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Title: Species richness and redundancy promote persistence of exploited mutualisms in yeast

Mutualisms, or reciprocally beneficial interspecific interactions, constitute the foundation of many ecological communities and agricultural systems. Mutualisms come in different forms, from pairwise interactions to extremely diverse communities, and they are continually challenged with exploitation by nonmutualistic community members (exploiters). Thus, understanding how mutualisms persist remains an essential question in ecology. Theory suggests that high species richness and functional redundancy could promote mutualism persistence in complex mutualistic communities. Using a yeast system (Saccharomyces cerevisiae), we experimentally show that communities with the greatest mutualist richness and functional redundancy are nearly two times more likely to survive exploitation than are simple communities. Persistence increased because diverse communities were better able to mitigate the negative effects of competition with exploiters. Thus, large mutualistic networks may be inherently buffered from exploitation.

 
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Award ID(s):
1655544
NSF-PAR ID:
10200414
Author(s) / Creator(s):
 ;  ;  ;  ;  
Publisher / Repository:
American Association for the Advancement of Science (AAAS)
Date Published:
Journal Name:
Science
Volume:
370
Issue:
6514
ISSN:
0036-8075
Page Range / eLocation ID:
p. 346-350
Format(s):
Medium: X
Sponsoring Org:
National Science Foundation
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  1. null (Ed.)
    Mutualisms, or reciprocally beneficial interspecific interactions, constitute the foundation of many ecological communities and agricultural systems. Mutualisms come in different forms, from pairwise interactions to extremely diverse communities, and they are continually challenged with exploitation by nonmutualistic community members (exploiters). Thus, understanding how mutualisms persist remains an essential question in ecology. Theory suggests that high species richness and functional redundancy could promote mutualism persistence in complex mutualistic communities. Using a yeast system (Saccharomyces cerevisiae), we experimentally show that communities with the greatest mutualist richness and functional redundancy are nearly two times more likely to survive exploitation than are simple communities. Persistence increased because diverse communities were better able to mitigate the negative effects of competition with exploiters. Thus, large mutualistic networks may be inherently buffered from exploitation. 
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  2. A long-standing problem in the study of mutualism is to understand the effects of non-mutualistic community members that exploit the benefits of mutualism without offering commodities in exchange (i.e., ‘exploiters’). Mutualisms are continually challenged by exploiters and their persistence may depend on the costliness of exploitation or on adaptations that allow mutualists to avoid the negative effects of exploiters. Coevolution could lead to changes in mutualists and exploiters that allow mutualisms to persist. Although coevolution is considered essential for mutualism persistence and resistance to disturbance, we have yet to obtain direct experimental evidence of the role of coevolution in resistance to exploitation. Additionally, resistance to exploitation via coevolutionary processes might vary with the degree of dependency between mutualistic partners, as facultative mutualisms are thought to be under weaker coevolutionary selection than obligate mutualisms. Here, we conducted an experimental evolution study using a synthetic yeast mutualism to test how coevolution in facultative and obligate mutualisms affects their resistance to exploitation. We found that naïve facultative mutualisms were more likely to breakdown under exploitation than naïve obligate mutualisms. After 15 weeks of coevolution, both facultative and obligate evolved mutualists were more likely to survive exploitation than naïve mutualists when we reassembled mutualist communities. Additionally, coevolved exploiters were more likely to survive with mutualists, whereas naïve exploiters frequently went extinct. These results suggest that coevolution between mutualists and exploiters can lead to mutualism persistence, potentially explaining why exploitation is ubiquitous but rarely associated with mutualism breakdown.

     
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  3. Abstract

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  4. Summary

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  5. Abstract Aim

    Functional traits mediate the interactions of species among themselves and with their environment, providing a link between diversity and ecosystem function. Crucially, the loss of biodiversity can jeopardize the functionality of ecosystems. Much focus is on predicting the impacts of current and future species loss; however, modern ecosystems have undergone biodiversity decline throughout the Late Quaternary, starting with the Pleistocene megafaunal extinctions. Thus, the fossil record offers the opportunity to investigate the long‐term legacy of biodiversity erosion and how this is affecting modern ecosystems in a cumulative manner. We aimed to investigate changes in functional diversity and redundancy of a local mammal community at Hall’s Cave, a site with a continuous record from 21,000 years ago to the present. Additionally, we included several common introduced species in the modern community to test whether they restore some lost ecological function.

    Location

    Central Texas.

    Time period

    Late Pleistocene to Present.

    Major taxa studied

    Mammals.

    Methods

    We used eight functional traits (mass, diet, arboreality, cursoriality, soil disturbance, group size, activity period and migration habit), which, collectively, describe the ecological role of a species and its influence on ecosystem processes, to construct a multidimensional functional space. The functional richness, range and distribution of the Hall’s Cave community and the degree of functional redundancy were characterized statistically over time.

    Results

    We found that declines in functional diversity were greater than expected given the decrease in species richness, implying that lost taxa contributed higher than average distinct ecological function. Functional distances between the remaining species increased through time, leading to reduced functional redundancy in younger communities. However, recently introduced taxa increased functional diversity to levels similar to those in the Holocene and partly restored the functional space occupied by Late Pleistocene fauna.

    Main conclusions

    Our local‐scale analysis demonstrates how prolonged biodiversity erosion not only leads to functionally depauperate communities, but, crucially, lowers ecological resilience to future disturbance.

     
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