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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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Phenotype distribution in an ontogenetic-phylogenetic model.(A) The average pairwise Hamming distance between visible phenotypeswithin and between phyla. Each phylum corresponds to a developmentalplan, and the set of the most frequent visible phenotypes produced bythis plan represent species. The ancestral phyla is employing adevelopmental plan withr = 4 andk = 14. In eachbranching event, each of the two descendant phyla add an additionalregulatory element with random connectivities preserving the ancestralcomponent of the developmental plan (Figure 9). This branching processcontinues until we get the 1024 most recent phyla, each employing adevelopmental plan withr = 14 andk = 14. (B) Aphylogenetic tree including phenotypes from derived and ancestral phyla.The tree is reconstructed by computing the pairwise Hamming distancematrix between all phenotypes and applying a neighbor-joiningalgorithms. Rectangular, triangular, and circular nodes representphenotypes from the ancestral phylum, intermediate phyla, and derivedphyla respectively. Phyla within each phylogenetic level are illustratedwith different colors. The small tree on the bottom left cornerillustrates the phylogenetic tree of different developmental plans(using the same color coding as that used in the main tree). Phenotypes(or ‘species’) of different phyla differ only in thedevelopmental plan and not in genotype, but the resulting treesuccessfully clusters the members of each phyla. Furthermore, themembers of intermediate phyla are correctly clustered, spanning the samephylogenetic space as their descendants. Members of the ancestral phylum(represented by black rectangles) span similar regions to those coveredby all derived phenotypes. (C) Representation of ancestral,intermediate, and derived phenotypes according to the first twoprinciple components. Ellipses illustrate the mean and variance for eachphylum. The color coding is identical to that used in the phylogenetictree.
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pcbi-1000202-g010: Phenotype distribution in an ontogenetic-phylogenetic model.(A) The average pairwise Hamming distance between visible phenotypeswithin and between phyla. Each phylum corresponds to a developmentalplan, and the set of the most frequent visible phenotypes produced bythis plan represent species. The ancestral phyla is employing adevelopmental plan withr = 4 andk = 14. In eachbranching event, each of the two descendant phyla add an additionalregulatory element with random connectivities preserving the ancestralcomponent of the developmental plan (Figure 9). This branching processcontinues until we get the 1024 most recent phyla, each employing adevelopmental plan withr = 14 andk = 14. (B) Aphylogenetic tree including phenotypes from derived and ancestral phyla.The tree is reconstructed by computing the pairwise Hamming distancematrix between all phenotypes and applying a neighbor-joiningalgorithms. Rectangular, triangular, and circular nodes representphenotypes from the ancestral phylum, intermediate phyla, and derivedphyla respectively. Phyla within each phylogenetic level are illustratedwith different colors. The small tree on the bottom left cornerillustrates the phylogenetic tree of different developmental plans(using the same color coding as that used in the main tree). Phenotypes(or ‘species’) of different phyla differ only in thedevelopmental plan and not in genotype, but the resulting treesuccessfully clusters the members of each phyla. Furthermore, themembers of intermediate phyla are correctly clustered, spanning the samephylogenetic space as their descendants. Members of the ancestral phylum(represented by black rectangles) span similar regions to those coveredby all derived phenotypes. (C) Representation of ancestral,intermediate, and derived phenotypes according to the first twoprinciple components. Ellipses illustrate the mean and variance for eachphylum. The color coding is identical to that used in the phylogenetictree.

Mentions: Finally, we consider the effects of the developmental map on phylogeneticregularities. Since we are focusing on the evolution of development bearing onphenotypic diversity and disparity, we do not consider the evolution of thestructural genes, but only regulatory interactions. We assume in the followingtreatment that developmental plans evolve incrementally and neutrally byaddition of new genetic regulatory elements into existing regulatory networks.Consider, for example, an ancestral developmental plan that possessesra transcription factors, controllingk target genes. Descendant developmental plans acquirerb>ratranscription factors (still controlling the same k genes),where all descendant plans share an identical regulatory wiring for theancestral ra transcription factors, and differ inthe wiring of the derived factors (Figure 9). Following findings in the previous section, we focus onlyon the most frequent phenotypes produced by each plan as evolutionarilyrepresentative of the complete, visible phenotype set. By focusing on the mostfrequent phenotypes, we are considering those phenotypes most likely to beobserved. We are interested in the phylogenetic distribution of phenotypesgenerated by the evolutionary sequence of developmental plans. We observe thatthe phenotypes comprising a single developmental plan, become more similarthroughout the evolutionary process, whereas disparity among members ofdifferent plans increases (Figure10A). This process relates to an increase in the regulatory dimensionof the genome, and hence illustrates how regulatory evolution promotesincreasing phyletic disparity while decreasing phenotypic disparity.


