Selection against somatic parasitism can maintain allorecognition in fungi

T. Czárán, Rolf F. Hoekstra, Duur K. Aanen

Research output: Contribution to journalArticle

13 Citations (Scopus)

Abstract

Fusion between multicellular individuals is possible in many organisms with modular, indeterminate growth, such as marine invertebrates and fungi. Although fusion may provide various benefits, fusion usually is restricted to close relatives by allorecognition, also called heterokaryon or somatic incompatibility in fungi. A possible selective explanation for allorecognition is protection against somatic parasites. Such mutants contribute less to colony functions but more to reproduction. However, previous models testing this idea have failed to explain the high diversity of allorecognition alleles in nature. These models did not, however, consider the possible role of spatial structure. We model the joint evolution of allorecognition and somatic parasitism in a multicellular organism resembling an asexual ascomycete fungus in a spatially explicit simulation. In a 1000-by-1000 grid, neighbouring individuals can fuse, but only if they have the same allotype. Fusion with a parasitic individual decreases the total reproductive output of the fused individuals, but the parasite compensates for this individual-level fitness reduction by a disproportional share of the offspring. Allorecognition prevents the invasion of somatic parasites, and vice versa, mutation towards somatic parasitism provides the selective conditions for extensive allorecognition diversity. On the one hand, if allorecognition diversity did not build up fast enough, somatic parasites went to fixation; conversely, once parasites had gone to fixation no allorecognition diversity built up. On the other hand, the mere threat of parasitism could select for high allorecognition diversity, preventing invasion of somatic parasites. Moderate population viscosity combined with weak global dispersal was optimal for the joint evolution of allorecognition and protection against parasitism. Our results are consistent with the widespread occurrence of allorecognition in fungi and the low degree of somatic parasitism. We discuss the implications of our results for allorecognition in other organism groups.

Original languageEnglish
Pages (from-to)128-137
Number of pages10
JournalFungal Genetics and Biology
Volume73
DOIs
Publication statusPublished - Dec 1 2014

Fingerprint

Parasites
Fungi
Joints
Clonal Evolution
Ascomycota
Invertebrates
Viscosity
Reproduction
Alleles
Mutation
Growth
Population

Keywords

  • Cheating
  • Fungi
  • Heterokaryon incompatibility
  • Kin selection
  • Levels of selection
  • Somatic incompatibility

ASJC Scopus subject areas

  • Medicine(all)

Cite this

Selection against somatic parasitism can maintain allorecognition in fungi. / Czárán, T.; Hoekstra, Rolf F.; Aanen, Duur K.

In: Fungal Genetics and Biology, Vol. 73, 01.12.2014, p. 128-137.

Research output: Contribution to journalArticle

Czárán, T. ; Hoekstra, Rolf F. ; Aanen, Duur K. / Selection against somatic parasitism can maintain allorecognition in fungi. In: Fungal Genetics and Biology. 2014 ; Vol. 73. pp. 128-137.
@article{4b49ecc8c9ce49a8b394047624a16932,
title = "Selection against somatic parasitism can maintain allorecognition in fungi",
abstract = "Fusion between multicellular individuals is possible in many organisms with modular, indeterminate growth, such as marine invertebrates and fungi. Although fusion may provide various benefits, fusion usually is restricted to close relatives by allorecognition, also called heterokaryon or somatic incompatibility in fungi. A possible selective explanation for allorecognition is protection against somatic parasites. Such mutants contribute less to colony functions but more to reproduction. However, previous models testing this idea have failed to explain the high diversity of allorecognition alleles in nature. These models did not, however, consider the possible role of spatial structure. We model the joint evolution of allorecognition and somatic parasitism in a multicellular organism resembling an asexual ascomycete fungus in a spatially explicit simulation. In a 1000-by-1000 grid, neighbouring individuals can fuse, but only if they have the same allotype. Fusion with a parasitic individual decreases the total reproductive output of the fused individuals, but the parasite compensates for this individual-level fitness reduction by a disproportional share of the offspring. Allorecognition prevents the invasion of somatic parasites, and vice versa, mutation towards somatic parasitism provides the selective conditions for extensive allorecognition diversity. On the one hand, if allorecognition diversity did not build up fast enough, somatic parasites went to fixation; conversely, once parasites had gone to fixation no allorecognition diversity built up. On the other hand, the mere threat of parasitism could select for high allorecognition diversity, preventing invasion of somatic parasites. Moderate population viscosity combined with weak global dispersal was optimal for the joint evolution of allorecognition and protection against parasitism. Our results are consistent with the widespread occurrence of allorecognition in fungi and the low degree of somatic parasitism. We discuss the implications of our results for allorecognition in other organism groups.",
keywords = "Cheating, Fungi, Heterokaryon incompatibility, Kin selection, Levels of selection, Somatic incompatibility",
author = "T. Cz{\'a}r{\'a}n and Hoekstra, {Rolf F.} and Aanen, {Duur K.}",
year = "2014",
month = "12",
day = "1",
doi = "10.1016/j.fgb.2014.09.010",
language = "English",
volume = "73",
pages = "128--137",
journal = "Fungal Genetics and Biology",
issn = "1087-1845",
publisher = "Academic Press Inc.",

}

TY - JOUR

T1 - Selection against somatic parasitism can maintain allorecognition in fungi

AU - Czárán, T.

