Integration, Modularity, and Vertebrate Evolution and Development
Background: As part of my Ph.D. research in the Committee on Evolutionary Biology at the University of Chicago, I collected 3-D landmark data from more than 2000 osteological specimens and developed new analytical tools to assess landmark correlations and their relationship to phylogeny, diet, encephalization, and sequence heterochrony. Using taxa with convergent ecologies and morphologies to isolate the relationships among trait integration, phylogeny, and diet, she demonstrated that modularity does evolve during mammalian evolution, with significant differences between monotremes and therians (marsupials and placentals). The strength of within-module trait correlations varies across the skull and across taxa, probably reflecting developmental influences. The recognition that modularity is an evolving feature has great significance for understanding and testing how trait correlations influence morphological evolution.
In recent years, we have expanded this research in several ways. We have used computer simulations, based on empirical and theoretical models of modularity, and analyses of morphological disparity within modules to assess the long-standing hypothesis that trait correlations influence morphological variation and, thus, morphological evolution (with P.D. Polly, Indiana University). Our simulations and empirical analyses demonstrate how trait integration may shape morphological diversity, but also suggests that it does not necessarily affect evolutionary rates. We have also simulated the effect of character correlations on discrete character states, with relevance for cladistic analyses. We have recently developed a new likelihood tool for the analysis of modularity from correlation matrices (with J. Finarelli, University College Dublin), and we have also developed methods to analyse morphological rates of evolution using 3D landmarks and other multivariate metrics (with C. Soligo, UCL Anthropology and J. Smaers, SUNY Stony Brook).
With funding from the European Research Council, we are now conducting an extensive analysis of modularity and diversity across tetrapods, involving surface scanning and analysis of thousands of living and extinct taxa spanning their past and present ecological, morphological, developmental, and phylogenetic breadth. With these data, we will assess shifts in modularity, evolutionary rates, and morphological disparity through the evolution of terrestrial vertebrates and identify if these shifts are associated with changes in ecology, development, or environment. Combined this study will provide unprecedented power to reconstruct the major intrinsic and extrinsic factors shaping vertebrate evolution and identify trends in modularity and its evolutionary significance.
C. Bardua, M. Wilkinson, D.J. Gower, E. Sherratt, and A. Goswami. 2019. Morphological evolution and modularity of the caecilian skull. BMC Evolutionary Biology 19 (1), 30. https://doi.org/10.1186/s12862-018-1342-7
R.N. Felice, J. Tobias, A. Pigot, and A. Goswami. 2019. Dietary Niche and the Evolution of Cranial Morphology in Birds. Proceedings of the Royal Society B, in press.
A. Marshall, C. Bardua, D.J. Gower, M. Wilkinson, E. Sherratt, and A. Goswami. High-dimensional 3D morphometric analysis supports conserved static (intraspecific) modularity in caecilian (Amphibia: Gymnophiona) crania. Biological Journal of the Linnean Society, in press.
M. Churchill, J. Miguel, B.L. Beatty, A. Goswami, and J.H. Geisler. 2018. Asymmetry drives modularity of the skull in the common dolphin (Delphinus delphis). Biological Journal of the Linnean Society, in press (published online early). https://doi.org/10.1093/biolinnean/bly190
R.N. Felice and A. Goswami. 2017. Developmental origins of mosaic evolution in the avian cranium. Proceedings of the National Academy of Sciences, USA, 115: 555-560.
M. Randau & A. Goswami. 2018. Shape covariation (or the lack thereof) between vertebrae and other skeletal traits in felids: the whole is not always greater than the sum of parts. Evolutionary Biology, in press (published online)
M. Randau and A. Goswami. 2017. Morphological modularity in the vertebral column of Felidae (Mammalia, Carnivora). BMC Evolutionary Biology 17, 133
M. Randau and A. Goswami. 2017. Unravelling intra-vertebral integration, modularity and disparity in Felidae (Mammalia). Evolution & Development, 19: 85-95
A. Goswami and J.A. Finarelli. 2016. EMMLi: a maximum likelihood approach to the analysis of modularity. Evolution, 70: 1622-1637. Supplementary Information
A. Goswami, M. Randau, P.D. Polly, V. Weisbecker, C. V. Bennett, L. Hautier, and M.R. Sanchez-Villagra. 2016. Do high integration and developmental constraints limit the evolution of the marsupial cranium? Integrative and Comparative Biology, 56: 404-414.
