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Orangutan Canine Linear Enamel Hypoplasia Defects Assessed in Association with Flanging Status

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Abstract

Orangutans exhibit intrasex bimaturism, a trait rare among primates. Males exist in two morphs: flanged, with large bidiscoid cheek pads on their face and a laryngeal throat pouch, and unflanged, lacking secondary sexual characteristics and displaying “developmental arrest.” Flanged males in captivity are shown to have higher levels of testosterone and cortisol than unflanged males. However, research on wild orangutan remains has a greater potential to inform differences in early life stress experiences, as zoo orangutans rarely remain developmentally arrested. Here, we use associated orangutan skins and skulls to assess flanging status, canine height (n=37), and measure an early life stress indicator, linear enamel hypoplasia (LEH) defect depth, using confocal profilometry (n=7). Of the 24 defects measured, flanged male defects were deeper (range 24.7-126.6, mean 73.4) than in unflanged adult males (range 12.1-63.5, mean 31.04) (t test p=0.026). While the majority of population-level variation in defect depth is related to how rapidly canines grow in height, when assessing intrasex variation, evidence from great apes suggests that deeper defects might reflect more severe stress events during development. Flanged and unflanged males likely have similar canine development given that canine projective crown heights are similar across all males regardless of morph (p=0.47) with no overlap between males and females (p<0.001) (means: flanged 23.15, unflanged 24.55, female 14.75). Therefore, our results may indicate an adaptive benefit to arresting development is avoiding chronic stress and its associated physiological impacts. Future directions include examining differences in microanatomical growth between morphs via histologic and surface analyses.
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Alexandra E. Kralick1and Kate McGrath2,3
Background
Discussion
Acknowledgements
This project received funding from the European Union’s Horizon 2020 research and innovation program under the Marie Sklodowska-Curie grant agreement No 798117, Penn Museum, and NSF Graduate
Research Internship Program (GRIP). Work done in collaboration with Dr. Janet Monge, Adjunct Professor and Keeper of Collections, University of Pennsylvania Museum of Archaeology and Anthropology.
Thanks to Dr. Morgan Hoke and Dr. Theodore Schurr for feedback. Thanks to Alain Queffelec, the Smithsonian National Museum of Natural History (NMNH), the Academy of Natural Sciences of
Philadelphia (ANSP), and the American Museum of Natural History (AMNH) for making available their collections and equipment for research.
Materials & Sample Size
Orangutans (Pongo spp.) were analyzed at the National
Museum of Natural History, Washington, DC (NMNH;N=24),
Academy of Natural Sciences, Philadelphia (ANSP;N=6), and
American Museum of Natural History, NYC (AMNH;N=7).
In the wild, there are two types of adult male orangutans,
flanged and unflanged.Flanged males are socially
dominant and have large visible cheek pads on their face
and athroat pouch for mate calling, while unflanged adult
males lack secondary sexual characteristics, thus
displaying ‘developmental arrest.’
Captive flanged males have higher levels of testosterone
and the stress hormone cortisol than unflanged males.
However, zoo orangutans rarely remain developmentally
arrested into adulthood.For this reason, it is necessary to
study wild individuals.
Linear enamel hypoplasia (LEH) defects reflect episodes of
stress during early life. Evidence from great apes suggests
that deeper defects might reflect more severe stress events
during development.
Hypothesis:Unflanged male orangutans exhibit less
severe markers of developmental stress (LEH defects)
than flanged males
Courtesy of Meredith Bastian, Sungai Lading Orangutan Field Project
143588
Unflanged
male
145301
Flanged
male
Future Directions
Significance
Orangutan Canine Linear Enamel Hypoplasia Defects Assessed
in Association with Flanging Status
LEH Methods & Results
A-B: Defects were identified
by surface visualization and
imaged with the Sensofar S
Neox confocal profilometer
C-D: The resulting digital
elevation models (DEMs)
were read into ImageJ
D-E: A transect was drawn
across each DEM so that
maximum LEH defect depth
could be measured using the
FindPeaks plug-in (following
McGrath et al., 2018)
Evidence from studies of great ape canines
suggests that sexes and species with faster-
growing teeth have shallower LEH defects.
