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

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.

A linkage map for the Newt Notophthalmus viridescens: Insights in vertebrate genome and chromosome evolution

“…In total, our low-coverage laser capture sequence data support six linkage groups as corresponding to discrete chromosomes (LGs 1, 2, 8, 9, 10 11), whereas other chromosomes could not be directly resolved at current sampling depths (Supplementary Figure 3). The relatively large size of the newt linkage map and individual LGs is consistent with previous linkage analyses in another salamander species ( Ambystoma ) and microscopic observations of chiasmata in salamander oocytes (Callan, 1966; Smith et al, 2005; Voss et al, 2011). As such, the large recombinational size of the newt linkage map lends support to the idea that the ancestral salamander genome expansion resulted in a proportional increase in rates of meiotic recombination (Smith et al, 2005; Voss et al, 2011).…”

“…As previously observed, many conserved segments correspond to large portions of chicken macrochromosomes or entire microchromosomes. Previous analyses showed that these segments and microchromosomes were derived from individual chromosomes that trace their ancestry at least to the common ancestor of all bony vertebrates (Braasch et al, 2016; Venkatesh et al, 2014; Voss et al, 2011). By examining the distribution of these conserved segments in newt, Ambystoma and Xenopus , it is possible to reconstruct several evolutionary events that define the karyotypes of these three model amphibian taxa (Table 1).…”

“…Linkage maps are valuable resources that not only facilitate the identification of QTL and mapped-based cloning, they are also useful for reconstructing the evolution of chromosomal rearrangements and chromosome number. Comparative mapping studies have leveraged the Ambystoma linkage map to reveal insights about vertebrate genome evolution (Smith and Voss, 2006; Voss et al, 2011; Voss et al, 2001). These studies found extensive conservation of microchromosomes and chromosomal segments from the tetrapod ancestor and independent decreases in chromosome number among lineages leading to Ambystoma, Xenopus and mammals.…”

“…This increase in size is thought to reflect an ancient expansion of repetitive DNA sequences (Keinath et al, 2015). This expansion appears to have affected salamander genome structure in a global sense because introns, intergenic regions and linkage map size are dramatically expanded in the axolotl (Smith et al, 2005; Smith et al, 2009; Voss et al, 2011). Interestingly, genome expansion does not appear to influence the rate of chromosome evolution.…”

Neuronal Regeneration from Ependymo-Radial Glial Cells: Cook, Little Pot, Cook!

“…A prominent model species is the axolotl (Ambystoma mexicanum), which is neotenic, that is it retains larval features as an adult, such as gills and larval skin histology, but is fully capable of reproduction. Metamorphosis can be induced by injection of thyroxine, which, however, has little influence on their regenerative capacity (Ehrlich and Mark, 1977;Voss et al, 2013). Salamanders regenerate their spinal cord as adults (Butler and Ward, 1967;Diaz Quiroz and Echeverri, 2013).…”