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

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.

SUBMITTER: Borenstein E

PROVIDER: S-EPMC2562988 | biostudies-literature |

REPOSITORIES: biostudies-literature

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Project description:BACKGROUND:Evolution in one selective environment often latently generates phenotypic change that is manifested only later in different environments, but the complexity of behavior important to fitness in the original environment might influence the character of such latent-phenotype evolution. Using Myxococcus xanthus, a bacterium possessing two motility systems differing in effectiveness on hard vs. soft surfaces, we test (i) whether and how evolution while swarming on one surface-the selective surface-latently alters motility on the alternative surface type and (ii) whether patterns of such latent-phenotype evolution depend on the complexity of ancestral motility, specific ancestral motility genotypes and/or the selective surface of evolution. We analysze an experiment in which populations established from three ancestral genotypes-one with both motility systems intact and two others with one system debilitated-evolved while swarming across either hard or soft agar in six evolutionary treatments. We then compare motility-phenotype patterns across selective vs. alternative surface types. RESULTS:Latent motility evolution was pervasive but varied in character as a function of the presence of one or two functional motility systems and, for some individual-treatment comparisons, the specific ancestral genotype and/or selective surface. Swarming rates on alternative vs. selective surfaces were positively correlated generally among populations with one functional motility system but not among those with two. This suggests that opportunities for pleiotropy and epistasis generated by increased genetic complexity underlying behavior can alter the character of latent-phenotype evolution. No tradeoff between motility performance across surface types was detected in the dual-system treatments, even after adaptation on a surface on which one motility system dominates strongly over the other in driving movement, but latent-phenotype evolution was instead idiosyncratic in these treatments. We further find that the magnitude of stochastic diversification at alternative-surface swarming among replicate populations greatly exceeded diversification of selective-surface swarming within some treatments and varied across treatments. CONCLUSION:Collectively, our results suggest that increases in the genetic and mechanistic complexity of behavior can increase the complexity of latent-phenotype evolution outcomes and illustrate that diversification manifested during evolution in one environment can be augmented greatly by diversification of latent phenotypes manifested later.

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

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