The genetic basis of vertebrate morphological evolution has traditionally been very difficult to examine in naturally occurring populations. Here we describe the generation of a genome-wide linkage map to allow quantitative trait analysis of evolutionarily derived morphologies in the Mexican cave tetra, a species that has, in a series of independent caves, repeatedly evolved specialized characteristics adapted to a unique and well-studied ecological environment. We focused on the trait of albinism and discovered that it is linked to Oca2, a known pigmentation gene, in two cave populations. We found different deletions in Oca2 in each population and, using a cell-based assay, showed that both cause loss of function of the corresponding protein, OCA2. Thus, the two cave populations evolved albinism independently, through similar mutational events.
A study of genetic diversity at microsatellite loci and the mitochondrial DNA (mtDNA) cytochrome b gene was carried out to assess genetic relationships among four Mexican cave (Pachon, Sabinos, Tinaja, Chica) and four surface populations of Astyanax fasciatus (Characidae) from northeast Mexico and the Yucatan. With the exception of Chica, the cave populations were all characterized by extremely low microsatellite variability, which most likely resulted from bottleneck events. Population analyses of the microsatellite data indicated no measurable levels of gene flow between all cave and surface populations (F(ST) > 0.0707). Phylogenetic analyses of mtDNA data showed that only two cave populations - Sabinos and Tinaja - group together to the exclusion of surface populations. From the microsatellite data these cave populations cluster with the Pachon cave fish population. The mtDNA thus appears to have been replaced in Pachon because of introgressive hybridization. It is likely that these three cave populations have descended from a surface ancestor in common with current surface populations, rather than evolving recently from one of the extant surface populations. Like Pachon, the Chica population clustered with the surface populations according to mtDNA data, but was not clearly associated with either the surface or the other cave populations according to the microsatellite data. Our data indicate that the Chica population evolved recently from a surface population, and subsequently hybridized with a phylogenetically older cave population. In conclusion, both the microsatellite and mtDNA data suggest multiple origins of cave populations and the Chica and Sabinos/Tinaja/Pachon were founded after at least two independent invasions from surface populations.
More than 20 populations of the cave-dwelling characid Astyanax occur within a restricted karst area in Mexico. The fish possess reduced eyes without lenses and visual cells. It is still an open question as to whether this condition evolved convergently after multiple entries of the surface ancestor into the different caves or whether a single cave ancestor, already characterized by reduced eyes, spread secondarily within them. In the crosses between specific populations, specimens appear that deviate considerably from those of the parents. They possess larger and better-developed eyes with histologically intact lenses and visual cells; they thus have the structural potential for vision. This indicates that in different cave populations, different mutations in the eye gene system have occurred. In cases where these non-functional rudimentary genes are recombined in hybrid specimens, gene expression may be restored. This is the result of separate evolution of several Astyanax cave populations.
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