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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The effect of malaria control on Plasmodium falciparum in Africa between 2000 and 2015

12672
S. Bhatt, D. J. Weiss, E. Cameron, D. Bisanzio, B. Mappin, U. Dalrymple, K. E. Battle, C. L. Moyes, A. Henry, P. A. Eckhoff, E. A. Wenger, O. Briët, M. A. Penny, T. A. Smith, A. Bennett, J. Yukich, T. P. Eisele, J. T. Griffin, C. A. Fergus, M. Lynch, F. L,  Nature,  526:207-211. 2015-09-16 17:16:47.
Since the year 2000, a concerted campaign against malaria has led to unprecedented levels of intervention coverage across sub-Saharan Africa. Understanding the effect of this control effort is vital to inform future control planning. H

The Trojan Female Technique for pest control: a candidate mitochondrial mutation confers low male fertility across diverse nuclear backgrounds in Drosophila melanogaster

13733
D. K. Dowling, D. M. Tompkins and N. J. Gemmell,  Evolutionary Applications,  8:8710880. 2015-07-15 19:28:56.
The Trojan Female Technique (TFT) was recently proposed as a prospective approach to biological pest control. However, applicability of the TFT relies on mitochondrial mutations whose male-sterilizing effects are general across nuclear genomic contexts. We test this assumption, expressing the candidate TFT-mutation bearing haplotype alongside a range of nuclear backgrounds and comparing its fertility in males, relative to that of control haplotypes

Back to the future: the sterile insect technique against mosquito disease vectors

25916
R. S. Lees, J. R. L. Gilles, J. Hendrichs, M. J. B. Vreysen and K. Bourtzis,  Current Opinion in Insect Science,  10:156-162. 2015-06-03 13:09:41.
With the global burden of mosquito-borne diseases increasing, and some conventional vector control tools losing effectiveness, the sterile insect technique (SIT) is a potential new tool in the arsenal. Equipment and protocols have been developed and validated for efficient mass-rearing, irradiation and release of Aedines and Anophelines that could be useful for several control approaches. Assessment of male quality is becoming more sophisticated, and several groups are well advanced in pilot site selection and population surveillance. It will not be long before SIT feasibility has been evaluated in various settings. Until perfect sexing mechanisms exist, combination of Wolbachia-induced phenotypes, such as cytoplasmic incompatibility and pathogen interference, and irradiation may prove to be the safest solution for population suppression.

Ecological and evolutionary applications for environmental sex reversal of fish

11518
A. McNair, P. M. Lokman, G. P. Closs and S. Nakagawa,  Quarterly Review of Biology,  90:23-44. 2015-03-01 15:38:29.
Environmental sex reversal (ESR), which results in a mismatch between genotypic and phenotypic sex, is well documented in numerous fish species and may be induced by chemical exposure. Historically, research involving piscine ESR has been carried out with a view to improving profitability in aquaculture or to elucidate the processes governing sex determination and sexual differentiation. However, recent studies in evolution and ecology suggest research on ESR now has much wider applications and ramifications. We begin with an overview of ESR in fish and a brief review of the traditional applications thereof We then discuss ESR and its potential demographic consequences in wild populations. Theory even suggests sex-reversed fish may be purposefully released to manipulate population dynamics. We suggest new research directions that may prove fruitful in understanding how ESR at the individual level translates to population-level processes. In the latter portion of the review we focus on evolutionary applications of ESR Sex-reversal studies from the aquaculture literature provide insight in to the evolvability of determinants of sexual phenotype. Additionally, induced sex reversal can provide information about the evolution of sex chromosomes and sex-linked traits. Recently, naturally occurring ESR has been implicated as a mechanism contributing to the evolution of sex chromosomes.

