Introgression maintains the genetic integrity of the mating-type determining chromosome of the fungus Neurospora tetrasperma

Abstract

Genome evolution is driven by a complex interplay of factors, including selection, recombination, and introgression. The regions determining sexual identity are particularly dynamic parts of eukaryotic genomes that are prone to molecular degeneration associated with suppressed recombination. In the fungus Neurospora tetrasperma, it has been proposed that this molecular degeneration is counteracted by the introgression of nondegenerated DNA from closely related species. In this study, we used comparative and population genomic analyses of 92 genomes from eight phylogenetically and reproductively isolated lineages of N. tetrasperma, and its three closest relatives, to investigate the factors shaping the evolutionary history of the genomes. We found that suppressed recombination extends across at least 6 Mbp (∼63%) of the mating-type (mat) chromosome in N. tetrasperma and is associated with decreased genetic diversity, which is likely the result primarily of selection at linked sites. Furthermore, analyses of molecular evolution revealed an increased mutational load in this region, relative to recombining regions. However, comparative genomic and phylogenetic analyses indicate that the mat chromosomes are temporarily regenerated via introgression from sister species; six of eight lineages show introgression into one of their mat chromosomes, with multiple Neurospora species acting as donors. The introgressed tracts have been fixed within lineages, suggesting that they confer an adaptive advantage in natural populations, and our analyses support the presence of selective sweeps in at least one lineage. Thus, these data strongly support the previously hypothesized role of introgression as a mechanism for the maintenance of mating-type determining chromosomal regions.

Genetic and genomic analyses reveal boundaries between species closely related to Cryptococcus pathogens

“…Species that are products of recent divergence may still display signatures of continued exchange of genes [63][64][65][66]. Given that DSM27421 can still produce viable progeny and undergo meiotic recombination with at least one strain of C. amylolentus, we searched for genomic signatures that could be suggestive of recent introgression between C. amylolentus, DSM27421 and CBS7118.…”

Supergene evolution triggered by the introgression of a chromosomal inversion

“…This scenario may underlie the evolution of many complex polymorphisms under balancing selection in a wide variety of organisms, such as the MHC loci in vertebrates 32 , self-incompatibility systems in plants 33 , mating types in fungi 34 or, much more generally, sex chromosomes. Our results therefore shed new light on the importance of introgression as a mechanism shaping the architecture of genomes and assisting the evolution of complex adaptive strategies.…”

RADSex: a computational workflow to study sex determination using Restriction Site-Associated DNA Sequencing data

“…These findings have spawned both theoretical and empirical interest in sex chromosomes as models to study the consequences of recombination suppression and associated processes (Bachtrog, 2008;Charlesworth & Charlesworth, 2000;Corcoran et al, 2016;Doorn & Kirkpatrick, 2007; L. Gu, Walters, & Knipple, 2017;Huylmans, Macon, & Vicoso, 2017;Muyle et al, 2012;Peichel et al, 2004) . More recent studies investigating sex chromosomes in insects (Blackmon, Ross, & Bachtrog, 2017) , non-avian reptilia (Modi & Crews, 2005) , amphibians (Miura, 2017) , and fishes (Kikuchi & Hamaguchi, 2013) have found many homomorphic sex chromosomes displaying varying levels of differentiation, with the extreme case of a sex locus restricted to allelic variation of a single nucleotide as reported in the Japanese pufferfish (Kamiya et al, 2012) .…”