The 'biomineralization toolkit' and the origin of animal skeletons.

Duncan J E Murdock

doi:10.1111/brv.12614

Abstract

Biomineralized skeletons are widespread in animals, and their origins can be traced to the latest Ediacaran or early Cambrian fossil record, in virtually all animal groups. The origin of animal skeletons is inextricably linked with the diversification of animal body plans and the dramatic changes in ecology and geosphere-biosphere interactions across the Ediacaran-Cambrian transition. This apparent independent acquisition of skeletons across diverse animal clades has been proposed to have been driven by co-option of a conserved ancestral genetic toolkit in different lineages at the same time. This 'biomineralization toolkit' hypothesis makes predictions of the early evolution of the skeleton, predictions tested herein through a critical review of the evidence from both the fossil record and development of skeletons in extant organisms. Furthermore, the distribution of skeletons is here plotted against a time-calibrated animal phylogeny, and the nature of the deep ancestors of biomineralizing animals interpolated using ancestral state reconstruction. All these lines of evidence point towards multiple instances of the evolution of biomineralization through the co-option of an inherited organic skeleton and genetic toolkit followed by the stepwise acquisition of more complex skeletal tissues under tighter biological control. This not only supports the 'biomineralization toolkit' hypothesis but also provides a model for describing the evolution of complex biological systems across the Ediacaran-Cambrian transition.

Highlights

Biomineralized skeletons are widespread in animals, and their origins can be traced to the latest Ediacaran or early Cambrian fossil record, in virtually all animal groups
First-appearance data from fossil evidence of animal phyla and classes, coupled with molecular clock divergence dates, indicate that all major phyla originate in the Ediacaran–Cambrian transition, and all bilaterian classes are in place by the end of the Cambrian, with virtually no innovation at higher taxonomic levels in the subsequent 500 million years (Erwin et al, 2011)
This hypothesis makes a number of predictions of the fossil record of the earliest skeletons: (i) mineralized tissues should appear independently in different biomineralizing lineages; (ii) biomineralized taxa should be pre-dated by soft-bodied representatives; (iii) the first skeletal tissues should show greater disparity than their descendants, being subject to looser biological control prior to canalization

Summary

THE PHYLOGENETIC DISTRIBUTION OF ANIMAL SKELETONS

I compile records of the first fossil appearances of extant biomineralizing groups, at (predominantly) class level, for all animal phyla. The tree was time-calibrated using the method described above, to assign branch lengths, and, along with the dominant mineralogy of the extant biomineralizing representatives of the clade, was used to estimate the ancestral state of each node (Fig. 7) This was achieved using the rerooting Method (Yang, Kumar, & Nei, 1995) in the R package phytools (Revell, 2012), using an equal rates model. This methodology was chosen as it makes the fewest possible assumptions of character evolution, and can accommodate uncertainty of tree topology by randomly resolving polytomies with branches of zero length matching nodes to derive the original topology This analysis strongly supports soft-bodied common ancestors to virtually all extant biomineralizing phyla and classes, which is consistent with the fossil and molecular evidence reviewed here. With more fossils resolved as stem taxa to the crown-poriferan classes, and/or less uncertainty in the divergence time estimates, there would be much longer branch length between the origin of crown-Porifera and the origin of its constituent classes, and more time to accommodate the independent origin of sponge skeletons in each class, rather than inheriting an ancestral siliceous skeleton

SKELETONS AND THE ‘METAZOAN TOOLKIT’

CONCLUSIONS

Supporting information