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Proceedings. Biological Sciences Sep 2023Obligately parthenogenetic species are expected to be short lived since the lack of sex and recombination should translate into a slower adaptation rate and increased...
Obligately parthenogenetic species are expected to be short lived since the lack of sex and recombination should translate into a slower adaptation rate and increased accumulation of deleterious alleles. Some, however, are thought to have been reproducing without males for millions of years. It is not clear how these old parthenogens can escape the predicted long-term costs of parthenogenesis, but an obvious explanation is cryptic sex. In this study, we screen for signatures of cryptic sex in eight populations of four parthenogenetic species of stick insects, some estimated to be older than 1 Myr. Low genotype diversity, homozygosity of individuals and high linkage disequilibrium (LD) unaffected by marker distances support exclusively parthenogenetic reproduction in six populations. However, in two populations (namely, of the species and ) we find strong evidence for cryptic sex, most likely mediated by rare males. These populations had comparatively high genotype diversities, lower LD, and a clear LD decay with genetic distance. Rare sex in species that are otherwise largely parthenogenetic could help explain the unusual success of parthenogenesis in the genus and raises the question whether episodes of rare sex are in fact the simplest explanation for the persistence of many old parthenogens in nature.
Topics: Humans; Male; Animals; Female; Alleles; Genotype; Linkage Disequilibrium; Parthenogenesis; Insecta
PubMed: 37727092
DOI: 10.1098/rspb.2023.0404 -
Genome Biology and Evolution Sep 2023Although asexual lineages evolved from sexual lineages in many different taxa, the genetics of sex loss remains poorly understood. We addressed this issue in the pea...
Although asexual lineages evolved from sexual lineages in many different taxa, the genetics of sex loss remains poorly understood. We addressed this issue in the pea aphid Acyrthosiphon pisum, whose natural populations encompass lineages performing cyclical parthenogenesis (CP) and producing one sexual generation per year, as well as obligate parthenogenetic (OP) lineages that can no longer produce sexual females but can still produce males. An SNP-based, whole-genome scan of CP and OP populations sequenced in pools (103 individuals from 6 populations) revealed that an X-linked region is associated with the variation in reproductive mode. This 840-kb region is highly divergent between CP and OP populations (FST = 34.9%), with >2,000 SNPs or short Indels showing a high degree of association with the phenotypic trait. In OP populations specifically, this region also shows reduced diversity and Tajima's D, consistent with the OP phenotype being a derived trait in aphids. Interestingly, the low genetic differentiation between CP and OP populations at the rest of the genome (FST = 2.5%) suggests gene flow between them. Males from OP lineages thus likely transmit their op allele to new genomic backgrounds. These genetic exchanges, combined with the selection of the OP and CP reproductive modes under different climates, probably contribute to the long-term persistence of the cp and op alleles.
Topics: Humans; Male; Animals; Female; Aphids; Pisum sativum; Genetic Variation; Parthenogenesis; Genomics; Reproduction, Asexual
PubMed: 37717171
DOI: 10.1093/gbe/evad168 -
Current Biology : CB Sep 2023New work reveals differences in oogenic gene expression between parthenogenetic and sexually reproducing Drosophila mercatorum strains. Recapitulating those changes in...
New work reveals differences in oogenic gene expression between parthenogenetic and sexually reproducing Drosophila mercatorum strains. Recapitulating those changes in D. melanogaster oocytes induced parthenogenesis in this normally sexually reproducing species, providing molecular insight into how these reproductive modes arise.
Topics: Animals; Drosophila melanogaster; Drosophila; Oocytes; Parthenogenesis; Biology
PubMed: 37699347
DOI: 10.1016/j.cub.2023.07.055 -
Phylloxera and aphids show distinct features of genome evolution despite similar reproductive modes.BioRxiv : the Preprint Server For... Aug 2023Genomes of aphids (family Aphididae) show several unusual evolutionary patterns. In particular, within the XO sex determination system of aphids, the X chromosome...
