Evolutionary strata on young mating-type chromosomes despite the lack of sexual antagonism

Abstract

Sex chromosomes can display successive steps of recombination suppression known as "evolutionary strata," which are thought to result from the successive linkage of sexually antagonistic genes to sex-determining genes. However, there is little evidence to support this explanation. Here we investigate whether evolutionary strata can evolve without sexual antagonism using fungi that display suppressed recombination extending beyond loci determining mating compatibility despite lack of male/female roles associated with their mating types. By comparing full-length chromosome assemblies from five anther-smut fungi with or without recombination suppression in their mating-type chromosomes, we inferred the ancestral gene order and derived chromosomal arrangements in this group. This approach shed light on the chromosomal fusion underlying the linkage of mating-type loci in fungi and provided evidence for multiple clearly resolved evolutionary strata over a range of ages (0.9-2.1 million years) in mating-type chromosomes. Several evolutionary strata did not include genes involved in mating-type determination. The existence of strata devoid of matingtype genes, despite the lack of sexual antagonism, calls for a unified theory of sex-related chromosome evolution, incorporating, for example, the influence of partially linked deleterious mutations and the maintenance of neutral rearrangement polymorphism due to balancing selection on sexes and mating types.evolutionary strata | chromosomal rearrangements | fungi | genomic degeneration | mating-type chromosomes

Sex‐antagonistic genes, XY recombination and feminized Y chromosomes

“…As pointed out by Ironside (2010), an inversion occurring on an autosome is expected to segregate for some time in populations, temporarily preventing recombination in heterozygous individuals, but will ultimately be either fixed or lost by drift, which will restore full recombination; if, by contrast, such an inversion is fixed by drift on the X or on the Y chromosomes, it will definitively stop recombination between sex chromosomes. Recent evidence for evolutionary strata on fungal mating-type chromosomes demonstrates that sex chromosomes may stop recombining and differentiate in the absence of sexual conflict (Branco et al, 2017). When such a drift-induced recombination arrest occurs in species with sexes and sexual conflicts, then SA genes will subsequently accumulate on sex chromosomes, but as a consequence of recombination arrest, and not as a cause.…”

Congruent population genetic structures and divergence histories in anther‐smut fungi and their host plants Silene italica and the Silene nutans species complex

“…We thus analysed a total of 109 Microbotryum genomes. For read mapping, we used as reference genome the high‐quality haploid genome assembly of the MvSn‐1249 M. violaceum s.s. strain corresponding to the a 2 mating type (collected on S. nutans ) previously obtained with P6/C4 Pacific Biosciences SMRT technology and annotated for gene models (Branco et al, 2017). The MvSn‐1249‐A2 assembly was accessed from GenBank BioProject accession number PRJEB12080 (BioSample ID: SAMEA3706514, assembly: GCA_900014965).…”

“…To increase our power to distinguish between different evolutionary scenarios, we performed model choice and parameter estimation by comparing scenarios or groups of scenarios in sequential rounds, each round testing a particular type of evolutionary event, either divergence time, order of divergence or presence of gene flow (Estoup, Raynal, Verdu, & Marin, 2018;Liu et al, 2019) (Table 1; Table S5). We built scenarios based on the genetic clusters obtained using microsatellite markers and on previous analyses of divergence of anther-smut fungi and their host species (Badouin et al, 2017;Gladieux et al, 2013;Martin et al, 2016Martin et al, , 2017Van Rossum et al, 2018). The tested scenarios varied regarding the time of divergence, the relative order of divergence of fungal genetic clusters and the occurrence of gene flow among genetic fungal clusters (Table S5).…”

“…The plant Silene latifolia and its anther-smut fungus Microbotryum lychnidis-dioicae display strong congruence of population genetic structures and plant local adaptation at regional and continental scales, suggesting the existence of co-evolution in the system (Delmotte, Bucheli, & Shykoff, 1999;Feurtey et al, 2016;Kaltz et al, 1999). Population genetic structures of both the host and the fungal pathogen probably resulted from past climatic events, showing the hallmarks of recolonization from former glacial refugia in Europe (Badouin et al, 2017;Gladieux, Devier, Aguileta, Cruaud, & Giraud, 2013;Gladieux et al, 2011;Taylor & Keller, 2007;Vercken et al, 2010). The congruence of host and pathogen population genetic structures has not been investigated in other anther-smut fungi-Silene pairs despite their importance as models of pathosystems in natural ecosystems (Bernasconi et al, 2009;Toh & Perlin, 2016) and the importance of assessing whether congruence in population genetic subdivision is a general pattern (Croll & Laine, 2016).…”

“…The congruence of host and pathogen population genetic structures has not been investigated in other anther-smut fungi-Silene pairs despite their importance as models of pathosystems in natural ecosystems (Bernasconi et al, 2009;Toh & Perlin, 2016) and the importance of assessing whether congruence in population genetic subdivision is a general pattern (Croll & Laine, 2016). Furthermore, the evolutionary history of population genetic divergence and of gene flow levels occurring between pathogens infecting closely related hosts with overlapping distribution ranges remain poorly studied at the genome-wide scale (but see Badouin et al, 2017).…”