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1. The mechanism of cytoplasmic incompatibility is conserved in Wolbachia-infected Aedes aegypti mosquitoes deployed for arbovirus control

   https://doi.org/10.1371/journal.pbio.3002573  

   Kaur, Rupinder; Meier, Cole J; McGraw, Elizabeth A; Hillyer, Julian F; Bordenstein, Seth R (March 2024, PLOS Biology)

   Wolfner, Mariana Federica (Ed.)

   The rising interest and success in deploying inherited microorganisms and cytoplasmic incompatibility (CI) for vector control strategies necessitate an explanation of the CI mechanism. Wolbachia-induced CI manifests in the form of embryonic lethality when sperm from Wolbachia-bearing testes fertilize eggs from uninfected females. Embryos from infected females however survive to sustain the maternally inherited symbiont. Previously in Drosophila melanogaster flies, we demonstrated that CI modifies chromatin integrity in developing sperm to bestow the embryonic lethality. Here, we validate these findings using wMel-transinfected Aedes aegypti mosquitoes released to control vector-borne diseases. Once again, the prophage WO CI proteins, CifA and CifB, target male gametic nuclei to modify chromatin integrity via an aberrant histone-to-protamine transition. Cifs are not detected in the embryo, and thus elicit CI via the nucleoprotein modifications established pre-fertilization. The rescue protein CifA in oogenesis localizes to stem cell, nurse cell, and oocyte nuclei, as well as embryonic DNA during embryogenesis. Discovery of the nuclear targeting Cifs and altered histone-to-protamine transition in both Aedes aegypti mosquitoes and D. melanogaster flies affirm the Host Modification Model of CI is conserved across these host species. The study also newly uncovers the cell biology of Cif proteins in the ovaries, CifA localization in the embryos, and an impaired histone-to-protamine transition during spermiogenesis of any mosquito species. Overall, these sperm modification findings may enable future optimization of CI efficacy in vectors or pests that are refractory to Wolbachia transinfections. 

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2. The life history of Drosophila sperm involves molecular continuity between male and female reproductive tracts

   https://doi.org/10.1073/pnas.2119899119  

   McCullough, Erin L.; Whittington, Emma; Singh, Akanksha; Pitnick, Scott; Wolfner, Mariana F.; Dorus, Steve (March 2022, Proceedings of the National Academy of Sciences)

   Interactions between sperm and the female reproductive tract (FRT) are critical to reproductive success and yet are poorly understood. Because sperm complete their functional maturation within the FRT, the life history of sperm is likely to include a molecular “hand-off” from males to females. Although such intersexual molecular continuity is likely to be widespread among all internally fertilizing species, the identity and extent of female contributions are largely unknown. We combined semiquantitative proteomics with sex-specific isotopic labeling to catalog the posttesticular life history of the sperm proteome and determine the extent of molecular continuity between male and FRTs. We show that the Drosophila melanogaster sperm proteome undergoes substantial compositional changes after being transferred to the FRT. Multiple seminal fluid proteins initially associate with sperm, but most become undetectable after sperm are stored. Female-derived proteins also begin to associate with sperm immediately after mating, and they comprise nearly 20% of the postmating sperm proteome following 4 d of storage in the FRT. Female-derived proteins that associate with sperm are enriched for processes associated with energy metabolism, suggesting that female contributions support sperm viability during the prolonged period between copulation and fertilization. Our research provides a comprehensive characterization of sperm proteome dynamics and expands our understanding of the critical process of sperm–FRT interactions. 

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3. Bindin is essential for fertilization in the sea urchin

   https://doi.org/10.1073/pnas.2109636118  

   Wessel, Gary M.; Wada, Yuuko; Yajima, Mamiko; Kiyomoto, Masato (August 2021, Proceedings of the National Academy of Sciences)

   null (Ed.)

