Scholarly Literature

This is a database of scholarly literature that concentrates currently on natural and engineered selfish genetic elements (gene drives).  The latest are shown here.
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An Initial Framework for the Environmental Risk Assessment of Synthetic Biology-Derived Organisms with a Focus on Gene Drives.

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W. G. Landis, E. A. Brown and S. Eikenbary,  Synthetic Biology 2020: Frontiers in Risk Analysis and Governance. Risk, Systems and Decisions.,  2019-11-29 17:16:37.
We apply the structure of source-stressor-habitat-effect-impact pathway derived from the relative risk model (Landis and Wiegers 2005) and as was demonstrated to be applicable in the National Academy of Sciences, Engineering and Medicine (NASEM) 2016 report Gene Drives on the Horizon. This relative risk model is now calculated employing Bayesian networks and has been applied to forestry management (Ayre and Landis 2012), infectious disease (Ayre et al. 2014), invasive species (Herring et al. 2015), contaminated sites (Landis et al. 2017a; Johns et al. 2017), and watershed management (Hines and Landis 2014; Graham et al. 2019).

An X-linked meiotic drive allele has strong, recessive fitness costs in female Drosophila pseudoobscura

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W. Larner, T. Price, L. Holman and N. Wedell,  Proceedings of the Royal Society B-Biological Sciences,  286:9. 2019-11-27 18:44:20.
Selfish 'meiotic drive' alleles are transmitted to more than 50% of offspring, allowing them to rapidly invade populations even if they reduce the fitness of individuals carrying them. Theory predicts that drivers should either fix or go extinct, yet some drivers defy these predictions by persisting at low, stable frequencies for decades. One possible explanation for this discrepancy is that drivers are especially costly when homozygous, although empirical tests of this idea are rare and equivocal. Here, we measure the fitness of female Drosophila pseudoobscura carrying zero, one or two copies of the X-linked driver sex ratio (SR). SR had strong negative effects on female offspring production and the probability of reproductive failure, and these effects were largely similar across four genetic backgrounds. SR was especially costly when homozygous. We used our fitness measurements to parametrize a population genetic model, and found that the female fitness costs observed here can explain the puzzlingly low allele frequency of SR in nature. We also use the model to show how spatial variation in female mating behaviour, fitness costs of SR and the reduced siring success of SR males can jointly explain the north-south cline in SR frequencies across North America.

Establishment of Wolbachia Strain wAlbB in Malaysian Populations of Aedes aegypti for Dengue Control

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W. A. Nazni, A. A. Hoffmann, A. NoorAfizah, Y. L. Cheong, M. V. Mancini, N. Golding, G. M. R. Kamarul, M. A. K. Arif, H. Thohir, H. NurSyamimi, M. Z. ZatilAqmar, M. NurRuqqayah, A. NorSyazwani, A. Faiz, F.-R. M. N. Irfan, S. Rubaaini, N. Nuradila, N. M. N,  Current Biology,  29:4241-4248.e5. 2019-11-21 15:20:44.
Dengue has enormous health impacts globally. A novel approach to decrease dengue incidence involves the introduction of Wolbachia endosymbionts that block dengue virus transmission into populations of the primary vector mosquito, Aedes aegypti. The wMel Wolbachia strain has previously been trialed in open releases of Ae. aegypti; however, the wAlbB strain has been shown to maintain higher density than wMel at high larval rearing temperatures. Releases of Ae. aegypti mosquitoes carrying wAlbB were carried out in 6 diverse sites in greater Kuala Lumpur, Malaysia, with high endemic dengue transmission. The strain was successfully established and maintained at very high population frequency at some sites or persisted with additional releases following fluctuations at other sites. Based on passive case monitoring, reduced human dengue incidence was observed in the release sites when compared to control sites. The wAlbB strain of Wolbachia provides a promising option as a tool for dengue control, particularly in very hot climates.

