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Garza-Garcia, A. Evidence for the local evolution of mechanisms underlying limb regeneration in salamanders. Geng, J. Identification of the orphan gene Prod 1 in basal and other salamander families. Evodevo Ghosh, S.
Analysis of the expression and function of Wnt-5a and Wnt-5b in developing and regenerating axolotl Ambystoma mexicanum limbs. Godwin, J. Chasing the recipe for a pro-regenerative immune system. Scar-free wound healing and regeneration in amphibians: immunological influences on regenerative success. Differentiation 87, 66— Goss, R. The evolution of regeneration: adaptive or inherent? Grigoryan, E. High regenerative ability of tailed amphibians Urodela as a result of the expression of juvenile traits by mature animals.
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Reddien, P. Identification of genes needed for regeneration, stem cell function, and tissue homeostasis by systematic gene perturbation in Planaria. Cell 8, — Reddy, P. Cellular and molecular mechanisms of hydra regeneration. Results Prob. Cell Differ. Reinhardt, B. Robert, J. Comparative and developmental study of the immune system in Xenopus. Regeneration in the metazoans: why does it happen? Bioessays 22, — Sattler, S.
The neonate versus adult mammalian immune system in cardiac repair and regeneration. Acta Mol. Cell Res. Seifert, A. The influence of fundamental traits on mechanisms controlling appendage regeneration. The blastema and epimorphic regeneration in mammals. Sidorova, V. Slack, J. Animal regeneration: ancestral character or evolutionary novelty?
EMBO Rep. Sunderland, M. Suzuki, Y. Evolution and regulation of limb regeneration in arthropods. Results Probl. Tiozzo, S. Reconsidering regeneration in metazoans: an evo-devo approach. Tokin, B. In some animal groups, the case for loss of regeneration is quite strong. One of the clearest examples comes from a recent study on annelids indicating that multiple losses of the ability to regenerate the head have occurred within a subfamily of aquatic clitellates, the Naidinae Bely and Sikes ; see penultimate section.
Mapping results onto a molecular phylogeny indicated that three losses of the ability to regenerate the head have occurred in this group.
Although this study represents the first to explicitly map regenerative ability onto a phylogeny as a means of reconstructing the pattern of losses, data from several other groups suggest additional likely losses when interpreted in the context of current understanding of phylogenetic relationships.
For example, in lepidosaur vertebrates lizards and close relatives , the ability to regenerate the tail is widespread, having been reported in the tuatara the sister group to the rest of the lepidosaurs , geckos, skinks, iguanids, some agamids, chameleons, and lacertids, but it appears to be absent in a few groups, including snakes, amphisbaenids, and some agamids Gans ; Arnold ; Bellairs and Bryant ; Seligmann et al.
Based on a recent phylogeny of the group Vidal and Hedges , this distribution strongly suggests that tail regeneration is ancestral for lepidosaurs and that the non-regenerating groups likely represent at least three independent losses of the ability to regenerate the tail. Further support for tail regeneration being ancestral and thus for the lack of tail regeneration being derived comes from the regeneration process itself.
When regeneration of the tail occurs in lepidosaurs, it consistently produces a regenerated tail that is distinctly different from the original; most notably, the regenerated tail has a continuous, cartilaginous rod at its center rather than an articulated column composed of vertebrae Etheridge ; Arnold ; Bellairs and Bryant ; Seligmann et al. The distribution of regeneration of fins in fish provides another likely example of regeneration loss.
Fin regeneration occurs in lungfish an outgroup to the teleosts , salmoniforms and esociforms which together likely represent the sister group to the spiny-rayed teleosts , and numerous species of spiny-rayed teleosts the most diverse group of living teleosts , including the cyprinodontiforms, atheriniforms, and perciforms Wagner and Misof and references therein.
However, regeneration of fins appears to be absent or heteromorphic producing a misshapen, abnormal fin in representatives of at least three groups of spiny-rayed teleosts: the scorpaeniforms, the cyprinodontiforms, and the perciforms Wagner and Misof In the context of a recent summary of fish phylogeny Nelson , this distribution would suggest that regeneration of fins is ancestral for fish and that there have been multiple losses of normal fin regeneration.
A number of additional animal groups are known to possess a mix of species sometimes even very closely related species that can and cannot regenerate a specific body region, a pattern suggestive of loss of regeneration. Although it is likely that many of the non-regenerating taxa represent losses of regeneration, better sampling and formal phylogenetic mapping are needed in most cases to provide evidence for this. Finally, although comparisons of regeneration among phyla are inherently problematic, owing to the extreme morphological disparity among groups, a broad, phylum-level view of animal regeneration nevertheless suggests that an important restriction in regenerative ability occurred near the base of the Ecdysozoa, the molting clade of bilaterians.
Furthermore, while there is ample evidence that a broad range of body structures e. Regeneration of appendages occurs in many, although by no means all, arthropods, and because regeneration in arthropods depends on molting, no regeneration can occur in individuals after their terminal molt. The inferred restriction of regenerative ability near the base of the Ecdysozoa likely represents the oldest major loss of regeneration represented among metazoans, and may have been related to the evolution of the protective cuticle characteristic of this clade.
