Genomic evidence suggests the balanced lethal system in Triturus newts originated in an instantaneous speciation event

Abstract

The balanced lethal system found in crested and marbled newts of the genus Triturus presents an intriguing mystery. All adults possess two distinct forms of their largest chromosome, resulting in 50% of offspring inheriting two copies of one of these forms. These homomorphic individuals undergo fatal developmental arrest during embryogenesis. How could such an obviously maladaptive trait, destroying half of an organism’s reproductive output, evolve? We construct a high-density linkage maps for Triturus and its sister genus Lissotriton, identifying genes involved in the balanced lethal system. We find that each of the two forms of Triturus chromosome 1 is characterized by a single massive deletion. Ploidy analysis shows that each deletion is compensated for by a duplication of the same region on the opposite chromosome. This suggests that the balanced lethal system was created suddenly, as the result of an unequal exchange between chromosomes in a single individual. We simulate the consequences of such a mutation, finding that, if the rearranged chromosomes exert a fitness penalty when combined with the ancestral version, a stable balanced lethal system can become fixed within a population. Counterintuitively, the deleterious nature of the rearranged chromosomes causes reproductive isolation that protects them from invasion by their fitter ancestor. We conclude that the origin of the Triturus balanced lethal system is effectively an instantaneous speciation event, which resulted in the fixation of the balanced lethal system.