Genetic drift and mutational hazard in the evolution of salamander genomic gigantism

Abstract

GENETIC DRIFT AND MUTATIONAL HAZARD IN THE EVOLUTION OF SALAMANDER GENOMIC GIGANTISMSalamanders have the largest nuclear genome sizes among tetrapods and, with the exception of lungfishes, among vertebrates as a whole. Lynch and Conery (2003) have proposed the mutational hazard hypothesis to explain variation in genome size and complexity. Under this hypothesis, non-coding DNA imposes a selective cost by increasing the target for degenerative mutations, i.e. the mutational hazard. Expansion of non-coding DNA, and thus genome size, is expected to be driven by increased levels of genetic drift and/or decreased mutation rates; the former determines the efficiency with which excess non-coding DNA can be selected against, while the latter determines the level of mutational hazard. Here, we test the hypothesis that salamanders have experienced stronger long-term, persistent genetic drift than frogs, a clade with more typically sized vertebrate genomes. To test this hypothesis, we compared dN/dS and Kr/Kc values between these clades. Our results reject this hypothesis; we find that salamanders have not experienced stronger genetic drift than frogs. Additionally, we find evidence consistent with a lower nucleotide substitution rate in salamanders. This result, along with previous work showing lower rates of small deletions and ectopic recombination in salamanders, suggests that a lower mutational hazard may contribute to genome expansion in this clade. Taken together, these results further underscore the importance of studying large genomes and indicate that salamanders provide an important model system for the study of how non-drift processes (i.e. mutation, natural selection) shape the evolution of genome size.iii ACKNOWLEDGEMENTS I would like to thank my parents, Roger and Susan. My father instilled in me the sense of wonder and curiosity that guide my life and work. My mother has been my biggest supporter since day one (literally), and none of this would have been possible without her love.

Genome diversity and species richness in mammals

“…The large salamander genomes, and other giant genomes in plants and insects, have been attributed to a slow deletion rate of DNA (Bensasson, Petrov et al 2001, Sun, López Arriaza et al 2012, Kelly, Renny-Byfield et al 2015, suggesting that these genomes are genetically more stable compared to taxa with smaller genomes. In the case of salamanders, the slow loss of DNA has been associated with significantly lower mutation rates in these organisms compared to other vertebrates (Mohlhenrich and Mueller 2016). Other studies have shown a similar negative relationship between genome size and mutation rates (Dores, Sollars et al 1999, Herrick andSclavi 2014), but the exact nature of the relationship, if any, remains to be elucidated.…”

Is There an Upper Limit to Genome Size?

“…Insights into how their genomes are structured and function therefore remain limited [e.g. 12, [13][14][15].…”

“…Certainly, recent studies (e.g. genome skimming approaches using high throughput sequencing technologies) of giant genomes in animals and plants suggest that the composition, regulation and evolution of their genomes may be following different trajectories compared with species possessing smaller genomes [12][13][14][15]27].…”

The Evolution Force of Genome Reduction in Carnivorous Plants

“…Therefore, there was still some controversy about the mutational-hazard hypothesis (Whitney and Garland 2010;Cohen et al, 2012). For example, Mohlhenrich analyzed the non-coding genes of salamanders and frogs, he concluded that the mutational hazard did not play a mainly role in the genomic gigantism of salamanders (Mohlhenrich and Mueller, 2016). But there are still some studies that support the mutational-hazard hypothesis.…”