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

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

Phenotype distribution in an ontogenetic-phylogenetic model.(A) The average pairwise Hamming distance between visible phenotypeswithin and between phyla. Each phylum corresponds to a developmentalplan, and the set of the most frequent visible phenotypes produced bythis plan represent species. The ancestral phyla is employing adevelopmental plan withr = 4 andk = 14. In eachbranching event, each of the two descendant phyla add an additionalregulatory element with random connectivities preserving the ancestralcomponent of the developmental plan (Figure 9). This branching processcontinues until we get the 1024 most recent phyla, each employing adevelopmental plan withr = 14 andk = 14. (B) Aphylogenetic tree including phenotypes from derived and ancestral phyla.The tree is reconstructed by computing the pairwise Hamming distancematrix between all phenotypes and applying a neighbor-joiningalgorithms. Rectangular, triangular, and circular nodes representphenotypes from the ancestral phylum, intermediate phyla, and derivedphyla respectively. Phyla within each phylogenetic level are illustratedwith different colors. The small tree on the bottom left cornerillustrates the phylogenetic tree of different developmental plans(using the same color coding as that used in the main tree). Phenotypes(or ‘species’) of different phyla differ only in thedevelopmental plan and not in genotype, but the resulting treesuccessfully clusters the members of each phyla. Furthermore, themembers of intermediate phyla are correctly clustered, spanning the samephylogenetic space as their descendants. Members of the ancestral phylum(represented by black rectangles) span similar regions to those coveredby all derived phenotypes. (C) Representation of ancestral,intermediate, and derived phenotypes according to the first twoprinciple components. Ellipses illustrate the mean and variance for eachphylum. The color coding is identical to that used in the phylogenetictree.
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Related In: Results  -  Collection

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

pcbi-1000202-g010: Phenotype distribution in an ontogenetic-phylogenetic model.(A) The average pairwise Hamming distance between visible phenotypeswithin and between phyla. Each phylum corresponds to a developmentalplan, and the set of the most frequent visible phenotypes produced bythis plan represent species. The ancestral phyla is employing adevelopmental plan withr = 4 andk = 14. In eachbranching event, each of the two descendant phyla add an additionalregulatory element with random connectivities preserving the ancestralcomponent of the developmental plan (Figure 9). This branching processcontinues until we get the 1024 most recent phyla, each employing adevelopmental plan withr = 14 andk = 14. (B) Aphylogenetic tree including phenotypes from derived and ancestral phyla.The tree is reconstructed by computing the pairwise Hamming distancematrix between all phenotypes and applying a neighbor-joiningalgorithms. Rectangular, triangular, and circular nodes representphenotypes from the ancestral phylum, intermediate phyla, and derivedphyla respectively. Phyla within each phylogenetic level are illustratedwith different colors. The small tree on the bottom left cornerillustrates the phylogenetic tree of different developmental plans(using the same color coding as that used in the main tree). Phenotypes(or ‘species’) of different phyla differ only in thedevelopmental plan and not in genotype, but the resulting treesuccessfully clusters the members of each phyla. Furthermore, themembers of intermediate phyla are correctly clustered, spanning the samephylogenetic space as their descendants. Members of the ancestral phylum(represented by black rectangles) span similar regions to those coveredby all derived phenotypes. (C) Representation of ancestral,intermediate, and derived phenotypes according to the first twoprinciple components. Ellipses illustrate the mean and variance for eachphylum. The color coding is identical to that used in the phylogenetictree.
Mentions: Finally, we consider the effects of the developmental map on phylogeneticregularities. Since we are focusing on the evolution of development bearing onphenotypic diversity and disparity, we do not consider the evolution of thestructural genes, but only regulatory interactions. We assume in the followingtreatment that developmental plans evolve incrementally and neutrally byaddition of new genetic regulatory elements into existing regulatory networks.Consider, for example, an ancestral developmental plan that possessesra transcription factors, controllingk target genes. Descendant developmental plans acquirerb>ratranscription factors (still controlling the same k genes),where all descendant plans share an identical regulatory wiring for theancestral ra transcription factors, and differ inthe wiring of the derived factors (Figure 9). Following findings in the previous section, we focus onlyon the most frequent phenotypes produced by each plan as evolutionarilyrepresentative of the complete, visible phenotype set. By focusing on the mostfrequent phenotypes, we are considering those phenotypes most likely to beobserved. We are interested in the phylogenetic distribution of phenotypesgenerated by the evolutionary sequence of developmental plans. We observe thatthe phenotypes comprising a single developmental plan, become more similarthroughout the evolutionary process, whereas disparity among members ofdifferent plans increases (Figure10A). This process relates to an increase in the regulatory dimensionof the genome, and hence illustrates how regulatory evolution promotesincreasing phyletic disparity while decreasing phenotypic disparity.

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