Dataset Information

Modularity of stress response evolution.

ABSTRACT: Responses to extracellular stress directly confer survival fitness by means of complex regulatory networks. Despite their complexity, the networks must be evolvable because of changing ecological and environmental pressures. Although the regulatory networks underlying stress responses are characterized extensively, their mechanism of evolution remains poorly understood. Here, we examine the evolution of three candidate stress response networks (chemotaxis, competence for DNA uptake, and endospore formation) by analyzing their phylogenetic distribution across several hundred diverse bacterial and archaeal lineages. We report that genes in the chemotaxis and sporulation networks group into well defined evolutionary modules with distinct functions, phenotypes, and substitution rates as compared with control sets of randomly chosen genes. The evolutionary modules vary in both number and cohesiveness among the three pathways. Chemotaxis has five coherent modules whose distribution among species shows a clear pattern of interdependence and rewiring. Sporulation, by contrast, is nearly monolithic and seems to be inherited vertically, with three weak modules constituting early and late stages of the pathway. Competence does not seem to exhibit well defined modules either at or below the pathway level. Many of the detected modules are better understood in engineering terms than in protein functional terms, as we demonstrate using a control-based ontology that classifies gene function according to roles such as "sensor," "regulator," and "actuator." Moreover, we show that combinations of the modules predict phenotype, yet surprisingly do not necessarily correlate with phylogenetic inheritance. The architectures of these three pathways are therefore emblematic of different modes and constraints on evolution.

SUBMITTER: Singh AH

PROVIDER: S-EPMC2396705 | biostudies-literature | 2008 May

REPOSITORIES: biostudies-literature

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Modularity of stress response evolution.

Singh Amoolya H AH Wolf Denise M DM Wang Peggy P Arkin Adam P AP

Proceedings of the National Academy of Sciences of the United States of America 20080521 21

Responses to extracellular stress directly confer survival fitness by means of complex regulatory networks. Despite their complexity, the networks must be evolvable because of changing ecological and environmental pressures. Although the regulatory networks underlying stress responses are characterized extensively, their mechanism of evolution remains poorly understood. Here, we examine the evolution of three candidate stress response networks (chemotaxis, competence for DNA uptake, and endospor ...[more]

PMID: 18495925

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Project description:BackgroundCaecilians (Gymnophiona) are the least speciose extant lissamphibian order, yet living forms capture approximately 250 million years of evolution since their earliest divergences. This long history is reflected in the broad range of skull morphologies exhibited by this largely fossorial, but developmentally diverse, clade. However, this diversity of form makes quantification of caecilian cranial morphology challenging, with highly variable presence or absence of many structures. Consequently, few studies have examined morphological evolution across caecilians. This extensive variation also raises the question of degree of conservation of cranial modules (semi-autonomous subsets of highly-integrated traits) within this clade, allowing us to assess the importance of modular organisation in shaping morphological evolution. We used an intensive surface geometric morphometric approach to quantify cranial morphological variation across all 32 extant caecilian genera. We defined 16 cranial regions using 53 landmarks and 687 curve and 729 surface sliding semilandmarks. With these unprecedented high-dimensional data, we analysed cranial shape and modularity across caecilians assessing phylogenetic, allometric and ecological influences on cranial evolution, as well as investigating the relationships among integration, evolutionary rate, and morphological disparity.ResultsWe found highest support for a ten-module model, with greater integration of the posterior skull. Phylogenetic signal was significant (Kmult = 0.87, p < 0.01), but stronger in anterior modules, while allometric influences were also significant (R2 = 0.16, p < 0.01), but stronger posteriorly. Reproductive strategy and degree of fossoriality were small but significant influences on cranial morphology (R2 = 0.03-0.05), after phylogenetic (p < 0.03) and multiple-test (p < 0.05) corrections. The quadrate-squamosal 'cheek' module was the fastest evolving module, perhaps due to its pivotal role in the unique dual jaw-closing mechanism of caecilians. Highly integrated modules exhibited both high and low disparities, and no relationship was evident between integration and evolutionary rate.ConclusionsOur high-dimensional approach robustly characterises caecilian cranial evolution and demonstrates that caecilian crania are highly modular and that cranial modules are shaped by differential phylogenetic, allometric, and ecological effects. More broadly, and in contrast to recent studies, this work suggests that there is no simple relationship between integration and evolutionary rate or disparity.

Project description:Insect wings show a high variability in wing venation. Selection for function, developmental pathways and phylogeny likely influenced wing vein diversification, however, quantitative data to estimate these influences and their interplay are missing. Here, it is tested how dragonfly wing vein configuration is influenced by functional demands, development, phylogeny and allometry using the concepts of modularity and integration. In an evolutionary context, modules are sets of characters that evolve in relative independence to other characters, while integration refers to a high degree of association between subparts of a structure. Results show allometric and phylogenetic signal in the wing shape variation, however, patterns of integration and modularity are not influenced by these two factors. Overall, dragonfly wings are highly integrated structures with almost no modular signal. Configuration changes in one wing vein or wing area thus influence wing shape as a whole. Moreover, the fore- and hindwings correlate with each other in their evolutionary shape variation supporting biomechanical data of wing interdependence. Despite the overall high degree of evolutionary integration, functional hypotheses of modularity could be confirmed for two wing areas, the arculus-triangle complex at the base of the wing which is responsible for passive wing folding especially during flapping flight and the location of the pterostigma, a coloured wing cell which is more heavy that other wing cells and passively regulates wing pitch as well as critical flight speeds during gliding. Although evolving as distinct modules, these specific vein regions also show high integration and evolve at the same rates like the whole wing which suggests an influence of these structures on the shape evolution of the rest of the wing. Their biomechanical role as passive regulators of wing corrugation and wing pitch suggests that these structures decisively influenced the evolution of advanced modern flight styles and explains their retention once they had evolved early within the lineage Odonatoptera.

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Modularity of stress response evolution.

Publications

Modularity of stress response evolution.

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