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The moment of tooth: rate, fate and pattern of Pacific lingcod dentition revealed by pulse-chase

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Proceedings of the Royal Society B
Authors:
Emily Carr at American Museum of Natural History
Emily Carr
Adam P Summers at University of Washington
Adam P Summers
Karly E Cohen at California State University, Fullerton
Karly E Cohen
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Abstract

Tooth replacement rates of polyphyodont cartilaginous and bony fishes are hard to determine because of a lack of obvious patterning and maintaining specimens long enough to observe replacement. Pulse-chase is a fluorescent technique that differentially colours developing mineralized tissue. We present in situ tooth replacement rate and position data for the oral and pharyngeal detentions of Ophiodon elongatus (Pacific lingcod). We assessed over 10 000 teeth, in 20 fish, and found a daily replacement rate of about two teeth (3.6% of the dentition). The average tooth is in the dental battery for 27 days. The replacement was higher in the lower pharyngeal jaw (LPJ). We found no difference between replacement rates of feeding and non-feeding fish, suggesting feeding was not a driver of tooth replacement. Lingcod teeth have both a size and location fate; smaller teeth at one spot will not grow into larger teeth, even if a large tooth nearby is lost. We also found increased rates of replacement at the posterior of the LPJ relative to the anterior. We propose that lingcod teeth do not migrate in the jaw as they develop; their teeth are fated in size and location, erupting in their functional position.
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Research
Cite this article: Carr EM, Summers AP,
Cohen KE. 2021 The moment of tooth: rate,
fate and pattern of Pacific lingcod dentition
revealed by pulse-chase. Proc. R. Soc. B 288:
20211436.
https://doi.org/10.1098/rspb.2021.1436
Received: 24 June 2021
Accepted: 21 September 2021
Subject Category:
Morphology and biomechanics
Subject Areas:
physiology, developmental biology, evolution
Keywords:
replacement, teeth, polyphyodont, fluorescence
Author for correspondence:
E. M. Carr
e-mail: emilycarr1@mail.usf.edu
Electronic supplementary material is available
online at https://doi.org/10.6084/m9.figshare.
c.5647960.
The moment of tooth: rate, fate and
pattern of Pacific lingcod dentition
revealed by pulse-chase
E. M. Carr
1
, A. P. Summers
2
and K. E. Cohen
3
1
Integrative Biology, University of South Florida, Tampa, FL, USA
2
Friday Harbor Labs, University of Washington, Friday Harbor, WA, USA
3
Biology Department, University of Washington, Seattle, WA, USA
EMC, 0000-0001-7985-863X
Tooth replacement rates of polyphyodont cartilaginous and bony fishes are
hard to determine because of a lack of obvious patterning and maintaining
specimens long enough to observe replacement. Pulse-chase is a fluorescent
technique that differentially colours developing mineralized tissue. We pre-
sent in situ tooth replacement rate and position data for the oral and
pharyngeal detentions of Ophiodon elongatus (Pacific lingcod). We assessed
over 10 000 teeth, in 20 fish, and found a daily replacement rate of about
two teeth (3.6% of the dentition). The average tooth is in the dental battery
for 27 days. The replacement was higher in the lower pharyngeal jaw (LPJ).
We found no difference between replacement rates of feeding and non-
feeding fish, suggesting feeding was not a driver of tooth replacement.
Lingcod teeth have both a size and location fate; smaller teeth at one spot
will not grow into larger teeth, even if a large tooth nearby is lost. We
also found increased rates of replacement at the posterior of the LPJ relative
to the anterior. We propose that lingcod teeth do not migrate in the jaw as
they develop; their teeth are fated in size and location, erupting in their
functional position.
1. Background
Vertebrate dentitions fall into two loose categories—diphyodont dentitions
with a single set of replacement teeth, and polyphyodont dentitions where
teeth are replaced continuously. Genetic pathways for tooth development are
conserved across both types of dentition [1,2], and the diversity of tooth
shapes and dental batteries lie in differential regulation of the same genetic tool-
box [3,4]. Some polyphyodonts have fated replacement teeth, where an
individual tooth is destined to replace a functional tooth at a specific location
[2]. Sharks present an interesting example of tooth fate because though the
teeth are morphologically similar, they nevertheless have a distinct identity.
Each functional tooth has a file of replacements lined up behind it [5,6]. Bony
fishes offer many examples where it is difficult to see a replacement tooth
having an identity relative to a functional tooth, the non-fated condition. For
example, in the fine, dense, spatulate dentition of loricariid catfishes, any par-
ticular well-hooked tooth is much like any other, and replacements come in
from behind without a clear link to an old tooth [7]. It remains to be determined
whether morphologically homodont teleosts have identifiable replacement
teeth that will emerge to fill a particular position or role in the dental battery [8].
A fundamental question in polyphyodont dentitions is whether replacement
is driven by damage [9,10]—does a new tooth grow in response to a broken tooth,
or does it appear because certain regions of the jawexperience greater mechanical
stress [8,9,11]? This complexity is best showcased in the en bloc replacement of one-
quarter of the entire dental battery by piranhas [11]. This maintainsthe integrity of
an interlocked, sharp and serrated dental battery, and certainly is not a response to
every tooth becoming damaged. However, we do not know whether it is a
© 2021 The Author(s) Published by the Royal Society. All rights reserved.
... One of the most important benefits of this method is that it allows a simplified process of obtaining time series data of detailed morphological changes in dentition and oral-pharyngeal cavity in animals such as fish. This method may be useful for studies of dental microwear analysis (Hoffman, Fraser, and Clementz 2015) as well as growth, tooth replacement, and development (Carr, Summers, and Cohen 2021;Streelman et al. 2003;Trapani, Yamamoto, and Stock 2005). It can be used to record detailed intraoral soft-tissue anatomy of living animals, including features that previously could only be evaluated on dead specimens (Luczkovich, Norton, and Gilmore 1995). ...
... Soft tissue and high-resolution dental models created from scans of impressions can also be of use with the physical replication of skeletal movements and feeding mechanics for (XROMM) studies of individuals, which typically depend on whole-body CT scans at low resolution (Camp and Brainerd 2015). Although tooth replacement has been extensively studied from a histological and developmental perspective, there is little data on tooth growth and replacement in living non-mammal individuals (Brink et al. 2021;Carr, Summers, and Cohen 2021;Ellis et al. 2015), especially with time series from a single individual. The recurring creation of whole-dentition tooth records via dental impression provides an opportunity to not only study replacement patterns but also examine external factors that can affect them. ...
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... Thus, gizzards may be a more cost-efficient way to process food, rather than maintaining both a gut and a dentition. Data in support of the metabolic expense of teeth are currently lacking (Mongle et al., 2020) but they are also central to larger questions in understanding the diversity of tooth replacement modes across vertebrates (Carr et al., 2021;Cohen & Summers, 2023). While data defining the metabolic investment for maintaining a dentition are scarce, current studies in primates suggest that the mineralization of teeth is particularly costly (Smith et al., 2017). ...
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