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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 phenotypes                            within and between phyla. Each phylum corresponds to a developmental                            plan, and the set of the most frequent visible phenotypes produced by                            this plan represent species. The ancestral phyla is employing a                            developmental plan with                            r = 4 and                            k = 14. In each                            branching event, each of the two descendant phyla add an additional                            regulatory element with random connectivities preserving the ancestral                            component of the developmental plan (Figure 9). This branching process                            continues until we get the 1024 most recent phyla, each employing a                            developmental plan with                            r = 14 and                            k = 14. (B) A                            phylogenetic tree including phenotypes from derived and ancestral phyla.                            The tree is reconstructed by computing the pairwise Hamming distance                            matrix between all phenotypes and applying a neighbor-joining                            algorithms. Rectangular, triangular, and circular nodes represent                            phenotypes from the ancestral phylum, intermediate phyla, and derived                            phyla respectively. Phyla within each phylogenetic level are illustrated                            with different colors. The small tree on the bottom left corner                            illustrates 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 the                            developmental plan and not in genotype, but the resulting tree                            successfully clusters the members of each phyla. Furthermore, the                            members of intermediate phyla are correctly clustered, spanning the same                            phylogenetic space as their descendants. Members of the ancestral phylum                            (represented by black rectangles) span similar regions to those covered                            by all derived phenotypes. (C) Representation of ancestral,                            intermediate, and derived phenotypes according to the first two                            principle components. Ellipses illustrate the mean and variance for each                            phylum. The color coding is identical to that used in the phylogenetic                            tree.
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pcbi-1000202-g010: Phenotype distribution in an ontogenetic-phylogenetic model.(A) The average pairwise Hamming distance between visible phenotypes within and between phyla. Each phylum corresponds to a developmental plan, and the set of the most frequent visible phenotypes produced by this plan represent species. The ancestral phyla is employing a developmental plan with r = 4 and k = 14. In each branching event, each of the two descendant phyla add an additional regulatory element with random connectivities preserving the ancestral component of the developmental plan (Figure 9). This branching process continues until we get the 1024 most recent phyla, each employing a developmental plan with r = 14 and k = 14. (B) A phylogenetic tree including phenotypes from derived and ancestral phyla. The tree is reconstructed by computing the pairwise Hamming distance matrix between all phenotypes and applying a neighbor-joining algorithms. Rectangular, triangular, and circular nodes represent phenotypes from the ancestral phylum, intermediate phyla, and derived phyla respectively. Phyla within each phylogenetic level are illustrated with different colors. The small tree on the bottom left corner illustrates 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 the developmental plan and not in genotype, but the resulting tree successfully clusters the members of each phyla. Furthermore, the members of intermediate phyla are correctly clustered, spanning the same phylogenetic space as their descendants. Members of the ancestral phylum (represented by black rectangles) span similar regions to those covered by all derived phenotypes. (C) Representation of ancestral, intermediate, and derived phenotypes according to the first two principle components. Ellipses illustrate the mean and variance for each phylum. The color coding is identical to that used in the phylogenetic tree.

