Cryptic sex? Estimates of genome exchange in unisexual mole salamanders (Ambystoma sp.).

Abstract

Cryptic sex has been argued to explain the exceptional longevity of certain parthenogenetic vertebrate lineages, yet direct measurements of genetic exchange between sexual and apparently parthenogenetic forms are rare. Female unisexual mole salamanders (Ambystoma sp.) are the oldest known unisexual vertebrate lineage (~5 million years), and one hypothesis for their persistence is that allopolyploid female unisexuals periodically exchange haploid genomes 'genome exchange' during gynogenetic reproduction with males from sympatric sexual species. We test this hypothesis by using genome-specific microsatellite DNA markers to estimate the rates of genome exchange between sexual males and unisexual females in two ponds in NE Ohio. We also test the prediction that levels of gene flow should be higher for 'sympatric' (sexual males present) genomes in unisexuals compared to 'allopatric' (sexual males absent) unisexual genomes. We used a model testing framework in the coalescent-based program MIGRATE-N to compare models where unidirectional gene flow is present and absent between sexual species and unisexuals. As predicted, our results show higher levels of gene flow between sexuals and sympatric unisexual genomes compared to lower (likely artefactual) levels of gene flow between sexuals and allopatric unisexual genomes. Our results provide direct evidence that genome exchange between sexual and unisexual Ambystoma occurs and demonstrate that the magnitude depends on which sexual species are present. The relatively high levels of gene flow suggest that unisexuals must be at a selective advantage over sexual forms so as to avoid extinction due to genetic swamping through genome exchange.