Abstract:Hybrid sterility is one of the earliest postzygotic isolating mechanisms to evolve between two recently diverged species. Here we identify causes underlying hybrid infertility of two recently diverged fission yeast species Schizosaccharomyces pombe and S. kambucha, which mate to form viable hybrid diploids that efficiently complete meiosis, but generate few viable gametes. We find that chromosomal rearrangements and related recombination defects are major but not sole causes of hybrid infertility. At least thr… Show more
“…Many fungi are known to have evolved inversions of parts of their chromosomes, which can block recombination between chromosomes during meiosis [42,43]. Such recombination blocks are most easily observed when the effects are severe, which is the case in meiotic drive elements as seen in S. pombe [44] or the spore killers in Neurospora intermedia [45]. In both cases, rearrangements cause linkage between elements that together are beneficial.…”
Section: Sexual Reproduction and Recombinationmentioning
One contribution of 15 to a theme issue 'Weird sex: the underappreciated diversity of sexual reproduction'. Fungi are a diverse group of organisms with a huge variation in reproductive strategy. While almost all species can reproduce sexually, many reproduce asexually most of the time. When sexual reproduction does occur, large variation exists in the amount of in-and out-breeding. While budding yeast is expected to outcross only once every 10 000 generations, other fungi are obligate outcrossers with well-mixed panmictic populations. In this review, we give an overview of the costs and benefits of sexual and asexual reproduction in fungi, and the mechanisms that evolved in fungi to reduce the costs of either mode. The proximate molecular mechanisms potentiating outcrossing and meiosis appear to be present in nearly all fungi, making them of little use for predicting outcrossing rates, but also suggesting the absence of true ancient asexual lineages. We review how population genetic methods can be used to estimate the frequency of sex in fungi and provide empirical data that support a mixed mode of reproduction in many species with rare to frequent sex in between rounds of mitotic reproduction. Finally, we highlight how these estimates might be affected by the fungus-specific mechanisms that evolved to reduce the costs of sexual and asexual reproduction.This article is part of the themed issue 'Weird sex: the underappreciated diversity of sexual reproduction'.
“…Many fungi are known to have evolved inversions of parts of their chromosomes, which can block recombination between chromosomes during meiosis [42,43]. Such recombination blocks are most easily observed when the effects are severe, which is the case in meiotic drive elements as seen in S. pombe [44] or the spore killers in Neurospora intermedia [45]. In both cases, rearrangements cause linkage between elements that together are beneficial.…”
Section: Sexual Reproduction and Recombinationmentioning
One contribution of 15 to a theme issue 'Weird sex: the underappreciated diversity of sexual reproduction'. Fungi are a diverse group of organisms with a huge variation in reproductive strategy. While almost all species can reproduce sexually, many reproduce asexually most of the time. When sexual reproduction does occur, large variation exists in the amount of in-and out-breeding. While budding yeast is expected to outcross only once every 10 000 generations, other fungi are obligate outcrossers with well-mixed panmictic populations. In this review, we give an overview of the costs and benefits of sexual and asexual reproduction in fungi, and the mechanisms that evolved in fungi to reduce the costs of either mode. The proximate molecular mechanisms potentiating outcrossing and meiosis appear to be present in nearly all fungi, making them of little use for predicting outcrossing rates, but also suggesting the absence of true ancient asexual lineages. We review how population genetic methods can be used to estimate the frequency of sex in fungi and provide empirical data that support a mixed mode of reproduction in many species with rare to frequent sex in between rounds of mitotic reproduction. Finally, we highlight how these estimates might be affected by the fungus-specific mechanisms that evolved to reduce the costs of sexual and asexual reproduction.This article is part of the themed issue 'Weird sex: the underappreciated diversity of sexual reproduction'.
“…In the case of Sp/Sk hybrids (and likely other pairings), the infertility is caused by both chromosomal rearrangements and multiple meiotic drivers (Zanders et al, 2014; Avelar et al, 2013). Indeed, we previously found that genes on each of the three Sk chromosomes are capable of enacting gamete (spore)-killing meiotic drive against their Sp homologs (Figure 1A) (Zanders et al, 2014). However, the genes responsible for the drive phenotypes were unknown.10.7554/eLife.26033.003Figure 1.A complex meiotic drive landscape on Sk and Sp chromosome 3 is revealed by recombination mapping.( A ) A cross between Sk and Sp generates a heterozygote that has low fertility and preferentially transmits Sk alleles on all three chromosomes into viable gametes (Zanders et al, 2014).…”
Section: Introductionmentioning
confidence: 99%
“…In Sp , this region contains wtf4 and the wtf3 pseudogene. The syntenic region in Sk contains only one wtf gene, wtf4 . DOI:
http://dx.doi.org/10.7554/eLife.26033.00310.7554/eLife.26033.004Breakpoints between Sp and Sk -derived DNA sequences.The introgression strains used in diploids 1–8 were sequenced and genotyped for single-nucleotide polymorphisms (SNPs) that reliably distinguish Sk and Sp as in (Zanders et al, 2014). The SNPs flanking the recombination event (left and right boundaries) that generated each breakpoint between Sp and Sk DNA for each introgression strain are shown.…”
Section: Introductionmentioning
confidence: 99%
“…This effort was complicated by the different karyotypes of Sp and Sk chromosomes 2 and 3 (Zanders et al, 2014). We used rec12∆ strains to limit recombination, but rare recombinants (e.g.…”
Meiotic drivers are selfish genes that bias their transmission into gametes, defying Mendelian inheritance. Despite the significant impact of these genomic parasites on evolution and infertility, few meiotic drive loci have been identified or mechanistically characterized. Here, we demonstrate a complex landscape of meiotic drive genes on chromosome 3 of the fission yeasts Schizosaccharomyces kambucha and S. pombe. We identify S. kambucha wtf4 as one of these genes that acts to kill gametes (known as spores in yeast) that do not inherit the gene from heterozygotes. wtf4 utilizes dual, overlapping transcripts to encode both a gamete-killing poison and an antidote to the poison. To enact drive, all gametes are poisoned, whereas only those that inherit wtf4 are rescued by the antidote. Our work suggests that the wtf multigene family proliferated due to meiotic drive and highlights the power of selfish genes to shape genomes, even while imposing tremendous costs to fertility.DOI:
http://dx.doi.org/10.7554/eLife.26033.001
“…When suppressed and no longer able to manifest their selfish action, such genetic elements are predicted to decay with mutation in a manner similar to inactive transposable elements. In instances where they have not fully decayed but are nonetheless successfully suppressed, their presence can be revealed by crosses between closely related species which may genetically separate the toxinantidote locus from its suppressor (Tao et al, 2001(Tao et al, , 2007aZanders et al, 2014). Fig.…”
Selfishness is pervasive and manifests at all scales of biology, from societies, to individuals, to genetic elements within a genome. The relentless struggle to seek evolutionary advantages drives perpetual cycles of adaptation and counter-adaptation, commonly referred to as Red Queen interactions. In this review, we explore insights gleaned from molecular and genetic studies of such genetic conflicts, both extrinsic (between genomes) and intrinsic (within genomes or cells). We argue that many different characteristics of selfish genetic elements can be distilled into two types of advantages: an overreplication advantage (e.g. mobile genetic elements in genomes) and a transmission distortion advantage (e.g. meiotic drivers in populations). These two general categories may help classify disparate types of selfish genetic elements.
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