Gene drive turns mosquitoes into malaria fighters

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Pennisi, E,  Science,  350:1014-1014. 2015-01-21 00:00:00.
The war against malaria has a new ally: a controversial technology for spreading genes throughout a population of animals. In the laboratory, researchers have harnessed a so-called gene drive to efficiently endow mosquitoes with genes that make them immune to the malaria parasite—and unable to spread it. On its own, gene drive won't get rid of malaria, but if successfully applied in the wild the method could help wipe out the disease, at least in some corners of the world. The approach “can bring us to zero [cases],” says Nora Besansky, a geneticist at the University of Notre Dame in South Bend, Indiana, who specializes in malaria-carrying mosquitoes

Female house mice avoid fertilization by t haplotype incompatible males in a mate choice experiment

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Manser, AK, B.; Lindholm, A. K.,  Journal of Evolutionary Biology,  28:54-64. 2015-01-20 00:00:00.
The t haplotype in house mice is a well-known selfish genetic element with detrimental, nonadditive fitness consequences to its carriers: recessive lethal mutations cause t/t homozygotes to perish in utero. Given the severe genetic incompatibility imposed by the t haplotype, we predict females to avoid fertilization by t haplotype incompatible males. Indeed, some of the strongest evidence for compatibility mate choice is related to the t haplotype in house mice. However, all previous evidence for compatibility mate choice in this system is based on olfactory preference. It is so far unknown how general these preferences are and whether they are relevant in an actual mating context. Here, we assess female compatibility mate choice related to t haplotypes in a setting that - for the first time - allowed females to directly interact and mate with males. This approach enabled us to analyse female behaviour during the testing period, and the resulting paternity success and fitness consequences of a given choice. We show that genetic incompatibilities arising from the t haplotype had severe indirect fitness consequences and t females avoided fertilization by t incompatible males. The results are inconclusive whether this avoidance of t fertilization by t females was caused by pre- or post-copulatory processes.

Can systematic reviews inform GMO risk assessment and risk management?

4121
Kohl, CF, G.; Sweet, J.; Spok, A.; Haddaway, N.R.; Wilhelm, R.; Unger, S.; Schiemann, J.,  Frontiers in Bioengineering and Biotechnology,  3:113. 2015-01-19 00:00:00.
Systematic reviews represent powerful tools to identify, collect, synthesize, and evaluate primary research data on specific research questions in a highly standardized and reproducible manner. They enable the defensible synthesis of outcomes by increasing precision and minimizing bias whilst ensuring transparency of the methods used. This makes them especially valuable to inform evidence-based risk analysis and decision making in various topics and research disciplines. Although seen as a “gold standard” for synthesizing primary research data, systematic reviews are not without limitations as they are often cost, labor and time intensive and the utility of synthesis outcomes depends upon the availability of sufficient and robust primary research data. In this paper, we (1) consider the added value systematic reviews could provide when synthesizing primary research data on genetically modified organisms (GMO) and (2) critically assess the adequacy and feasibility of systematic review for collating and analyzing data on potential impacts of GMOs in order to better inform specific steps within GMO risk assessment and risk management. The regulatory framework of the EU is used as an example, although the issues we discuss are likely to be more widely applicable.

A prezygotic transmission distorter acting equally in female and male zebra finches Taeniopygia guttata

