Crowded growth leads to the spontaneous evolution of semistable coexistence in laboratory yeast populations

Evgeni M. Frenkel, Michael J. McDonald, James Van Dyken, Katya Kosheleva, Gregory I. Lang, Michael M. Desai

Research output: Contribution to journalArticle

15 Citations (Scopus)

Abstract

Identifying the mechanisms that create and maintain biodiversity is a central challenge in biology. Stable diversification of microbial populations often requires the evolution of differences in resource utilization. Alternatively, coexistence can be maintained by specialization to exploit spatial heterogeneity in the environment. Here, we report spontaneous diversification maintained bya related but distinct mechanism: crowding avoidance. During experimental evolution of laboratory Saccharomyces cerevisiae populations, we observed the repeated appearance of "adherent" (A) lineages able to grow as a dispersed film, in contrast to their crowded "bottomdweller" (B) ancestors. These two types stably coexist because dispersal reduces interference competition for nutrients among kin, at the cost of a slower maximum growth rate. This tradeoff causes the frequencies of the two types to oscillate around equilibrium over the course of repeated cycles of growth, crowding, and dispersal. However, further coevolution of the A and B types can perturb and eventually destroy their coexistence over longer time scales. We introduce a simple mathematical model of this "semistable" coexistence, which explains the interplay between ecological and evolutionary dynamics. Because crowded growth generally limits nutrient access in biofilms, the mechanism we report here may be broadly important in maintaining diversity in these natural environments.

Original languageEnglish (US)
Pages (from-to)11306-11311
Number of pages6
JournalProceedings of the National Academy of Sciences of the United States of America
Volume112
Issue number36
DOIs
StatePublished - Sep 8 2015

Fingerprint

Yeasts
Growth
Population
Food
Biodiversity
Biofilms
Saccharomyces cerevisiae
Theoretical Models

Keywords

  • Coexistence
  • Crowding
  • Experimental evolution
  • Fungal adherence

ASJC Scopus subject areas

  • General

Cite this

Crowded growth leads to the spontaneous evolution of semistable coexistence in laboratory yeast populations. / Frenkel, Evgeni M.; McDonald, Michael J.; Van Dyken, James; Kosheleva, Katya; Lang, Gregory I.; Desai, Michael M.

In: Proceedings of the National Academy of Sciences of the United States of America, Vol. 112, No. 36, 08.09.2015, p. 11306-11311.

Research output: Contribution to journalArticle

Frenkel, Evgeni M. ; McDonald, Michael J. ; Van Dyken, James ; Kosheleva, Katya ; Lang, Gregory I. ; Desai, Michael M. / Crowded growth leads to the spontaneous evolution of semistable coexistence in laboratory yeast populations. In: Proceedings of the National Academy of Sciences of the United States of America. 2015 ; Vol. 112, No. 36. pp. 11306-11311.
@article{17da5b73c3d3435fa0accbaccffb81b8,
title = "Crowded growth leads to the spontaneous evolution of semistable coexistence in laboratory yeast populations",
abstract = "Identifying the mechanisms that create and maintain biodiversity is a central challenge in biology. Stable diversification of microbial populations often requires the evolution of differences in resource utilization. Alternatively, coexistence can be maintained by specialization to exploit spatial heterogeneity in the environment. Here, we report spontaneous diversification maintained bya related but distinct mechanism: crowding avoidance. During experimental evolution of laboratory Saccharomyces cerevisiae populations, we observed the repeated appearance of {"}adherent{"} (A) lineages able to grow as a dispersed film, in contrast to their crowded {"}bottomdweller{"} (B) ancestors. These two types stably coexist because dispersal reduces interference competition for nutrients among kin, at the cost of a slower maximum growth rate. This tradeoff causes the frequencies of the two types to oscillate around equilibrium over the course of repeated cycles of growth, crowding, and dispersal. However, further coevolution of the A and B types can perturb and eventually destroy their coexistence over longer time scales. We introduce a simple mathematical model of this {"}semistable{"} coexistence, which explains the interplay between ecological and evolutionary dynamics. Because crowded growth generally limits nutrient access in biofilms, the mechanism we report here may be broadly important in maintaining diversity in these natural environments.",
keywords = "Coexistence, Crowding, Experimental evolution, Fungal adherence",
author = "Frenkel, {Evgeni M.} and McDonald, {Michael J.} and {Van Dyken}, James and Katya Kosheleva and Lang, {Gregory I.} and Desai, {Michael M.}",
year = "2015",
month = "9",
day = "8",
doi = "10.1073/pnas.1506184112",
language = "English (US)",
volume = "112",
pages = "11306--11311",
journal = "Proceedings of the National Academy of Sciences of the United States of America",
issn = "0027-8424",
number = "36",