A. Goswami, W. Binder, J. Meachen, and F.R. O'Keefe. 2015. The fossil record of phenotypic integration and modularity: A deep-time perspective on developmental and evolutionary dynamics. Proceedings of the National Academy of Sciences, USA, 112: 4891-4896.
A. Goswami, J.B. Smaers, C. Soligo, and P.D. Polly. 2014. The macroevolutionary consequences of phenotypic integration. Philosophical Transactions of the Royal Society of London, B, 369: 20130254.
A.-C. Fabre, A. Goswami, S. Peigné, and R. Cornette. 2014. Morphological integration in the forelimb of musteloid carnivorans. Journal of Anatomy, 225:19-30.
L. Rager, L. Hautier, A. Forasiepi, A. Goswami, M.R. Sanchez-Villagra. 2014. Timing of cranial suture closure in placental mammals: Phylogenetic patterns, intraspecific variation, and comparison with marsupials. Journal of Morphology, 275: 125-140.
V. Weisbecker and A. Goswami. 2014. Reassessing the relationship between brain size, life history, and metabolism at the marsupial/placental dichotomy. Zoological Science, 31: in press.
C.V. Bennett, A. Goswami. 2013. Statistical support for the hypothesis of developmental constraint in marsupial skull evolution. BMC Biology, 11, 1: 52.
P.D. Polly, A.M. Lawing, A.-C. Fabre, A. Goswami. 2013. Phylogenetic Principal Components Analysis and Geometric Morphometrics. Hystrix, the Italian Journal of Mammalogy, 24, 1: 9
T.J.D. Halliday, A. Goswami. 2013. Testing the inhibitory cascade model in Mesozoic and Cenozoic mammaliaforms. BMC Evolutionary Biology, 13, 1: 79.
A. Goswami, L. Foley, V. Weisbecker, V. 2013. Patterns and implications of extensive heterochrony in carnivoran cranial suture closure. Journal of Evolutionary Biology, 26, 6: 1294- 1306.
L. Hautier, N.C. Bennett, H. Viljoen, L. Howard, M. Milinkovitch, A.C. Tzika, A. Goswami, R.J. Asher. 2013. Patterns of ossification in southern versus northern placental mammals. Evolution, 67, 7: 1994-2010.
A. Goswami, P.D. Polly, O. Mock, and M.R. Sánchez-Villagra. 2012. Shape, variance and integration during craniogenesis: contrasting marsupial and placental mammals. Journal of Evolutionary Biology, 25: 862-872.
A. Goswami, N. Milne, and S. Wroe. 2011. Biting through constraints: cranial morphology, disparity, and convergence across living and fossil carnivorous mammals. Proceedings of the Royal Society of London B, Biological Sciences, 278: 1831-1839. Supplementary Files.
Bennett, C.V. and A. Goswami. 2011. Does reproductive strategy drive limb integration in marsupials and monotremes? Mammalian Biology, 76: 79-83.
V. Weisbecker and A. Goswami. 2011. Neonatal maturity as the key to understanding brain size evolution in homeothermic vertebrates. Bioessays, 33: 155-158.
V. Weisbecker and A. Goswami. 2011. Marsupials indeed confirm an ancestral mammalian pattern: a reply to Isler. Bioessays, 33: 358-361.
L. Hautier, V. Weisbecker, A. Goswami, N. Kardjilov, and R. Asher. 2011. Skeletal ossification and sequence heterochrony in xenarthran evolution. Evolution & Development, 13: 460–476.
Bell, E., B. Andres, and A. Goswami. 2011. Limb integration and dissociation in flying vertebrates: a comparison of birds, bats, and pterosaurs. Journal of Evolutionary Biology, 24: 2586-2599.
A. Goswami and P.D. Polly. 2010. The influence of modularity on cranial morphological disparity in Carnivora and Primates (Mammalia). PLoSOne, 5(3):e9517.