The Competitive Mating of Irradiated Brown Marmorated Stink Bugs, Halyomorpha halys, for the Sterile Insect Technique

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D. M. Suckling, M. Cristofaro, G. Roselli, M. C. Levy, A. Cemmi, V. Mazzoni, L. D. Stringer, V. Zeni, C. Ioriatti and G. Anfora,  Insects,  10. 2019-11-16 15:14:41.
The sterility of eggs and nymphs from gamma-irradiated male Halyomorpha halys was investigated to determine the potential for the sterile insect technique (SIT). Males irradiated at 0, 16, 24 and 32 Gy were placed with untreated virgin females, and egg sterility was determined, showing 54.3% at 16 Gy. The percentage of sterility from irradiation was 26 percent lower than previous results from the USA and the variance was very high. Competitive overflooding ratio trials between irradiated virgin males and fertile virgin males at a 5:1 ratio resulted in the expected egg sterility, indicating competitive performance by irradiated males. By July and August, older, irradiated overwintered males were significantly less competitive than similar, non-irradiated males. There is a need to revisit the irradiation delivery method to achieve proper precision around the paternal dose required for an expected >80% egg sterility and subsequent ~99% endpoint sterility estimated at adult emergence in the F1 phase. These results suggest that the mating competitiveness and competency of males after irradiation at 16 Gy is not limiting to the sterile insect technique for suppression. A wild harvest of overwintering males using the aggregation pheromone, followed by irradiation and male release, might replace rearing. Mass-collected, sterilized bugs could be transported from an area of high H. halys density and shipped for release to enable suppression or eradication elsewhere. This concept is under development but further work is needed now to understand the difference in results between the US and Italian irradiators and increase the reliability of dosimetry.

Effects of a male meiotic driver on male and female transcriptomes in the house mouse

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A. Lindholm, A. Sutter, S. Kunzel, D. Tautz and H. Rehrauer,  Proceedings of the Royal Society B-Biological Sciences,  286:1-8. 2019-11-13 20:18:05.
Not all genetic loci follow Mendel's rules, and the evolutionary consequences of this are not yet fully known. Genomic conflict involving multiple loci is a likely outcome, as restoration of Mendelian inheritance patterns will be selected for, and sexual conflict may also arise when sexes are differentially affected. Here, we investigate effects of the t haplotype, an autosomal male meiotic driver in house mice, on genome-wide gene expression patterns in males and females. We analysed gonads, liver and brain in adult same-sex sibling pairs differing in genotype, allowing us to identify t-associated differences in gene regulation. In testes, only 40% of differentially expressed genes mapped to the approximately 708 annotated genes comprising the t haplotype. Thus, much of the activity of the t haplotype occurs in trans, and as upregulation. Sperm maturation functions were enriched among both cis and trans acting t haplotype genes. Within the t haplotype, we observed more downregulation and differential exon usage. In ovaries, liver and brain, the majority of expression differences mapped to the t haplotype, and were largely independent of the differences seen in the testis. Overall, we found widespread transcriptional effects of this male meiotic driver in the house mouse genome.

Rodent gene drives for conservation: opportunities and data needs

6386
J. Godwin, M. Serr, K. Barnhill-Dilling, D. V. Blondel, P. R. Brown, K. Campbell, J. Delborne, A. L. Lloyd, K. P. Oh, T. A. A. Prowse, R. Saah and P. Thomas,  Proceedings of the Royal Society B-Biological Sciences,  286:20191606. 2019-11-10 16:22:06.
Invasive rodents impact biodiversity, human health and food security worldwide. The biodiversity impacts are particularly significant on islands, which are the primary sites of vertebrate extinctions and where we are reaching the limits of current control technologies. Gene drives may represent an effective approach to this challenge, but knowledge gaps remain in a number of areas. This paper is focused on what is currently known about natural and developing synthetic gene drive systems in mice, some key areas where key knowledge gaps exist, findings in a variety of disciplines relevant to those gaps and a brief consideration of how engagement at the regulatory, stakeholder and community levels can accompany and contribute to this effort. Our primary species focus is the house mouse, Mus musculus, as a genetic model system that is also an important invasive pest. Our primary application focus is the development of gene drive systems intended to reduce reproduction and potentially eliminate invasive rodents from islands. Gene drive technologies in rodents have the potential to produce significant benefits for biodiversity conservation, human health and food security. A broad-based, multidisciplinary approach is necessary to assess this potential in a transparent, effective and responsible manner.

