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Olfaction in Bats
by Liliana M. Dávalos

Natural History of the Senses

AMNH, 5 November 2018
Energy flows
upward
But cannot be fully
recovered
Food is more
abundant
At lower trophic levels
Lower trophic
level, more
species
A consistent finding
across groups
Dumont, Dávalos et al. 2012 Proc Royal Soc B
Most bats are
insectivorous
How to detect plant
foods?
Experimental visualization of two interacting
odor plumes (red and blue) in a turbulent flow
Credit: J. Crimaldi and M. Soltys
Photo by Carlos Mancina
Photo by Carlos Mancina
Bats use their
sense of smell
to find fruit
Thies et al. 1998 Behav
Ecol Sociobiol
SearchExploreApproach
Olfactory sensory neurons (in green) transfer
information to olfactory projection neurons (in yellow).
Credit: J. McGann and M. Wachowiak
Olfaction
happens in th
brain
Arthropod model more
tractable
2005 PLoS Biol
Perception
begins with
receptors
Mammalian olfactory
receptor model
embedded in a
biological membrane
Model by Claire de March
Receptors
bind to volatile
molecules
After binding, the
receptors activate a
switch that starts mental
representation of odor
Model by Claire de March
volatile
volatile
volatile
Source Odorants Receptors
A typical example of evolution
Single-copy gene (Understanding Evolution site)
Olfactory
receptor genes
are arranged in
arrays
Physical maps of OR
functional genes and
pseudogenes in several
genomic clusters
Niimura & Nei 2003 PNAS
Source Odorants Receptors
Diverse
odors =
diverse
receptors
As a result
OR genes
make up
~5% of
protein-
coding
genoms
Tan et al. 2013 PNAS
Source Odorants Receptors
Receptors reflect diversity of odorants Each receptor is encoded by one OR gene
Rat
Odorants
Volatile Organic CompoundsOR genes Ecology
Mate
Risk
Food
Food
But olfactory gene evolution
is hard to study
• Data collection

• Requires high-
quality genomes

• Expensive!
Niimura et al. 2018 Mol Biol Evol
To get DNA sequences
Requires combining technologies
OR genes vary by species
But there are so many how to analyze?
Species OR	1/3/7 OR	2/13
OR	
5/8/9
Myo$s	lucifugus 15 2 0
74 24 55
89 26 55
Anoura	geoffroyi 38 7 26
91 30 48
129 37 74
Reduce dimensions
From many gene subfamilies and numbers to two
dimensions
If related to
fruit eating
One or more dimensions
should differ in
frugivores compared to
others
Photo by Carlos Mancina
Frugivores
differ
Have more OR gene
copies in subfamilies
1/3/7 and 2/13
Hayden et al. 2014 Mol Biol Evol
Bats and fruit
Bats use olfaction to
locate fruit and have
distinctive genes to
encode relevant
receptors
Photo by Merlin Tuttle
Neuweiler 2000 Biology of Bats
The
vomeronasal
A whole other
chemosensory system
Neuweiler 2000 Biology of Bats
Neuweiler 2000 Biology of Bats
Did you ever wonder why?
Dogs smell hierarchy and sexual condition
Most bats have atrophied vomeronasal
(top)
Bhatnagar & Meisami 1998 Mic Res & Tech
Diversity of
bats not fully
studied
Almost 1400 species
described as of last
week!
