Multilevel Selection in the Filamentous AscomyceteNeurospora tetrasperma

Abstract

The history of life has been driven by evolutionary transitions in individuality, that is, the aggregation of autonomous individuals to form a new, higher-level individual. The fungus Neurospora tetrasperma has recently undergone an evolutionary transition in individuality from homokaryosis (one single type of nuclei in the same cytoplasm) to heterokaryosis (two genetically divergent and free-ranging nuclear types). In this species, selection can act at different levels: while nuclei can compete in their replication and transmission into shortlived asexual spores, at the level of the heterokaryotic individual, cooperation between nuclear types is required to produce the long-lived sexual spores. Conflicts can arise between these two levels of selection if the coevolution between nuclear types is disrupted. Here, we investigated the extent of multilevel selection in three strains of N. tetrasperma. We assessed the ratio between nuclear types under different conditions and measured fitness traits of homo-and heterokaryotic mycelia with varying nuclear ratios. We show that the two nuclei have complementary traits, consistent with division of labor and cooperation. In one strain, for which a recent chromosomal introgression was detected, we observed the occurrence of selfish nuclei, enjoying better replication and transmission than sister nuclei at the same time as being detrimental to the heterokaryon. We hypothesize that introgression has disrupted the coevolution between nuclear types in this strain.

Recombination suppression and evolutionary strata around mating‐type loci in fungi: documenting patterns and understanding evolutionary and mechanistic causes

“…RIP has been found in the nonrecombining region around mating‐type genes (Hood et al ., 2005; Grognet et al ., 2014). RIP and TE methylation have further been shown to ‘leak’ further than just transposable elements (Van de Wouw et al, 2010e Wouw et al, 2010; Meunier et al ., 2018). Here, the silencing mechanisms of transposable elements constitute proximate causes of recombination suppression whereas the evolutionary cause is the lack of effective selection against TE insertions and the selection for genomic defense against repeat multiplication.…”

“…Rearrangements also could be beneficial by changing gene regulation (Fleiss et al, 2019) or if the breakpoint in itself induces an advantageous mutation or by suppressing recombination between a spore killer and its antidote (Svedberg et al, 2018). Actually, some genetic selfish elements have been found associated with fungal mating-type loci (Meunier et al, 2018). Some of the recent evolutionary strata identified in Microbotryum anther-smut fungi involve inversions or movement 3) the more recent pink evolutionary stratum (gene mRNA_2177).…”

Evolutionary maintenance of genomic diversity within arbuscular mycorrhizal fungi

“…Between-individual selection disfavours such nuclei (μ = 0), but we see that they can still coexist alongside functional nuclei if the between-individual selection to purge the deleterious nuclei is (a) stronger that their replicative advantage within individuals ((1 − s)θ > s; this means that the equilibrium is a stable absorption point), and (b) not maximal, corresponding to lethal nuclei (s < 1; this means that the absorption point is E[X*] > 0). As predicted by this, deleterious 'cheating' nuclei have been observed in heterokaryotic fungi (Meunier et al 2018;Bastiaans et al 2016). A theoretical treatment of when such cheating nuclei will arise in the first place is a question for future study; here we are content to show that such nuclei, if they arise, can be maintained stably.…”

“…First, it is likely that nuclei replicate at different rates within hyphal networks (Jany & Pawlowska, 2010;Roberts & Gladfelter, 2015), so we would expect the most competitive and fast-growing nucleus lineage to outcompete the rest. In other words, we would expect within-individual selection to lead to genomic purity (Gilbert, Foster, Mehdiabadi, Strassmann, & Queller, 2007;Inglis, Ryu, Asikhia, Strassmann, & Queller, 2017;Kooij, Aanen, Schiøtt, & Boomsma, 2015;Meunier, Hosseini, Heidari, Maryush, & Johannesson, 2018;Vreeburg, Nygren, & Aanen, 2016). Within-individual evolution would eventually lead to genomic purity even if nuclei are equally competitive, through drift, because not all nuclei migrate from parent hyphal networks into daughter cells (Angelard et al, 2010;Boon, Zimmerman, St-Arnaud, & Hijri, 2013;Marleau, Dalpé, St-Arnaud, & Hijri, 2011;Masclaux, Wyss, Mateus-Gonzalez, Aletti, & Sanders, 2018).…”

“…Consequently, individuals with high genomic variation could be outcompeted by individuals with genomic homogeneity. In other words, we would expect between-individual selection to also lead to genomic purity (Bastiaans, Debets, & Aanen, 2016;Meunier et al, 2018).…”