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Tympanic Bulla Morphology and Desert Adaptation in Rodents

Authors:
Bader H. Alhajeri at Kuwait University
Bader H. Alhajeri
John Jeffrey Schenk at Ohio University
John Jeffrey Schenk
Scott J. Steppan
Scott J. Steppan
Scott J. Steppan
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Abstract

Background/Question/Methods Phylogenetic history, adaptation, and drift are the primary determinants of phenotype, although each can differ in magnitude and direction (i.e. complementary or antagonistic). Desert rodents share many distinctive features. Among the most distinctive features is the hypertrophy of the tympanic bulla. A common functional explanation for this trait is that it is an adaptation for increased sensitivity to sound that is necessary for both prey capture and predator avoidance in open habitats where sound tends to dissipate quickly. Using a new composite phylogeny of >1,000 myodont and heteromyid rodents that documents multiple transitions into deserts, we conducted phylogenetic independent contrasts to determine whether variation in tympanic bullae morphology of rodents is associated with aridity. Morphology of the bulla was quantified from specimens photographed at natural history museums using geometric morphometric approaches. We tested whether size (centroid size and relative size of the bulla to the rest of the skull) and shape variables (using semi-landmarks) are correlated with environmental variables (temperature, precipitation, and net primary productivity). Co-variation of skull shape variables with environmental variables was compared in three primarily desert dwelling rodent taxa (dipodoids, heteromyids, and gerbils) and their mesic relatives. Results/Conclusions There was significant phylogenetic signal in the size and shape of the tympanic bulla. These were strongly correlated with habitat aridity. When desert and mesic species were pooled into two bins after discretizing environmental variables, a clear and significant difference was detected. This effect was detected in all taxa even after the effect of phylogeny was removed (i.e. phylogenetic ANOVA analysis). The pattern was less clear when environmental variables were treated as continuous variables (i.e. phylogenetic independent contrasts analysis). Other regions of the skull showed no correlation with aridity. This evidence supports the theory that adaptation plays a similar role in shaping the evolution of the tympanic bulla in various taxa of desert rodents. The general pattern that rodents in arid environments have significantly larger bulla than rodents in mesic environments holds true in most taxa even after phylogenetic correction. Evidence for the correlation between bulla shape variables with environmental variables is more tenuous.
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Tympanic Bulla Morphology and
Desert Adaptation in Rodents
Bader H. Alhajeri, John J. Schenk, and Scott J. Steppan
Department of Biological Science -Florida State University
alhajeri@bio.fsu.edu
98th Annual Meeting of the Ecological Society of America
August 5th 2013
Sundevall's Jird
Tympanic Bulla
Mount Apo
Forest Mouse
Tympanic Bulla
Adaptation of bulla morphology
–Gerbils
–Kangaroo rats
–Hopping mice
–Jerboas
–Spiny rats
Eastern Namib Desert/ ComQuat/CC-BY-SA
–Caviomorphs
–Dormice
–Pikas
–Armadillos
–Many others…
Is bulla morphology an adaptation to aridity?
–Phylogenetic relationship
More Similar
Gerbils
Spiny rats
Maned rat
Order Rodentia
•2277 species -474 genera
•Found in all continents -all
terrestrial ecosystems
•11% of rodent species are
classified as ‘desert’ by
IUCN red list
Great gerbil
Cairo spiny mouse
Yuriy75/ CC-BY-SA
o.leillinger@web.de/ CC-BY-SA
Desert Rodent Clades
1. Sciuromorpha= 26/307 (8%)
2. Castorimorpha= 40/102 (40%)
3. Myodonta= 172/1569 (11%)
•Subfamily: Gerbillinae: 51/103 (50%)
•Rodent supertree from Fabre (2012)
–2260 species
•Muroidea (1516 species) replaced with a an
unpublished tree from Steppan et al.
–More molecular data and better resolution
•All absent rodent species re-grafted
–Final tree = all extant rodent species (2414 OTUs)
How many times did rodent clades
transition to desert environments?
How many times did rodent clades
transition to desert environments?
Gerbil 1
Gerbil 2
Maned rat
More likely to be desert
Less likely to be desert
DesertMesic
How many times did rodent clades
transition to desert environments?
Mesic
No desert transition
Desert transition
DesertMesic
Myodonta
Anomaluromorpha
Sciuromorpha
Hystricomorpha
Castorimorpha
2414 OTU phylogenetic
tree of rodents
Myodonta
Anomaluromorpha
Sciuromorpha
Hystricomorpha
Castorimorpha
18 independent transitions
to desert ecosystems
from mesic
ecosystems
13
0
1
2
2
Is bulla size an adaptation to
aridity?
•579 species randomly sampled from the tree
–All superfamilies
•4 specimens measured per species
–2075 specimens total
•Includes both desert and mesic species
Bulla Size Index
BI = Bulla Length /Skull Length
Bulla Size Index
Width
Length
Aridity Index
•GIS
–WorldClim bioclimatic variables (2.5 min)
–IUCN species ranges
•Aridity index calculated from bioclimatic variables
following De Martonne (1942)
Annual average rainfall (mm)
Annual average temp (°C) + 10
12 x Average rainfall of driest quarter (mm)
Average temp of driest quarter (°C) + 10
+
2
Is bulla size an adaptation to
aridity?