The impact of local population genetic background on the spread of the selfish element Medea-1 in red flour beetles

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S. A. Cash, M. A. Robert, M. D. Lorenzen and F. Gould,  Ecology and Evolution,  12:1-12. 2019-11-10 16:06:41.
Selfish genetic elements have been found in the genomes of many species, yet our understanding of their evolutionary dynamics is only partially understood. A number of distinct selfish Medea elements are naturally present in many populations of the red flour beetle (Tribolium castaneum). Although these Medea elements are predicted by models to increase in frequency within populations because any offspring of a Medea-bearing mother that do not inherit at least one Medea allele will die, experiments demonstrating an increase in a naturally occurring Medea element are lacking. Our survey of the specific Medea element, M-1, in the United States showed that it had a patchy geographic distribution. From the survey, it could not be determined if this distribution was caused by a slow process of M-1 colonization of discrete populations or if some populations lacked M-1 because they had genetic factors conferring resistance to the Medea mechanism. We show that populations with naturally low to intermediate M-1 frequencies likely represent transient states during the process of Medea spread. Furthermore, we find no evidence that genetic factors are excluding M-1 from US populations where the element is not presently found. We also show how a known suppressor of Medea can impair the increase of M-1 in populations and discuss the implications of our findings for pest-management applications of Medea elements.

The distribution and spread of naturally occurring Medea selfish genetic elements in the United States

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S. A. Cash, M. D. Lorenzen and F. Gould,  Ecology and Evolution,  9:14407–14416.. 2019-11-09 16:17:38.
Selfish genetic elements (SGEs) are DNA sequences that are transmitted to viable offspring in greater than Mendelian frequencies. Medea SGEs occur naturally in some populations of red flour beetle (Tribolium castaneum) and are expected to increase in frequency within populations and spread among populations. The large-scale U.S. distributions of Medea-4 (M4) had been mapped based on samples from 1993 to 1995. We sampled beetles in 2011?2014 and show that the distribution of M4 in the United States is dynamic and has shifted southward. By using a genetic marker of Medea-1 (M1), we found five unique geographic clusters with high and low M1 frequencies in a pattern not predicted by microsatellite-based analysis of population structure. Our results indicate the absence of rigid barriers to Medea spread in the United States, so assessment of what factors have limited its current distribution requires further investigation. There is great interest in using synthetic SGEs, including synthetic Medea, to alter or suppress pest populations, but there is concern about unpredicted spread of these SGEs and potential for populations to become resistant to them. The finding of patchy distributions of Medea elements suggests that released synthetic SGEs cannot always be expected to spread uniformly, especially in target species with limited dispersal.

Meiotic drive mechanisms: lessons from Drosophila

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C. Courret, C.-H. Chang, K. H.-C. Wei, C. Montchamp-Moreau and A. M. Larracuente,  Proceedings of the Royal Society B: Biological Sciences,  286:20191430. 2019-10-23 20:28:42.
Meiotic drivers are selfish genetic elements that bias their transmission into gametes, often to the detriment of the rest of the genome. The resulting intragenomic conflicts triggered by meiotic drive create evolutionary arms races and shape genome evolution. The phenomenon of meiotic drive is widespread across taxa but is particularly prominent in the Drosophila genus. Recent studies in Drosophila have provided insights into the genetic origins of drivers and their molecular mechanisms. Here, we review the current literature on mechanisms of drive with an emphasis on sperm killers in Drosophila species. In these systems, meiotic drivers often evolve from gene duplications and targets are generally linked to heterochromatin. While dense in repetitive elements and difficult to study using traditional genetic and genomic approaches, recent work in Drosophila has made progress on the heterochromatic compartment of the genome. Although we still understand little about precise drive mechanisms, studies of male drive systems are converging on common themes such as heterochromatin regulation, small RNA pathways, and nuclear transport pathways. Meiotic drive systems are therefore promising models for discovering fundamental features of gametogenesis.

Does meiotic drive alter male mate preference?

