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Modularity and its evolutionary consequences

Grant number: 11/14295-7
Support type:Research Projects - Thematic Grants
Duration: February 01, 2012 - January 31, 2018
Field of knowledge:Biological Sciences - Genetics
Principal Investigator:Gabriel Henrique Marroig Zambonato
Grantee:Gabriel Henrique Marroig Zambonato
Home Institution: Instituto de Biociências (IB). Universidade de São Paulo (USP). São Paulo , SP, Brazil
Associated scholarship(s):14/26262-4 - Direct estimates of evolutionary parameters via quantitative trait loci analysis, BP.DR
14/12632-4 - Morphological evolution and cranial integration in Phyllostomidae, BP.PD
13/07299-1 - Skull morphological integration and evolution of cranial morphology in Feliformia (Carnivora; Mammalia), BP.MS
+ associated scholarships 13/06577-8 - Morphologic integration in Lemuriform (primates: Strepsirrhini) skull, BP.MS
12/24937-9 - Xenarthran (Mammalia) cranial evolution: modularity and its evolutionary consequences on the morphological diversification, BP.PD
11/21674-4 - Evolutionary consequences of morphological integration in the skull and mandible of Caniformia (Carnivora; Mammalia), BP.DR - associated scholarships


Modularity in Biology refers to the pattern of connections among elements: genes, proteins, morphological traits. This pattern emerges whenever a high connectivity between some elements in the system exists, forming modules, and at the same time those same elements are more loosely connected to other elements that compose other modules. Many types of modules have been recognized in Biology, such as: a) functional, composed of characters that work together to perform a function, b) development, which correspond to parts of an embryo that are relatively autonomous with respect to the developing pattern and differentiation, or an independent signaling cascade, c) variation modules, composed of characters that vary together and are relatively independent of other sets of characters. One way to study the modularity of organisms is to investigate the pattern of genetic covariances and correlations between their characters, because traits with common function or development tend to form relatively independent groups of variation among themselves, or modules. If modular organization exists in a organism, the expectation would be a pattern of high correlations between traits within the modules and low correlations between traits in different modules. Studying the modularity, or the morphological integration of organisms, is fundamental to understanding the evolution of complex features, as the modular structure influences the multivariate evolution: the relationship between the inherited patterns of modular covariation and patterns of selection may, for example, restrict or facilitate certain evolutionary paths for a population. In this project we aim to analyze the patterns of modularity and its evolutionary consequences for the phenotypic evolution in mammals in a comparative way, explicitly incorporating the phylogeny of the groups. Those Phylogenies will be obtained in the literature for some groups and others will be produced within the scope of the project itself. (AU)

Articles published in Revista Pesquisa FAPESP about the project
Theory under construction 