F= 174.29
p= 0.001
DesertMesic
Bulla Size
Is bulla size an adaptation to
aridity?
F= 6.29
p= 0.012
R2= 0.01
Aridity
Bulla Size
Are other regions of the
skull correlated with
aridity?
9 additional size corrected
measurements
–Bullar width (F= 119.00; p= 0.001)
–Incisors (F= 85.83; p= 0.011)
–Diastema
–Molars (length + width)
–Pterygoid region
–basicranial width (F= 105.06; p= 0.002)
–Basioccipital
–Occipital condyle
Are other regions of the
skull correlated with
aridity?
9 additional size corrected
measurements
–Bullar width (F= 119.00; p= 0.001)
–Incisors (F= 85.83; p= 0.011)
–Diastema
–Molars (length + width)
–Pterygoid region
–basicranial width (F= 105.06; p= 0.002)
–Basioccipital
–Occipital condyle
Subfamily: Gerbillinae
•83 gerbil species + outgroups
–4 specimens/ species
Is bulla size an adaptation to aridity?
Length Index
LI = Bulla Length
/Skull Length
Area Index
AI = Bulla Area /Skull Area
Bulla Area Index
Is bulla size an adaptation to aridity?
F= 23.71
p= 0.001
DesertMesic
Is bulla size an adaptation to aridity?
F= 12.13
p= 2.46e-05
R2= 0.11
Bulla Area Index
Aridity Index
Is bulla shape an adaptation to aridity?
Bulla shape index (estimated using GM):
–Ventral outline
–GPA analysis –shape variables independent of size (relative warps)
Is bulla shape an adaptation to aridity?
F= 9.17; p= 0.032
DesertMesic
Relative Warp 1
Is bulla shape an adaptation to aridity?
Bulla Shape RW1
Aridity Index
F= 10.38
p= 9.69e-05
R2= 0.10
What generalizations can be made?
Order Rodentia
–Desert rodents have significantly larger bulla when
using discrete variables
–Relationship weaker when aridity is treated as a
continuous variable
What generalizations can be made?
Subfamily Gerbillinae
–Desert gerbils have significantly larger bullae than
mesic gerbils
–Within deserts: aridity = bulla size
–Bulla shape correlated with aridity
•Aridity = anterior-posterior bulla elongation
Acknowledgements
Museums
American Museum of Natural History:
–Nancy B. Simmons, Ross MacPhee, Robert S. Voss, and Eileen Westwig
Field Museum of Natural History:
–Lawrence Heaney, Bruce Patterson, and William Stanley
Florida Museum of Natural History:
–David L. Reed and Candace McCaffery
Museum of Vertebrate Zoology:
–Christopher J. Conroy
National Museum of Natural History:
–Michael D. Carleton and Darrin P. Lunde
Funding
-Kuwait University Fellowship
-National Science Foundation
Grant DEB-0841447 to SJS
... In this study, we found that the change in annual average precipitation had the most obvious effects on the tympanic bulla. The areas with the least precipitation in the seven regions had the largest tympanic bulla and the most sensitive hearing; this is similar to the findings of some scholars (Lay, 1972;Squarcia et al., 2007;Alhajeri et al., 2013), that is, the rodents that live in arid environments have larger tympanic bulla than those living in wet environments. Hence, we speculated that the water content of the soil has a great influence on the tympanic bulla of the plateau zokor. ...
Geometric morphometric analysis of the plateau zokor (Eospalax baileyi) revealed significant effects of environmental factors on skull variations
Article
  • Apr 2020
  • ZOOLOGY
The plateau zokor (Eospalax baileyi) is employed as an ideal model for examining the relationships between phenotypic and ecological adaptations to the underground conditions in which the skull morphology evolves to adapt to tunnel environment. We evaluated the influence of environmental factors (altitude, temperature, and precipitation) and geographical distance on the variations in skull morphology of a native subterranean rodent plateau zokor population. Thin-plate spline showed that the trend of morphological changes along the CV1 axis was as follows: the two zygomatic arch and the two postorbital processes moved down, the two mastoid processes and the tooth row moved upward, and the tympanic bulla grew longer. The changes along the CV2 axis were as follows: the nasal bone and the tooth row became longer, the distance between the two anterior tips of zygomatic arch lengthened, the infraorbital foramen became smaller, the whole posterior part of the skull became shorter, the zygomatic bone and the two posterior tips of zygomatic arch moved down, and the foramen magnum became bigger. Thus we found significant differences in the skull shape among the seven populations studied. Along with the reduction in the altitude and increase in the mean annual temperature and mean annual precipitation, the nasal bone became shorter, the distance between the two anterior tips of the zygomatic arch became shorter, the whole posterior part of the skull lengthened, the infraorbital foramen became smaller, the two mastoid processes moved upward, and the occipital bone moved down on the dorsal surface of the skull. On the ventral surface of the skull, with an increase in the altitude, mean annual temperature, and mean annual precipitation, the tympanic bulla became shorter, the tooth row moved down, and the foramen magnum became smaller. The morphological changes in the skull were significantly positively correlated with environmental factors. Finally, there was a significant positive correlation between the Procrustes distance matrix of the skull and the geographic distance matrix, which indicates that the evolution of the plateau zokor follows the distance isolation model, but it needs to be further explored from genetic perspectives.
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