Genomes of aphids (family Aphididae) show several unusual evolutionary patterns. In particular, within the XO sex determination system of aphids, the X chromosome exhibits a lower rate of interchromosomal rearrangements, fewer highly expressed genes, and faster evolution at nonsynonymous sites compared to the autosomes. In contrast, other hemipteran lineages have similar rates of interchromosomal rearrangement for autosomes and X chromosomes. One possible explanation for these differences is the aphid's life cycle of cyclical parthenogenesis, where multiple asexual generations alternate with one sexual generation. If true, we should see similar features in the genomes of Phylloxeridae, an outgroup of aphids which also undergoes cyclical parthenogenesis. To investigate this, we generated a chromosome-level assembly for the grape phylloxera, an agriculturally important species of Phylloxeridae, and identified its single X chromosome. We then performed synteny analysis using the phylloxerid genome and 30 high-quality genomes of aphids and other hemipteran species. Unexpectedly, we found that the phylloxera does not share aphids' patterns of chromosome evolution. By estimating interchromosomal rearrangement rates on an absolute time scale, we found that rates are elevated for aphid autosomes compared to their X chromosomes, but this pattern does not extend to the phylloxera branch. Potentially, the conservation of X chromosome gene content is due to selection on XO males that appear in the sexual generation. We also examined gene duplication patterns across Hemiptera and uncovered horizontal gene transfer events contributing to phylloxera evolution.
PubMed: 37693541
DOI: 10.1101/2023.08.28.555181 -
Frontiers in Plant Science 2023var. (syn. ; ) is a versatile model used to study gametophytic apomixis. In this system apomixis is controlled by three loci: one that controls the avoidance of...
var. (syn. ; ) is a versatile model used to study gametophytic apomixis. In this system apomixis is controlled by three loci: one that controls the avoidance of meiosis (), one that controls the avoidance of fertilization () and a third that controls autonomous endosperm formation (). Using a unique polyhaploid mapping approach the locus was mapped to a 654 kb genomic interval syntenic to linkage group 8 of . Polyhaploids form through the gametophytic action of a dominant determinant at , so the mapped region represents both a functional and a physical domain for in . Allele sequence divergence (ASD) analysis of the ( gene within the locus revealed that dominant alleles in remain highly similar across the genus, whilst the recessive alleles are more divergent. A previous report noted that dominant alleles in both and are modified by the presence of a class II transposable element (TE) in the promoter of the gene. This observation was confirmed and further extended to the related genus . Sufficient differences were noted in the structure and location of the TE elements to conclude that TE insertional events had occurred independently in the three genera. Measures of allele crossover amongst the polyhaploids revealed that is an autopolyploid species with tetrasomic inheritance. It was also noted that the dominant determinant of in could transmit via a diploid gamete (pollen or egg) but not via a haploid gamete. Using this information, a model is presented of how gametophytic apomixis may have evolved in several members of the Lactuceae, a tribe of the Asteraceae.
PubMed: 37692427
DOI: 10.3389/fpls.2023.1239191 -
Journal of Evolutionary Biology Sep 2023The adaptive value of sexual reproduction is still debated in evolutionary theory. It has been proposed that the advantage of sexual reproduction over asexual...
The adaptive value of sexual reproduction is still debated in evolutionary theory. It has been proposed that the advantage of sexual reproduction over asexual reproduction is to promote genetic diversity, to prevent the accumulation of harmful mutations or to preserve heterozygosity. Since these hypothetical advantages depend on the type of asexual reproduction, understanding how selection affects the taxonomic distribution of each type could help us discriminate between existing hypotheses. Here, I argue that soft selection, competition among embryos or offspring in selection arenas prior to the hard selection of the adult phase, reduces loss of heterozygosity in certain types of asexual reproduction. Since loss of heterozygosity leads to the unmasking of recessive deleterious mutations in the progeny of asexual individuals, soft selection facilitates the evolution of these types of asexual reproduction. Using a population genetics model, I calculate how loss of heterozygosity affects fitness for different types of apomixis and automixis, and I show that soft selection significantly reduces loss of heterozygosity, hence increases fitness, in apomixis with suppression of the first meiotic division and in automixis with central fusion, the most common types of asexual reproduction. Therefore, if sexual reproduction evolved to preserve heterozygosity, soft selection should be associated with these types of asexual reproduction. I discuss the evidence for this prediction and how this and other observations on the distribution of different types of asexual reproduction in nature is consistent with the heterozygosity hypothesis.
