The Role of Nuclear Genes in Intraspecific Evolutionary Inference: Genealogy of the transferrin Gene in the Brown Trout

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Abstract
Technical and biological hurdles have precluded the retrieval of nuclear gene genealogies within most species. Among these obstacles, the possibility of intragenic recombination is one of the most demanding challenges. We studied the utility of nuclear genes for intraspecific evolutionary inferences by selecting a nuclear gene that exhibits patterns of considerable geographic differentiation in the brown trout (Salmo trutta) species complex. Haplotype variation from a nucleotide sequence of ∼3.7 kb encompassing a portion of the transferrin (TF) gene was surveyed in 31 brown trout individuals collected across the native Eurasian range. Statistically significant recombination and gene conversion events were detected. However, we showed that the substantial cladistic structure was not disrupted by recombination or gene conversion events and the additional structure was estimated to have emerged after those events. Because loci with unusually high levels of variation might indicate the presence of selection, we tested the hypothesis of neutrality and found some evidence for directional selection. The strong geographic signal observed in the TF genealogy, coupled with the current spatial distribution of electromorphs, gave us the ability to draw empirical phylogeographic inferences. We delineated the composition of current brown trout populations on the basis of 3,625 individuals electrophoretically scored for the TF locus. We hypothesized scenarios of historical radiation and dispersal events, thus providing new insights refining previous allozyme and mtDNA inferences. We infer that the most ancestral brown trout populations inhabited tributaries from the Black, Caspian, and Aral Sea drainages. An early radiation of the species occurred throughout the Mediterranean, followed by independent dispersal events from the Adriatic to the southernmost Iberian Atlantic and, more recently, a rapid expansion throughout most of the Atlantic drainages.