Having sex, yes, but with whom? Inferences from fungi on the evolution of anisogamy and mating types. Biol Rev Camb Philos Soc

Université Lille Nord de France, USTL, GEPV, CNRS, FRE 3268, Villeneuve d'Ascq, France.
Biological Reviews (Impact Factor: 9.67). 05/2011; 86(2):421-42. DOI: 10.1111/j.1469-185X.2010.00153.x
Source: PubMed


The advantage of sex has been among the most debated issues in biology. Surprisingly, the question of why sexual reproduction generally requires the combination of distinct gamete classes, such as small and large gametes, or gametes with different mating types, has been much less investigated. Why do systems with alternative gamete classes (i.e. systems with either anisogamy or mating types or both) appear even though they restrict the probability of finding a compatible mating partner? Why does the number of gamete classes vary from zero to thousands, with most often only two classes? We review here the hypotheses proposed to explain the origin, maintenance, number, and loss of gamete classes. We argue that fungi represent highly suitable models to help resolve issues related to the evolution of distinct gamete classes, because the number of mating types vary from zero to thousands across taxa, anisogamy is present or not, and because there are frequent transitions between these conditions. We review the nature and number of gamete classes in fungi, and we attempt to draw inferences from these data on the evolutionary forces responsible for their appearance, loss or maintenance, and number.

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    • "This division works regardless of primary or secondary traits. For a recent review about why in most species there are only two sexes and why fungi are an exception can help to understand the origins of binary sex, see Billiard et al. (2011). Gender matters but we cannot agree with the simplified definition of gender which is ''how some groups make distinctions ,''equaling gender to femininity and masculinity (p. "
    Archives of Sexual Behavior 09/2015; DOI:10.1007/s10508-015-0630-1 · 3.53 Impact Factor
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    • "These non-homologous recombination events brought together both mating-type alleles in the same haploid genome, which conferred both mating-type functions and thus universal mating compatibility in most ascomycetes (Gioti et al., 2012). Such a rearrangement to the genomic structures affecting mating compatibility may confer an advantage when waiting for a compatible haploid mate is costly (Billiard et al., 2011), as it confers a universal compatibility for mating, and therefore increases the chance to find a compatible mate (Billiard et al., 2011, 2012). Such events of unusual recombination can cause changes in breeding systems from heterothallism to homothallism as observed in Aspergillus nidulans (Paoletti et al., 2007), Neurospora spp. "
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    ABSTRACT: It is striking that, while central to sexual reproduction, the genomic regions determining sex or mating-types are often characterized by suppressed recombination that leads to a decrease in the efficiency of selection, shelters genetic load, and inevitably contributes to their genic degeneration. Research on model and lesser-explored fungi has revealed similarities in recombination suppression of the genomic regions involved in mating compatibility across eukaryotes, but fungi also provide opposite examples of enhanced recombination in the genomic regions that determine their mating types. These contrasted patterns of genetic recombination (sensu lato, including gene conversion and ectopic recombination) in regions of the genome involved in mating compatibility point to important yet complex processes occurring in their evolution. A number of pieces in this puzzle remain to be solved, in particular on the unclear selective forces that may cause the patterns of recombination, prompting theoretical developments and experimental studies. This review thus points to fungi as a fascinating group for studying the various evolutionary forces at play in the genomic regions involved in mating compatibility.
    Fungal Biology Reviews 07/2015; DOI:10.1016/j.fbr.2015.06.001
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    • "Some fungal mating-type chromosomes can also display recombination suppression and size dimorphism analogous to sex chromosomes (Fraser, et al. 2004; Menkis, et al. 2008; Hood, et al. 2013; Grognet, et al. 2014). Mating-type chromosomes carry the genes regulating mating compatibility (e.g., via pre-mating pheromones and receptors and post-mating homeodomain proteins) but not those determining male/female functions (Billiard, et al. 2011). Mating occurs in the haploid stage in fungi, and consequently their mating–type chromosomes are always in a heterogametic condition in diploids. "
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    ABSTRACT: Dimorphic mating-type chromosomes in fungi are excellent models for understanding the genomic consequences of recombination suppression. Their suppressed recombination and reduced effective population size are expected to limit the efficacy of natural selection, leading to genomic degeneration. Our aim was to identify the sequences of the mating-type chromosomes (a1 and a2) of the anther smut fungi and to investigate degeneration in their non-recombining regions. We used the haploid a1 Microbotryum lychnidis-dioicae reference genome sequence. The a1 and a2 mating-type chromosomes were both isolated electrophoretically and sequenced. Integration with restriction-digest optical maps identified regions of recombination and non-recombination in the mating-type chromosomes. Genome sequence data was also obtained for twelve other Microbotryum species. We found strong evidence of degeneration across the genus in the non-recombining regions of the mating-type chromosomes, with significantly higher rates of non-synonymous substitution (dN/dS) than in non-mating-type chromosomes or in recombining regions of the mating-type chromosomes. The non-recombining regions of the mating-type chromosomes also showed high transposable element content, weak gene expression and gene losses. The levels of degeneration did not differ between the a1 and a2 mating-type chromosomes, consistent with the lack of homogametic/heterogametic asymmetry between them, and contrasting with X/Y or Z/W sex chromosomes. © The Author(s) 2014. Published by Oxford University Press on behalf of the Society for Molecular Biology and Evolution.
    12/2014; 32(4):msu396. DOI:10.1093/molbev/msu396
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