Regular bottlenecks and restrictions to somatic fusion prevent the accumulation of mitochondrial defects in<i>Neurospora</i>

Bastiaans, Eric; Aanen, Duur K.; Debets, A.J.M.; Hoekstra, Rolf F.; Lestrade, B.; Maas, Marc F.P.M.

doi:10.1098/rstb.2013.0448

Cited by 27 publications

(21 citation statements)

References 48 publications

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“…Selection on the lower level therefore increases the frequency of non-cooperative mitochondria, but cells with a significant proportion of selfish lower-level units suffer a fitness cost and replicate slower. This is an example of the evolutionary conflict between levels of selection, endangering the stability of the higher-level unit -the eukaryotic cell (Schable and Wise, 1998;Taylor et al, 2002;Clark et al, 2012;Bastiaans et al, 2014). This time, I assume that mutants arise at a low rate ( μ = 0.0001) and proliferate mostly due to their ability to outcompete the cooperative mitochondria within the same cell.…”

Section: Fast Replicating "Selfish" Mutantsmentioning

confidence: 96%

Evolutionary dynamics of cytoplasmic segregation and fusion: Mitochondrial mixing facilitated the evolution of sex at the origin of eukaryotes

Radzvilavicius

2016

Journal of Theoretical Biology

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Meiotic sex evolved in a cell that already possessed mitochondria. Cytoplasmic fusion and mitochondrial mixing evolve under negative epistasis. Mitochondrial mixing could have driven the early evolution of sexual life cycles. a b s t r a c t Sexual reproduction is a trait shared by all complex life, but the complete account of its origin is missing. Virtually all theoretical work on the evolution of sex has been centered around the benefits of reciprocal recombination among nuclear genes, paying little attention to the evolutionary dynamics of multi-copy mitochondrial genomes. Here I develop a mathematical model to study the evolution of nuclear alleles inducing cell fusion in an ancestral population of clonal proto-eukaryotes. Segregational drift maintains high mitochondrial variance between clonally reproducing hosts, but the effect of segregation is opposed by cytoplasmic mixing which tends to reduce variation between cells in favor of higher heterogeneity within the cell. Despite the reduced long-term population fitness, alleles responsible for sexual cell fusion can spread to fixation. The evolution of sex requires negative epistatic interactions between mi-tochondrial mutations under strong purifying selection, low mutation load and weak mitochondrial-nuclear associations. I argue that similar conditions could have been maintained during the late stages of eukaryogenesis, facilitating the evolution of sexual cell fusion and meiotic recombination without compromising the stability of the emerging complex cell.

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Section: Fast Replicating "Selfish" Mutantsmentioning

confidence: 96%

Evolutionary dynamics of cytoplasmic segregation and fusion: Mitochondrial mixing facilitated the evolution of sex at the origin of eukaryotes

Radzvilavicius

2016

Journal of Theoretical Biology

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“…Grosberg and Strathmann (1998) argued that the multicellular stage reduces genetic variability and leads to inefficient selection compared to the unicellular stage (Grosberg and Strathmann 1998). For instance, the unicellular stage in the life cycle of multicellular organisms allows for the purging of deleterious mutations by exposing the individual gametes as well as the resulting zygote to selection, while at the same time this unicellular stage reduces conflicts of interest among genetically different replicators (e.g., mitochondria) within a multicellular organism (Grosberg and Strathmann 1998;Bastiaans et al 2014). Moreover, the alternation of multicellular and unicellular stages also promotes the selection of beneficial mutations.…”

Section: Emergence Of Azole Resistancementioning

confidence: 99%

Asexual sporulation facilitates adaptation: The emergence of azole resistance inAspergillus fumigatus

et al. 2015

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Understanding the occurrence and spread of azole resistance in Aspergillus fumigatus is crucial for public health. It has been hypothesized that asexual sporulation, which is abundant in nature, is essential for phenotypic expression of azole resistance mutations in A. fumigatus facilitating subsequent spread through natural selection. Furthermore, the disease aspergilloma is associated with asexual sporulation within the lungs of patients and the emergence of azole resistance. This study assessed the evolutionary advantage of asexual sporulation by growing the fungus under pressure of one of five different azole fungicides over seven weeks and by comparing the rate of adaptation between scenarios of culturing with and without asexual sporulation. Results unequivocally show that asexual sporulation facilitates adaptation. This can be explained by the combination of more effective selection because of the transition from a multicellular to a unicellular stage, and by increased mutation supply due to the production of spores, which involves numerous mitotic divisions. Insights from this study are essential to unravel the resistance mechanisms of sporulating pathogens to chemical compounds and disease agents in general, and for designing strategies that prevent or overcome the emerging threat of azole resistance in particular.

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“…; Bastiaans et al. ). Recently, it has been proposed that allorecognition in fungi is a secondary consequence of selection for xenorecognition, that is, recognition of parasites belonging to a different species, similar to allorecognition in animals (Paoletti and Saupe ).…”

Section: Discussionmentioning

confidence: 98%

“…A related hypothesis is that allorecognition in fungi has evolved as a protection against cytoplasmic parasitic elements, which can easily be transmitted via fusion (Debets et al 1994). There is experimental evidence that restriction to fusion at least partially prevents transfer of cytoplasmic elements, such as plasmids, viruses, and mitochondria (Debets et al 1994;van Diepeningen et al 1997;Debets and Griffiths 1998;Cortesi et al 2001;Brusini et al 2011;Bastiaans et al 2014a). Recently, it has been proposed that allorecognition in fungi is a secondary consequence of selection for xenorecognition, that is, recognition of parasites belonging to a different species, similar to allorecognition in animals (Paoletti and Saupe 2009).…”

Section: Erodes Allorecognition Diversitymentioning

confidence: 99%

Experimental demonstration of the benefits of somatic fusion and the consequences for allorecognition

2015

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Allorecognition, the ability to distinguish "self" from "nonself" based on allelic differences at allorecognition loci, is common in all domains of life. Allorecognition restricts the opportunities for social parasitism, and is therefore crucial for the evolution of cooperation. However, the maintenance of allorecognition diversity provides a paradox. If allorecognition is costly relative to cooperation, common alleles will be favored. Thus, the cost of allorecognition may reduce the genetic variation upon which allorecognition crucially relies, a prediction now known as "Crozier's paradox." We establish the relative costs of allorecognition, and their consequences for the short-term evolution of recognition labels theoretically predicted by Crozier. We use fusion among colonies of the fungus Neurospora crassa, regulated by highly variable allorecognition genes, as an experimental model system. We demonstrate that fusion among colonies is mutually beneficial, relative to absence of fusion upon allorecognition. This benefit is due not only to absence of mutual antagonism, which occurs upon allorecognition, but also to an increase in colony size per se. We then experimentally demonstrate that the benefit of fusion selects against allorecognition diversity, as predicted by Crozier. We discuss what maintains allorecognition diversity.

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Regular bottlenecks and restrictions to somatic fusion prevent the accumulation of mitochondrial defects inNeurospora

Cited by 27 publications

References 48 publications

Evolutionary dynamics of cytoplasmic segregation and fusion: Mitochondrial mixing facilitated the evolution of sex at the origin of eukaryotes

Evolutionary dynamics of cytoplasmic segregation and fusion: Mitochondrial mixing facilitated the evolution of sex at the origin of eukaryotes

Asexual sporulation facilitates adaptation: The emergence of azole resistance inAspergillus fumigatus

Experimental demonstration of the benefits of somatic fusion and the consequences for allorecognition

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