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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 average distance between the the most frequent phenotypes and thepatchiness of the visible phenotypic subspace.(A) The average Hamming distance among visible phenotypes as a functionof their frequency (dots). Visible phenotypes are ranked according totheir frequency level. For each rank, we calculate the average Hammingdistance between all visible phenotypes with this or higher rank. Themost abundant phenotypes are very similar. This similarity decreases asless frequent phenotypes are included in the analysis. We also calculatewhich fraction of all visible phenotypes are included in thesephenotypes (solid line). The inset shows a zoom of the same plot,focusing only on the top 5% most frequent phenotypes. Thephenotypes that are included in this small fraction of the distinctvisible phenotypes, are, on average, only 4 bits different, and stillcover 50% of the phenotypes. (B) The one mutant neighbornetwork of the visible phenotypes. The size of the node is proportionalto the logarithm of its frequency. In this plot,r = k = 12.
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pcbi-1000202-g004: The average distance between the the most frequent phenotypes and thepatchiness of the visible phenotypic subspace.(A) The average Hamming distance among visible phenotypes as a functionof their frequency (dots). Visible phenotypes are ranked according totheir frequency level. For each rank, we calculate the average Hammingdistance between all visible phenotypes with this or higher rank. Themost abundant phenotypes are very similar. This similarity decreases asless frequent phenotypes are included in the analysis. We also calculatewhich fraction of all visible phenotypes are included in thesephenotypes (solid line). The inset shows a zoom of the same plot,focusing only on the top 5% most frequent phenotypes. Thephenotypes that are included in this small fraction of the distinctvisible phenotypes, are, on average, only 4 bits different, and stillcover 50% of the phenotypes. (B) The one mutant neighbornetwork of the visible phenotypes. The size of the node is proportionalto the logarithm of its frequency. In this plot,r = k = 12.

Mentions: To examine this observation in greater detail we measure the average Hammingdistance between visible phenotypes as a function of their frequency andrepresent them on a frequency-rank versus distance plot. The highest rankedphenotypes are presented as the lowest rank values. As shown in Figure 4A, the distancebetween the most frequent phenotypes is significantly smaller than the averagedistance (which in this case is ∼6), and increases as more visiblephenotypes (with lower frequencies) are considered. Considering the case whereall the visible phenotypes are included in this analysis, the average distanceis still smaller than that expected by chance. We find that the top5% most frequent phenotypes are very similar (average Hammingdistance is smaller than 4) yet cover approximately 50% of all thevisible phenotypes (4A inset). An additional illustration of this patchiness canbe observed in Figure 4B,plotting the one mutant-neighbor network of all the visible phenotypes. Here weobserve that the nodes that represent the most frequent phenotypes tend to beseparated in most cases by a single edge.


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

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

The average distance between the the most frequent phenotypes and thepatchiness of the visible phenotypic subspace.(A) The average Hamming distance among visible phenotypes as a functionof their frequency (dots). Visible phenotypes are ranked according totheir frequency level. For each rank, we calculate the average Hammingdistance between all visible phenotypes with this or higher rank. Themost abundant phenotypes are very similar. This similarity decreases asless frequent phenotypes are included in the analysis. We also calculatewhich fraction of all visible phenotypes are included in thesephenotypes (solid line). The inset shows a zoom of the same plot,focusing only on the top 5% most frequent phenotypes. Thephenotypes that are included in this small fraction of the distinctvisible phenotypes, are, on average, only 4 bits different, and stillcover 50% of the phenotypes. (B) The one mutant neighbornetwork of the visible phenotypes. The size of the node is proportionalto the logarithm of its frequency. In this plot,r = k = 12.
© Copyright Policy
Related In: Results  -  Collection

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

pcbi-1000202-g004: The average distance between the the most frequent phenotypes and thepatchiness of the visible phenotypic subspace.(A) The average Hamming distance among visible phenotypes as a functionof their frequency (dots). Visible phenotypes are ranked according totheir frequency level. For each rank, we calculate the average Hammingdistance between all visible phenotypes with this or higher rank. Themost abundant phenotypes are very similar. This similarity decreases asless frequent phenotypes are included in the analysis. We also calculatewhich fraction of all visible phenotypes are included in thesephenotypes (solid line). The inset shows a zoom of the same plot,focusing only on the top 5% most frequent phenotypes. Thephenotypes that are included in this small fraction of the distinctvisible phenotypes, are, on average, only 4 bits different, and stillcover 50% of the phenotypes. (B) The one mutant neighbornetwork of the visible phenotypes. The size of the node is proportionalto the logarithm of its frequency. In this plot,r = k = 12.
Mentions: To examine this observation in greater detail we measure the average Hammingdistance between visible phenotypes as a function of their frequency andrepresent them on a frequency-rank versus distance plot. The highest rankedphenotypes are presented as the lowest rank values. As shown in Figure 4A, the distancebetween the most frequent phenotypes is significantly smaller than the averagedistance (which in this case is ∼6), and increases as more visiblephenotypes (with lower frequencies) are considered. Considering the case whereall the visible phenotypes are included in this analysis, the average distanceis still smaller than that expected by chance. We find that the top5% most frequent phenotypes are very similar (average Hammingdistance is smaller than 4) yet cover approximately 50% of all thevisible phenotypes (4A inset). An additional illustration of this patchiness canbe observed in Figure 4B,plotting the one mutant-neighbor network of all the visible phenotypes. Here weobserve that the nodes that represent the most frequent phenotypes tend to beseparated in most cases by a single edge.

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