However, when comparing among teeth with
similar growth patterns, deeper defects likely
reflect more severe and/or longer-lasting growth
disruptions. For example, apes captured from
the wild as infants and raised in captivity have
particularly deep defects (McGrath et al., 2018).
Male orangutans have similar canine crown
heights regardless of morph, but flanged
males have significantly deeper LEH defects
than unflanged males.
This result may reflect more severe stress
events and/or longer disruptions during the
juvenile phase of development for orangutans
that end up as adult flanged males compared to
those who remain in arrested development as
adult unflanged males.
These results may indicate an adaptive benefit to
arresting development is avoiding chronic stress
and its associated physiological impacts.
Future directions include expanding sample sizes
at additional museums and examining differences
in microanatomical growth between morphs via
histologic and surface analyses.
Canine Height Method & Results
Flanging Status Method & Results
Skins were visually examined for flanges following Kralick (2018,
2019). The skin was measured from ear to eye, showing that flanged
males have distinctive measures compared to unflanged and females.
Canine projective crown height was measured with
calipers from the lowest extent of the cementum-
enamel junction to the apex on the mesio-buccal
side. Teeth with moderate wear were excluded.
Flanged
(N=20)
Unflanged
(N=14)
1Department of Anthropology, University of Pennsylvania; 2UMR 5199 PACEA, Université
de Bordeaux; 3Department of Anthropology, The George Washington University
Unflanged Flanged
Sample for
canine height
analysis:
Sex Type N
M
Flanged 7
Unflanged 3
Unknown – likely flanged 3
Unknown – likely unflanged 4
Juvenile – complete canines 2
FAdult and young adult 18
TOTAL 37
Sample for
LEH analysis:
Sex Type N
M
Flanged 7
Unflanged 3
Unknown – likely unflanged 1
TOTAL 11
Permanent canine impressions were made using Coltene’s
President Jet regular body.High-resolution positive replicas
were made using Loctite Hysol epoxy.
Flanged males have significantly deeper LEH defects than
unflanged males (N=34 defects; F(1,7)=15.8, p=0.0053). We
conducted a linear mixed effects model with specimen ID as a
random effect as multiple defects were measured per specimen.
A
B
C
D
Canine projective crown heights are similar across
males regardless of morph (t-test; p=0.47), with no
overlap between males and females (p<0.001)
Defect Depth (µm)
125
75
25
Defect depth
1000
0 µm
30
10
E
Materials & Sample Size
... At the population level, mountain gorillas that developed their teeth during a period of intense human encroachment have defects that are almost twice as deep as those that lived under increased protection 17 . Further, flanged orangutans, which exhibit higher levels of the stress hormone cortisol throughout development, have defects that are more than twice as deep as unflanged or developmentally arrested males with either the same or lower cortisol levels 28 . The duration of the disruption is also likely to affect classic furrow-form defect dimensions, as is usually approximated by counting the number of perikymata involved in the defect, with each additional perikyma carving more deeply into the enamel wall 20,21 . ...
Article
Full-text available
Early life stress disrupts growth and creates horizontal grooves on the tooth surface in humans and other mammals, yet there is no consensus for their quantitative analysis. Linear defects are considered to be nonspecific stress indicators, but evidence suggests that intermittent, severe stressors create deeper defects than chronic, low-level stressors. However, species-specific growth patterns also influence defect morphology, with faster-growing teeth having shallower defects at the population level. Here we describe a method to measure the depth of linear enamel defects and normal growth increments (i.e., perikymata) from high-resolution 3D topographies using confocal profilometry and apply it to a diverse sample of Homo neanderthalensis and H. sapiens anterior teeth. Debate surrounds whether Neanderthals exhibited modern human-like growth patterns in their teeth and other systems, with some researchers suggesting that they experienced more severe childhood stress. Our results suggest that Neanderthals have shallower features than H. sapiens from the Upper Paleolithic, Neolithic, and medieval eras, mirroring the faster growth rates in Neanderthal anterior teeth. However, when defect depth is scaled by perikymata depth to assess their severity, Neolithic humans have less severe defects, while Neanderthals and the other H. sapiens groups show evidence of more severe early life growth disruptions.
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