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An end to endless forms: epistasis, phenotype distribution bias, and nonuniform evolution.

Borenstein E, Krakauer DC - PLoS Comput. Biol. (2008)

Bottom Line: Ancestral phenotypes, produced by early developmental programs with a low level of gene interaction, are found to span a significantly greater volume of the total phenotypic space than derived taxa.We suggest that early and late evolution have a different character that we classify into micro- and macroevolutionary configurations.These findings complement the view of development as a key component in the production of endless forms and highlight the crucial role of development in constraining biotic diversity and evolutionary trajectories.

View Article: PubMed Central - PubMed

Affiliation: Department of Biological Sciences, Stanford University, Stanford, California, United States of America. ebo@stanford.edu

ABSTRACT
Studies of the evolution of development characterize the way in which gene regulatory dynamics during ontogeny constructs and channels phenotypic variation. These studies have identified a number of evolutionary regularities: (1) phenotypes occupy only a small subspace of possible phenotypes, (2) the influence of mutation is not uniform and is often canalized, and (3) a great deal of morphological variation evolved early in the history of multicellular life. An important implication of these studies is that diversity is largely the outcome of the evolution of gene regulation rather than the emergence of new, structural genes. Using a simple model that considers a generic property of developmental maps-the interaction between multiple genetic elements and the nonlinearity of gene interaction in shaping phenotypic traits-we are able to recover many of these empirical regularities. We show that visible phenotypes represent only a small fraction of possibilities. Epistasis ensures that phenotypes are highly clustered in morphospace and that the most frequent phenotypes are the most similar. We perform phylogenetic analyses on an evolving, developmental model and find that species become more alike through time, whereas higher-level grades have a tendency to diverge. Ancestral phenotypes, produced by early developmental programs with a low level of gene interaction, are found to span a significantly greater volume of the total phenotypic space than derived taxa. We suggest that early and late evolution have a different character that we classify into micro- and macroevolutionary configurations. These findings complement the view of development as a key component in the production of endless forms and highlight the crucial role of development in constraining biotic diversity and evolutionary trajectories.

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The effect of developmental plan density on phenotype distribution.(A) The percentage of visible phenotypes out of the potential phenotypesas a function of the developmental plan density, c. Theregulatory dimension, r, and the phenotypic dimension,k, are both set to 14. Each point represent theaverage of 1,000 different plans. For a given density value,c, each entry in the matrix is attributed with anonzero value (either +1 or −1) with probabilityc. (B) The number of variable traits,ν (i.e., phenotypic elements that areactive in at least one phenotype) as a function of the developmentalplan density, c. The experimental settings areidentical to those described in Figure 7A. (C) The percentage ofvisible phenotypes out of the 2ν achievable phenotypes as a function of the developmental plandensity, c.
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pcbi-1000202-g007: The effect of developmental plan density on phenotype distribution.(A) The percentage of visible phenotypes out of the potential phenotypesas a function of the developmental plan density, c. Theregulatory dimension, r, and the phenotypic dimension,k, are both set to 14. Each point represent theaverage of 1,000 different plans. For a given density value,c, each entry in the matrix is attributed with anonzero value (either +1 or −1) with probabilityc. (B) The number of variable traits,ν (i.e., phenotypic elements that areactive in at least one phenotype) as a function of the developmentalplan density, c. The experimental settings areidentical to those described in Figure 7A. (C) The percentage ofvisible phenotypes out of the 2ν achievable phenotypes as a function of the developmental plandensity, c.

Mentions: We find that sparse matrices generate a smaller fraction of visible phenotypes(Figure 7A). Forexample, in comparison to the 8.2% visible phenotypes obtained for afully connected plan (c = 1),only 3.4% of the phenotypes are visible for a matrix withc = 0.25 and only0.6% are visible forc = 0.1 (see Models). It alsoappears that the maximum number of visible phenotypes (which is still only8.7% of the total number of potential phenotypes) is produced for anintermediate value of c≈0.85. This could be the outcomeof a trade-off between the two competing effects discussed above. We note,however, that the influence of an increase in matrix density on the fraction ofvisible phenotypes diminishes for c>0.5.


