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Origins of multicellular evolvability in snowflake yeast.

Ratcliff WC, Fankhauser JD, Rogers DW, Greig D, Travisano M - Nat Commun (2015)

Bottom Line: A key step in this process is the origin of higher-level evolvability, but little is known about how higher-level entities originate and gain the capacity to evolve as an individual.Snowflake yeast develop through deterministic rules that produce geometrically defined clusters that preclude genetic conflict and display a high broad-sense heritability for multicellular traits; as a result they are preadapted to multicellular adaptation.This work demonstrates that simple microevolutionary changes can have profound macroevolutionary consequences, and suggests that the formation of clonally developing clusters may often be the first step to multicellularity.

View Article: PubMed Central - PubMed

Affiliation: School of Biology, Georgia Institute of Technology, Atlanta, Georgia 30332-0230, USA.

ABSTRACT
Complex life has arisen through a series of 'major transitions' in which collectives of formerly autonomous individuals evolve into a single, integrated organism. A key step in this process is the origin of higher-level evolvability, but little is known about how higher-level entities originate and gain the capacity to evolve as an individual. Here we report a single mutation that not only creates a new level of biological organization, but also potentiates higher-level evolvability. Disrupting the transcription factor ACE2 in Saccharomyces cerevisiae prevents mother-daughter cell separation, generating multicellular 'snowflake' yeast. Snowflake yeast develop through deterministic rules that produce geometrically defined clusters that preclude genetic conflict and display a high broad-sense heritability for multicellular traits; as a result they are preadapted to multicellular adaptation. This work demonstrates that simple microevolutionary changes can have profound macroevolutionary consequences, and suggests that the formation of clonally developing clusters may often be the first step to multicellularity.

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The snowflake yeast body plan ensures genetic segregation.(a) We model the settling rate of propagules produced by 16-celled snowflake yeast clusters (open circles) or cellular aggregates (filled circles) that contain 50% small and large cells. Snowflake yeast produce offspring in which small- and large-cell alleles are completely segregated into different clusters (resulting in either slow or fast settling speed), while most aggregates contain a mixture of both cell types. (b) We model the probability that a propagule produced by a 256-cell cluster containing both wild-type cells and a mutant lineage will contain only mutant cells as a function of mutant frequency in the cluster. Snowflake yeast clusters have a far higher probability of producing mutant-only propagules than aggregate clusters. (c) Rare mutants in 256-cell snowflake yeast clusters initially have a low probability of forming their own propagules, but mutant-only propagules are eventually assured.
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f5: The snowflake yeast body plan ensures genetic segregation.(a) We model the settling rate of propagules produced by 16-celled snowflake yeast clusters (open circles) or cellular aggregates (filled circles) that contain 50% small and large cells. Snowflake yeast produce offspring in which small- and large-cell alleles are completely segregated into different clusters (resulting in either slow or fast settling speed), while most aggregates contain a mixture of both cell types. (b) We model the probability that a propagule produced by a 256-cell cluster containing both wild-type cells and a mutant lineage will contain only mutant cells as a function of mutant frequency in the cluster. Snowflake yeast clusters have a far higher probability of producing mutant-only propagules than aggregate clusters. (c) Rare mutants in 256-cell snowflake yeast clusters initially have a low probability of forming their own propagules, but mutant-only propagules are eventually assured.

Mentions: Cluster-level selection can easily favour cellular traits that provide no within-group fitness advantage (such as large cell size) when genetic variation is effectively partitioned between groups. To examine how the dynamics of cluster developmental mode affect the genetic composition of propagules, we model ideal snowflake yeast clusters and contrast this with cellular aggregates. Cellular aggregates, which can be thought of as biofilm-like structures (similar to yeast flocs), do not necessarily undergo a genetic bottleneck when producing propagules. We assume propagules are up to half of the parent cluster’s size, and that the mutation leading to larger cells only occurs once within a cluster, after which it is passed on to daughter cells within the cluster. Consider a 16-celled cluster containing 50% small and large cells. Snowflake yeast, whose propagules pass through a unicellular genetic bottleneck, completely segregate genetic variation among offspring, while only 0.6% of the propagules produced by aggregative clusters contain just the large-celled mutant (Fig. 5a). We arrive at this result as follows: in this snowflake yeast cluster, all cell–cell connections that are broken must be between either two mutant cells (yielding a mutant-only propagule), a mutant cell and a wild-type cell (yielding two equal-sized uniclonal mutant and wild-type clusters) or between two wild-type cells (yielding a wild-type-only propagule). Within aggregative clusters, n cells (up to half the size of the cluster) are chosen randomly for inclusion in propagules. The number of ways the aggregative cluster can produce 100% large-celled propagules is , where nl is the number of large cells in the cluster, and x is propagule size. Similarly, the probability of getting 100% small cells is , where ns is the number of small cells in the cluster. Finally, the total number of non-clonal propagules can be determined by . We generate the result in Fig. 5a by dividing the total number of clonal propagules from the total number of non-clonal propagules for offspring size 1–8.


Origins of multicellular evolvability in snowflake yeast.