4120
Knief, US, H.; Ellegren, H.; Kempenaers, B.; Forstmeier, W.,  Molecular Ecology,  24:3846-3859. 2015-01-18 00:00:00.
The two parental alleles at a specific locus are usually inherited with equal probability to the offspring. However, at least three processes can lead to an apparent departure from fair segregation: early viability selection, biased gene conversion and various kinds of segregation distortion. Here, we conduct a genome-wide scan for transmission distortion in a captive population of zebra finches (Taeniopygia guttata) using 1302 single-nucleotide polymorphisms (SNPs) followed by confirmatory analyses on independent samples from the same population. In the initial genome-wide scan, we found significant distortion at three linked loci on chromosome Tgu2 and we were able to replicate this finding in each of two follow-up data sets [overall transmission ratio=0.567 (95% CI=0.536-0.600), based on 1101 informative meioses]. Although the driving allele was preferentially transmitted by both heterozygous females [ratio=0.560 (95% CI=0.519-0.603)] and heterozygous males [ratio=0.575 (95% CI=0.531-0.623)], we could rule out postzygotic viability selection and biased gene conversion as possible mechanisms. Early postzygotic viability selection is unlikely, because it would result in eggs with no visible embryo and hence no opportunity for genotyping, and we confirmed that both females and males heterozygous for the driving allele did not produce a larger proportion of such eggs than homozygous birds. Biased gene conversion is expected to be rather localized, while we could trace transmission distortion in haplotypes of several megabases in a recombination desert. Thus, we here report the rare case of a prezygotically active transmission distorter operating equally effectively in female and male meioses.

Double trouble: combined action of meiotic drive and Wolbachia feminization in Eurema butterflies

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Kern, PC, J. M.; Kageyama, D.; Riegler, M.,  Biology Letters,  11:20150095. 2015-01-17 00:00:00.
Arthropod sex ratios can be manipulated by a diverse range of selfish genetic elements, including maternally inherited Wolbachia bacteria. Feminization by Wolbachia is rare but has been described for Eurema mandarina butterflies. In this species, some phenotypic and functional females, thought to be ZZ genetic males, are infected with a feminizing Wolbachia strain, wFem. Meanwhile, heterogametic WZ females are not infected with wFem. Here, we establish a quantitative PCR assay allowing reliable sexing in three Eurema species. Against expectation, all E. mandarina females, including wFem females, had only one Z chromosome that was paternally inherited. Observation of somatic interphase nuclei confirmed that W chromatin was absent in wFem females, but present in females without wFem. We conclude that the sex bias in wFem lines is due to meiotic drive (MD) that excludes the maternal Z and thus prevents formation of ZZ males. Furthermore, wFem lines may have lost the W chromosome or harbour a dysfunctional version, yet rely on wFem for female development; removal of wFem results in all-male offspring. This is the first study that demonstrates an interaction between MD and Wolbachia feminization, and it highlights endosymbionts as potentially confounding factors in MD of sex chromosomes.

Coevolutionary dynamics of polyandry and sex-linked meiotic drive

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Holman, LP, T. A. R.; Wedell, N.; Kokko, H.,  Evolution,  69:709-720. 2015-01-16 00:00:00.
Segregation distorters located on sex chromosomes are predicted to sweep to fixation and cause extinction via a shortage of one sex, but in nature they are often found at low, stable frequencies. One potential resolution to this longstanding puzzle involves female multiple mating (polyandry). Because many meiotic drivers severely reduce the sperm competitive ability of their male carriers, females are predicted to evolve more frequent polyandry and thereby promote sperm competition when a meiotic driver invades. Consequently, the driving chromosome's relative fitness should decline, halting or reversing its spread. We used formal modeling to show that this initially appealing hypothesis cannot resolve the puzzle alone: other selective pressures (e.g., low fitness of drive homozygotes) are required to establish a stable meiotic drive polymorphism. However, polyandry and meiotic drive can strongly affect one another's frequency, and polyandrous populations may be resistant to the invasion of rare drive mutants.

Sex chromosome drive

4117
Helleu, QG, P. R.; Montchamp-Moreau, C.,  Cold Spring Harbor Perspectives in Biology,  7:a017616. 2015-01-15 00:00:00.
Sex chromosome drivers are selfish elements that subvert Mendel's first law of segregation and therefore are over represented among the products of meiosis. The sex-biased progeny produced then fuels an extended genetic conflict between the driver and the rest of the genome. Many examples of sex chromosome drive are known, but the occurrence of this phenomenon is probably largely underestimated because of the difficulty to detect it. Remarkably, nearly all sex chromosome drivers are found in two clades, Rodentia and Diptera. Although very little is known about the molecular and cellular mechanisms of drive, epigenetic processes such as chromatin regulation could be involved in many instances. Yet, its evolutionary consequences are far-reaching, from the evolution of mating systems and sex determination to the emergence of new species.

