Evidence of Late Pleistocene origin of Astyanax mexicanus cavefish

Abstract

BackgroundCavefish populations belonging to the Mexican tetra species Astyanax mexicanus are outstanding models to study the tempo and mode of adaptation to a radical environmental change. They share similar phenotypic changes such as blindness and depigmentation resulting from independent and convergent evolution. As such they allow examining whether their evolution involved the fixation of preexisting standing genetic variations and/or de novo mutations. Cavefish populations are currently assigned to two main groups, the so-called \"old\" and \"new\" lineages, which would have populated several caves independently and at different times. However, we do not have yet accurate estimations of the time frames of evolution of these populations.\n\nResultsFirst, we reanalyzed the geographic distribution of mitochondrial and nuclear DNA polymorphisms and we found that these data do not support the existence of two cavefish lineages, neither the ancient origin of the \"old\" lineage. Using IMa2, a program based on a method that does not assume that populations are at mutation/migration/drift equilibrium and thus allows dating population divergence in addition to demographic parameters, we found that microsatellite polymorphism strongly supports a very recent origin of cave populations (i.e. less than 20,000 years). Second, we identified a large number of single-nucleotide polymorphisms (SNPs) in transcript sequences of pools of embryos (Pool-seq) belonging to the \"old\" Pachon cave population and a surface population from Texas. Pachon cave population has accumulated more neutral substitutions than the surface population and we showed that it could be another signature of its recent origin. Based on summary statistics that can be computed with this SNP data set together with simulations of evolution of SNP polymorphisms in two recently isolated populations, we looked for sets of demographic parameters that allow the computation of summary statistics with simulated populations that are similar to the ones with the sampled populations. In most simulations for which we could find a good fit between the summary statistics of observed and simulated data, the best fit occurred when the divergence between simulated populations was less than 30,000 years.\n\nConclusionsAlthough it is often assumed that some cave populations such as Pachon cavefish have a very ancient origin, within the range of the late Miocene to the middle Pleistocene, a recent origin of these populations is strongly supported by our analyses of two independent sets of nuclear DNA polymorphism using two very different methods of analysis. Moreover, the observation of two divergent haplogroups of mitochondrial and nuclear genes with different geographic distributions support a recent admixture of two divergent surface populations before the isolation of cave populations. If cave populations are indeed only several thousand years old, many phenotypic changes observed in cavefish would thus have mainly involved the fixation of genetic variants present in surface fish populations and within a very short period of time.