scholarly journals The t haplotype, a selfish genetic element, manipulates migration propensity in free-living wild house mice Mus musculus domesticus

2018 ◽  
Author(s):  
Jan-Niklas Runge ◽  
Anna K. Lindholm

AbstractLife is built on cooperation between genes, which makes it vulnerable to parasitism. However, selfish genetic elements that exploit this cooperation can achieve large fitness gains by increasing their transmission unfairly relative to the rest of the genome. This leads to counter-adaptations that generate unique selection pressures on the selfish genetic element. This arms race is similar to host-parasite co-evolution. Some multi-host parasites alter the host’s behaviour to increase the chance of transmission to the next host. Here we ask if, similarly to these parasites, a selfish genetic element in house mice, the t haplotype, also manipulates host behaviour, specifically the host’s migration propensity. Variants of the t that manipulate migration propensity could increase in fitness in a meta-population. We show that juvenile mice carrying the t haplotype were more likely to emigrate from and were more often found as migrants within a long-term free-living house mouse population. This result may have applied relevance as the t has been proposed as a basis for artificial gene drive systems for use in population control.

2018 ◽  
Vol 285 (1888) ◽  
pp. 20181333 ◽  
Author(s):  
Jan-Niklas Runge ◽  
Anna K. Lindholm

Life is built on cooperation between genes, which makes it vulnerable to parasitism. Selfish genetic elements that exploit this cooperation can achieve large fitness gains by increasing their transmission relative to the rest of the genome. This leads to counter-adaptations that generate unique selection pressures on the selfish genetic element. This arms race is similar to host–parasite coevolution, as some multi-host parasites alter the host’s behaviour to increase the chance of transmission to the next host. Here, we ask if, similarly to these parasites, a selfish genetic element in house mice, the t haplotype, also manipulates host behaviour, specifically the host’s migration propensity. Variants of the t that manipulate migration propensity could increase in fitness in a meta-population. We show that juvenile mice carrying the t haplotype were more likely to emigrate from and were more often found as migrants within a long-term free-living house mouse population. This result may have applied relevance as the t has been proposed as a basis for artificial gene drive systems for use in population control.


2018 ◽  
Vol 5 (3) ◽  
pp. 172099 ◽  
Author(s):  
Madeleine Geiger ◽  
Marcelo R. Sánchez-Villagra ◽  
Anna K. Lindholm

Similar phenotypic changes occur across many species as a result of domestication, e.g. in pigmentation and snout size. Experimental studies of domestication have concentrated on intense and directed selection regimes, while conditions that approximate the commensal and indirect interactions with humans have not been explored. We examine long-term data on a free-living population of wild house mice that have been indirectly selected for tameness by regular exposure to humans. In the course of a decade, this mouse population exhibited significantly increased occurrence of white patches of fur and decreased head length. These phenotypic changes fit to the predictions of the ‘domestication syndrome'.


2020 ◽  
Vol 11 (1) ◽  
Author(s):  
Andri Manser ◽  
Barbara König ◽  
Anna K. Lindholm

Abstract Gene drives are genetic elements that manipulate Mendelian inheritance ratios in their favour. Understanding the forces that explain drive frequency in natural populations is a long-standing focus of evolutionary research. Recently, the possibility to create artificial drive constructs to modify pest populations has exacerbated our need to understand how drive spreads in natural populations. Here, we study the impact of polyandry on a well-known gene drive, called t haplotype, in an intensively monitored population of wild house mice. First, we show that house mice are highly polyandrous: 47% of 682 litters were sired by more than one male. Second, we find that drive-carrying males are particularly compromised in sperm competition, resulting in reduced reproductive success. As a result, drive frequency decreased during the 4.5 year observation period. Overall, we provide the first direct evidence that the spread of a gene drive is hampered by reproductive behaviour in a natural population.