Topics: Humans; Biological Evolution; Reproduction, Asexual; Parthenogenesis; Reproduction; Loss of Heterozygosity; Selection, Genetic
PubMed: 37584223
DOI: 10.1111/jeb.14209 -
BMC Genomics Aug 2023Biocontrol is a key technology for the control of pest species. Microctonus parasitoid wasps (Hymenoptera: Braconidae) have been released in Aotearoa New Zealand as...
BACKGROUND
Biocontrol is a key technology for the control of pest species. Microctonus parasitoid wasps (Hymenoptera: Braconidae) have been released in Aotearoa New Zealand as biocontrol agents, targeting three different pest weevil species. Despite their value as biocontrol agents, no genome assemblies are currently available for these Microctonus wasps, limiting investigations into key biological differences between the different species and strains.
METHODS AND FINDINGS
Here we present high-quality genomes for Microctonus hyperodae and Microctonus aethiopoides, assembled with short read sequencing and Hi-C scaffolding. These assemblies have total lengths of 106.7 Mb for M. hyperodae and 129.2 Mb for M. aethiopoides, with scaffold N50 values of 9 Mb and 23 Mb respectively. With these assemblies we investigated differences in reproductive mechanisms, and association with viruses between Microctonus wasps. Meiosis-specific genes are conserved in asexual Microctonus, with in-situ hybridisation validating expression of one of these genes in the ovaries of asexual Microctonus aethiopoides. This implies asexual reproduction in these Microctonus wasps involves meiosis, with the potential for sexual reproduction maintained. Investigation of viral gene content revealed candidate genes that may be involved in virus-like particle production in M. aethiopoides, as well as a novel virus infecting M. hyperodae, for which a complete genome was assembled.
CONCLUSION AND SIGNIFICANCE
These are the first published genomes for Microctonus wasps which have been deployed as biocontrol agents, in Aotearoa New Zealand. These assemblies will be valuable resources for continued investigation and monitoring of these biocontrol systems. Understanding the biology underpinning Microctonus biocontrol is crucial if we are to maintain its efficacy, or in the case of M. hyperodae to understand what may have influenced the significant decline of biocontrol efficacy. The potential for sexual reproduction in asexual Microctonus is significant given that empirical modelling suggests this asexual reproduction is likely to have contributed to biocontrol decline. Furthermore the identification of a novel virus in M. hyperodae highlights a previously unknown aspect of this biocontrol system, which may contribute to premature mortality of the host pest. These findings have potential to be exploited in future in attempt to increase the effectiveness of M. hyperodae biocontrol.
Topics: Animals; Wasps; Weevils; Reproduction; Parthenogenesis; Chromosomes
PubMed: 37543591
DOI: 10.1186/s12864-023-09538-4 -
Frontiers in Cell and Developmental... 2023Neurotrophin-4 (NT-4), a neurotrophic factor, appears to affect early embryonic development because it is secreted not only by neurons but also by oviductal and uterine...
