Limits...
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.

Show MeSH
The average distance between the the most frequent phenotypes and the                            patchiness of the visible phenotypic subspace.(A) The average Hamming distance among visible phenotypes as a function                            of their frequency (dots). Visible phenotypes are ranked according to                            their frequency level. For each rank, we calculate the average Hamming                            distance between all visible phenotypes with this or higher rank. The                            most abundant phenotypes are very similar. This similarity decreases as                            less frequent phenotypes are included in the analysis. We also calculate                            which fraction of all visible phenotypes are included in these                            phenotypes (solid line). The inset shows a zoom of the same plot,                            focusing only on the top 5% most frequent phenotypes. The                            phenotypes that are included in this small fraction of the distinct                            visible phenotypes, are, on average, only 4 bits different, and still                            cover 50% of the phenotypes. (B) The one mutant neighbor                            network of the visible phenotypes. The size of the node is proportional                            to the logarithm of its frequency. In this plot,                                r = k = 12.
© Copyright Policy
Related In: Results  -  Collection


getmorefigures.php?uid=PMC2562988&req=5

pcbi-1000202-g004: The average distance between the the most frequent phenotypes and the patchiness of the visible phenotypic subspace.(A) The average Hamming distance among visible phenotypes as a function of their frequency (dots). Visible phenotypes are ranked according to their frequency level. For each rank, we calculate the average Hamming distance between all visible phenotypes with this or higher rank. The most abundant phenotypes are very similar. This similarity decreases as less frequent phenotypes are included in the analysis. We also calculate which fraction of all visible phenotypes are included in these phenotypes (solid line). The inset shows a zoom of the same plot, focusing only on the top 5% most frequent phenotypes. The phenotypes that are included in this small fraction of the distinct visible phenotypes, are, on average, only 4 bits different, and still cover 50% of the phenotypes. (B) The one mutant neighbor network of the visible phenotypes. The size of the node is proportional to the logarithm of its frequency. In this plot, r = k = 12.

Mentions: To examine this observation in greater detail we measure the average Hamming distance between visible phenotypes as a function of their frequency and represent them on a frequency-rank versus distance plot. The highest ranked phenotypes are presented as the lowest rank values. As shown in Figure 4A, the distance between the most frequent phenotypes is significantly smaller than the average distance (which in this case is ∼6), and increases as more visible phenotypes (with lower frequencies) are considered. Considering the case where all the visible phenotypes are included in this analysis, the average distance is still smaller than that expected by chance. We find that the top 5% most frequent phenotypes are very similar (average Hamming distance is smaller than 4) yet cover approximately 50% of all the visible phenotypes (4A inset). An additional illustration of this patchiness can be observed in Figure 4B, plotting the one mutant-neighbor network of all the visible phenotypes. Here we observe that the nodes that represent the most frequent phenotypes tend to be separated 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 the                            patchiness of the visible phenotypic subspace.(A) The average Hamming distance among visible phenotypes as a function                            of their frequency (dots). Visible phenotypes are ranked according to                            their frequency level. For each rank, we calculate the average Hamming                            distance between all visible phenotypes with this or higher rank. The                            most abundant phenotypes are very similar. This similarity decreases as                            less frequent phenotypes are included in the analysis. We also calculate                            which fraction of all visible phenotypes are included in these                            phenotypes (solid line). The inset shows a zoom of the same plot,                            focusing only on the top 5% most frequent phenotypes. The                            phenotypes that are included in this small fraction of the distinct                            visible phenotypes, are, on average, only 4 bits different, and still                            cover 50% of the phenotypes. (B) The one mutant neighbor                            network of the visible phenotypes. The size of the node is proportional                            to the logarithm of its frequency. In this plot,                                r = k = 12.
© Copyright Policy
Related In: Results  -  Collection

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

pcbi-1000202-g004: The average distance between the the most frequent phenotypes and the patchiness of the visible phenotypic subspace.(A) The average Hamming distance among visible phenotypes as a function of their frequency (dots). Visible phenotypes are ranked according to their frequency level. For each rank, we calculate the average Hamming distance between all visible phenotypes with this or higher rank. The most abundant phenotypes are very similar. This similarity decreases as less frequent phenotypes are included in the analysis. We also calculate which fraction of all visible phenotypes are included in these phenotypes (solid line). The inset shows a zoom of the same plot, focusing only on the top 5% most frequent phenotypes. The phenotypes that are included in this small fraction of the distinct visible phenotypes, are, on average, only 4 bits different, and still cover 50% of the phenotypes. (B) The one mutant neighbor network of the visible phenotypes. The size of the node is proportional to the logarithm of its frequency. In this plot, r = k = 12.
Mentions: To examine this observation in greater detail we measure the average Hamming distance between visible phenotypes as a function of their frequency and represent them on a frequency-rank versus distance plot. The highest ranked phenotypes are presented as the lowest rank values. As shown in Figure 4A, the distance between the most frequent phenotypes is significantly smaller than the average distance (which in this case is ∼6), and increases as more visible phenotypes (with lower frequencies) are considered. Considering the case where all the visible phenotypes are included in this analysis, the average distance is still smaller than that expected by chance. We find that the top 5% most frequent phenotypes are very similar (average Hamming distance is smaller than 4) yet cover approximately 50% of all the visible phenotypes (4A inset). An additional illustration of this patchiness can be observed in Figure 4B, plotting the one mutant-neighbor network of all the visible phenotypes. Here we observe that the nodes that represent the most frequent phenotypes tend to be separated 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