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. 2013 Jul 3;8(7):e67274.
doi: 10.1371/journal.pone.0067274. Print 2013.

Variation in Salamander Tail Regeneration Is Associated With Genetic Factors That Determine Tail Morphology

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Free PMC article

Variation in Salamander Tail Regeneration Is Associated With Genetic Factors That Determine Tail Morphology

Gareth J Voss et al. PLoS One. .
Free PMC article

Abstract

Very little is known about the factors that cause variation in regenerative potential within and between species. Here, we used a genetic approach to identify heritable genetic factors that explain variation in tail regenerative outgrowth. A hybrid ambystomatid salamander (Ambystoma mexicanum x A. andersoni) was crossed to an A. mexicanum and 217 offspring were induced to undergo metamorphosis and attain terrestrial adult morphology using thyroid hormone. Following metamorphosis, each salamander's tail tip was amputated and allowed to regenerate, and then amputated a second time and allowed to regenerate. Also, DNA was isolated from all individuals and genotypes were determined for 187 molecular markers distributed throughout the genome. The area of tissue that regenerated after the first and second amputations was highly positively correlated across males and females. Males presented wider tails and regenerated more tail tissue during both episodes of regeneration. Approximately 66-68% of the variation in regenerative outgrowth was explained by tail width, while tail length and genetic sex did not explain a significant amount of variation. A small effect QTL was identified as having a sex-independent effect on tail regeneration, but this QTL was only identified for the first episode of regeneration. Several molecular markers significantly affected regenerative outgrowth during both episodes of regeneration, but the effect sizes were small (<4%) and correlated with tail width. The results show that ambysex and minor effect QTL explain variation in adult tail morphology and importantly, tail width. In turn, tail width at the amputation plane largely determines the rate of regenerative outgrowth. Because amputations in this study were made at approximately the same position of the tail, our results resolve an outstanding question in regenerative biology: regenerative outgrowth positively co-varies as a function of tail width at the amputation site.

Conflict of interest statement

Competing Interests: The authors have declared that no competing interests exist.

Figures

Figure 1
Figure 1. A representative tail tip that was sampled during the process of regeneration.
The picture shows areas that were measured proximal and distal to the amputation plane.
Figure 2
Figure 2. Plot showing the amount of tail tissue regenerated after the first (300 days post fertilization - dpf) and second (351 dpf) amputations.
Spearman’s correlation coefficients (r) are shown for males and females.
Figure 3
Figure 3. Plot showing the average amount of tail tissue regenerated after the first (300 dpf) and second (351 dpf) tail amputations for males and females.
The error bars are standard deviations.
Figure 4
Figure 4. Plot showing the average width of tail area proximal to the amputation plane after the first (300 dpf) and second (351 dpf) tail amputations for males and females.
The error bars are standard deviations.
Figure 5
Figure 5. LOD plots of QTL scans for tail width (A) and tail outgrowth (B) at 351 dpf. Markers defining 16 ambystomatid linkage groups are concatenated on the x-axis.
The black lines reference QTL scans after the effect of sex was removed by treating the sex-determining locus (ambysex) as an additive covariate. Horizontal dashed lines show QTL significance thresholds (p = 0.05).

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