An apparent progressive and recurrent evolutionary restriction in tissue expression of a gene, the lactate dehydrogenase-C gene, within a family of bony fish (Salmoniformes: Umbridae)

Abstract

Unexpectedly large differences in the tissue patterns of lactate dehydrogenase-C (Ldh-C) gene regulation were observed among species of fish within the family Umbridae (Salmoniformes). Normally, all the species within a family or order of advanced fishes exhibit the same, tissue-restricted pattern ofl-latate dehydrogenase C₄ isozyme synthesis—either eye- or liver-restricted expression, but not both. However, within the Umbridae the more anciently derived species had a more generalized (primitive) tissue expression, whereas the more recently derived species had a more tissue-restricted expression, predominating in the eye. Given the relative divergence times among the species estimated by genetic distance (using 51 protein-coding loci), divergence from the presumed primitive expression of the Ldh-C gene appears to have been proceeding more rapidly in some species lineages than others. This narrowing of Ldh-C gene tissue regulatory specificity within the family Umbridae is similar to the general trend observed over much greater evolutionary times within the class of bony fishes. The results support the hypothesis of repeated evolutionary canalizations of Ldh-C gene regulation from the generalized tissue expression in more primitive species to a predictable tissue-restricted expression (in either eye or liver) in advanced species. Furthermore, in the Umbridae, this progressive restriction of tissue expression of isozymes has taken place during the evolution of both the Ldh-C and Ldh-B genes. These evolutionary trends in the regulation of isozyme-locus tissue expression in the bony fishes are consistent with either an intrinsically conditioned trend of change in gene regulation or with a response to natural selection.