Scientific publications (15)
(References retrieved automatically from Web of Science and SciELO through information on FAPESP grants and their corresponding numbers as mentioned in the publications by the authors)
ROSSONI, DANIELA M.; COSTA, BARBARA M. A.; GIANNINI, NORBERTO P.; MARROIG, GABRIEL. A multiple peak adaptive landscape based on feeding strategies and roosting ecology shaped the evolution of cranial covariance structure and morphological differentiation in phyllostomid bats. Evolution, v. 73, n. 5, p. 961-981, MAY 2019. Web of Science Citations: 0.
ANDRADE MACHADO, FABIO; GONCALVES ZAHN, THIAGO MACEK; MARROIG, GABRIEL. Evolution of morphological integration in the skull of Carnivora (Mammalia): Changes in Canidae lead to increased evolutionary potential of facial traits. Evolution, v. 72, n. 7, p. 1399-1419, JUL 2018. Web of Science Citations: 4.
SIMON, MONIQUE NOUAILHETAS; MARROIG, GABRIEL. Evolution of a complex phenotype with biphasic ontogeny: Contribution of development versus function and climatic variation to skull modularity in toads. ECOLOGY AND EVOLUTION, v. 7, n. 24, p. 10752-10769, DEC 2017. Web of Science Citations: 3.
PENNA, ANNA; MELO, DIOGO; BERNARDI, SANDRA; OYARZABAL, MARIA INES; MARROIG, GABRIEL. The evolution of phenotypic integration: How directional selection reshapes covariation in mice. Evolution, v. 71, n. 10, p. 2370-2380, OCT 2017. Web of Science Citations: 4.
ROSSONI, DANIELA M.; ASSIS, ANA PAULA A.; GIANNINI, NORBERTO P.; MARROIG, GABRIEL. Intense natural selection preceded the invasion of new adaptive zones during the radiation of New World leaf-nosed bats. SCIENTIFIC REPORTS, v. 7, SEP 11 2017. Web of Science Citations: 6.
ASSIS, ANA PAULA A.; ROSSONI, DANIELA M.; PATTON, JAMES L.; MARROIG, GABRIEL. Evolutionary processes and its environmental correlates in the cranial morphology of western chipmunks (Tamias). Evolution, v. 71, n. 3, p. 595-609, MAR 2017. Web of Science Citations: 4.
PAVAN, ANA C.; MARROIG, GABRIEL. Timing and patterns of diversification in the Neotropical bat genus Pteronotus (Mormoopidae). Molecular Phylogenetics and Evolution, v. 108, p. 61-69, MAR 2017. Web of Science Citations: 8.
PORTO, ARTHUR; SCHMELTER, RYAN; VANDEBERG, JOHN L.; MARROIG, GABRIEL; CHEVERUD, JAMES M. Evolution of the Genotype-to-Phenotype Map and the Cost of Pleiotropy in Mammals. Genetics, v. 204, n. 4, p. 1601+, DEC 2016. Web of Science Citations: 4.
ASSIS, A. P. A.; PATTON, J. L.; HUBBE, A.; MARROIG, G. Directional selection effects on patterns of phenotypic (co)variation in wild populations. PROCEEDINGS OF THE ROYAL SOCIETY B-BIOLOGICAL SCIENCES, v. 283, n. 1843 NOV 30 2016. Web of Science Citations: 4.
SIMON, MONIQUE NOUAILHETAS; MACHADO, FABIO ANDRADE; MARROIG, GABRIEL. High evolutionary constraints limited adaptive responses to past climate changes in toad skulls. PROCEEDINGS OF THE ROYAL SOCIETY B-BIOLOGICAL SCIENCES, v. 283, n. 1841 OCT 26 2016. Web of Science Citations: 8.
PAVAN, ANA CAROLINA; MARROIG, GABRIEL. Integrating multiple evidences in taxonomy: species diversity and phylogeny of mustached bats (Mormoopidae: Pteronotus). Molecular Phylogenetics and Evolution, v. 103, p. 184-198, OCT 2016. Web of Science Citations: 14.
HUBBE, ALEX; MELO, DIOGO; MARROIG, GABRIEL. A case study of extant and extinct Xenarthra cranium covariance structure: implications and applications to paleontology. PALEOBIOLOGY, v. 42, n. 3, p. 465-488, SUM 2016. Web of Science Citations: 3.
WOLF, JASON B.; HOWIE, JENNIFER A.; PARKINSON, KATIE; GRUENHEIT, NICOLE; MELO, DIOGO; ROZEN, DANIEL; THOMPSON, CHRISTOPHER R. L. Fitness Trade-offs Result in the Illusion of Social Success. Current Biology, v. 25, n. 8, p. 1086-1090, APR 20 2015. Web of Science Citations: 18.
MELO, DIOGO; MARROIG, GABRIEL. Directional selection can drive the evolution of modularity in complex traits. Proceedings of the National Academy of Sciences of the United States of America, v. 112, n. 2, p. 470-475, JAN 13 2015. Web of Science Citations: 32.

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