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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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Pr(pj = 1),as a function of sj, the number of+1 elements in .The total number of elements in ,r = 18.
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pcbi-1000202-g005: Pr(pj = 1),as a function of sj, the number of+1 elements in .The total number of elements in ,r = 18.

Mentions: Figure 5 illustrates thatPr(pj = 1)is a sigmoidal function of zj. Ifpj had been determined by only one, randomlydrawn, element of ,Pr(pj = 1)would be proportional (linearly) to the fraction of +1 elements in . However, since pj is determinedby a random subset, the consequences of a larger fraction of +1elements is a combinatorial amplification. For example consider the case where is comprised mostly of −1's with only veryfew +1 elements. A subset of will typically have many more −1's than+1's, as there are exponentially many more ways to choose−1 elements than the +1 elements. We argue that this strongdependence of the phenotypic element on the number of +1 elements inthe corresponding developmental matrix row is the source for the nonuniformdistribution of degeneracy levels.


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

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

Pr(pj = 1),as a function of sj, the number of+1 elements in .The total number of elements in ,r = 18.
© Copyright Policy
Related In: Results  -  Collection

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

pcbi-1000202-g005: Pr(pj = 1),as a function of sj, the number of+1 elements in .The total number of elements in ,r = 18.
Mentions: Figure 5 illustrates thatPr(pj = 1)is a sigmoidal function of zj. Ifpj had been determined by only one, randomlydrawn, element of ,Pr(pj = 1)would be proportional (linearly) to the fraction of +1 elements in . However, since pj is determinedby a random subset, the consequences of a larger fraction of +1elements is a combinatorial amplification. For example consider the case where is comprised mostly of −1's with only veryfew +1 elements. A subset of will typically have many more −1's than+1's, as there are exponentially many more ways to choose−1 elements than the +1 elements. We argue that this strongdependence of the phenotypic element on the number of +1 elements inthe corresponding developmental matrix row is the source for the nonuniformdistribution of degeneracy levels.

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