Vomerolfaction
resembles
olfaction
If TRPC2
breaks,
signaling
breaks
A first
assessment
A couple of independent
losses
Zhao et al. 2010 Mol Biol Evol
Phyllostomidae
Miniopteridae
Thyropteridae
Noctilionoidae
Furipteridae
Mormoopidae
Molossidae
Pteropodidae
Rhinolophidae
stopcodonorindel
1
2
3
4
5
6
7
8
9
10
11
14
16
18
ωtest
ω0
Morphology
structurepresent
𝜑structureabsent
𝜑
𝜑
𝜑
𝜑
𝜑
𝜑
𝜑
𝜑
𝜑
𝜑
𝜑
Natalidae
Emballonuridae
19
Yangochiroptera
Megadermatidae
Yinpterochiroptera
Hipposideridae
Lonchorhinaaurita(11)
Glyphonycterissylvestris
Carolliasowelli
Leptonycteriscuraosae
Hipposiderospratti
Lionycterisspurrelli
Glossophagalongirostris
Artibeusintermedius
Platyrrhinusnigellus
Chirodermavillosum
Vampyressathyone
Carolliabrevicauda
Eonycterisspelaea
Brachyphyllapumila(14)
Platyrrhinusinfuscus
Lophostomaevotis
Platyrrhinusaurarius
Anourageoffroyi(13)
Megadermaspasma(1)
Noctilioleporinus
Cormurabrevirostris
Erophyllasezekorni
Rhinolophusferrumequinum(2)
Hipposiderosarmiger
Acerodoncelebensis
Miniopterusfuliginosus
Sturniratildae
Artibeuscinereus
Diphyllaecaudata
Lonchophyllahesperia
Choeroniscusgodmani
Artibeuslituratus
Cynopterussphinx
Lophostomabrasiliense
Thyropteralavali
Miniopterusaelleni
Mormoopsblainvillei(6)
Miniopterussororculus
Chirodermaimprovisum(16)
Tadaridabrasiliensis(3)
Urodermamagnirostrum
Pteronotusmacleayii
Lophostomasilvicolum
Anouralatidens
Sphaeronycteristoxophyllum(20)
Pteronotusparnellii(7)
Brachyphyllacavernarum
Phyllonycterispoeyi
Carolliacastanea
Chilonatalusmicropus
Enchistheneshartii
Lonchophyllachocoana
Ariteusflavescens
Artibeusconcolor
Diaemusyoungi
Tonatiasaurophila
Chirodermadoriae
Musonycterisharrisoni
Micronycterisminuta
Leptonycterisnivalis
Sturniramagna
Dobsoniaviridis
Artibeusphaeotis
Trinycterisnicefori
Sturniralilium
Platyrrhinusdorsalis
Miniopterusminor
Phyllopsfalcatus(18)
Thoopterusnigrescens
Platyrrhinusalbericoi
Anouracaudifer
Carolliasubrufa
Artibeusobscurus
Micronycterisschmidtorum
Phyllostomuselongatus(10)
Miniopteruspetersoni
Lampronycterisbrachyotis
Platyrrhinuslineatus
Artibeusfimbriatus
Mesophyllamacconnelli
Rhinophyllafischerae
Ectophyllaalba
Artibeusincomitatus
Artibeusinopinatus
Thyropteratricolor
Furipterushorrens(5)
Micronycterismicrotis(8)
Artibeusglaucus
Sturnirabogotensis
Carolliaperspicillata
Artibeusjamaicensis
Platalinagenovensium
Mormoopsmegalophylla
Vamypressabidens
Vampyrodescaraccioli(17)
Lonchorhinainusitata
Miniopterusgleni
Sturniraoporaphilum
Pygodermabilabiatum
Glossophagacommissarisi
Erophyllabombifrons(15)
Pteronotusquadridens
Artibeusgnomus
Miniopterusschreibersii(4)
Vampyressabrocki
Artibeuswatsoni
Glossophagasoricina
Desmodusrotundus(9)
Ardopsnichollsi
Centuriosenex(19)
Tonatiabidens
Choeronyterismexicana(12)
Megadermalyra
12
15
+activeflight
-echolocation
-dichromacy
-dichromacy
-dichromacy
-dichromacy
-dichromacy
+traitgain
traitloss
_
Caribbean
colonization
+CF-echo
+CF-echo
+UV
+distinctORprofile
Musmusculus
Pteronotusdavyi
13
+thermoperception
17
20
Yohe et al. 2017 Evolution
13 independent losses of
vomeronasal function
But 2 families conserve
the system

Why?
