Genomic Insights into bat Senses
Liliana M. Dávalos

Max Planck Institute for Animal Behavior

3 July 2019
Ecology &
Evolution
A double mission
Biological
diversity
Evolution Extinctionincrease decrease
What biological
processes fuel
biodiversity?
What are the social
factors of
environmental
degradation?
How does
biodiversity
change in time/
space?
Research
What biological
processes fuel
biodiversity?
What are the social
factors of
environmental
degradation?
How does
biodiversity
change in time/
space?
Research
BetsyDumont
Stephen Rossiter
KarenSears
two senses
Vision
Olfaction
Credit: Jon Flanders
Molecular ecology of the senses
how does ecology
shape evolution?
can a chemo-
sense be
gained?
Molecular ecology of the senses
how does ecology
shape evolution?
can a chemo-
sense be
gained?
Mormoopidae
Macrotinae
Rhinophyllinae
Stenodermatinae
Carolliinae
Phyllostominae
Noctilionidae
Micronycterinae
Desmodontinae
Glyphonycterinae
Lonchorhininae
Glossophaginae
Million Years Ago
5 10 15 20 25 30 35 40 45
95% CI Node Age
Lonchophyllinae
Dumont, Dávalos et al. 2012 Proc R Soc
Lond B Biol Sci
Credits: Merlin Tuttle/Bat Conservation
International, Bryan Bongey
Genetics & evolution Crick 1958 The Biological Replication of
Macromolecules
But ecological info must
travel upstream
Crick 1958 The Biological Replication of
Macromolecules
Sensory
info
Adaptation
Credit: Stephen Rossiter
Alexa Sadier Kalina Davies
Typical results using
DNA
Wu et al. 2018 Proc R Soc Lond B Biol Sci
But not all genes are
expressed
Sadier et al. 2018 eLife
The protein is closest to
phenotype, but painstaking
Sadier et al. 2018 eLife
Ultimately we care
about traits
• phenotype ~ genotype
Credit: Stephen Rossiter
And this maps out to
the central dogma
• genotype 

• RNA transcript

• cones & vision
Credit: Jon Flanders
Many traits
• foraging 

• Gutierrez et al. 2018 Proc
R Soc

• caves
• Simões et al. 2018 Mol
Biol Evol

• caves & diet 

• Kries et al. 2018 Mol Ecol
& Li et al. 2018 Sci Rep
• sensory tradeoff
• Wu et al. 2018 Proc R
Soc
Credit: Stephen Rossiter
Analyses of the sample-wide or fixed portion of cone density mod
logarithm of the cone density y for each observation i as a function o
variables defined by an diet group j, or S-cone group k. ln(yi) was mo
normally distributed variable with mean mu and variance, as below:
lnðyiÞ~dnormðmu;varianceÞ
lnðyiÞ ¼ a þ b:diet½dietjŠ
lnðyiÞ ¼ a þ b:S:cone½S:conekŠ
Unlike the presence/absence analyses, these response variables w
with the sample-wide portion of the model accounting for the effect
whether known roosts included caves or not. In the sample-wide or fix
models, observations y for each species from one to i for each ecolog
correspond to a single-trial binomial response of the probability of ob
genotype or phenotype given by pri such that:
yi ~dbernðpriÞ
logitðpriÞ ¼ a þ b:ecology½ecologyjŠ
Models for each of the dietary categorizations were then compared
coefficients. For dummy predicators indicating presence/absence, the
the presence indicates the strength of the association with the respon
genotype or phenotype). The predictor variable identified as the most
the presence/absence of S-cones was then used in subsequent analyse
412. DOI: https://doi.org/10.7554/eLife.37412
Credit: Stephen Rossiter
Sadier et al. 2018 eLife
ORFmRNAS−cone
plant fruit insects cave roosting
−10
−5
0
5
10
−10
−5
0
5
10
−10
−5
0
5
10
Ecological variable
Posteriorestimateofcoefficient
predictor
plant
fruit
insects
cave roosting
Sadier et al. 2018 eLife
Understanding color
vision in bats
• Phenotype ~ ecology

• Protein detection
critical

• DNA-only analyses
limited

• Pseudogenization
comes in last

• Actual behavior,
response requires more
work
Credit: Jon Flanders
Molecular ecology of the senses
how does ecology
shape evolution?
can a chemo-
sense be
gained?
Neuweiler 2000 Biology of Bats
The
vomeronasal
A whole other
chemosensory system
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
semester!
Vomerolfaction
resembles olfaction
If TRPC2 breaks,
signaling breaks
A first assessment Quite a few 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
13 independent losses, but
two families conserve it
Yohe et al. 2017 Evolution
Laurel Yohe
Loss, not gain Yohe et al. 2017 Evolution
simulating loss simulating gain
There is more than
TRPC2
Vomeronasal receptors
• Help recognize
species (mice,
lemurs?)

• If similar in bats then
we should see gene
duplications
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
Pseudogene
V1rs
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) and
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 reference.
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
• Conserved

• Phyllostomidae

• Miniopteridae

• But receptors not
expanded

• Unlikely involved in
species recognition
Credit: Stephen Rossiter
Molecular ecology of the senses
how does ecology
shape evolution?
can a chemo-
sense be
gained?
Molecular ecology of the senses
slowly and starting
with the phenotype
no, but
ancestor
conserved it
Thank you!

Genomic Insights into bat Senses