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Adaptive evolution of hearing genes in
echolocating dolphins
Magpali, L.1
; Freitas, L.1
; Ramos, E. K. S.1
; de Souza, E. M. S.1
; Nery, M. F1
.
1. University of Campinas / Biology Institute, Brazil
Correspondence email: leticiamagpali@gmail.com
Twitter: @leticiamagpali
I Meeting of Systematics, Biogeography and Evolution (SBE)
Introduction
Cetaceans share a unique
evolutionary history, marked
by the transition from land to
the ocean
Followed by a rapid
diversification through
multiple habitats: polar
waters, estuaries,
coastal waters, rivers,
deep ocean
was essential to the
evolution of echolocation
and is mediated by the
activity of hearing genes
mostly inside inner and
outer hair cells of the
cochlea
Inia geoffrensis, Amazon river dolphin
Sotalia guianensis, Guiana dolphin.
Estuaries and coastal waters
Orcinus orca, Killer Whale.
Such radical
environmental changes
likely posed strong
constraints on their
echolocation systems
through the evolution of different acoustic patterns
(Jensen et al. 2018) and cochlear morphologies (Costeur et
al. 2019) in echolocating dolphins
BACKGROUND
GOAL
Study the molecular evolution
of hearing genes among
dolphins from different
habitats, looking for patterns
of adaptive convergence and
positive selection
HYPOTHESIS
Dolphins from riverine,
oceanic and coastal
habitats have evolved
under different
selective regimes on
hearing genes
HIGH FREQUENCY
HEARING
Cochlear hair cell
Material and methods
Selected GENES CLDN141
(adhesion protein; ion flow)
TMC11
(development)
SLC26A52
(motor protein)
CDH231,2
(adhesion protein; ion flow)
SMPX1
(stereocilia movement regulation)
Branch-model
analyses performed
on PAML → two
model x one model
Directly required for
hair cell function and
development
Previously reported under:
1- positive selection in odontocetes
(Davies et al. 2011, McGowen et al. 2014, Foote et al. 2015).
2- molecular convergence between dolphins and bats
(Liu et al. 2010, Shen et al. 2012, Xu et al. 2013, Liu et al. 2014)
5 nucleotide gene trees
5 protein gene trees
Sequence extraction
with BLAST + python
script
Coding sequences
only
Results
Minkewhale
Baiji dolphin
Beluga
NarwhalNarrow ridged
finless porpoise
Orca
Pacific
White-Sided
Dolphin
Long-finned pilot
whale
Guiana dolphin
Tucuxi river
dolphin
Common
bottlenose
dolphin
Sperm
whale
Echolocating
dolphins
TMC1 protein gene tree recovered possible
bat-dolphin convergence, showing
echolocating dolphins and bats as sister groups.
Echolocating
bats
Branches under
positive selection
recovered by aBSREL
(highlighted).
Contrast-FEL
sites with different
overall dN/dS among
river and marine
dolphins in TMC1 (1)
and CDH23 (36)aBSREL
branches under
positive selection:
TMC1 and CDH23
alignments
CDH23 species tree with
branch under selection
highlighted
MEME
sites under positive
selection in dolphin
branches: CDH23
(8), SLC26A5 (1),
TMC1 (3)
Whale
No tree supported dolphin-dolphin
convergence
SUMMARY
Discussion and conclusion
Preliminary selection analysis on codeml indicates
altered selective regimes in at least one branch (among
cetaceans and reference species) for all genes
TMC1 and CDH23
possible targets to investigate adaptive
convergence/differential selection between river
and marine dolphins?
Contrast-FEL results suggest that some sites
within these genes have evolved differently
between freshwater and marine dolphins
BUSTED + aBSREL results indicate
gene-wide episodic diversifying selection
among dolphin branches
Codeml: two model and branch-site models to locate
branches and sites positively selected
More accurate convergence tests will allow examine
convergence within dolphins from different habitats
Locate and characterize sites under selection
dolphins showed proportionally
less selected sites compared to
reference species
*reference tree= dolphins
+ whales + other species
*dolphin tree = only
dolphins
Future directions
SLC26A5, TMC1,
CDH23 under
positive selection in
some, but not all,
dolphin lineages
S.guianensis has
recently split from
sister species and P.
