skip to main content
US FlagAn official website of the United States government
dot gov icon
Official websites use .gov
A .gov website belongs to an official government organization in the United States.
https lock icon
Secure .gov websites use HTTPS
A lock ( lock ) or https:// means you've safely connected to the .gov website. Share sensitive information only on official, secure websites.


Title: Conflict, Competition, and Cooperation Regulate Social Interactions in Filamentous Fungi
Social cooperation impacts the development and survival of species. In higher taxa, kin recognition occurs via visual, chemical, or tactile cues that dictate cooperative versus competitive interactions. In microbes, the outcome of cooperative versus competitive interactions is conferred by identity at allorecognition loci, so called kind recognition. In syncytial filamentous fungi, the acquisition of multicellularity is associated with somatic cell fusion within and between colonies. However, such intraspecific cooperation entails risks, as fusion can transmit deleterious genotypes or infectious components that reduce fitness, or give rise to cheaters that can exploit communal goods without contributing to their production. Allorecognition mechanisms in syncytial fungi regulate somatic cell fusion by operating precontact during chemotropic interactions, during cell adherence, and postfusion by triggering programmed cell death reactions. Alleles at fungal allorecognition loci are highly polymorphic, fall into distinct haplogroups, and show evolutionary signatures of balancing selection, similar to allorecognition loci across the tree of life. Expected final online publication date for the Annual Review of Microbiology, Volume 74 is September 8, 2020. Please see http://www.annualreviews.org/page/journal/pubdates for revised estimates.  more » « less
Award ID(s):
1818283
PAR ID:
10181965
Author(s) / Creator(s):
; ; ; ; ;
Date Published:
Journal Name:
Annual Review of Microbiology
Volume:
74
Issue:
1
ISSN:
0066-4227
Format(s):
Medium: X
Sponsoring Org:
National Science Foundation
More Like this
  1. Organisms require the ability to differentiate themselves from organisms of different or even the same species. Allorecognition processes in filamentous fungi are essential to ensure identity of an interconnected syncytial colony to protect it from exploitation and disease. Neurospora crassa has three cell fusion checkpoints controlling formation of an interconnected mycelial network. The locus that controls the second checkpoint, which allows for cell wall dissolution and subsequent fusion between cells/hyphae, cwr (cell wall remodeling) , encodes two linked genes, cwr-1 and cwr-2 . Previously, it was shown that cwr-1 and cwr-2 show severe linkage disequilibrium with six different haplogroups present in N. crassa populations. Isolates from an identical cwr haplogroup show robust fusion, while somatic cell fusion between isolates of different haplogroups is significantly blocked in cell wall dissolution. The cwr-1 gene encodes a putative polysaccharide monooxygenase (PMO). Herein we confirm that CWR-1 is a C1-oxidizing chitin PMO. We show that the catalytic (PMO) domain of CWR-1 was sufficient for checkpoint function and cell fusion blockage; however, through analysis of active-site, histidine-brace mutants, the catalytic activity of CWR-1 was ruled out as a major factor for allorecognition. Swapping a portion of the PMO domain (V86 to T130) did not switch cwr haplogroup specificity, but rather cells containing this chimera exhibited a novel haplogroup specificity. Allorecognition to mediate cell fusion blockage is likely occurring through a protein–protein interaction between CWR-1 with CWR-2. These data highlight a moonlighting role in allorecognition of the CWR-1 PMO domain. 
    more » « less
  2. Abstract A multinucleate syncytium is a common growth form in filamentous fungi. Comprehensive functions of the syncytial state remain unknown, but it likely allows for a wide range of adaptations to enable filamentous fungi to coordinate growth, reproduction, responses to the environment, and to distribute nuclear and cytoplasmic elements across a colony. Indeed, the underlying mechanistic details of how syncytia regulate cellular and molecular processes spatiotemporally across a colony are largely unexplored. Here, we implemented a strategy to analyze the relative fitness of different nuclear populations in syncytia of Neurospora crassa, including nuclei with loss-of-function mutations in essential genes, based on production of multinucleate asexual spores using flow cytometry of pairings between strains with differentially fluorescently tagged nuclear histones. The distribution of homokaryotic and heterokaryotic asexual spores in pairings was assessed between different auxotrophic and morphological mutants, as well as with strains that were defective in somatic cell fusion or were heterokaryon incompatible. Mutant nuclei were compartmentalized into both homokaryotic and heterokaryotic asexual spores, a type of bet hedging for maintenance and evolution of mutational events, despite disadvantages to the syncytium. However, in pairings between strains that were blocked in somatic cell fusion or were heterokaryon incompatible, we observed a “winner-takes-all” phenotype, where asexual spores originating from paired strains were predominantly one genotype. These data indicate that syncytial fungal cells are permissive and tolerate a wide array of nuclear functionality, but that cells/colonies that are unable to cooperate via syncytia formation actively compete for resources. 
