Research Article: Karyological evidence of hybridogenesis in Greenlings (Teleostei: Hexagrammidae)

Date Published: July 5, 2017

Publisher: Public Library of Science

Author(s): Shota Suzuki, Katsutoshi Arai, Hiroyuki Munehara, Renfu Shao.


Two types of natural hybrids were discovered in populations of three Hexagrammos species (Teleostei: Hexagrammidae) distributed off the southern coast of Hokkaido in the North Pacific Ocean. Both hybrids reproduce by hybridogenesis, in which the maternal haploid genome is transmitted to offspring without recombination and the paternal haploid genome is eliminated during gametogenesis. While natural hybrids are unisexual and reproduce hemiclonally by backcrossing with the paternal species (BC-P), artificial F1-hybrids between the pure species produce recombinant gametes. Thus, despite having the same genome composition, the natural hybrids and the F1-hybrids are not genetically identical. Here, to clarify the differences between both hybrids, we examined the karyotypes of the three Hexagrammos species, their natural hybrids, the artificial F1-hybrids, and several backcrosses. Artificial F1-hybrids have karyotypes and chromosome numbers that are intermediate between those of the parental species. Conversely, the natural hybrids differed from F1-hybrids by having several large metacentric chromosomes and microchromosomes. Since the entire maternal haploid genome is inherited by the natural hybrids, maternal backcrosses (BC-M) between natural hybrids and males of the maternal species (H. octogrammus; Hoc) have a hemiclonal Hoc genome with large chromosomes from the mother and a normal Hoc genome from the father. However, the large chromosomes disappear in offspring of BC-M, probably due to fissuring during gametogenesis. Similarly, microsatellite DNA analysis revealed that chromosomes of BC-M undergo recombination. These findings suggest that genetic factors associated with hemiclonal reproduction may be located on the large metacentric chromosomes of natural hybrids.

Partial Text

Hybridization between two closely related species can result in the production of fertile intermediate hybrids that produce gametes by meiosis and genetic recombination [1]. Conversely, hybridization between two distantly related species is typically associated with a disruption of normal meiosis due to pairing incompatibilities between homoeologous chromosomes. The consequences of hybridization primarily affect the genetic affinity between the two parental species, and most hybridization events result in the production of progeny with little, if any, survival potential, or even in sterility [2]. Gynogenesis, parthenogenesis and hybridogenesis are reproductive modes that have evolved in approximately 70 taxa in Animalia in order to avoid defective meiosis by incompatibilities between homoeologous chromosomes [3, 4, 5, 6]. In hybridogenesis, or hemiclonal reproduction, the haploid genome of one parent is transmitted to offspring without genetic recombination, while the other haploid genome is eliminated during gametogenesis [7, 8]. Unlike gynogenesis and parthenogenesis which involve clonal reproduction without the contribution of the spermatozoan genome, in hybridogenesis, the spermatozoan genome is used only in the replication of somatic cells and is eliminated from germ cells [9, 10]. Hybridogenesis has been reported in hybrids of freshwater fish, such as Poeciliopsis hybrids [11, 12], Rutilus alburnoides [13], and Hypseleotris [14]; the stick insect Bacillus [15]; the frog Pelophylax esculentus (Rana esculentus) [16]; and the marine fish Hexagrammos [17].




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