Mating type and spore killing characterization of Fusarium verticillioides strains

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Guo, LB, A. Z.; Geiser, D. M.; Jimenez-Gasco, M. D.; Kuldau, G. A.,  Mycological Progress,  14:1045. 2015-01-14 00:00:00.
Fusarium verticillioides is a heterothallic ascomycete causing maize ear rot, and produces fumonisin mycotoxins harmful to livestock and human health. A meiotic drive phenomenon called spore killing has been reported in several filamentous fungi including F. verticillioides. F. verticillioides reference genome strain M-3125 (FGSC 7600) is spore killer sensitive (SKS), and genetic crosses of M-3125 with a strain carrying SKK (the killer element) result in only four viable ascospores per ascus instead of the normal eight ascospores. We sought to identify a strain of F. verticillioides that is SKS and MAT1-2 for use in genetic analysis with M-3125. To accomplish this, we screened 50 F. verticillioides strains from the Fusarium Research Center at The Pennsylvania State University, USA for spore killing. To characterize the mating types of these strains, portions of the MAT locus idiomorphs were amplified using polymerase chain reaction, and genetic crosses were performed. The PCR amplification results show that 18 of the 50 strains are MAT1-2 and 32 are MAT1-1. Genetic crosses between M-3125 and 11 of the 18 MAT1-2 strains produced normal perithecia. Crosses between two (M-8024 and M-7815) of the 11 strains and M-3125 produced perithecia with eight ascospores per ascus, and nine others had only four ascospores per ascus, suggesting that M-8024 and M-7815 are SKS and the other nine are SKK. This study expands our knowledge of mating type and spore killing in F. verticillioides and identifies two SKS, MAT1-2 strains for use in genetic crosses with genome reference strain M-3125.

Highly efficient Cas9-mediated gene drive for population modification of the malaria vector mosquito Anopheles stephensi

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Gantz, VMJ, N.; Tatarenkova, O.; Fazekas, A.; Macias, V. M.; Bier, E.; James, A. A.,  Proceedings of the National Academy of Sciences of the United States of America,  112:e6736-e6743. 2015-01-13 00:00:00.
Genetic engineering technologies can be used both to create transgenic mosquitoes carrying antipathogen effector genes targeting human malaria parasites and to generate gene-drive systems capable of introgressing the genes throughout wild vector populations. We developed a highly effective autonomous Clustered Regularly Interspaced Short Palindromic Repeats (CRISPR)-associated protein 9 (Cas9)-mediated gene-drive system in the Asian malaria vector Anopheles stephensi, adapted from the mutagenic chain reaction (MCR). This specific system results in progeny of males and females derived from transgenic males exhibiting a high frequency of germ-line gene conversion consistent with homology-directed repair (HDR). This system copies an similar to 17-kb construct from its site of insertion to its homologous chromosome in a faithful, site-specific manner. Dual anti-Plasmodium falciparum effector genes, a marker gene, and the autonomous gene-drive components are introgressed into similar to 99.5% of the progeny following outcrosses of transgenic lines to wild-type mosquitoes. The effector genes remain transcriptionally inducible upon blood feeding. In contrast to the efficient conversion in individuals expressing Cas9 only in the germ line, males and females derived from transgenic females, which are expected to have drive component molecules in the egg, produce progeny with a high frequency of mutations in the targeted genome sequence, resulting in near-Mendelian inheritance ratios of the transgene. Such mutant alleles result presumably from non-homologous end-joining (NHEJ) events before the segregation of somatic and germ-line lineages early in development. These data support the design of this system to be active strictly within the germ line. Strains based on this technology could sustain control and elimination as part of the malaria eradication agenda.