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S. R. Finnegan, L. Nitsche, M. Mondani, M. F. Camus, K. Fowler and A. Pomiankowski,  Behavioral Ecology,  13:194-201. 2019-10-20 14:14:20.
Male mate preferences have been demonstrated across a range of species, including the Malaysian stalk-eyed fly, Teleopsis dalmanni. This species is subject to sex-ratio (SR), an X-linked male meiotic driver, which causes the dysfunction of Y-sperm and the production of all-female broods. While there has been work considering female avoidance of meiotic drive males, the mating decisions of drive-bearing males have not been considered previously. Drive males may be less able to bear the cost of choice as SR is associated with a low-frequency inversion that causes reduced organismal fitness. Drive males may also experience weaker selection for preference maintenance if they are avoided by females. Using binary choice trials, across two experiments, we confirmed male preference for large (fecund) females but found no evidence that the strength of male preference differs between drive and standard males. We showed that large eyespan males displayed strong preference for large females, whereas small eyespan males showed no preference. Taken together, these results suggest that, even though meiotic drive is associated with lower genetic quality, it does not directly interfere with male mate preference among available females. However, as drive males tend to have smaller eyespan (albeit only similar to 5% on average), this will to a minor extent weaken their strength of preference.

Fitness consequences of the selfish supergene Segregation Distorter

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H. W. S. Wong and L. Holman,  Journal of Evolutionary Biology,  33:89-100. 2019-10-11 20:21:24.
Segregation distorters are selfish genetic elements that subvert Mendelian inheritance, often by destroying gametes that do not carry the distorter. Simple theoretical models predict that distorter alleles will either spread to fixation or stabilize at some high intermediate frequency. However, many distorters have substantially lower allele frequencies than predicted by simple models, suggesting that key sources of selection remain to be discovered. Here, we measured the fitness of Drosophila melanogaster adults and juveniles carrying zero, one or two copies of three different variants of the naturally occurring supergene Segregation Distorter (SD), in order to investigate why SD alleles remain relatively rare within populations despite being preferentially inherited. First, we show that the three SD variants differ in the severity and dominance of the fitness costs they impose on individuals carrying them. Second, SD-carrying parents produced less fit offspring in some crosses, independent of offspring genotype, indicating that SD alleles can have nongenetic, transgenerational costs in addition to their direct costs. Third, we found that SD carriers sometimes produce a biased offspring sex ratio, perhaps due to off-target effects of SD on the sex chromosomes. Finally, we used a theoretical model to investigate how sex ratio and transgenerational effects alter the population genetics of distorter alleles; accounting for these additional costs helps to explain why real-world segregation distorter alleles are rarer than predicted.

Evolutionary simulations of Z-linked suppression gene drives

6643
L. Holman,  Proceedings of the Royal Society B-Biological Sciences,  286:1-9. 2019-10-09 20:23:58.
Synthetic gene drives may soon be used to suppress or eliminate populations of disease vectors, pathogens, invasive species, and agricultural pests. Recent proposals have focused on using Z-linked gene drives to control species with ZW sex determination, which include Lepidopteran pests, parasitic trematodes, and cane toads. These proposals include Z-linked 'W-shredders', which would suppress populations by cleaving the W chromosome and causing females to produce only sons, as well as Z-linked female-sterilizing gene drives. Here, I use eco-evolutionary simulations to evaluate the potential of some proposed Z-linked gene drives, and to produce recommendations regarding their design and use. The simulations show that W-shredders are likely to be highly effective at eradicating populations provided that resistance to W-shredding cannot evolve. However, W-shredder alleles can invade populations from very low frequencies, making it difficult to eliminate specific populations while leaving nearby populations untouched; this issue may restrict their possible uses.

Peri-Urban Community Attitudes towards Codling Moth Trapping and Suppression Using the Sterile Insect Technique in New Zealand

