Relative developmental success of interspecific Lepomis hybrids as an estimate of gene regulatory divergence between species

Abstract

The developmental success of interspecific Lepomis hybrids is used as an index of gene regulatory divergence between the green sunfish, L. cyanellus, and each of three other parental species, longear sunfish, L. megalotis, warmouth, L. gulosus, and bluegill, L. macrochirus. This gene regulatory divergence is compared to the degree of structural gene divergence among these four species (genetic distance [Nei, '78], D, ranged from 0.206 to 0.586). The developmental success of the hybrid embryos at the level of morphogenesis was higher than expected from the genetic distance between the parental species. The rates of morphogenesis of the hybrid embryos were the same as that for the green sunfish embryos. The percentage of embryos that hatched was relatively high in all crosses. However, two of the hybrid crosses resulted in enhanced percentages of hatched embryos. Slight increases in the extent of morphological abnormalities were observed in hybrids from crosses between more distantly related parental species. The schedules and levels of enzyme locus expression of the hybrids, assessed spectrophotometrically and electrophoretically for nine enzyme systems (encoded in a total of 14 loci), were different from each other and from those of the green sunfish embryos. Alterations in the time of first enzyme appearance and in the time of first increase in enzyme activity in the developing hybrid embryos were not correlated with genetic distance between parental species. However, the extents of alteration of enzyme activities over the entire period of hybrid embryogenesis were correlated with the genetic distance. We attribute the morphological and molecular anomalies observed in the hybrids to gene regulatory incompatibilities between species. Although the exact number of mutational differences and their relative developmental impacts are not known, some inferences can be drawn about the degree of divergence in gene regulation between species. It appears that an uncoupling of the rates of structural and regulatory gene evolution can occur between species of some taxa, an observation that has implications for the roles of gene regulatory differences in organismic evolution.

Developmental stability, heterozygosity, and fitness in two introduced fire ants (Solenopsis invicta and S. richteri) and their hybrid

“…The possible with some fishes and Drosophila (e.g., Parker et a!., 1985;Ferguson et a!., 1988;Coyne and Orr, 1989). Perhaps the most important point to be made regarding genomic incompatibility between S. invicta and S. richteri is that it is certainly too slight to serve as an effective postzygotic isolating mechanism between the two species, as is also suggested by the considerable width and genetic structure of the hybrid zone in the U.S.A. (see below).…”

Hybridization in Sunfish Influences the Muscle Metabolic Phenotype

“…Fish from the sunfish (Lepomis) branch of the centrarchid family have been popular models to study the origins and consequences of hybridization in vertebrates (Wheat et al 1973;Parker et al 1985;Konkle and Philipp 1992;Bolnick and Near 2005;Bolnick et al 2008;Immler et al 2011). Though they last shared a common ancestor 14.6 million years ago (Near et al 2004), viable hybrids can be generated from crosses.…”

Arylsulfatase and beta-glucuronidase expression in green sunfish, bluegill, and their reciprocal interspecific hybrids

“…Preferential expression of the GSF ARSA phenotype in GSF x BG hybrids and approximately equal expression of the GSF and BG phenotypes in the BG x GSF hybrids represent a more extreme departure than previously reported for interspecific sunfish hybrids (Parker et al, 1985;. These studies described disruptions of the temporal and spatial expression of enzyme activities and the inheritance of quantitative differences in enzyme activity.…”

“…Reciprocal interspecific hybrids were provided by Dr. D. P. Philipp. The hybrids were prepared in the laboratory (Parker et al, 1985), and each hybrid type was maintained in separate ponds for 1-2 years. Fish were collected by electroshock or trapping and frozen at -20°C until use.…”

“…These authors proposed that the perturbations resulted from interspecific divergence in the concentrations of trans-acting maternal regulatory molecules or the affinities of these diffusable molecules for regulatory elements located near or within the respective paternal alleles. Other studies using this approach have demonstrated considerable variation among enzymes with regard to the effects of interspeeific hybridization upon their temporal and spatial expression Parker et al, 1985). Although the model outlined above assumes that events at the DNA level are responsible for the patterns observed, evidence for alterations at the transcriptional level in these interspecific hybrids is currently lacking, and mechanisms operating at other steps in gene expression could also explain the anomalous enzyme profiles observed in the hybrids.…”