There is more
than TRPC2
Vomeronasal
receptors help
recognize
species (mice)
If similar in bats then we
should see gene
expansions
Sorex araneus
Erinaceus europaeus
Canis familiaris
Felis catus
Equus caballus
Vicugna vicugna
Bos taurus
Tursiops truncatus
Pteropus vampyrus
Pteropus alecto
Rousettus aegyptiacus
Hipposideros armiger
Rhinolophus ferrumequinum
Rhinolophus sinicus
Megaderma lyra
Miniopterus natalensis
Eptesicus fuscus
Myotis lucifugus
Myotis davidii
Myotis brandtii
Pteronotus parnellii
Desmodus rotundus (genome)
Desmodus rotundus
Glossophaga soricina
Carollia brevicauda
Sturnira ludovici
Sturnira lilium
Artibeus fraterculus
Eulipotyphyla
Carnivora
Perissodactyla
Artiodactyla
Chiroptera
Order Species Trpc2 Intact
V1rs
Pseudo
V1
ψ
ψ
ψ
ψ
ψ
ψ
*
*
*
*
*
*
*
*
*
*
*
44
39
6
17
30
22
40
0
0
0
0
2
0
1
1
6
0
0
0
0
3
14
8
2
1
4
4
7
80
84
28
79
48
36
43
33
21
23
18
18
22
22
17
3
3
1
2
3
19
2
--
--
--
--
--
--
V1r numbers taken from the values in the supplement (not adjusted) of Young, et al. (2010)
therefore may be an underestimate as genome assemblies have improved.
ψ
* Trpc2 is intact; Trpc2 is a pseudogene. See (Zhao et al. 2011; Yohe et al. 2017) for refere
A few
receptors in
each case
Instead of gene
expansion
Yohe et al. In Review
*
*
B
A
*
Yinpterochiroptera
Yangochiroptera(noTrpc2)
non-phyllostomidswithintactTrpc2
intactV1R
pseudogeneV1R
0.2
A
C
Rousettusaegyptiacus|XM_016129349.1|V1R|PSEUDOGENE
Pteronotusparnellii|KE854661.1_11589-12504_functional
Sturniraludovici|MG812210|V1R
Pteropusvampyrus|NW_011889304.1_83054-83939|V1R|PSEUDOGENE
Pteropusalecto|NW_006431909.1_43873-44757|V1R|PSEUDOGENE
Sturniralilium|MG812192|V1R
Equuscaballus|NM_001167528.1|V1R
Sturniralilium|MG812191|V1R
Megadermalyra|KI124397.1_7621-6732|V1R|PSEUDOGENE
Pteronotusparnellii|KE858350.1_13033-13940
Eidolonhelvum|KE766962.1_25820-26706|V1R|PSEUDOGENE
Rhinolophussinicus|XM_019711635.1|V1R|PSEUDOGENE
Artibeusfraterculus|MG812202|V1R
Miniopterusnatalensis|XM_016215914.1|V1R
Pteropusalecto|XM_015592506.1|V1R|PSEUDOGENE
Pteropusvampyrus|XM_011379300.1|V1R|PSEUDOGENE
820
1000
1000
1000
1000
788
1000
994
1000
999
1000
926
943
1000
969
942
999
654
1000
Pteropusvampyrus|NW_011889332.1_152788-152164|V1R|PSEUDOGENE
Pteropusvampyrus|NW_011889109.1_915949-916553|V1R|PSEUDOGENE
Rhinolophussinicus|NW_017739251.1_2311634-2310975|V1R|PSEUDOGENE
Rousettusaegyptiacus|NW_015493370.1_55119-54488|V1R|PSEUDOGENE
Rhinolophusferrumequinum|KI143012.1_5636-6299|V1R|PSEUDOGENE