Neurotrophin-4 (NT-4), a neurotrophic factor, appears to affect early embryonic development because it is secreted not only by neurons but also by oviductal and uterine epithelial cells. However, no studies have characterized the effects of NT-4 on early embryonic development in pigs. In this study, we applied the experimental model of parthenogenetic-activation (PA)-derived embryos. Herein, we investigated the effect of NT-4 supplementation during the culture (IVC) of embryos, analyzed the transcription levels of specific genes, and outlined the first cell lineage specification for porcine PA-derived blastocysts. We confirmed that NT-4 and its receptor proteins were localized in both the inner cell mass (ICM) and trophectoderm (TE) in porcine blastocysts. Across different concentrations (0, 1, 10, and 100 ng/mL) of NT-4 supplementation, the optimal concentration of NT-4 to improve the developmental competence of porcine parthenotes was 10 ng/mL. NT-4 supplementation during porcine IVC significantly ( < 0.05) increased the proportion of TE cells by inducing the transcription of TE lineage markers (, , and transcripts). NT-4 also reduced blastocyst apoptosis by regulating the transcription of apoptosis-related genes ( and transcripts) and improved blastocyst quality via the interaction of neurotrophin-, Hippo-yes-associated protein (Hippo-YAP) and mitogen-activated protein kinase/extracellular regulated kinase (MAPK/ERK) pathway. Additionally, NT-4 supplementation during IVC significantly ( < 0.05) increased transcript levels and significantly ( < 0.01) decreased transcript levels, respectively, in the porcine PA-derived blastocysts. We also confirmed through fluorescence intensity that the YAP1 protein was significantly ( < 0.001) increased in the NT-4-treated blastocysts compared with that in the control. NT-4 also promoted differentiation into the TE lineage rather than into the ICM lineage during porcine early embryonic development. In conclusion, 10 ng/mL NT-4 supplementation enhanced blastocyst quality by regulating the apoptosis- and TE lineage specification-related genes and interacting with neurotrophin-, Hippo-YAP-, and MAPK/ERK signaling pathway during porcine embryo development.
PubMed: 37519302
DOI: 10.3389/fcell.2023.1194596 -
Current Biology : CB Sep 2023Facultative parthenogenesis enables sexually reproducing organisms to switch between sexual and asexual parthenogenetic reproduction. To gain insights into this...
Facultative parthenogenesis enables sexually reproducing organisms to switch between sexual and asexual parthenogenetic reproduction. To gain insights into this phenomenon, we sequenced the genomes of sexually reproducing and parthenogenetic strains of Drosophila mercatorum and identified differences in the gene expression in their eggs. We then tested whether manipulating the expression of candidate gene homologs identified in Drosophila mercatorum could lead to facultative parthenogenesis in the non-parthenogenetic species Drosophila melanogaster. This identified a polygenic system whereby increased expression of the mitotic protein kinase polo and decreased expression of a desaturase, Desat2, caused facultative parthenogenesis in the non-parthenogenetic species that was enhanced by increased expression of Myc. The genetically induced parthenogenetic Drosophila melanogaster eggs exhibit de novo centrosome formation, fusion of the meiotic products, and the onset of development to generate predominantly triploid offspring. Thus, we demonstrate a genetic basis for sporadic facultative parthenogenesis in an animal.
Topics: Animals; Drosophila; Drosophila melanogaster; Parthenogenesis; Centrosome
PubMed: 37516115
DOI: 10.1016/j.cub.2023.07.006 -
International Journal of Molecular... Jul 2023The increasing frequency of general and particularly male cancer coupled with the reduction in male fertility seen worldwide motivated us to seek a potential... (Review)
Review
The increasing frequency of general and particularly male cancer coupled with the reduction in male fertility seen worldwide motivated us to seek a potential evolutionary link between these two phenomena, concerning the reproductive transcriptional modules observed in cancer and the expression of cancer-testis antigens (CTA). The phylostratigraphy analysis of the human genome allowed us to link the early evolutionary origin of cancer via the reproductive life cycles of the unicellulars and early multicellulars, potentially driving soma-germ transition, female meiosis, and the parthenogenesis of polyploid giant cancer cells (PGCCs), with the expansion of the CTA multi-families, very late during their evolution. CTA adaptation was aided by retrovirus domestication in the unstable genomes of mammals, for protecting male fertility in stress conditions, particularly that of humans, as compensation for the energy consumption of a large complex brain which also exploited retrotransposition. We found that the early and late evolutionary branches of human cancer are united by the immunity-proto-placental network, which evolved in the Cambrian and shares stress regulators with the finely-tuned sex determination system. We further propose that social stress and endocrine disruption caused by environmental pollution with organic materials, which alter sex determination in male foetuses and further spermatogenesis in adults, bias the development of PGCC-parthenogenetic cancer by default.
Topics: Pregnancy; Animals; Humans; Male; Female; Testis; Placenta; Spermatogenesis; Reproduction; Neoplasms; Mammals; Polyploidy; Fertility
PubMed: 37511419
DOI: 10.3390/ijms241411660