Comprehensive Analysis of Salamander Hybridization Suggests a Consistent Relationship between Genetic Distance and Reproductive Isolation across Tetrapods
Hybridization between populations along the path to complete reproductive isolation can provide snapshots of speciation in action. Here, we present a comprehensive list of salamander hybrids and estimate genetic distances between the parental hybridizing species using one mitochondrial and one nuclear gene (MT-CYB and RAG1). Salamanders are outliers among tetrapod vertebrates in having low metabolic rates and highly variable sex chromosomes. Both of these features might be expected to impact speciation; mismatches between the mitochondrial and nuclear genomes that encode the proteins for oxidative metabolism, as well as mismatches in heteromorphic sex chromosomes, can lead to reproductive isolation. We compared the genetic distances between hybridizing parental species across four main tetrapod groups that differ in metabolic rates and sex chromosome diversity: salamanders, lizards, mammals, and birds. Our results reveal no significant differences, suggesting that variation in these traits across vertebrates does not translate into predictable patterns of genetic divergence and incompatible loci in hybrids.

Salamander hybrids are found in most families (Pyron and Wiens, 2011). About 12.1% of salamanders are known to hybridize with over half belonging to Plethodontidae. There was no significant correlation between the number of papers per species and the proportion of salamanders found to hybridize (Kendall's rank correlation P = 0.236).

(A) Histogram of cytochrome b (MT-CYB) genetic distance estimates (HKY85 + Γ) between salamanders that hybridize. Graph bin width is 0.0125. (B) Ratio of mitochondrial MT-CYB genetic distance to nuclear recombination activating 1 (RAG1) genetic distance between parental species of salamanders that hybridize on a log scale. The ratio of genetic distance ranged from 0.6 to 162 with the majority of species pairs having a higher mitochondrial genetic distance (median = 21.1).

Cytochrome b (MT-CYB) genetic distances between parental species that hybridize in different tetrapod groups. Kruskal-Wallis H test showed no significant differences across the groups (P = 0.661). Salamanders are not hybridizing across greater genetic distances.

Genetic distance ratio of mitochondrial cytochrome b (MT-CYB) to nuclear recombination activating 1 (RAG1) for pairs of species that hybridize in major tetrapod clade on a log scale. Kruskal-Wallis H test showed no strong significant differences across the four groups (P = 0.108).

Genetic distances between salamanders that hybridize with heteromorphic sex chromosomes (median = 0.109) and salamanders that hybridize without sex chromosomes (median = 0.152). There is no significant difference (P = 0.5293) between salamanders with sex chromosomes and salamanders without sex chromosomes.
Contributor Notes