Very little work has been aimed at understanding the process of regeneration loss, and we therefore know little about why and how this process occurs. For well over a century there has been speculation about the factors leading to loss of regeneration Morgan ; Dinsmore ; Goss ; Wagner and Misof ; Bely and Nyberg , but there remains a real need to define and evaluate specific evolutionary and developmental scenarios that could account for this phenomenon.
To begin developing a framework for investigating this process, below I discuss some possible scenarios for both why and how regeneration could be lost. It will be important to evaluate such scenarios using actual data, ideally by investigating very recent losses in which the signatures of regeneration loss are most likely to still be detectable. With regard to the ultimate, or evolutionary, causes of regeneration loss, a range of possible explanations have recently been outlined and discussed Bely and Nyberg In summary, regeneration could be lost either because it is selected against in some way, or because it is a neutral trait.
Regeneration could also be disfavored indirectly, for example if there is an energetic trade-off between regeneration and another process, such as growth e. Adaptive explanations need not be invoked for loss of regeneration, however. If regeneration confers no significant selective advantage, then it could be lost as a neutral trait. A straightforward scenario under which regeneration might be neutral is if the structure in question is infrequently lost or damaged in nature.
There is ample evidence that even traits recently under strong selection can be rapidly lost or modified when selection in the wild becomes relaxed Lahti et al.
Sublethal predation is a prevalent cause of regeneration in nature Lindsay , and thus this is presumably a common selective force maintaining regeneration. A simple change in predator-prey dynamics that decreases the frequency of sublethal predation in a population could therefore lead to regeneration no longer being actively maintained.
Regeneration could also be neutral if the functional importance of the structure in question is so high that the animal cannot survive without it long enough to regenerate it, or so low that the structure is not worth replacing given the costs of replacement Goss ; Reichman Neutral loss of regeneration could also occur if previously tight developmental pleiotropies between regeneration and another process e.
This scenario could explain decreases in regenerative ability that correlate with changes in morphology or changes in the developmental processes underlying the morphology.
Distinguishing between these possible ultimate explanations for loss of regeneration is no small task. Doing so will require collecting and integrating functional, ecological, and developmental data for both regenerating and non-regenerating species, preferably closely related ones.
Only by tackling this problem with hypothesis testing and actual data, however, can we begin moving away from the pervasive speculation that has thus far characterized discussions about the ultimate causes of regeneration loss. Uncovering the proximate causes of regeneration loss involves deciphering which steps of regeneration have become abrogated. Some of the broader questions we should be aiming to address with such data include: Does regeneration fail in different ways in different groups of animals?
Are certain steps of regeneration particularly prone to becoming blocked? Does loss of regeneration occur all at once or gradually, and, if the latter, what do intermediate stages of the process look like? The first step towards addressing these questions is to determine when and how the regenerative process halts or becomes abnormal. Does wound-healing fail?
Does a blastema the mass of undifferentiated cells from which new structures form not develop? Is the blastema improperly patterned? Is the regenerated structure missing certain functionally important elements? Although data are still limited, it is clear that failure to regenerate can manifest itself in a variety of ways and, interestingly, that there may be phylogenetic trends in how regeneration tends to fail.
Thus, available evidence suggests that regeneration may fail in predictable ways within a taxonomic group. This could occur if, within a given lineage, certain steps of the regenerative process are particularly prone to becoming blocked. Although loss of regeneration theoretically could occur by the evolution of a single mutation that completely abrogates regeneration, it is also possible that regeneration is lost gradually, with populations at successively more advanced stages of regeneration loss showing increasingly restricted or poorer regenerative abilities.
Specific hypotheses for how such gradual losses might occur need to be developed. It is already known that speed or success of regeneration can be sensitive to a variety of factors, such as the developmental age of the stump tissue and the energetic resources of the individual e.
In populations that are in the process of losing regenerative abilities, the success of regeneration could be contingent upon such factors as well, and, if so, identifying the specific factors that are still permissive of regeneration may point to an underlying mechanism for the loss. Figure 2 shows several possible scenarios for how regeneration success could change through time in a lineage that is gradually losing regenerative abilities. One possibility is that successful regeneration becomes increasingly restricted across the life cycle.
For example, regeneration could become restricted to earlier ontogenetic stages Fig. Another possibility is that the energetic threshold for investment in regeneration gradually increases Fig. Energetic tradeoffs between regeneration and other process, such as growth, are common Maginnis ; Lawrence , and if investment in other processes becomes favored at the expense of regeneration, the energy threshold for investment into regeneration could increase to the point that investment in regeneration effectively never occurs.
Yet another possibility is that the environmental conditions permissive of regeneration could become increasingly narrow Fig. For example, regeneration might only occur within an increasingly narrow range of temperature or salinity. Other models for a gradual loss of regeneration may involve less easily quantifiable factors. For instance, success in regeneration may correlate with the degree of pleiotropy between regeneration and a core process, such as embryogenesis.