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G. Paterson, G. L. W. Perry, J. T. S. Walker and D. M. Suckling,  Insects,  10. 2019-10-09 15:21:37.
New, more socially-acceptable technologies are being developed to suppress horticultural pests, because suppression is technically difficult with current technologies, especially in urban areas. One technique involves the release of sterile insects to prevent offspring in the next generation. This technology involves aerial or ground release systems, but this could also create issues for the public. This study investigated community perceptions of a recently-introduced response to codling moth control in New Zealand—Sterile Insect Technique (SIT). Community attitudes to SIT were examined in Hastings, New Zealand, in April, 2018. Eighty-six detailed interviews were undertaken with a random sample of households. This community was very willing (98% agreement) to host a sex pheromone trap in their gardens, and condoned regular visits to monitor traps. Attitudes to SIT were very positive (98% in favor). Once explained, the concept of using unmanned aerial vehicles to deliver sterile insects was also acceptable (98%) to the community. Use of unmanned aerial vehicles to release sterile insects during a hypothetical incursion response of an exotic fruit fly was also supported at 98% by respondent householders. Investigation of community attitudes can be valuable to guide practitioners in determining suitable technologies before an area-wide programme is launched.

Efforts to enhance safety measures for CRISPR/Cas-based gene drive technology in Japan

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T. Tanaka, N. Tanaka, Y. Nagano, H. Kanuka, D. S. Yamamoto, N. Yamamoto, E. Nanba and T. Nishiuch,  Journal of Environment and Safety,  2019-10-07 20:47:13.
Gene drive is a powerful system that can spread a desirable genetic trait into an entire species and/or population of a certain region, bypassing Mendelian rules of inheritance. Recently, one of the genome editing technologies, CRISPR/Cas, has been developed, making it easier to use gene drive in many different organisms. However, gene drive has potential risks that impact genetic diversity when organisms produced by CRISPR/Cas-based Gene Drive Technology (CCGDT) are accidentally released; therefore, a high degree of prudence is required when CCGDT is used. In Japan, a Working Group on Gene Drive has been established in the Academic Association for Promotion of Genetic Studies (AAPGS), and a Statement on the Handling of Gene Drive was issued to the public including research institute across Japan, after comprehensive and extensive discussions by the working group in order to reduce risks posed by CCGDT. A national-wide survey on CCGDT was implemented. The survey revealed that those in managerial positions including members and secretariats of institutional review boards on recombinant DNA, and biosafety officers are conscious of CCGDT, and efforts to grasp experimental plans involving CCGDT are made by utilizing an application form for recombinant DNA experiment. In contrast, potential risks of CCGDT are not understood by many researchers. All stakeholders need to disseminate potential risks and preventive measures regarding CCGDT to all researchers who may wish to use this technology. Researchers should use CCGDT upon understanding its potential risks and taking necessary measures. This report refers to how safety measures for CRISPR/Cas-based gene drive technology which has potential risks to ecological system has been discussed and results of national-wide questionnaire survey on gene drive in Japan based on the poster presentation at the Asian Conference on Safety & Education in Laboratory 2018.

Gene Drives: Dynamics and Regulatory Matters-A Report from the Workshop “Evaluation of Spatial and Temporal Control of Gene Drives,” April 4-5, 2019, Vienna

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B. Giese, J. L. Friess, N. H. Barton, P. W. Messer, F. Debarre, M. F. Schetelig, N. Windbichler, H. Meimberg and C. Boete,  Bioessays,  41:3. 2019-10-07 18:26:19.
Gene Drives are regarded as future tools with a high potential for population control. Due to their inherent ability to overcome the rules of Mendelian inheritance, gene drives (GD) may spread genes rapidly through populations of sexually reproducing organisms. A release of organisms carrying a GD would constitute a paradigm shift in the handling of genetically modified organisms because gene drive organisms (GDO) are designed to drive their transgenes into wild populations and thereby increase the number of GDOs. The rapid development in this field and its focus on wild populations demand a prospective risk assessment with a focus on exposure related aspects. Presently, it is unclear how adequate risk management could be guaranteed to limit the spread of GDs in time and space, in order to avoid potential adverse effects in socio‐ecological systems. The recent workshop on the “Evaluation of Spatial and Temporal Control of Gene Drives” hosted by the Institute of Safety/Security and Risk Sciences (ISR) in Vienna aimed at gaining some insight into the potential population dynamic behavior of GDs and appropriate measures of control. Scientists from France, Germany, England, and the USA discussed both topics in this meeting on April 4–5, 2019. This article summarizes results of the workshop.

