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Breaking constraint of mammalian axial formulae.

ABSTRACT: The vertebral column of individual mammalian species often exhibits remarkable robustness in the number and identity of vertebral elements that form (known as axial formulae). The genetic mechanism(s) underlying this constraint however remain ill-defined. Here, we reveal the interplay of three regulatory pathways (Gdf11, miR-196 and Retinoic acid) is essential in constraining total vertebral number and regional axial identity in the mouse, from cervical through to tail vertebrae. All three pathways have differing control over Hox cluster expression, with heterochronic and quantitative changes found to parallel changes in axial identity. However, our work reveals an additional role for Hox genes in supporting axial elongation within the tail region, providing important support for an emerging view that mammalian Hox function is not limited to imparting positional identity as the mammalian body plan is laid down. More broadly, this work provides a molecular framework to interrogate mechanisms of evolutionary change and congenital anomalies of the vertebral column.

SUBMITTER: Hauswirth GM

PROVIDER: S-EPMC8752674 | biostudies-literature | 2022 Jan

REPOSITORIES: biostudies-literature

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Breaking constraint of mammalian axial formulae.

Hauswirth Gabriel M GM Garside Victoria C VC Wong Lisa S F LSF Bildsoe Heidi H Manent Jan J Chang Yi-Cheng YC Nefzger Christian M CM Firas Jaber J Chen Joseph J Rossello Fernando J FJ Polo Jose M JM McGlinn Edwina E

Nature communications 20220111 1

The vertebral column of individual mammalian species often exhibits remarkable robustness in the number and identity of vertebral elements that form (known as axial formulae). The genetic mechanism(s) underlying this constraint however remain ill-defined. Here, we reveal the interplay of three regulatory pathways (Gdf11, miR-196 and Retinoic acid) is essential in constraining total vertebral number and regional axial identity in the mouse, from cervical through to tail vertebrae. All three pathw ...[more]

PMID: 35017475

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Project description:Complexity, defined as the number of parts and their degree of differentiation, is a poorly explored aspect of macroevolutionary dynamics. The maximum anatomical complexity of organisms has undoubtedly increased through evolutionary time. However, it is unclear whether this increase is a purely diffusive process or whether it is at least partly driven, occurring in parallel in most or many lineages and with increases in the minima as well as the means. Highly differentiated and serially repeated structures, such as vertebrae, are useful systems with which to investigate these patterns. We focus on the serial differentiation of the vertebral column in 1,136 extant mammal species, using two indices that quantify complexity as the numerical richness and proportional distribution of vertebrae across presacral regions and a third expressing the ratio between thoracic and lumbar vertebrae. We address three questions. First, we ask whether the distribution of complexity values in major mammal groups is similar or whether clades have specific signatures associated with their ecology. Second, we ask whether changes in complexity throughout the phylogeny are biased towards increases and whether there is evidence of driven trends. Third, we ask whether evolutionary shifts in complexity depart from a uniform Brownian motion model. Vertebral counts, but not complexity indices, differ significantly between major groups and exhibit greater within-group variation than recognized hitherto. We find strong evidence of a trend towards increasing complexity, where higher values propagate further increases in descendant lineages. Several increases are inferred to have coincided with major ecological or environmental shifts. We find support for multiple-rate models of evolution for all complexity metrics, suggesting that increases in complexity occurred in stepwise shifts, with evidence for widespread episodes of recent rapid divergence. Different subclades evolve more complex vertebral columns in different configurations and probably under different selective pressures and constraints, with widespread convergence on the same formulae. Further work should therefore focus on the ecological relevance of differences in complexity and a more detailed understanding of historical patterns.

Dataset Information

Breaking constraint of mammalian axial formulae.

Publications

Breaking constraint of mammalian axial formulae.

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