If regeneration is being lost because this pleiotropy is breaking down, the fidelity of regenerated structures might gradually decrease through time. Models such as the ones shown in Fig. To test the validity of such models, the contingency of regeneration success on internal and external factors should be evaluated in taxa that have lost or appear to be losing regenerative abilities, as well as in closely related, fully-regenerating taxa which can serve as a proxy for the ancestral, fully-regenerating population.
Some hypothetical models for the gradual loss of regenerative abilities in a lineage. Graphs on the left A1, B1, and C1 show scenarios in which loss of regeneration is sensitive to a particular factor developmental stage, energy available in an organism, and environmental conditions ; graphs on the right A2, B2, and C2 show scenarios in which loss of regeneration is insensitive to these factors. Solid lines denote the ancestral condition; dashed and dotted lines denote populations progressively farther along on the trajectory to total loss of regeneration.
Curves for populations that have completely lost regenerative abilities would lie along the x -axis. The holy grail for understanding how regeneration has been lost is to identify the actual genetic change s responsible for the original failure of regeneration. Although this is an important goal, it is essential to recognize that once a block to normal regeneration has evolved in a lineage, rendering regeneration non-functional, additional blocks may rapidly accumulate.
Thus, in all but the most recently evolved cases of regeneration loss, regeneration is likely to fail for multiple reasons, and pinpointing the first block s responsible for the abrogation of regeneration will be challenging at best.
Currently no species are known that show natural, intraspecific variation in success of regeneration, but if such species can be identified, they will be extremely useful for elucidating the earliest steps of loss of regeneration at the molecular level.
Annelids exhibit extensive variation in regenerative ability, making them useful models for understanding regeneration loss. The ability to regenerate a new tail is widespread across the phylum, having been lost in only a few taxa Bely The ability to regenerate the head is much more variable, however, suggesting numerous losses. Evidence for regeneration of anterior segments was recently compiled for the phylum Bely By mapping this information onto a molecular phylogeny for the group from Struck et al.
There is still considerable uncertainty about the deep-level phylogeny of annelids Rousset et al. Some groups, most notably the Hirudinida and Nereididae, are large clades thought to be comprised entirely of species that cannot regenerate anterior segments; these taxa likely represent relatively old losses of the ability to regenerate anteriorly.
However, seven annelid families representing over one quarter of the families for which there are relevant data possess both anteriorly regenerating and anteriorly non-regenerating species Fig. As sampling for regenerative ability is increased, the number of suggested losses is likely to increase as well.
Groups in which regeneration has been lost relatively recently are particularly useful for investigating the mechanisms underlying the loss of regeneration. Phylogenetic distribution of anterior regeneration in the annelids across A the entire phylum and B the clitellate subfamily Naidinae. Phylogenetic relationships are based on A Struck et al. In A , all taxa are annelids, and most, although not all, groups represented are families.
In B , all species shown are naidines with the exception of the outgroups Monopylephorus , Pristina , Branchiura , Tubifex , and Lumbriculus. To identify recent regeneration losses rigorously, fine-scale sampling and detailed phylogenies must be obtained. Naidines are a group of small freshwater oligochaetes that reproduce asexually by fission, a process thought to have evolved from regeneration Bely and Wray Because several naidine species possess excellent abilities to regenerate both the anterior and posterior ends, and because naidines are all capable of asexual reproduction, it had long been assumed that this entire group consisted of excellent regenerators.
However, Bely demonstrated that at least one naidine species, Paranais litoralis , could not regenerate anterior segments, even though it could regenerate posterior segments. Following up on this study, Bely and Sikes sampled more widely within the naidines and found that six of the 18 naidine species investigated are incapable of regenerating the head segments.
Mapping these comparative data onto a robust, five-gene molecular phylogeny of the group indicates that these six species represent three independent losses of the ability to regenerate the head region, with the genera Paranais , Chaetogaster , and Amphichaeta each representing a loss Fig. It should be noted, however, that other phylogenetic studies of naidines, based on smaller datasets, indicate the possibility of fewer losses Bely and Wray ; Envall et al. One of the species found incapable of regenerating anterior segments, Chaetogaster diaphanus , is a common and abundant species and one of the naidine subjects of an early, thorough description focusing on fission and, to a lesser extent, regeneration Dehorne The microniche helps determine whether a stem cell will divide asymmetrically division of 1 stem cell into 1 daughter stem cell and 1 daughter cell that is committed to differentiate or symmetrically division of 1 adult stem cell into 2 daughter stem cells 4 Creation of Stem Cells via Dedifferentiation Cells that have already developed to their end fate differentiated cells are capable of turning back into adult stem cells dedifferentiation.
This is seen primarily in low order vertebrates such as fish, lizards, and amphibians. These organisms are able to regenerate limbs, tails, fins, jaws, parts of the eye, nerves, and intestine. Cells work by using signaling pathways to talk to themselves and to other cells within the body. It is this communication that enables our systems to operate as the giant symphony we know as the human body. For example, the endocrine system is spread over 8 different organs throughout the body that must communicate with each other on a constant basis.
These organs use signaling pathways throughout the bloodstream to interact and function as an entire system.
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