   Species-specific sperm−egg interactions are essential for sexual reproduction. Broadcast spawning of marine organisms is under particularly stringent conditions, since eggs released into the water column can be exposed to multiple different sperm. Bindin isolated from the sperm acrosome results in insoluble particles that cause homospecific eggs to aggregate, whereas no aggregation occurs with heterospecific eggs. Therefore, Bindin is concluded to play a critical role in fertilization, yet its function has never been tested. Here we report that Cas9-mediated inactivation of the bindin gene in a sea urchin results in perfectly normal-looking embryos, larvae, adults, and gametes in both males and females. What differed between the genotypes was that the bindin −/− sperm never fertilized an egg, functionally validating Bindin as an essential gamete interaction protein at the level of sperm–egg cell surface binding. 

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4. Informative predictors of pregnancy after first IVF cycle using eIVF practice highway electronic health records

   https://doi.org/10.1038/s41598-022-04814-x  

   Xu, Tingting; de Figueiredo Veiga, Alexis; Hammer, Karissa C.; Paschalidis, Ioannis Ch.; Mahalingaiah, Shruthi (December 2022, Scientific Reports)

   Abstract The aim of this study is to determine the most informative pre- and in-cycle variables for predicting success for a first autologous oocyte in-vitro fertilization (IVF) cycle. This is a retrospective study using 22,413 first autologous oocyte IVF cycles from 2001 to 2018. Models were developed to predict pregnancy following an IVF cycle with a fresh embryo transfer. The importance of each variable was determined by its coefficient in a logistic regression model and the prediction accuracy based on different variable sets was reported. The area under the receiver operating characteristic curve (AUC) on a validation patient cohort was the metric for prediction accuracy. Three factors were found to be of importance when predicting IVF success: age in three groups (38–40, 41–42, and above 42 years old), number of transferred embryos, and number of cryopreserved embryos. For predicting first-cycle IVF pregnancy using all available variables, the predictive model achieved an AUC of 68% + /− 0.01%. A parsimonious predictive model utilizing age (38–40, 41–42, and above 42 years old), number of transferred embryos, and number of cryopreserved embryos achieved an AUC of 65% + /− 0.01%. The proposed models accurately predict a single IVF cycle pregnancy outcome and identify important predictive variables associated with the outcome. These models are limited to predicting pregnancy immediately after the IVF cycle and not live birth. These models do not include indicators of multiple gestation and are not intended for clinical application. 

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5. Post-meiotic mechanism of facultative parthenogenesis in gonochoristic whiptail lizard species

   https://doi.org/10.7554/eLife.97035  

   Ho, David V; Tormey, Duncan; Odell, Aaron; Newton, Aracely A; Schnittker, Robert R; Baumann, Diana P; Neaves, William B; Schroeder, Morgan R; Sigauke, Rutendo F; Barley, Anthony J; et al (June 2024, eLife)

   Facultative parthenogenesis (FP) has historically been regarded as rare in vertebrates, but in recent years incidences have been reported in a growing list of fish, reptile, and bird species. Despite the increasing interest in the phenomenon, the underlying mechanism and evolutionary implications have remained unclear. A common finding across many incidences of FP is either a high degree of homozygosity at microsatellite loci or low levels of heterozygosity detected in next-generation sequencing data. This has led to the proposal that second polar body fusion following the meiotic divisions restores diploidy and thereby mimics fertilization. Here, we show that FP occurring in the gonochoristicAspidoscelisspeciesA. marmoratusandA. arizonaeresults in genome-wide homozygosity, an observation inconsistent with polar body fusion as the underlying mechanism of restoration. Instead, a high-quality reference genome forA. marmoratusand analysis of whole-genome sequencing from multiple FP and control animals reveals that a post-meiotic mechanism gives rise to homozygous animals from haploid, unfertilized oocytes. Contrary to the widely held belief that females need to be isolated from males to undergo FP, females housed with conspecific and heterospecific males produced unfertilized eggs that underwent spontaneous development. In addition, offspring arising from both fertilized eggs and parthenogenetic development were observed to arise from a single clutch. Strikingly, our data support a mechanism for facultative parthenogenesis that removes all heterozygosity in a single generation. Complete homozygosity exposes the genetic load and explains the high rate of congenital malformations and embryonic mortality associated with FP in many species. Conversely, for animals that develop normally, FP could potentially exert strong purifying selection as all lethal recessive alleles are purged in a single generation. 

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