Ratcliff WC, Fankhauser JD, Rogers DW, Greig D, Travisano M - Nat Commun (2015)

The snowflake yeast body plan ensures genetic segregation.(a) We model the settling rate of propagules produced by 16-celled snowflake yeast clusters (open circles) or cellular aggregates (filled circles) that contain 50% small and large cells. Snowflake yeast produce offspring in which small- and large-cell alleles are completely segregated into different clusters (resulting in either slow or fast settling speed), while most aggregates contain a mixture of both cell types. (b) We model the probability that a propagule produced by a 256-cell cluster containing both wild-type cells and a mutant lineage will contain only mutant cells as a function of mutant frequency in the cluster. Snowflake yeast clusters have a far higher probability of producing mutant-only propagules than aggregate clusters. (c) Rare mutants in 256-cell snowflake yeast clusters initially have a low probability of forming their own propagules, but mutant-only propagules are eventually assured.
© Copyright Policy - open-access
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC4309424&req=5

f5: The snowflake yeast body plan ensures genetic segregation.(a) We model the settling rate of propagules produced by 16-celled snowflake yeast clusters (open circles) or cellular aggregates (filled circles) that contain 50% small and large cells. Snowflake yeast produce offspring in which small- and large-cell alleles are completely segregated into different clusters (resulting in either slow or fast settling speed), while most aggregates contain a mixture of both cell types. (b) We model the probability that a propagule produced by a 256-cell cluster containing both wild-type cells and a mutant lineage will contain only mutant cells as a function of mutant frequency in the cluster. Snowflake yeast clusters have a far higher probability of producing mutant-only propagules than aggregate clusters. (c) Rare mutants in 256-cell snowflake yeast clusters initially have a low probability of forming their own propagules, but mutant-only propagules are eventually assured.
Mentions: Cluster-level selection can easily favour cellular traits that provide no within-group fitness advantage (such as large cell size) when genetic variation is effectively partitioned between groups. To examine how the dynamics of cluster developmental mode affect the genetic composition of propagules, we model ideal snowflake yeast clusters and contrast this with cellular aggregates. Cellular aggregates, which can be thought of as biofilm-like structures (similar to yeast flocs), do not necessarily undergo a genetic bottleneck when producing propagules. We assume propagules are up to half of the parent cluster’s size, and that the mutation leading to larger cells only occurs once within a cluster, after which it is passed on to daughter cells within the cluster. Consider a 16-celled cluster containing 50% small and large cells. Snowflake yeast, whose propagules pass through a unicellular genetic bottleneck, completely segregate genetic variation among offspring, while only 0.6% of the propagules produced by aggregative clusters contain just the large-celled mutant (Fig. 5a). We arrive at this result as follows: in this snowflake yeast cluster, all cell–cell connections that are broken must be between either two mutant cells (yielding a mutant-only propagule), a mutant cell and a wild-type cell (yielding two equal-sized uniclonal mutant and wild-type clusters) or between two wild-type cells (yielding a wild-type-only propagule). Within aggregative clusters, n cells (up to half the size of the cluster) are chosen randomly for inclusion in propagules. The number of ways the aggregative cluster can produce 100% large-celled propagules is , where nl is the number of large cells in the cluster, and x is propagule size. Similarly, the probability of getting 100% small cells is , where ns is the number of small cells in the cluster. Finally, the total number of non-clonal propagules can be determined by . We generate the result in Fig. 5a by dividing the total number of clonal propagules from the total number of non-clonal propagules for offspring size 1–8.

Bottom Line: A key step in this process is the origin of higher-level evolvability, but little is known about how higher-level entities originate and gain the capacity to evolve as an individual.Snowflake yeast develop through deterministic rules that produce geometrically defined clusters that preclude genetic conflict and display a high broad-sense heritability for multicellular traits; as a result they are preadapted to multicellular adaptation.This work demonstrates that simple microevolutionary changes can have profound macroevolutionary consequences, and suggests that the formation of clonally developing clusters may often be the first step to multicellularity.

View Article: PubMed Central - PubMed

Affiliation: School of Biology, Georgia Institute of Technology, Atlanta, Georgia 30332-0230, USA.

ABSTRACT
Complex life has arisen through a series of 'major transitions' in which collectives of formerly autonomous individuals evolve into a single, integrated organism. A key step in this process is the origin of higher-level evolvability, but little is known about how higher-level entities originate and gain the capacity to evolve as an individual. Here we report a single mutation that not only creates a new level of biological organization, but also potentiates higher-level evolvability. Disrupting the transcription factor ACE2 in Saccharomyces cerevisiae prevents mother-daughter cell separation, generating multicellular 'snowflake' yeast. Snowflake yeast develop through deterministic rules that produce geometrically defined clusters that preclude genetic conflict and display a high broad-sense heritability for multicellular traits; as a result they are preadapted to multicellular adaptation. This work demonstrates that simple microevolutionary changes can have profound macroevolutionary consequences, and suggests that the formation of clonally developing clusters may often be the first step to multicellularity.

Show MeSH