2019 ◽  
Vol 116 (13) ◽  
pp. 6250-6259 ◽  
Author(s):  
Georg Oberhofer ◽  
Tobin Ivy ◽  
Bruce A. Hay

There is great interest in being able to spread beneficial traits throughout wild populations in ways that are self-sustaining. Here, we describe a chromosomal selfish genetic element,CleaveR[Cleave and Rescue (ClvR)], able to achieve this goal.ClvRcomprises two linked chromosomal components. One, germline-expressed Cas9 and guide RNAs (gRNAs)—the Cleaver—cleaves and thereby disrupts endogenous copies of a gene whose product is essential. The other, a recoded version of the essential gene resistant to cleavage and gene conversion with cleaved copies—the Rescue—provides essential gene function.ClvRenhances its transmission, and that of linked genes, by creating conditions in which progeny lackingClvRdie because they have no functional copies of the essential gene. In contrast, those who inheritClvRsurvive, resulting in an increase inClvRfrequency.ClvRis predicted to spread to fixation under diverse conditions. To test these predictions, we generated aClvRelement inDrosophila melanogaster.ClvRtkois located on chromosome 3 and uses Cas9 and four gRNAs to disruptmelanogaster technical knockout(tko), an X-linked essential gene. Rescue activity is provided bytkofromDrosophila virilis.ClvRtkoresults in germline and maternal carryover-dependent inactivation ofmelanogaster tko(>99% per generation); lethality caused by this loss is rescued by thevirilistransgene;ClvRtkoactivities are robust to genetic diversity in strains from five continents; and uncleavable but functionalmelanogaster tkoalleles were not observed. Finally,ClvRtkospreads to transgene fixation. The simplicity ofClvRsuggests it may be useful for altering populations in diverse species.


2015 ◽  
Vol 282 (1811) ◽  
pp. 20150974 ◽  
Author(s):  
Andreas Sutter ◽  
Anna K. Lindholm

Female multiple mating (polyandry) is widespread across many animal taxa and indirect genetic benefits are a major evolutionary force favouring polyandry. An incentive for polyandry arises when multiple mating leads to sperm competition that disadvantages sperm from genetically inferior mates. A reduction in genetic quality is associated with costly selfish genetic elements (SGEs), and studies in invertebrates have shown that males bearing sex ratio distorting SGEs are worse sperm competitors than wild-type males. We used a vertebrate model species to test whether females can avoid an autosomal SGE, the t haplotype, through polyandry. The t haplotype in house mice exhibits strong drive in t heterozygous males by affecting spermatogenesis and is associated with homozygous in utero lethality. We used controlled matings to test the effect of the t haplotype on sperm competitiveness. Regardless of mating order, t heterozygous males sired only 11% of zygotes when competing against wild-type males, suggesting a very strong effect of the t haplotype on sperm quality. We provide, to our knowledge, the first substantial evidence that polyandry ameliorates the harmful effects of an autosomal SGE arising through genetic incompatibility. We discuss potential mechanisms in our study species and the broader implications for the benefits of polyandry.


Evolution ◽  
2011 ◽  
Vol 65 (9) ◽  
pp. 2435-2447 ◽  
Author(s):  
Andri Manser ◽  
Anna K. Lindholm ◽  
Barbara König ◽  
Homayoun C. Bagheri

2021 ◽  
Author(s):  
Jan-Niklas Runge ◽  
Hanna Kokko ◽  
Anna K. Lindholm

AbstractMeiotic drivers are selfish genetic elements that manipulate meiosis to increase their transmission to the next generation to the detriment of the rest of the genome. The t haplotype in house mice is a naturally occurring meiotic driver with deleterious traits—poor fitness in polyandrous matings and homozygote inviability or infertility—that prevent its fixation. Recently, we discovered a novel effect of t in a long-term field study on free-living wild house mice: t-carriers are more likely to disperse. To ask what known traits of the t haplotype can select for a difference in dispersal between t-carriers and wildtype mice, we built individual-based models with dispersal loci on the t and the homologous wildtype chromosomes. We allow for density-dependent expression of these loci. The t haplotype consistently evolved to increase the dispersal propensity of its carriers, particularly at high densities. By examining variants of the model that modify different costs caused by t, we show that the increase in dispersal is driven by the deleterious traits of t, disadvantage in polyandrous matings and lethal homozygosity or male sterility. Finally, we show that an increase in driver-carrier dispersal can evolve across a range of values in driver strength and disadvantages.


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