V. Weisbecker and A. Goswami. 2010. Brain size, life history, and metabolism at the marsupial/placental dichotomy. Proceedings of the National Academy of Sciences, USA, 107: 16216-16221. Supplemental Information
L. Hautier, V. Weisbecker, M.R. Sánchez-villagra, A. Goswami, R.J. Asher. 2010. Skeletal development in sloths and the evolution of mammalian vertebral patterning. Proceedings of the National Academy of Sciences USA.
A. Goswami and P.D. Polly. 2010. The influence of character correlations of phylogenetic analyses: a case study of the carnivoran cranium. In Carnivoran Evolution: New Views on Phylogeny, Form, and Function (A. Goswami and A. Friscia, eds.). Cambridge: Cambridge University Press, pp. 141-164.
A. Goswami and P.D. Polly. 2010. Methods for studying morphological integration and modularity. In Quantitative Paleontology (J. Alroy and G. Hunt, eds.). Paleontological Society Special Publications, pp 213-243.
A. Goswami, V. Weisbecker, and M. R. Sánchez-Villagra. 2009. Developmental modularity and the marsupial-placental dichotomy. Journal of Experimental Zoology B, 312B: 186–195.
V. Weisbecker, A. Goswami, S. Wroe, and M. R. Sánchez-Villagra. 2008. Ossification heterochrony in the therian postcranial skeleton and the marsupial-placental dichotomy. Evolution, 62 (8): 2027–2041
M. R. Sánchez-Villagra, A. Goswami, V. Weisbecker, O. Mock, and S. Kuratani. 2008. Conserved relative timing of cranial ossification patterns in early mammalian evolution. Evolution and Development, 10 (5): 519-530
A. Goswami and J. Prochel. 2007. Ontogenetic morphology and cranial allometry of the common European mole (Talpa europaea). Journal of Mammalogy, 88(3), 667-677.
A. Goswami. 2007. Modularity and sequence heterochrony in the mammalian skull. Evolution and Development, 9(3): 291-299.
A. Goswami. 2007. Phylogeny, diet, and cranial integration in australodelphian marsupials. PLoS ONE 2(10): e995
K.E. Sears, A. Goswami, J. J. Flynn, and L. Niswander. 2007. The correlated evolution of Runx2 tandem repeats and facial length in Carnivora. Evolution and Development, 9(6): 555-565.
J. Prochel, A. Goswami, F. David Carmona, and R. Jimenez. 2007. Ossification sequence in the mole Talpa occidentalis (Eulipotyphla, Talpidae) and comparisons with other mammals. Mammalian Biology, 73: 399-403.
A. Goswami. 2006. Morphological integration in the carnivoran skull. Evolution, 60: 122-136.
A. Goswami. 2006. Cranial modularity shifts during mammalian evolution. American Naturalist, 168:170-180.
N. Giannini, A. Goswami, and M. Sánchez-Villagra. 2006. Development of integumentary structures in Rousettus amplexicaudatus (Mammalia: Chiroptera: Pteropodidae) during late-embryonic and fetal stages. Journal of Mammalogy 87(5): 993-1001.
Modules, semi-autonomous subsets of highly-correlated traits, provide a practical framework for summarizing general patterns of trait interactions, which are often cited as a major influence on morphological variation. However, little comparative data on modularity exists, hindering the identification of trends in modularity and the application of hypotheses of modularity’s evolutionary significance to large-scale evolutionary patterns. Our research has primarily focused on broad, comparative study of cranial modularity and trait integration across vertebrates, spanning over 1800 fossil and extant species of mammals, birds, non-avian dinosaurs, crocodiles, turtles, squamates, frogs, salamanders, and caecilians. Other projects have examined integration in postcranial elements, including limbs of mammals, pterosaurs, and birds, and full skeletal analyses in felids. We have also tested hypotheses of ontogenetic variation and integration and their relationship to adult morphology, particularly as it relates to the marsupial-placental dichotomy in mammal evolution. Our current work expands these analyses with comprehensive sampling across all tetrapods. Most recently, we have started a project examining these questions in arthropods, specifically assessing how developmental mode, integration, and diversification relate across holometabolous and hemimetabolous insects.