Genotypic Males Play an Important Role in the Creation of Genetic Diversity in Gynogenetic Gibel Carp

Abstract

Unisexual lineages are commonly considered to be short-lived in the evolutionary process as accumulation of deleterious mutations stated by Muller’s ratchet. However, the gynogenetic hexaploid gibel carp (Carassius gibelio) with existence over 0.5 million years has wider ecological distribution and higher genetic diversity than its sexual progenitors, which provides an ideal model to investigate the underlying mechanisms on countering Muller’s ratchet in unisexual taxa. Unlike other unisexual lineages, the wild populations of gibel carp contain rare and variable proportions of males (1–26%), which are determined via two strategies including genotypic sex determination and temperature-dependent sex determination. Here, we used a maternal gibel carp from strain F to be mated with a genotypic male from strain A+, a temperature-dependent male from strain A+, and a male from another species common carp (Cyprinus carpio), respectively. When the maternal individual was mated with the genotypic male, a variant of gynogenesis was initiated, along with male occurrence, accumulation of microchromosomes, and creation of genetic diversity in the offspring. When the maternal individual was mated with the temperature-dependent male and common carp, typical gynogenesis was initiated that all the offspring showed the same genetic information as the maternal individual. Subsequently, we found out that the genotypic male nucleus swelled and contacted with the female nucleus after fertilization although it was extruded from the female nucleus eventually, which might be associated with the genetic variation in the offspring. These results reveal that genotypic males play an important role in the creation of genetic diversity in gynogenetic gibel carp, which provides insights into the evolution of unisexual reproduction.

Genomic anatomy of male-specific microchromosomes in a gynogenetic fish

“…In conclusion, we isolated three MSMs in gynogenetic C. gibelio and characterized abundant repetitive elements and some genes with male-specific/male-biased expression on MSMs. Our present results indicate that MSMs could be responsible for male occurrence in C. gibelio [18,23,31], which can facilitate further identification of the sex-determining gene/genes on MSMs. Besides, continued investigations on sex determination mechanism and reproduction mode of the gynogenetic C. gibelio with male occurrence will provide insights into the evolution of unisexual reproduction.…”

“…In contrast with other unisexual vertebrates composed of all females, males containing MSMs have been observed in wild populations and artificially propagated strains of C. gibelio [18,23]. These males with MSMs can initiate a variant of gynogenesis along with male occurrence, accumulation of microchromosomes, and creation of genetic diversity in the offspring [31,32], which can contribute to the environmental adaptation and evolutionary long existence of gynogenetic C. gibelio.…”

“…Although supernumerary chromosomes are nonessential genetic elements, many supernumerary chromosomes have the intrinsic ability to transmit themselves at frequencies above that predicted by Mendelian rules [54,55]. Similarly, the microchromosomes derived from genotypic males of C. gibelio also can be accumulated in the offspring [18,31]. So there is a possibility that the MSMs may be transmitted steadily across generations as a selfish genomic parasite, and the gynogenetic C. gibelio will maintain the present status with MSMs for male determination.…”

“…Although supernumerary chromosomes are dispensable for the normal life of host individuals [22,25], they have been revealed to contain genes with expression activity [25][26][27][28] and be associated with some phenotypes [29]. Especially, sex-ratio distortions related with the presence of supernumerary chromosomes have been identified in many species [30][31][32][33][34]. In hexaploid C. gibelio, supernumerary microchromosomes in males are also associated with male determination [23,30], and these males with supernumerary microchromosomes contribute to the creation of genetic diversity, which is able to counter Muller's ratchet at a certain level [19,31,32].…”

“…Especially, sex-ratio distortions related with the presence of supernumerary chromosomes have been identified in many species [30][31][32][33][34]. In hexaploid C. gibelio, supernumerary microchromosomes in males are also associated with male determination [23,30], and these males with supernumerary microchromosomes contribute to the creation of genetic diversity, which is able to counter Muller's ratchet at a certain level [19,31,32]. However, the genomic components of these supernumerary microchromosomes and the underlying mechanisms of male occurrence remain elusive in gynogenetic C. gibelio.…”