The mutagenic chain reaction: A method for converting heterozygous to homozygous mutations

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V. M. Gantz and E. Bier,  Science,  348:442. 2015-01-12 00:00:00.
Loss-of-function mutations may only produce a mutant phenotype when both copies of the gene are mutated. Gantz and Bier developed a method they call mutagenic chain reaction (MCR) that autocatalytically produces homozygous mutations. MCR uses the initial mutated allele to cause a mutation in the allele on the opposing chromosome and thus the homozygosity of the trait. MCR technology could have broad applications in diverse organisms.Science, this issue p. 442 An organism with a single recessive loss-of-function allele will typically have a wild-type phenotype, whereas individuals homozygous for two copies of the allele will display a mutant phenotype. We have developed a method called the mutagenic chain reaction (MCR), which is based on the CRISPR/Cas9 genome-editing system for generating autocatalytic mutations, to produce homozygous loss-of-function mutations. In Drosophila, we found that MCR mutations efficiently spread from their chromosome of origin to the homologous chromosome, thereby converting heterozygous mutations to homozygosity in the vast majority of somatic and germline cells. MCR technology should have broad applications in diverse organisms.

Centromere-associated meiotic drive and female fitness variation in Mimulus

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Fishman, LK, J. K.,  Evolution,  69:1208-1218. 2015-01-11 00:00:00.
Female meiotic drive, in which chromosomal variants preferentially segregate to the egg pole during asymmetric female meiosis, is a theoretically pervasive but still mysterious form of selfish evolution. Like other selfish genetic elements, driving chromosomes may be maintained as balanced polymorphisms by pleiotropic or linked fitness costs. A centromere-associated driver (D) with a approximate to 58:42 female-specific transmission advantage occurs at intermediate frequency (32-40%) in the Iron Mountain population of the yellow monkeyflower, Mimulus guttatus. Previously determined male fertility costs are sufficient to prevent the fixation of D, but predict a higher equilibrium frequency. To better understand the dynamics and effects of D, we developed a new population genetic model and measured genotype-specific lifetime female fitness in the wild. In three of four years, and across all years, D imposed significant recessive seedset costs, most likely due to hitchhiking by deleterious mutations. With both male and female costs as measured, and 58:42 drive, our model predicts an equilibrium frequency of D (38%) very close to the observed value. Thus, D represents a rare selfish genetic element whose local population genetic dynamics have been fully parameterized, and the observation of equilibrium sets the stage for investigations of coevolution with suppressors.

Sex ratio meiotic drive as a plausible evolutionary mechanism for hybrid male sterility

Zhang, LBS, T. N.; Woldesellassie, F.; Xiao, H. L.; Tao, Y.,  PLOS Genetics,  11:e1005073. 2015-01-11 00:00:00.
Biological diversity on Earth depends on the multiplication of species or speciation, which is the evolution of reproductive isolation such as hybrid sterility between two new species. An unsolved puzzle is the exact mechanism(s) that causes two genomes to diverge from their common ancestor so that some divergent genes no longer function properly in the hybrids. Here we report genetic analyses of divergent genes controlling male fertility and sex ratio in two very young fruitfly species, Drosophila albomicans and D. nasuta. A majority of the genetic divergence for both traits is mapped to the same regions by quantitative trait loci mappings. With introgressions, six major loci are found to contribute to both traits. This genetic colocalization implicates that genes for hybrid male sterility have evolved primarily for controlling sex ratio. We propose that genetic conflicts over sex ratio may operate as a perpetual dynamo for genome divergence. This particular evolutionary mechanism may largely contribute to the rapid evolution of hybrid male sterility and the disproportionate enrichment of its underlying genes on the X chromosome - two patterns widely observed across animals.