catodon has sonar
adaptations to deep
diving
HOWEVER...
no support for molecular
adaptive convergence so far
1
2

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Magpali et al (2020) Adaptive evolution of hearing genes in echolocating dolphins (1)

  • 1. Adaptive evolution of hearing genes in echolocating dolphins Magpali, L.1 ; Freitas, L.1 ; Ramos, E. K. S.1 ; de Souza, E. M. S.1 ; Nery, M. F1 . 1. University of Campinas / Biology Institute, Brazil Correspondence email: leticiamagpali@gmail.com Twitter: @leticiamagpali I Meeting of Systematics, Biogeography and Evolution (SBE)
  • 2. Introduction Cetaceans share a unique evolutionary history, marked by the transition from land to the ocean Followed by a rapid diversification through multiple habitats: polar waters, estuaries, coastal waters, rivers, deep ocean was essential to the evolution of echolocation and is mediated by the activity of hearing genes mostly inside inner and outer hair cells of the cochlea Inia geoffrensis, Amazon river dolphin Sotalia guianensis, Guiana dolphin. Estuaries and coastal waters Orcinus orca, Killer Whale. Such radical environmental changes likely posed strong constraints on their echolocation systems through the evolution of different acoustic patterns (Jensen et al. 2018) and cochlear morphologies (Costeur et al. 2019) in echolocating dolphins BACKGROUND GOAL Study the molecular evolution of hearing genes among dolphins from different habitats, looking for patterns of adaptive convergence and positive selection HYPOTHESIS Dolphins from riverine, oceanic and coastal habitats have evolved under different selective regimes on hearing genes HIGH FREQUENCY HEARING Cochlear hair cell
  • 3. Material and methods Selected GENES CLDN141 (adhesion protein; ion flow) TMC11 (development) SLC26A52 (motor protein) CDH231,2 (adhesion protein; ion flow) SMPX1 (stereocilia movement regulation) Branch-model analyses performed on PAML → two model x one model Directly required for hair cell function and development Previously reported under: 1- positive selection in odontocetes (Davies et al. 2011, McGowen et al. 2014, Foote et al. 2015). 2- molecular convergence between dolphins and bats (Liu et al. 2010, Shen et al. 2012, Xu et al. 2013, Liu et al. 2014) 5 nucleotide gene trees 5 protein gene trees Sequence extraction with BLAST + python script Coding sequences only
  • 4. Results Minkewhale Baiji dolphin Beluga NarwhalNarrow ridged finless porpoise Orca Pacific White-Sided Dolphin Long-finned pilot whale Guiana dolphin Tucuxi river dolphin Common bottlenose dolphin Sperm whale Echolocating dolphins TMC1 protein gene tree recovered possible bat-dolphin convergence, showing echolocating dolphins and bats as sister groups. Echolocating bats Branches under positive selection recovered by aBSREL (highlighted). Contrast-FEL sites with different overall dN/dS among river and marine dolphins in TMC1 (1) and CDH23 (36)aBSREL branches under positive selection: TMC1 and CDH23 alignments CDH23 species tree with branch under selection highlighted MEME sites under positive selection in dolphin branches: CDH23 (8), SLC26A5 (1), TMC1 (3) Whale No tree supported dolphin-dolphin convergence SUMMARY
  • 5. Discussion and conclusion Preliminary selection analysis on codeml indicates altered selective regimes in at least one branch (among cetaceans and reference species) for all genes TMC1 and CDH23 possible targets to investigate adaptive convergence/differential selection between river and marine dolphins? Contrast-FEL results suggest that some sites within these genes have evolved differently between freshwater and marine dolphins BUSTED + aBSREL results indicate gene-wide episodic diversifying selection among dolphin branches Codeml: two model and branch-site models to locate branches and sites positively selected More accurate convergence tests will allow examine convergence within dolphins from different habitats Locate and characterize sites under selection dolphins showed proportionally less selected sites compared to reference species *reference tree= dolphins + whales + other species *dolphin tree = only dolphins Future directions SLC26A5, TMC1, CDH23 under positive selection in some, but not all, dolphin lineages S.guianensis has recently split from sister species and P. catodon has sonar adaptations to deep diving HOWEVER... no support for molecular adaptive convergence so far 1 2