An end to endless forms: epistasis, phenotype distribution bias, and nonuniform evolution.

Borenstein E, Krakauer DC - PLoS Comput. Biol. (2008)

The effect of developmental plan density on phenotype distribution.(A) The percentage of visible phenotypes out of the potential phenotypesas a function of the developmental plan density, c. Theregulatory dimension, r, and the phenotypic dimension,k, are both set to 14. Each point represent theaverage of 1,000 different plans. For a given density value,c, each entry in the matrix is attributed with anonzero value (either +1 or −1) with probabilityc. (B) The number of variable traits,ν (i.e., phenotypic elements that areactive in at least one phenotype) as a function of the developmentalplan density, c. The experimental settings areidentical to those described in Figure 7A. (C) The percentage ofvisible phenotypes out of the 2ν achievable phenotypes as a function of the developmental plandensity, c.
© Copyright Policy
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC2562988&req=5

pcbi-1000202-g007: The effect of developmental plan density on phenotype distribution.(A) The percentage of visible phenotypes out of the potential phenotypesas a function of the developmental plan density, c. Theregulatory dimension, r, and the phenotypic dimension,k, are both set to 14. Each point represent theaverage of 1,000 different plans. For a given density value,c, each entry in the matrix is attributed with anonzero value (either +1 or −1) with probabilityc. (B) The number of variable traits,ν (i.e., phenotypic elements that areactive in at least one phenotype) as a function of the developmentalplan density, c. The experimental settings areidentical to those described in Figure 7A. (C) The percentage ofvisible phenotypes out of the 2ν achievable phenotypes as a function of the developmental plandensity, c.
Mentions: We find that sparse matrices generate a smaller fraction of visible phenotypes(Figure 7A). Forexample, in comparison to the 8.2% visible phenotypes obtained for afully connected plan (c = 1),only 3.4% of the phenotypes are visible for a matrix withc = 0.25 and only0.6% are visible forc = 0.1 (see Models). It alsoappears that the maximum number of visible phenotypes (which is still only8.7% of the total number of potential phenotypes) is produced for anintermediate value of c≈0.85. This could be the outcomeof a trade-off between the two competing effects discussed above. We note,however, that the influence of an increase in matrix density on the fraction ofvisible phenotypes diminishes for c>0.5.

Bottom Line: Ancestral phenotypes, produced by early developmental programs with a low level of gene interaction, are found to span a significantly greater volume of the total phenotypic space than derived taxa.We suggest that early and late evolution have a different character that we classify into micro- and macroevolutionary configurations.These findings complement the view of development as a key component in the production of endless forms and highlight the crucial role of development in constraining biotic diversity and evolutionary trajectories.

View Article: PubMed Central - PubMed

Affiliation: Department of Biological Sciences, Stanford University, Stanford, California, United States of America. ebo@stanford.edu

ABSTRACT
Studies of the evolution of development characterize the way in which gene regulatory dynamics during ontogeny constructs and channels phenotypic variation. These studies have identified a number of evolutionary regularities: (1) phenotypes occupy only a small subspace of possible phenotypes, (2) the influence of mutation is not uniform and is often canalized, and (3) a great deal of morphological variation evolved early in the history of multicellular life. An important implication of these studies is that diversity is largely the outcome of the evolution of gene regulation rather than the emergence of new, structural genes. Using a simple model that considers a generic property of developmental maps-the interaction between multiple genetic elements and the nonlinearity of gene interaction in shaping phenotypic traits-we are able to recover many of these empirical regularities. We show that visible phenotypes represent only a small fraction of possibilities. Epistasis ensures that phenotypes are highly clustered in morphospace and that the most frequent phenotypes are the most similar. We perform phylogenetic analyses on an evolving, developmental model and find that species become more alike through time, whereas higher-level grades have a tendency to diverge. Ancestral phenotypes, produced by early developmental programs with a low level of gene interaction, are found to span a significantly greater volume of the total phenotypic space than derived taxa. We suggest that early and late evolution have a different character that we classify into micro- and macroevolutionary configurations. These findings complement the view of development as a key component in the production of endless forms and highlight the crucial role of development in constraining biotic diversity and evolutionary trajectories.

Show MeSH