Abstract
The Ammonoidea is a group of extinct cephalopods ideal to study evolution through deep time. The evolution of the planispiral shell and complexly folded septa in ammonoids has been thought to have increased the functional surface area of the chambers permitting enhanced metabolic functions such as: chamber emptying, rate of mineralization and increased growth rates throughout ontogeny. Using nano-computed tomography and synchrotron radiation based micro-computed tomography, we present the first study of ontogenetic changes in surface area to volume ratios in the phragmocone chambers of several phylogenetically distant ammonoids and extant cephalopods. Contrary to the initial hypothesis, ammonoids do not possess a persistently high relative chamber surface area. Instead, the functional surface area of the chambers is higher in earliest ontogeny when compared to Spirula spirula. The higher the functional surface area the quicker the potential emptying rate of the chamber; quicker chamber emptying rates would theoretically permit faster growth. This is supported by the persistently higher siphuncular surface area to chamber volume ratio we collected for the ammonite Amauroceras sp. compared to either S. spirula or nautilids. We demonstrate that the curvature of the surface of the chamber increases with greater septal complexity increasing the potential refilling rates. We further show a unique relationship between ammonoid chamber shape and size that does not exist in S. spirula or nautilids. This view of chamber function also has implications for the evolution of the internal shell of coleoids, relating this event to the decoupling of soft-body growth and shell growth.
Highlights
Cephalopods are a group of marine mollusks that evolved in the Cambrian from a monoplacophoran-like ancestor [1,2,3,4]; the earliest known cephalopod is the Late Cambrian Plectronoceras [5,6]
Using nano-computed tomography and synchrotron radiation based micro-computed tomography, we present the first study of ontogenetic changes in surface area to volume ratios in the phragmocone chambers of several phylogenetically distant ammonoids and extant cephalopods
We further show a unique relationship between ammonoid chamber shape and size that does not exist in S. spirula or nautilids
Summary
Cephalopods are a group of marine mollusks that evolved in the Cambrian from a monoplacophoran-like ancestor [1,2,3,4]; the earliest known cephalopod is the Late Cambrian Plectronoceras [5,6]. Basal cephalopods possess a phragmocone that is distinct from other mollusk shells (conch) by the division into discrete chambers (Fig 1). The chambers are separated by mineralized partitions called septa that allows the shell to function as a buoyancy device. The multichambered, aragonitic cephalopod shell is a key adaptation that allows the animal to dwell in PLOS ONE | DOI:10.1371/journal.pone.0151404. Evolution and Ontogeny of Cephalopod Chamber Shape doi:10.1371/journal.pone.0151404.g001 the water column without constantly expending energy [7,8]. A thin organic strand, called the siphuncle, runs through all phragmocone chambers and connects this with the rear of the soft body that sits in the body chamber. Liquid and gas diffuse into and out of the chambers through the siphuncle and thereby allows for buoyancy adjustments [9,10]. The siphuncle was supported by the connecting pellicle, a thin (sub-micron) proteinaceous structure composed of conchiolin, that covers the inner surface of each chamber which stores and transports liquid to the siphuncle [9]
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