Duplication and adaptive evolution of a key centromeric protein in Mimulus, a genus with female meiotic drive

4112
Finseth, FRD, Y. Z.; Saunders, A.; Fishman, L.,  Molecular Biology and Evolution,  32:2694-2706. 2015-01-10 00:00:00.
The fundamental asymmetry of female meiosis creates an arena for genetic elements to compete for inclusion in the egg, promoting the selfish evolution of centromere variants that maximize their transmission to the future egg. Such "female meiotic drive" has been hypothesized to explain the paradoxically complex and rapidly evolving nature of centromeric DNA and proteins. Although theoretically widespread, few cases of active drive have been observed, thereby limiting the opportunities to directly assess the impact of centromeric drive on molecular variation at centromeres and binding proteins. Here, we characterize the molecular evolutionary patterns of CENH3, the centromere-defining histone variant, in Mimulus monkeyflowers, a genus with one of the few known cases of active centromere-associated female meiotic drive. First, we identify a novel duplication of CENH3 in diploid Mimulus, including in lineages with actively driving centromeres. Second, we demonstrate long-term adaptive evolution at several sites in the N-terminus of CENH3, a region with some meiosis-specific functions that putatively interacts with centromeric DNA. Finally, we infer that the paralogs evolve under different selective regimes; some sites in the N-terminus evolve under positive selection in the pro-orthologs or only one paralog (CENH3_B) and the paralogs exhibit significantly different patterns of polymorphism within populations. Our finding of long-term, adaptive evolution at CENH3 in the context of centromere-associated meiotic drive supports an antagonistic, coevolutionary battle for evolutionary dominance between centromeric DNA and binding proteins.

R2d2 and hyperdrive mechanisms (in Mouse meiosis)

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Zanders, SEM, H. S.,  PLOS Genetics,  11:1-4. 2015-01-10 00:00:00.
Mendelian transmission is established during meiosis, the cell division that generates haploidgametes (e.g., sperm and eggs) from diploid germ cells. Meiosis does not, however, have to befair. Selfish genetic elements, or meiotic drivers, have evolved to cheat this process in order tobe packaged into functional gametes more often than the expected 50% probability. By biasingallele transmission in their favor, meiotic drive alleles can short-circuit natural selection, caus-ing their spread even if they are harmful to organismal fitness. Indeed, meiotic drive alleles arethought to be directly or indirectly associated with infertility in diverse eukaryotes, from fungito flies to humans [2].

Opinion: Is CRISPR-based gene drive a biocontrol silver bullet or global conservation threat?

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Webber, BLR, S.; Edwards, O. R.,  Proceedings of the National Academy of Sciences of the United States of America,  112:10565-10567. 2015-01-09 00:00:00.
Scientists have recognized the potential for applying gene drive technologies to the control of invasive species for several years, yet debate about the application of gene drive has been primarily restricted to mosquitoes. Recent developments in clustered regularly interspaced short palindromic repeats (CRISPR)-Cas9 technology have restarted discussions of using gene drive for invasive species control.

Safeguarding CRISPR-Cas9 gene drives in yeast

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DiCarlo, JEC, A.; Dietz, S. L.; Esvelt, K. M.; Church, G. M.,  Nature Biotechnology,  33:1250-1255. 2015-01-09 00:00:00.
RNA-guided gene drives capable of spreading genomic alterations made in laboratory organisms through wild populations could be used to address environmental and public health problems. However, the possibility of unintended genome editing occurring through the escape of strains from laboratories, coupled with the prospect of unanticipated ecological change, demands caution. We report the efficacy of CRISPR-Cas9 gene drive systems in wild and laboratory strains of the yeast Saccharomyces cerevisiae. Furthermore, we address concerns surrounding accidental genome editing by developing and validating methods of molecular confinement that minimize the risk of unwanted genome editing. We also present a drive system capable of overwriting the changes introduced by an earlier gene drive. These molecular safeguards should enable the development of safe CRISPR gene drives for diverse organisms.

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