    more » « less
  3. The ability to recognize others is a frequent assumption of models of the evolution of cooperation. At the same time, cooperative behavior has been proposed as a selective agent favoring the evolution of individual recognition abilities. Although theory predicts that recognition and cooperation may co-evolve, data linking recognition abilities and cooperative behavior with evidence of selection are elusive. Here, we provide evidence of a selective link between individual recognition and cooperation in the paper wasp Polistes fuscatus through a combination of clinal, common garden, and population genomics analyses. We identified latitudinal clines in both rates of cooperative nesting and color pattern diversity, consistent with a selective link between recognition and cooperation. In behavioral experiments, we replicated previous results demonstrating individual recognition in cooperative and phenotypically diverse P. fuscatus from New York. In contrast, wasps from a less cooperative and phenotypically uniform Louisiana population showed no evidence of individual recognition. In a common garden experiment, groups of wasps from northern populations formed more stable and individually biased associations, indicating that recognition facilitates group stability. The strength of recent positive selection on cognition-associated loci likely to mediate individual recognition is substantially greater in northern compared with southern P. fuscatus populations. Collectively, these data suggest that individual recognition and cooperative nesting behavior have co-evolved in P. fuscatus because recognition helps stabilize social groups. This work provides evidence of a specific cognitive phenotype under selection because of social interactions, supporting the idea that social behavior can be a key driver of cognitive evolution. 
    more » « less
  4. Pleiotropy may affect the maintenance of cooperation by limiting cheater mutants if such mutants lose other important traits. If pleiotropy limits cheaters, selection may favor cooperation loci that are more pleiotropic. However, the same should not be true for private loci with functions unrelated to cooperation. Pleiotropy in cooperative loci has mostly been studied with single loci and has not been measured on a wide scale or compared to a suitable set of control loci with private functions. I remedy this gap by comparing genomic measures of pleiotropy in previously identified cooperative and private loci in Pseudomonas aeruginosa. I found that cooperative loci in P. aeruginosa tended to be more pleiotropic than private loci according to the number of protein–protein interactions, the number of gene ontology terms, and gene expression specificity. These results show that pleiotropy may be a general way to limit cheating and that cooperation may shape pleiotropy in the genome. 
    more » « less
  5. Barreda-Tarrazona, Iván (Ed.)
    Cooperation and competition are common in social interactions. It is not clear how individual differences in personality may predict performance strategies under these two contexts. We evaluated whether instructions to play cooperatively and competitively would differentially affect dyads playing a Pong video game. We hypothesized that instructions to play cooperatively would result in lower overall points scored and differences in paddle control kinematics relative to when participants were instructed to play competitively. We also predicted that higher scores in prosociality and Sportspersonship would be related to better performance during cooperative than competitive conditions. Methods: Pairs of participants played a Pong video game under cooperative and competitive instructions. During competitive trials, participants were instructed to score more points against one another to win the game. During the cooperative trials, participants were instructed to work together to score as few points against one another as possible. After game play, each participant completed surveys so we could measure their trait prosociality and Sportspersonship.Results: Condition was a significant predictor of where along the paddle participants hit the ball, which controlled ball exit angles. Specifically, during cooperation participants concentrated ball contacts on the paddle towards the center to produce more consistent rebound angles. We found a significant correlation of Sex and the average points scored by participants during cooperative games, competitive games, and across all trials. Sex was also significantly correlated with paddle kinematics during cooperative games. The overall scores on the prosociality and Sportspersonship surveys were not significantly correlated with the performance outcomes in cooperative and competitive games. The dimension of prosociality assessing empathic concern was significantly correlated with performance outcomes during cooperative video game play. Discussion: No Sportspersonship survey score was able to predict cooperative or competitive game performance, suggesting that Sportspersonship personality assessments are not reliable predictors of cooperative or competitive behaviors translated to a virtual game setting. Survey items and dimensions probing broader empathic concern may be more effective predictors of cooperative and competitive performance during interactive video game play. Further testing is encouraged to assess the efficacy of prosocial personality traits as predictors of cooperative and competitive video game behavior. 
    more » « less