeneration stunts wing growth and hinders flight performance in a stick insect ( Sipyloidea sipylus )

Maginnis

2006

Proc. R. Soc. B.

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Major morphological structures are sometimes produced not once, but twice. For example, stick insects routinely shed legs to escape a predator or tangled moult, and these legs are subsequently re-grown. Here, I show that in Sipyloidea sipylus, re-growth of a leg during development causes adults to have disproportionately smaller wings and increases wing loading. These morphological consequences of leg regeneration led to significant reductions in several biologically relevant measures of individual flight performance. This previously unrecognized tradeoff between legs and wings reveals the integrated nature of phasmid phenotypes, and I propose how this tradeoff may have shaped phasmid evolution.

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“…Animals were not anesthetized for the autotomy so that tail separation would occur at natural fracture planes with minimal trauma, postautotomy physiological recuperative processes would function normally, and the force/stimulus required to induce autotomy would be minimized (Arnold 1984). We also note that a large percentage of the natural population we examined demonstrated evidence of previous tail autotomy.…”

Section: Ethical Notementioning

confidence: 99%

“…On loss of their tail, lizards may incur a number of costs (reviewed in Arnold 1984Arnold , 1988Bateman and Fleming 2008). Many lizard species demonstrate a decrease in running speed following autotomy (Pond 1978;Ballinger et al 1979;Punzo 1982;Formanowicz et al 1990;Martín and Avery 1998;Downes and Shine 2001;Chapple and Swain 2002b;Shine 2003;Cooper et al 2004;Lin and Ji 2005).…”

Section: Energetics Of the Cape Dwarf Gecko Lygodactylus Capensis (Gementioning

confidence: 99%

Jettisoning Ballast or Fuel? Caudal Autotomy and Locomotory Energetics of the Cape Dwarf GeckoLygodactylus capensis(Gekkonidae)

Fleming

Verburgt²,

Scantlebury

et al. 2009

Physiological and Biochemical Zoology

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Many lizard species will shed their tail as a defensive response (e.g., to escape a putative predator or aggressive conspecific). This caudal autotomy incurs a number of costs as a result of loss of the tail itself, loss of resources (i.e., stored in the tail or due to the cost of regeneration), and altered behavior. Few studies have examined the metabolic costs of caudal autotomy. A previous study demonstrated that geckos can move faster after tail loss as a result of reduced weight or friction with the substrate; however, there are no data for the effects of caudal autotomy on locomotory energetics. We examined the effect of tail loss on locomotory costs in the Cape dwarf gecko Lygodactylus capensis (∼0.9 g) using a novel method for collecting data on small lizards, a method previously used for arthropods. We measured CO 2 production during 5-10 min of exhaustive exercise (in response to stimulus) and during a 45-min recovery period. During exercise, we measured speed (for each meter moved) as well as total distance traveled. Contrary to our expectations, tailless geckos overall expended less effort in escape running, moving both slower and for a shorter distance, compared with when they were intact. Tailless geckos also exhibited lower excess CO 2 production (CO 2 production in excess of normal resting metabolic rate) during exercising. This may be due to reduced metabolically active tissue (tails represent 8.7% of their initial body mass). An alternative suggestion is that a change in energy substrate use may take place after tail loss. This is an intriguing finding that warrants future biochemical investigation before we can predict the relative costs of tail loss that lizards might experience under natural conditions.

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Evolutionary aspects of tail shedding in lizards and their relatives

Cited by 292 publications

References 51 publications

Latent regeneration abilities persist following recent evolutionary loss in asexual annelids

Latent regeneration abilities persist following recent evolutionary loss in asexual annelids

Leg regeneration stunts wing growth and hinders flight performance in a stick insect ( Sipyloidea sipylus )

Jettisoning Ballast or Fuel? Caudal Autotomy and Locomotory Energetics of the Cape Dwarf GeckoLygodactylus capensis(Gekkonidae)

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