}

TY - JOUR

T1 - Crowded growth leads to the spontaneous evolution of semistable coexistence in laboratory yeast populations

AU - Frenkel, Evgeni M.

AU - McDonald, Michael J.

AU - Van Dyken, James

AU - Kosheleva, Katya

AU - Lang, Gregory I.

AU - Desai, Michael M.

PY - 2015/9/8

Y1 - 2015/9/8

N2 - Identifying the mechanisms that create and maintain biodiversity is a central challenge in biology. Stable diversification of microbial populations often requires the evolution of differences in resource utilization. Alternatively, coexistence can be maintained by specialization to exploit spatial heterogeneity in the environment. Here, we report spontaneous diversification maintained bya related but distinct mechanism: crowding avoidance. During experimental evolution of laboratory Saccharomyces cerevisiae populations, we observed the repeated appearance of "adherent" (A) lineages able to grow as a dispersed film, in contrast to their crowded "bottomdweller" (B) ancestors. These two types stably coexist because dispersal reduces interference competition for nutrients among kin, at the cost of a slower maximum growth rate. This tradeoff causes the frequencies of the two types to oscillate around equilibrium over the course of repeated cycles of growth, crowding, and dispersal. However, further coevolution of the A and B types can perturb and eventually destroy their coexistence over longer time scales. We introduce a simple mathematical model of this "semistable" coexistence, which explains the interplay between ecological and evolutionary dynamics. Because crowded growth generally limits nutrient access in biofilms, the mechanism we report here may be broadly important in maintaining diversity in these natural environments.

AB - Identifying the mechanisms that create and maintain biodiversity is a central challenge in biology. Stable diversification of microbial populations often requires the evolution of differences in resource utilization. Alternatively, coexistence can be maintained by specialization to exploit spatial heterogeneity in the environment. Here, we report spontaneous diversification maintained bya related but distinct mechanism: crowding avoidance. During experimental evolution of laboratory Saccharomyces cerevisiae populations, we observed the repeated appearance of "adherent" (A) lineages able to grow as a dispersed film, in contrast to their crowded "bottomdweller" (B) ancestors. These two types stably coexist because dispersal reduces interference competition for nutrients among kin, at the cost of a slower maximum growth rate. This tradeoff causes the frequencies of the two types to oscillate around equilibrium over the course of repeated cycles of growth, crowding, and dispersal. However, further coevolution of the A and B types can perturb and eventually destroy their coexistence over longer time scales. We introduce a simple mathematical model of this "semistable" coexistence, which explains the interplay between ecological and evolutionary dynamics. Because crowded growth generally limits nutrient access in biofilms, the mechanism we report here may be broadly important in maintaining diversity in these natural environments.

KW - Coexistence

KW - Crowding

KW - Experimental evolution

KW - Fungal adherence

UR - http://www.scopus.com/inward/record.url?scp=84941242209&partnerID=8YFLogxK

UR - http://www.scopus.com/inward/citedby.url?scp=84941242209&partnerID=8YFLogxK

U2 - 10.1073/pnas.1506184112

DO - 10.1073/pnas.1506184112

M3 - Article

VL - 112

SP - 11306

EP - 11311

JO - Proceedings of the National Academy of Sciences of the United States of America

JF - Proceedings of the National Academy of Sciences of the United States of America

SN - 0027-8424

IS - 36

ER -