AU - Hoekstra, Rolf F.

AU - Aanen, Duur K.

PY - 2014/12/1

Y1 - 2014/12/1

N2 - Fusion between multicellular individuals is possible in many organisms with modular, indeterminate growth, such as marine invertebrates and fungi. Although fusion may provide various benefits, fusion usually is restricted to close relatives by allorecognition, also called heterokaryon or somatic incompatibility in fungi. A possible selective explanation for allorecognition is protection against somatic parasites. Such mutants contribute less to colony functions but more to reproduction. However, previous models testing this idea have failed to explain the high diversity of allorecognition alleles in nature. These models did not, however, consider the possible role of spatial structure. We model the joint evolution of allorecognition and somatic parasitism in a multicellular organism resembling an asexual ascomycete fungus in a spatially explicit simulation. In a 1000-by-1000 grid, neighbouring individuals can fuse, but only if they have the same allotype. Fusion with a parasitic individual decreases the total reproductive output of the fused individuals, but the parasite compensates for this individual-level fitness reduction by a disproportional share of the offspring. Allorecognition prevents the invasion of somatic parasites, and vice versa, mutation towards somatic parasitism provides the selective conditions for extensive allorecognition diversity. On the one hand, if allorecognition diversity did not build up fast enough, somatic parasites went to fixation; conversely, once parasites had gone to fixation no allorecognition diversity built up. On the other hand, the mere threat of parasitism could select for high allorecognition diversity, preventing invasion of somatic parasites. Moderate population viscosity combined with weak global dispersal was optimal for the joint evolution of allorecognition and protection against parasitism. Our results are consistent with the widespread occurrence of allorecognition in fungi and the low degree of somatic parasitism. We discuss the implications of our results for allorecognition in other organism groups.

AB - Fusion between multicellular individuals is possible in many organisms with modular, indeterminate growth, such as marine invertebrates and fungi. Although fusion may provide various benefits, fusion usually is restricted to close relatives by allorecognition, also called heterokaryon or somatic incompatibility in fungi. A possible selective explanation for allorecognition is protection against somatic parasites. Such mutants contribute less to colony functions but more to reproduction. However, previous models testing this idea have failed to explain the high diversity of allorecognition alleles in nature. These models did not, however, consider the possible role of spatial structure. We model the joint evolution of allorecognition and somatic parasitism in a multicellular organism resembling an asexual ascomycete fungus in a spatially explicit simulation. In a 1000-by-1000 grid, neighbouring individuals can fuse, but only if they have the same allotype. Fusion with a parasitic individual decreases the total reproductive output of the fused individuals, but the parasite compensates for this individual-level fitness reduction by a disproportional share of the offspring. Allorecognition prevents the invasion of somatic parasites, and vice versa, mutation towards somatic parasitism provides the selective conditions for extensive allorecognition diversity. On the one hand, if allorecognition diversity did not build up fast enough, somatic parasites went to fixation; conversely, once parasites had gone to fixation no allorecognition diversity built up. On the other hand, the mere threat of parasitism could select for high allorecognition diversity, preventing invasion of somatic parasites. Moderate population viscosity combined with weak global dispersal was optimal for the joint evolution of allorecognition and protection against parasitism. Our results are consistent with the widespread occurrence of allorecognition in fungi and the low degree of somatic parasitism. We discuss the implications of our results for allorecognition in other organism groups.

KW - Cheating

KW - Fungi

KW - Heterokaryon incompatibility

KW - Kin selection

KW - Levels of selection

KW - Somatic incompatibility

UR - http://www.scopus.com/inward/record.url?scp=84927743082&partnerID=8YFLogxK

UR - http://www.scopus.com/inward/citedby.url?scp=84927743082&partnerID=8YFLogxK

U2 - 10.1016/j.fgb.2014.09.010

DO - 10.1016/j.fgb.2014.09.010

M3 - Article

VL - 73

SP - 128

EP - 137

JO - Fungal Genetics and Biology

JF - Fungal Genetics and Biology

SN - 1087-1845

ER -