Two unresolved issues in community engagement for field trials of genetically modified mosquitoes

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D. B. Resnik,  Pathogens and Global Health,  113:238-245. 2019-09-25 19:32:29.
There is an emerging consensus among scientists, ethicists, and public health officials that substantive and effective engagement with communities and the wider public is required prior to releasing genetically modified mosquitoes into the environment.

Threshold-Dependent Gene Drives in the Wild: Spread, Controllability, and Ecological Uncertainty

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G. A. Backus and J. A. Delborne,  BioScience,  69:900-907. 2019-09-18 16:02:59.
Gene drive technology could allow the intentional spread of a desired gene throughout an entire wild population in relatively few generations. However, there are major concerns that gene drives could either fail to spread or spread without restraint beyond the targeted population. One potential solution is to use more localized threshold-dependent drives, which only spread when they are released in a population above a critical frequency. However, under certain conditions, small changes in gene drive fitness could lead to divergent outcomes in spreading behavior. In the face of ecological uncertainty, the inability to estimate gene drive fitness in a real-world context could prove problematic because gene drives designed to be localized could spread to fixation in neighboring populations if ecological conditions unexpectedly favor the gene drive. This perspective offers guidance to developers and managers because navigating gene drive spread and controllability could be risky without detailed knowledge of ecological contexts.

Mosquito Control

Dye-Braumuller K, Fredregill C, Debboun M.,  Mosquitoes, Communities, and Public Health in Texas,  8:249-278. 2019-09-14 14:00:28.
Globally, mosquito control has evolved over centuries, as humans have learned more about the world’s deadliest animal,that is, the mosquito, and the pathogens they are capable of transmitting. Mosquitoes not only transmit pathogens but also cause severe allergic reactions, intense irritation, and even extensive blood loss to some animals such as livestock. These factors have led to the development of a multitude of techniques and approaches to control mosquitoes throughout centuries. They have been established since Sir Patrick Manson first linked mosquitoes to the transmission of human pathogens when he discovered that the house mosquito harbored and presumably—at that time—was transmitting intermediate larvae of the filarial worm, Wuchereria bancrofti (Manson, 1878; Chernin, 1983; Clements and Harbach, 2017). Due to the wide range of impacts mosquitoes have on humans, large quantities of resources have been dedicated to their control. For example, the United States (US) spends hundreds of millions of dollars to control mosquitoes annually (Foster and Walker, 2009). There were a few major points in US history that led to these expansive control efforts, and the first part of this chapter will describe these milestones

Malaria eradication within a generation: ambitious, achievable, and necessary

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R. G. A. Feachem, I. Chen, O. Akbari, A. Bertozzi-Villa, S. Bhatt, F. Binka, M. F. Boni, C. Buckee, J. Dieleman, A. Dondorp, A. Eapen, N. Sekhri Feachem, S. Filler, P. Gething, R. Gosling, A. Haakenstad, K. Harvard, A. Hatefi, D. Jamison, K. E. Jones, C.,  Lancet,  394:1056-1112. 2019-09-13 15:21:30.
50 years after a noble but flawed attempt to eradicate malaria in the mid-20th century, the global malaria community is once again seriously considering eradication. Momentum towards eradication has been building for decades, and more than half of the world’s countries are now malaria free.

Standard deviations: The biological bases of transmission ratio distortion

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L. Fishman and M. McIntosh,  Annual Review of Genetics,  53:347-372. 2019-09-10 18:59:40.
The rule of Mendelian inheritance is remarkably robust, but deviations from the equal transmission of alternative alleles at a locus [a.k.a. transmission ratio distortion (TRD)] are also commonly observed in genetic mapping populations. Such TRD reveals locus-specific selection acting at some point between the diploid heterozygous parents and progeny genotyping and therefore can provide novel insight into otherwise-hidden genetic and evolutionary processes. Most of the classic selfish genetic elements were discovered through their biasing of transmission, but many unselfish evolutionary and developmental processes can also generate TRD. In this review, we describe methodologies for detecting TRD in mapping populations, detail the arenas and genetic interactions that shape TRD during plant and animal reproduction, and summarize patterns of TRD from across the genetic mapping literature. Finally, we point to new experimental approaches that can accelerate both detection of TRD and characterization of the underlying genetic mechanisms.

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