Genome‐wide analysis facilitates estimation of the amount of male contribution in meiotic gynogenetic three‐spined stickleback (Gasterosteus aculeatus)

Abstract

Gynogenetic embryosthose inheriting only maternal DNAcan be experimentally created by fertilizing eggs with radiation-treated sperm containing inactivated paternal chromosomes. Diploidy in the zygotes can be maintained through prevention of the second meiosis or restored by preventing the first mitosis after the maternal chromosome complement has been replicated. These gynogenetic organisms are useful in many fields including aquaculture, evolutionary biology and genomics. Although gynogenetic organisms have been created in numerous species, the completeness of uni-parental inheritance has often been assumed rather than thoroughly quantified across the genome. Instead, when tests of uni-parental inheritance occur, they typically rely on well-studied genetically determined phenotypes that represent a very small sub-set of the genome. Only assessing small genomic regions for paternal inheritance leaves the question of whether some paternal contributions to offspring might still have occurred. In this study, the authors quantify the efficacy of creating gynogenetic diploid three-spined stickleback fish (Gasterosteus aculeatus). To this end, the authors mirrored previous assessments of paternal contribution using well-studied genetically determined phenotypes including sex and genetically dominant morphological traits but expanded on previous studies using dense restriction site-associated DNA sequencing (RAD-seq) markers in parents and offspring to assess paternal inheritance genome-wide. In the gynogenetic diploids, the authors found no male genotypes underlying their phenotypes of interestsex and dominant phenotypic traits. Using genome-wide assessments of paternal contribution, nevertheless, the authors found evidence of a small, yet potentially important, amount of paternally "leaked" genetic material. The application of this genome-wide approach identifies the need for more widespread assessment of paternal contributions to gynogenetic animals and promises benefits for many aspects of aquaculture, evolutionary biology and genomics.

Origin matters: Using a local reference genome improves measures in population genomics

“…The remaining SNPs identified in gynogen genome likely stem from paralogous sequences that were not identified by the genome assembler or from errors in the SNP calling process. Alternatively, a small paternal contribution in meiotic gynogenesis has been identified and may also contribute to our observations (Currey et al, 2023).…”

“…Alternatively, a small paternal contribution in meiotic gynogenesis has been identified and may also contribute to our observations (Currey et al, 2023).…”

Deciphering male influence in gynogenetic Pengze crucian carp (Carassius auratus var. pengsenensis): insights from Nanopore sequencing of structural variations

“…Similarly, in natural gynogenetic silver carp, it was discovered that homologous male microchromosomes could be inherited by offspring, playing a pivotal role in enhancing offspring genetic diversity ( Ding et al, 2021 ; Zhao et al, 2021 ). Furthermore, in gynogenetically reproduced offspring of the threespine stickleback ( Gasterosteus aculeatus ) using inactivated sperm, there was evidence of a minor, yet potentially significant, amount of male ‘leakage’ genetic material ( Currey et al, 2023 ). These findings challenge Müller’s ratchet theory ( Kondrashov, 1982 ), which posits that the accumulation of deleterious mutations in asexually reproducing organisms could lead to species extinction, underscoring the necessity to re-evaluate the genetic dynamics of asexual reproduction modes.…”