Eidolonhelvum|AWHC01287768.1_1707-2330|V1R|PSEUDOGENE
Rhinolophusferrumequinum|AWHA01229154.1_6963-6298|V1R|PSEUDOGENE
Canisfamiliaris|NC_006583.3_103953482-103954375.2
Pteronotusparnellii|KE823115.1_8391-9050|V1R|PSEUDOGENE
Myotisbrandtii|NW_005354543.1_204626-204000|V1R|PSEUDOGENE
Pteronotusparnellii|KE870141.1_5159-4523|V1R|PSEUDOGENE
Hipposiderosarmiger|NW_017732838.1_124037-124688|V1R|PSEUDOGENE
Canisfamiliaris|NC_006583.3_103953482-103954375
Miniopterusnatalensis|NW_015504026.1_4304-3677|V1R|PSEUDOGENE
Rousettusaegyptiacus|NW_015493018.1_189943-190545|V1R|PSEUDOGENE
Hipposiderosarmiger|NW_017732838.1_140299-139642|V1R|PSEUDOGENE
Pteropusalecto|NW_006433947.1_87061-87685|V1R|PSEUDOGENE
Pteropusalecto|NW_006431917.1_828306-828910|V1R|PSEUDOGENE
Megadermalyra|KI049987.1_6965-6281|V1R|PSEUDOGENE
Rhinolophussinicus|NW_017739251.1_2374154-2374762|V1R|PSEUDOGENE
1000
832
772
1000
1000
898
589
989
1000
994
758
362
1000
956
1000
1000
993
1000
1000
Rhinolophussinicus|NW_017740069.1_21725-20827|V1R|PSEUDOGENE
Desmodusrotundus|MG812199|V1R
Artibeusfraterculus|MG812204|V1R
Pteronotusparnellii|AWGZ01429722.1_1435-519|V1R|PSEUDOGENE
Hipposiderosarmiger|NW_017732944.1_73203-72305|V1R|PSEUDOGENE
Rhinolophusferrumequinum|AWHA01282185.1_3211-4107|V1R|PSEUDOGENE
Canisfamiliaris|NC_006588.3_16711026-16711932
Pteropusvampyrus|NW_011889066.1_2157585-2156705|V1R|PSEUDOGENE
Artibeusfraterculus|MG812206|V1R
Eidolonhelvum|KE778038.1_25207-26077|V1R|PSEUDOGENE
Pteropusalecto|NW_006435779.1_377403-378267|V1R|PSEUDOGENE
Artibeusfraterculus|MG812203|V1R
Pteronotusparnellii|AWGZ01427934.1_2-665|V1R|PSEUDOGENE
Rousettusaegyptiacus|NW_015494717.1_369965-370848|V1R|PSEUDOGENE
Artibeusfraterculus|MG812205|V1R
Pteronotusparnellii|AWGZ01227917.1_847-1768|V1R|PSEUDOGENE
Sturniralilium|MG812190|V1R
Sturniraludovici|MG812208|V1R
Megadermalyra|AWHB01121129.1_229-1108|V1R|PSEUDOGENE
1000
1000
1000
1000
954
898
757
971
1000
786
1000
1000
378
1000
1000
1000
1000
1000
*
*
Hipposiderosarmiger|NW_017732518.1_182161-183072|V1R|PSEUDOGENE
Rousettusaegyptiacus|NW_015495152.1_598933-599834|V1R|PSEUDOGENE
B
Hipposiderosarmiger|NW_017732884.1_117260-116366|V1R|PSEUDOGENE
Rhinolophusferrumequinum|KI136309.1_1552-665|V1R|PSEUDOGENE
C
*
*
*
*
*
Pattern: conserve a
few, lose a lot
Vomeronasal
in bats
Is conserved but does
not expand, not likely
involved in species
recognition
Neuweiler 2000 Biology of Bats
Neuweiler 2000 Biology of Bats
Thank you!

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