Mentions: Finally, we consider the effects of the developmental map on phylogenetic regularities. Since we are focusing on the evolution of development bearing on phenotypic diversity and disparity, we do not consider the evolution of the structural genes, but only regulatory interactions. We assume in the following treatment that developmental plans evolve incrementally and neutrally by addition of new genetic regulatory elements into existing regulatory networks. Consider, for example, an ancestral developmental plan that possesses ra transcription factors, controlling k target genes. Descendant developmental plans acquire rb>ra transcription factors (still controlling the same k genes), where all descendant plans share an identical regulatory wiring for the ancestral ra transcription factors, and differ in the wiring of the derived factors (Figure 9). Following findings in the previous section, we focus only on the most frequent phenotypes produced by each plan as evolutionarily representative of the complete, visible phenotype set. By focusing on the most frequent phenotypes, we are considering those phenotypes most likely to be observed. We are interested in the phylogenetic distribution of phenotypes generated by the evolutionary sequence of developmental plans. We observe that the phenotypes comprising a single developmental plan, become more similar throughout the evolutionary process, whereas disparity among members of different plans increases (Figure 10A). This process relates to an increase in the regulatory dimension of the genome, and hence illustrates how regulatory evolution promotes increasing 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 phenotypes                            within and between phyla. Each phylum corresponds to a developmental                            plan, and the set of the most frequent visible phenotypes produced by                            this plan represent species. The ancestral phyla is employing a                            developmental plan with                            r = 4 and                            k = 14. In each                            branching event, each of the two descendant phyla add an additional                            regulatory element with random connectivities preserving the ancestral                            component of the developmental plan (Figure 9). This branching process                            continues until we get the 1024 most recent phyla, each employing a                            developmental plan with                            r = 14 and                            k = 14. (B) A                            phylogenetic tree including phenotypes from derived and ancestral phyla.                            The tree is reconstructed by computing the pairwise Hamming distance                            matrix between all phenotypes and applying a neighbor-joining                            algorithms. Rectangular, triangular, and circular nodes represent                            phenotypes from the ancestral phylum, intermediate phyla, and derived                            phyla respectively. Phyla within each phylogenetic level are illustrated                            with different colors. The small tree on the bottom left corner                            illustrates 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 the                            developmental plan and not in genotype, but the resulting tree                            successfully clusters the members of each phyla. Furthermore, the                            members of intermediate phyla are correctly clustered, spanning the same                            phylogenetic space as their descendants. Members of the ancestral phylum                            (represented by black rectangles) span similar regions to those covered                            by all derived phenotypes. (C) Representation of ancestral,                            intermediate, and derived phenotypes according to the first two                            principle components. Ellipses illustrate the mean and variance for each                            phylum. The color coding is identical to that used in the phylogenetic                            tree.
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Related In: Results  -  Collection

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getmorefigures.php?uid=PMC2562988&req=5

pcbi-1000202-g010: Phenotype distribution in an ontogenetic-phylogenetic model.(A) The average pairwise Hamming distance between visible phenotypes within and between phyla. Each phylum corresponds to a developmental plan, and the set of the most frequent visible phenotypes produced by this plan represent species. The ancestral phyla is employing a developmental plan with r = 4 and k = 14. In each branching event, each of the two descendant phyla add an additional regulatory element with random connectivities preserving the ancestral component of the developmental plan (Figure 9). This branching process continues until we get the 1024 most recent phyla, each employing a developmental plan with r = 14 and k = 14. (B) A phylogenetic tree including phenotypes from derived and ancestral phyla. The tree is reconstructed by computing the pairwise Hamming distance matrix between all phenotypes and applying a neighbor-joining algorithms. Rectangular, triangular, and circular nodes represent phenotypes from the ancestral phylum, intermediate phyla, and derived phyla respectively. Phyla within each phylogenetic level are illustrated with different colors. The small tree on the bottom left corner illustrates 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 the developmental plan and not in genotype, but the resulting tree successfully clusters the members of each phyla. Furthermore, the members of intermediate phyla are correctly clustered, spanning the same phylogenetic space as their descendants. Members of the ancestral phylum (represented by black rectangles) span similar regions to those covered by all derived phenotypes. (C) Representation of ancestral, intermediate, and derived phenotypes according to the first two principle components. Ellipses illustrate the mean and variance for each phylum. The color coding is identical to that used in the phylogenetic tree.
Mentions: Finally, we consider the effects of the developmental map on phylogenetic regularities. Since we are focusing on the evolution of development bearing on phenotypic diversity and disparity, we do not consider the evolution of the structural genes, but only regulatory interactions. We assume in the following treatment that developmental plans evolve incrementally and neutrally by addition of new genetic regulatory elements into existing regulatory networks. Consider, for example, an ancestral developmental plan that possesses ra transcription factors, controlling k target genes. Descendant developmental plans acquire rb>ra transcription factors (still controlling the same k genes), where all descendant plans share an identical regulatory wiring for the ancestral ra transcription factors, and differ in the wiring of the derived factors (Figure 9). Following findings in the previous section, we focus only on the most frequent phenotypes produced by each plan as evolutionarily representative of the complete, visible phenotype set. By focusing on the most frequent phenotypes, we are considering those phenotypes most likely to be observed. We are interested in the phylogenetic distribution of phenotypes generated by the evolutionary sequence of developmental plans. We observe that the phenotypes comprising a single developmental plan, become more similar throughout the evolutionary process, whereas disparity among members of different plans increases (Figure 10A). This process relates to an increase in the regulatory dimension of the genome, and hence illustrates how regulatory evolution promotes increasing 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